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thesis entitled

INTRAHEMISPHERIC AND COMMISSURAL CONNECTIONS BETWEEN AND WITHII
COMMISSURALLY AND NONCOMMISSURALLY INTERCONNECTED REGIONS IN
THE PRIMARY AND SECONDARY SOMATIC SENSORY CEREBRAL CORTEX:

THEIR POSSIBLE ROLE IN INTERHEMISPHERIC TRANSFER OF

LEARN I fiefltw linRACOON

PAUL HERRON

has been accepted towards fulfillment
of the requirements for

_Ph._D_.__._ degree in laid-1511921 and
Neuroscience

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INTRAHEMISPHERIC AND COMMISSURAL CONNECTIONS BETWEEN AND WITHIN
COMMISSURALLY AND NONCOMMISSURALLY INTERCONNECTED REGIONS IN
THE PRIMARY AND SECONDARY SOMATIC SENSORY CEREBRAL CORTEx:
THEIR POSSIBLE ROLE IN INTERHEMISPHERIC TRANSFER OF

LEARNING IN THE RACCOON
By

Paul Herron

A DISSERTATION

Submitted to
Michigan State University
in partial fulfillment of the requirements
for the degree of

DOCTOR OF PHILOSOPHY

Department of Psychology and Neuroscience Program
1979

ABSTRACT
INTRAHEMISPHERIC AND COMMISSURAL CONNECTIONS BETWEEN AND WITHIN
COMMISSURALLY AND NONCOMMISSURALLY INTERCONNECTED REGIONS IN THE
PRIMARY AND SECONDARY SOMATIC SENSORY CEREBRAL CORTEX: THEIR

POSSIBLE ROLE IN INTERHEMISPHERIC TRANSFER OF LEARNING IN THE
RACCOON

by

Paul Herron

The intrahemispheric and commissural circuitry of the primary (SI)
and secondary (SII) somatic sensory cortical regions in the raccoon was
investigated utilizing horseradish peroxidase (HRP), autoradiographic
and anterograde degeneration techniques. The purpose of these
experiments was to determine if intrahemispheric or commissural axons
connect cortical fOci in SI and SII that receive projections from
unrelated parts of the peripheral body surface (nonhomotopic connections)
in addition to those which connect cortical fOci that receive projections
from related parts of the peripheral (homotopic connections). Four sites
were chosen fOr study: the fOrepaw regions of SI and SII (noncommissurally
connected regions) and the hindlimb and trunk regions of SI and SII
(commissurally connected regions).

The site of injection was determined by using:
(1) the electrical response after stimulating the appropriate receptors, and
(2) the gyral pattern which, in many instances, demarcates functional sub-
divisions of SI. The HR? was injected using pressure and iontophoresis
simultaneouSly. The tritiated amino acids were injected using pressure.
After survival periods of 12-72 hours, the HRP was visualized in 40pm
sections by using the chromogens dihydrochlorobenzidine and
tetramethylbenzidine on alternate sections. The distribution of tritiated
amino acids were visualized indirectly in a thin layer of photographic

emulsion above the 40mm sections.

Paul Herron

The results showed that injections of HRP in the hindlimb and
trunk regions (commissurally connected) regions of SII labelled the
cell bodies of intrahemispheric homotopic afferents in the ipsilateral
SI cortical area and commissural afferents in the contralateral SII
cortical region. Injections of HRP in this region also produced
labelled cell bodies of nonhomotopic afferents in the ipsilateral SII
fbrepaw region and the junctional area between the ipsilateral face
regions of SI and SII.

Injections of HRP in the hindlimb and trunk (commissurally
connected) regions of SI labelled the cell bodies of intrahemispheric
homotopic afferents in the ipsilateral SII cortical region as well as
nonhomotopic afferents in the ipsilateral hindpaw region. These HRP
injections also labelled the cell bodies of commissural afferents in
the contralateral SI hindlimb and trunk regions. Injections of tritiated
amino acids in the hindlimb and trunk regions of SI resulted in silver
grains above fibers and terminals in the ipsilateral SII hindlimb and
trunk regions.

Injections of HRP in the forepaw (noncommissurally connected) area of
SII labelled the cell bodies of homotopic afferents in the ipsilateral SI
forepaw area. In addition, these injections also labelled the cell bodies
of nonhomotopic afferents in the ipsilateral SII hindlimb area.

Injections of HRP in the fOrepaw (noncommissurally connected) region
of SI labelled the cell bodies of intrahemispheric homotopic afferents
in the ipsilateral SII fOrepaw region. Small injections in the distal
volar representation areas of digits 3 and 4 labelled the cell bodies of
intrahemispheric nonhomotopic afferents in the more proximal volar
representation areas of digits 3 and 4 in the SI forepaw region. A
lesion in the SI fbrepaw area resulted in degenerated fibers and terminals

in the SII fOrepaw area.

Paul Herron

The labelled cell bodies of each fiber system investigated were
organized into rostrocaudally oriented strips. The majority of the
neurons labelled have pyramidal Shaped cell bodies. The laminar distrib—
ution of the labelled cell bodies exhibited a variety of patterns. The
most common pattern was a focus of labelled cell bodies distributed in
all layers except layer 1. The heaviest concentration of labelled cell
bodies was in layers III and V.

In a pilot study, the functional significance of the SI fOrepaw,

SI face, and SII cortical representation areas was investigated using an
ablation technique. Seven subjects were trained to discriminate rough vs
smooth tactile and temperature tasks in one fOrepaw and sUbsequently
tested fOr perfOrmance with the second paw to determine if intermanual
transfer had occurred. Two subjects had bilateral ablation of the fore-
paw representation area in SI, one subject had bilateral ablation of the
gyral crown of the SI face representation area, and one subject had a
partial unilateral ablation of the SII fOrepaw area and bilateral ablation
of the gyral crown of SI face representation areas. There were also two
normal subjects and one sham Operated subject.

The subjects with bilateral ablation of the SI fOrepaw region were
unable to perfOrm the tasks while animals with SII and SI face ablations
were able to perform, learn and transfer the discrimination tasks. These
results are in sharp contrast to findings in the cat where SI lesions did
not prevent the acquisition of discrimination learning and SII lesions

interfered with transfer of discrimination learning.

ACKNOWLEDGEMENTS

This research was supported by NSF Grant No. 78-00897 and
the Neuroscience Program.

I am grateful to the Department of Natural Resources at Roselake,
Michigan for providing many of the experimental animals.

I would like to express my appreciation to: Bi111Armstrong for
sharing his experimental equipment and chemicals during the course
of the anatomical investigation; Lorraine Brooks who rendered
invaluable service in typing earlier drafts and the final copy of
this thesis; Nancy Duda and Susan Ferenc who were responsible for
collecting much of the behavioral data; Mike Ostapoffand Steve Warach
fOr being ready to help at very short notice; and Mike Peterson for
aid in the preparation of the histological material.

I am particularly grateful to Dr. Charles R. R. Watson for his
continued support and encouragement during my graduate carreer and
who made available the facilities of the Anatomy Department at the
University of New South Wales, Sydney, New South Wales, Australia,
fer the completion of this thesis. I am also grateful to Sharleen
Sakai who provided invaluable help in collecting the anatomical data.

Special thanks are due Drs. Charles Tweedle and James Zacks for
serving on my thesis committee.

I would like to express my greatest appreciation to Dr. J. 1.
Johnson for serving as the chairman of my thesis committee and Dr.
Glen I. Hatton fer serving on my thesis committee and who gaVe me
generous use of his photographic equipment.

To my wife Jan goes special thanks for all of her enthusiastic
support throughout my graduate carreer.

ii

TABLE OF CONTENTS

Page
LIST OF TABLES ............................................... iv
LIST OF FIGURES .............................................. v
INTRODUCTION
The role of the corpus callosum in the intermanual transfer
of tactile learning ........................................ 2
Functional localization in the corpus callosum ........... 3
Anatomical and electrophysiological organization of
commissural connections in the somatosensory areas ......... S
Cytoarchitectural areas of SI and SII .................... 5
Afferent connections of the cytoarchitectural areas ...... 6
Commissural and intracortical connections ...... . ......... 7
Electrophysiological activities of peripheral input
through the corpus callosum .............................. 9
The role Of SI and SII and their intracortical and
commissural connections in the interhemispheric transfer of
tactual learning ........................................... 9
Summary .................................................... 13
The rationale for this study ........................... .... 15
The subjects to be used in this study ...................... 18
METHODS ...................................................... 19
Anatomical techniques: intracellular transport of horse-
radish peroxidase and tritiated amino acids ................ 19
Anterograde degeneration technique ......................... 21
Analysis of data ................... . ....................... 23
RESULTS ...................................................... 25
Features of the injection site..... ....................... . 25
Nature of staining - horseradish peroxidase ........ . ....... 28
Nature Of staining - autoradiography .......... ... .......... 30
Topography of intrahemispheric and commissural connections. 30
Afferents of the SII fbrepaw area. . ........ .. ...... ..... . 31
The intrahemispheric and commissural afferents of the SII
hindpaw and trunk region ................................... 43

The intrahemispheric afferents of the SI forepaw region.... 57
Intrahemispheric distribution of terminals from the SI

fbrepaw region ............................................. 62
Intrahemispheric and commissural afferents of SI agranular
area. ..... .. ............ ........... ...... ... ........... . . 67
Intrahemispheric and commissural efferents Of SI agranular
cortex. .................................................... 78
Summary-of results 78
DISCUSSION ....... . ........................................... 85

iii

Laminar organization and the formation of strips ........... 89

BEHAVIOR PROCEDURE ........................................... 94
Surgical procedure ......................................... 94
Testing apparatus .......................................... 95
Controls.. ................................................. 97

RESULTS... ..... . ............................................. 101
Discrimination performance and transfer of the rough vs
smooth task ................................................ 101
Discrimination perfOrmance and transfer of the
temperature task ............... ...... ...................... 104

DISCUSSION. .................................................. 106
Summary .................................................... 107

LIST OF REFERENCES.... ....................................... 108

iv

LIST OF TABLES

Tables Page

1. Summary of the experiments and results
in this study ........................................ 32

2. Post-lesion placing and hopping behavior and
the saving scores in percentages between
acquisition trials and transfer test ................. 102

Figure

10.

11.

12.

13.

14.

15.
16.

17.

LIST OF FIGURES

Schematic diagram of postulated intrahemispheric
and commissural connections between SI and SII

Schematic diagram of the injection apparatus

The differential concentration of the reaction
product in an HRP injection site

Schematic diagram of the injection sites listed
in table I.

The cell bodies of origin of the SII hindpaw to SI

fOrepaw projection

The cell bodies of origin of the SI to SII projection

Photomicrograph of the cell bodies of the origin of

the SI to SII projection

Page

17

22

27

35

38

4O

42

The cell bodies of origin of the SI to SII projection 45

The cell bodies of INA projection
The cell bodies Of IHA projection

The cell bodies of CA projection to SII hindlimb
and trunk region of SII

Labelled cell bodies of the SII hindlimb to SI
hindlimb projection

The cell bodies of IHA projection to the SI
fOrepaw region

The cell bodies of INA projection to the SI
fOrepaw-region

Efferent projection of the SI forepaw region
Efferent projection of the SI fOrepaw region

The cell bodies of the SII hindlimb and trunk to
SI hindlimb and trunk projection

vi

47

50

53

S6

59

61

64

66

69

Figure

10.

11.

12.

13.

14.

15.
16.

17.

LIST OF FIGURES

Schematic diagram of postulated intrahemispheric
and commissural connections between SI and SII

Schematic diagram of the injection apparatus

The differential concentration of the reaction
product in an HRP injection site

Schematic diagram of the injection sites listed
in table I.

The cell bodies of origin of the SII hindpaw to SI

forepaw projection

The cell bodies of origin of the SI to SII projection

Photomicrograph of the cell bodies of the origin of

the SI to SII projection

Page

17

22

27

35

38

4O

42

The cell bodies of origin Of the SI to SII projection 45

The cell bodies of INA projection
The cell bodies of IHA projection

The cell bodies of CA projection to SII hindlimb
and trunk region of SII

Labelled cell bodies of the SII hindlimb to SI
hindlimb projection

The cell bodies of IHA projection to the SI
ferepaw region

The cell bodies of INA projection to the SI
fOrepaw‘region

Efferent projection of the SI forepaw region
Efferent projection of the SI fOrepaw region

The cell bodies of the SII hindlimb and trunk to
SI hindlimb and trunk projection

vi

47

SO

53

56

59

61

64

66

69

Figure

18.

19.

20.

21.

22.

23.
24.

25.

26.

27.

28.

29.

The cell bodies of the SII hindlimb and trunk to
SI hindlimb and trunk projection

Photomicrograph of the injection site in
experiment 77559

The cell bodies of CA afferents to SI trunk
region

The cell bodies of CA afferents to SI hindlimb
and trunk region

Distribution fibers and terminals originating
from SI trunk region

The IHE efferents of the SI trunk region
Summary diagram of results

Pyramidal cell bodies of origin of the SI
fOrepaw to SII forepaw projection

Schematic of the outside and the inside of
the testing apparatus

Schematic of the ablations in the experimental
animals

Learning curves for the training and subsequent
testing of animals on the rough vs smooth
discrimination tasks

Learning curves fur the training and subsequent
testing of animals on the temperature
discrimination task

Page

71

73

75

77

8O
82

87

91

96

99

103

105

INTRODUCTION

In their quest to understand the functional significance of
neural circuitry in complex mental activities of the brain, Sperry
and Myers used subjects whose forebrain commissures (notably the
corpus callosum) had been sectioned (Cazzaniga et al., 1965; Myers,
1959, 1962, 1965; Sperry, 1955, 1961, 1962, 1966, 1967). They fOund
that subjects without these commissures intact had essentially two
separate brains within one skull. Things experienced and remembered
in one hemisphere are unconnected with the things experienced and
remembered in the other hemisphere. Animals with surgically separated
hemispheres may be trained concurrently and simultaneously to do
diametrically opposite tasks, something that subjects with normal
unified brains could not do (Myers, 1962; Sperry, 1967; Trevarthen, 1960).

The ablation method was subsequently used to further localize the
site of learning and memory within one cerebral hemisphere. When the
somatic sensory cortical region is left intact and hippocampus, anterior
thalamus and most of the caudate and amygdaloid complex are removed in
one hemisphere of split brain cats, that hemisphere can still learn new
tactile discrimination (Sperry, 1959). It was shown that a small
island of somatic sensory cortex was sufficient fer tactile discrimination
learning in cats. Complete destruction of the somatic sensory cortical
region makes it impossible fer the animal to learn new tactile
discriminations. These data also showed that intracortical fibers
connecting related sensory cortical regions were functionally important.
In the monkey, intracortical connections between the visual cortex and

the temporal cortex was feund to be indispensible for learning visual
1

2

tasks other than brightness discrimination (Chow, 1967).

The role of the corpus callosum in the intermanual transfer of
taCtile‘learning

 

 

Several studies showed that the corpus callosum was necessary for
the transfer of sensory learning between the hemispheres. Bykov
(1924, from Ebner and Myers, 1962) first reported that sectioning

Of the corpus callosum tended to prevent the usual contralateral
transfer of cutaneous conditioning of salivary reflexes in dogs.
However, later investigations of the role of the corpus callosum in
intermanual transfer of tactile learning were not always consistent.
Normal subjects, of all mammals investigated, required considerably
less time for second hand solving after experience through the first
hand (Glickstein and Sperry, 1960; Myers, 1962). Smith (1951) worked
with patients whose corpus callosum had been sectioned and fbund
that intermanual transfer of stylus-maze learning was interfered
with but not blocked. A human patient with corpus callosum agenesis
showed complete absence of intermanual transfer of discrimination
learning (Russel and Reitan, 1955). In another study, a human patient
with corpus callosum agenesis showed excellent transfer of tactile
discrimination learning (Myers, 1962). In rhesus monkeys, Ebner and
Myers (1962) fOund that sectioning of the corpus callosum blocked
transfer of tactile discrimination between the extremities. Using
the same species of monkeys, Glickstein and Sperry (1960) fbund that
sectioning of the corpus callosum blocked transfer in a majority of
the tests. In callosal sectioned cats, there is complete absence of
intermanual transfer of tactile discrimination learning (Stamm and

Sperry, 1957).

3
Glickstein and Sperry (1960) argued that the corpus callosum

was responsible for the direct intermanual transfer of "distinctive
sensory knowledge" between the extremities in all species. However,
extra—callosal systems that are capable of transmitting infbrmation

to the "untrained" hemisphere have developed in primates. Factors

such as the type and difficulty of the tests or injury to the

"trained" hemisphere determine the potency of this extra-callosal
system in the transfer of learning. If the corpus callosum is sec—
tioned and the somatic sensory projection areas in the "trained"
hemisphere damaged prior to training, the extra—callosal system is

used to transfer the learning to the "untrained" hemisphere (Glickstein

and Sperry, 1960).

Functional localization in the corpus callosum. Localization of

 

functions in the corpus callosum was fOund in the cat and monkey.
Transection of the anterior part of the corpus callosum did not inter-
fere with the transfer of visual discrimination learning in cats.
However, a definite decrement in interocular transfer was observed
after destruction of about 25% of the corpus callosum along the posterior
end. When the transection extended beyond 50% of the posterior part of
the callosum, there was complete or nearly complete interference with
transfer (Myers, 1959; Sperry et al., 1956). Similar decremental
effects were observed on the transfer of tactual learning between
the hemispheres after transection of the posterior part of the corpus
callosum in monkeys (Myers and Ebner, 1976).

These data provided strong evidence fer the role of commissures
in the interhemispheric integration of learning and memory. The

infermation transferred across the corpus callosum is not, however,

4

a faithful reproduction of information received and learnedv in

the first hemisphere. Sperry (1967) suggested that only an
abbreviated and abstracted part of the original sensory input

crosses the callosum. This hypothesis received support from exper-
iments which demonstrated that neither cats nor monkeys showed a

100% saving in the "untrained" hemisphere when compared to the

final perfOrmance of the "trained" hemisphere (Myers, 1962; Glickstein
and Sperry, 1953).

Myers (1962) monocularly trained animals on a discrimination
task and made lesions of varying sizes in the "trained" hemisphere
of different animals; when the 'untrained' hemisphere was tested for
transfer, its performance was at or near chance level and remained so
fer a number of testing sequences. These data suggest that the
commissural connections are very important fer interhemispheric trans-
fer and must be intact in order fer the "untrained" hemisphere to Show
any savings.

The results of the studies discussed above and the fact that com-
plex mental functions like language and mathematics are consistently
found in one hemisphere (typically the left) led Sperry (1967) to
hypothesize that the role of the callosum was to inhibit the bilateral-
ization of learning and memory. Information transmitted across the
callosum is complemental and supplemental to design rather than
symmetrical (Sperry, 1965, 1967). He suggested that detailed anatomy
of the callosum might reveal greater assymmetry of callosum connections

than the strict homotopic projections suggested by Bremer (1958).

5
Anatomical and Electrophysiolggical Organization of

 

Commissural Connections in the Somatosensory Areas

 

Cytoarchitectural Areas of SI and SII. The projection of somesthetic

 

receptors to two separate and distinct areas of the cerebral neocortex -
the primary somatosensory area (SI) and the second somatosensory area
(SII) - has been established electrophysiologically in a variety of
mammals (Adrian, 1940; Herron, 1978; Johnson et al., 1974; Lende, 1963;
Pimentel-Souza et al., 1978; Pinto Hamuy et al., 1956; Pubols and
Pubols, 1971; Welker and Seidenstein, 1959; Woolsey and Fairman, 1946).
The receptive fields of both SI and SII are somatotopically organized;
that is, the somatic receptors are represented on the cortical surface
in a manner that reflect their actual relationships on the animal's
body surface.

The cell bodies in SI and SII are arranged into vertical columns.
Physiological investigations of columns in the sensory projection areas
have shown that the excitatory receptive fields of each neuron within a
vertical column are all situated in roughly the same receptor area
(Creutzfeldt, 1978; Powell and Mbuntcastle, 1959).

Based on the morphology of their cell bodies neurons in SI and SII
can be divided into two broad classes. Neurons with pyramidal shaped
cell bodies make up one class and neurons with nonpyramidal shaped cell
bodies constitute the other class (Jones, 1975). Mest nonpyramidal
shaped neurons have stellate shaped cell bodies. The two classes of
neurons are organised into six distinct laminae. There is considerable
variation in the concentration of each class of neurons in different
areas of SI and SII (Sanides, 1972). In some areas, the concentration
of pyramidal neurons in layers III and V is minimal and that of the
stellate cells in layer IV is maximal. These areas of SI and SII are

termed "granular" cortices.

6

The other areas in SI and SII have a maximum concentration of
pyramidal cells in layers IIIand V and a relatively small concentration
of stellate cells in layer IV. These areas are called "agranular"
cortices (Akers and Killackey, 1978; Ebner, 1967, 1969; Jones, 1975;

Welker, 1976).

Afferent'COnnections of the Cytoarchitectural Areas. The cytoarchitectural

 

differences between these cortices in SI and SII is a reflection of
different afferent and efferent connections. The granular cortices

of SI receive projections from the densely innervated regions of the
body such as the distal limb parts and, consequently, the bulk of the
thalamocortical afferents. Ebner (1967, 1969) studied the differential
distribution of thalamocortical afferents to SI in the opossum, cat, and
monkey and suggested that the granular cortices are specialized for
receiving specific thalamic projections. In rats, discrete aggregations
Of stellate cells in layer IV termed "barrels" (Woolsey and van der
Loos, 1970), receive equally discrete clusters of thalamocortical
afferents (Killackey, 1973; Killackey and Leshin, 1975).

Using the electron microscope to study serial sections, (White, 1978)
showed that most thalamocortical afferents, in SI of rats, terminate on
the dendrites and cell bodies of non-spiny stellate neurons in layer IV.
The remainder of the thalamocortical afferents terminate on the dendritic
spines of spiny stellate neurons, dendrites and cell bodies of bipolar
neurons, and apical dendrites of layer V pyramidal neurons, and the basal
dendrites of layer III pyramidal neurons (White, 1978).

Ebner and Myers (1965) first pointed out that, in the cat and
raccoon, the parts Of SI and SII containing the representation of the
forelimb and the distal segments of the hindlimb, i.e. the granular areas,
do not contain degenerating axons fOllowing section of the corpus

callosum. Similarly. the granular areas were acallosal in SI and SII ____

7
of monkeys (Jones and Powell, 1969; Jones and Wise, 1977; Pandya

and Vignolo, 1968), rats (Wise and Jones, 1976), cats (Jones and
Powell, 1968b) and mice (Caviness and York, 1972).

In contrast, the agranular cortices in SI and SII are character-
ized by their rich commissural connections and, in SI at least,
relatively sparse thalamic connections (Ebner, 1967, 1969; Jones and
Wise, 1976). The differential density in thalamic input to the .
granular and agranular cortices of SII has not been investigated.

I Electron microscopic studies by Sloper (1973) have shown that,
in the motor cortex of monkeys, commissural afferents terminate on the
apical and basal dendrites of pyramidal neurons. The thalamocortical
receiving zones in the agranular cortices of SI receive projections from
the lightly innervated regions of the body such as the axial body parts

(Ebner, 1967; Jones and Powell, 1968b).

Commissural and Intracortical Connections. Utilizing the anterograde

 

degeneration, horseradish peroxidase, and autoradiographic techniques,
several studies have shown that agranular cortices of SI and SII are
reciprocally and homotopically connected with the contralateral SI and
SII agranular cortices (Jacobson and Trojanowski, 1974; Jones and
Powell, 1968b, 1969b; Jones and Wise, 1977; Pandya and Vignolo, 1968;
Wise and Jones, 1976). The agranular cortex of SI also sends well-
ordered somatotopically organized projection to the contralateral SII
(Jones and Powell, 1968b, 1969b; Pandya and Vignolo, 1968). In those
instances where heterotopic commissural connections have been observed,
the heterotopic projections were never between agranular and granular
cortices. Jones et al (1975) suggest that commissural axons may arise

from and terminate upon exactly homotopic groups of pyramidal cells.

8

In nonprimates, horseradish peroxidase studies have shown that the
cells of origin of commissural afferents are in layer III and V and
arranged in distinct clusters. In the rat, cat (Jacobson and
Trojanowski, 1974) and monkey (Jones and Wise, 1977), the clusters have
an average diameter of 0.5-1.00 mm and are oriented in medial—lateral
strips. In monkeys, the commissural projecting cells Of SI and SII
originated from layer IIIV. That the commissural projecting cells may
also receive commissural terminals is inferred from autoradiographic
data in monkeys; this data showed that commissural fibers terminated
in patches, 0.5 - 0.8 in diameter, and were distributed over layers
II-IV in a pattern that resembles the shape of an hour glass. It was
suggested that this pattern is a result of callosal fibers terminating
preferentially on the apical and basal dendrites of pyramidal neurons in
layer IIIB (Jones et al., 1975).

The intracortical connections between SI and SII in the cat and
rhesus monkey were observed to be well-ordered and somatotopically
organized (Jones and Powell, 1968a, 1969a). There were topographical
and reciprocal connections between granular areas as well as agranular
areas of SI and SII but no connections between dissimilar cortices of
SI and SII.

Akers and Killackey (1978) made small lesions in the granular
cortex of SI in rats and observed degenerating fibers and terminals in
the surrounding agranular cortex of SI. Using autoradiography, Jones
et a1. (1978) investigated the intracortical projections of the
Brodmann's areas 3, l and 2 in SI. These data showed that neurons in
the more granular area 3 projected to neurons in the adjacent and less
granular area 1.

In the rhesus monkey )Loe et al., 1978) and raccoon (Herron, 1979),

the granular and agranular cortices of SI differ from the granular and

9

agranular cortices of SI differ from the granular and agranular
cortices of SII in their thalamic connections. The SI granular

and agranular cortices receive projections from the ventral posterior
lateral and ventral posterior medial nuclei (ventrobasal complex in
raccoons) whereas SII receives the bulk of its projections from the

ventral posterior inferior nucleus.

ElectrophysiOlOgical Resp0nses of Neurons in the Granular and Agranular

 

Cortices to Peripheral and Contralateral Cortex Stimulation

 

The electrophysiological activities of the granular cortices
differ from that of the agranular cortices. Welker (1976) mapped the
facial projections of SI of rats and fOund that units in the granular
cortices are small, modality specific and tOpographically organized.

On the other hand, recordings from narrow patches of agranular cortex,
intercalated between the barrels in the facial projection area of SI,
were found to be generally unresponsive to peripheral stimulation. The
agranular units that could be driven by peripheral stimulation were
responsive to the same kind of stimulation as that of units in the
adjacent granular cortex.

The receptive field properties fer some units in the agranular
cortices of SII are unusually large and are not somatotopically
organized with respect to adjacent units (Carreras and Andersson, 1963).
Many of the units that are somatotopically organized in SII receive
bilateral input. Over 90% of the units in the unanesthetized monkey
(Whitsel et al., 1969) and 63% in the unanesthetized cat (Robinson,
1973) were responsive to bilateral stimulation of the body surface.
Robinson (1973) and Innocenti et al (1972) have shown that the pathway

fer the major share of the input from the ipsilateral body parts to

10
these bilateral units involves input through the corpus callosum
from the contralateral SI and SII cortices.

There is a discrepancy between anatomical and electrophysiological
data concerning corpus callosum afferents to the SI and SII cortices.
In contrast to the acallosal zones observed in anatomical studies,
evoked potentials were recorded when stimulating and recording
electrodes were situated at all_symmetrical points in the somatosensory
areas of monkeys (Bremer, 1958; Curtis, 1940). In addition, Curtis
(1940) recorded potentials at points asymmetrical to the location of
the stimulating electrodes.

Innocenti et a1 (1974) recorded from single fibers in the anterior
part of the corpus callosum in cats and fbund that all parts of the
body were represented in the population of fibers they studied. The
amplitude of the responses did not change from area to area within the
corpus callosum. The average latency of responses from the distal
segments were longer than that of responses from the axial body parts
(Innocenti et al., 1972, 1973, 1974).

Innocenti et al., (1974) recorded from a small group of fibers in
the corpus callosum while stimulating a small area of SI. Several
short latency waves were elicited. The first wave had a latency of
0.4 to 0.6 msec. and was thought to be the result of direct asynaptic
excitation of callosal projecting cells. The second wave had a latency
of 0.8 to 1.0 msec. and was thought to be caused by excitation of pre-
synaptic fibers impinging on callosal projecting cells and consequent
transynaptic activation of the latter (Innocenti et al., 1974). They
did not identify the source of the presynaptic fibers.

In cats, a disproportionately large percentage of the callosal
fibers were responsive to stimulation of the face and distal segments

(Innocenti et al., 1974). The projections of facial and distal segments

11

through the corpus callosum is commensurate with the projections of
facial and distal segments to the SI and SII areas. These fibers had
localized receptive fields, were modality specific and possessed
electrophysiological properties that were the same as those Observed
fer units in the granular cortices of SI and SII. However, 90% of
the fibers terminated on units in SII that had unusually large and
bilateral receptive fields were not somatotopically organized with
respect to adjacent unit. Thus, in cats, the units which send axons
into the corpus callosum do not also receive callosal input.

Peripheral and commissural input were Observed to converge on
10% of the units investigated by Robinson (1973). Commissural
afferents from SI and SII were observed to converge on 36% of the

SII units that were recorded (Robinson, 1973).

The role of SI and SII and their intracortical and commissural

 

connections in the interhemiSpheric transfer of tactual learning

 

Teitelbaum et al (1968) showed that SI and SII were functionally
important for the intermanual transfer of learning in cats. Uni-
lateral ablation Of SII blocked interhemispheric transfer of learning
in both directions: the animals did not show transfer of learning when
the damaged hemisphere was trained first and the normal hemisphere
tested fer saving or when the normal hemisphere was trained first and
the damaged hemisphere tested for transfer. Similarly, unilateral
ablation of the fbrepaw area in SI blocked the interhemispheric trans-
fer of learning from the damaged to the normal hemisphere. Unilateral
ablation of SI forepaw areas did not block transfer of learning from
the normal to the damaged hemisphere (Teitelbaum et al., 1968). Thus,
in the cat at least, SII is necessary fer both receiving and transferring

tactual learning while SI is only necessary for transferring learning.

12

The role of SI and SII intracortical and commissural connectivity
in the interhemispheric transfer of tactual learning have been inter-
preted in several ways. One hypothesis is that only regions represent-
ing midline or axial body structures and/or bilateral input exchange
interhemispheric information; the commissural connections "sew"
together the midline body structures and provide to each hemisphere
a continuous mapping of the midline activities in the other hemisphere
(Choudhury et al., 1965; Jones and Powell, 1968b, 1969b; Pandya et al.,
1971; Pandya and Vignolo, 1968). Jones and Powell (1968b) wrote:

"The absence of callosal connexiOnss between the regions representing
the distal portions of the limbs make it unlikely that intermanual
transfer of tactual learning occurs through direct commissural
connexions."

However, in the sensory systems of rats and mice this hypothesis
is inconsistent with the anatomical data. In these species, an axial
body region, the face area, receives and sends very sparse commissural
projections (Akers and Killackey, 1978; Caviness and York, 1975; White
and De Amicis, 1977). Using autoradiography, Wise and Jones (1976)_
showed in rats that a few narrow patches of agranular cortex, inter-
calated between the barrels in the granular cortex, receive dense
commissural input. Similar results were obtained with the lesion method
(Akers and Killackey, 1978).

Another hypothesis is that the commissural connections between SI
and SII mediate the interhemispheric transfer of learning. Innocenti
et al., (1974) suggested that tactile information through the corpus
callosum is more related to the densely innervated regions of the body
than to midline body structures.

Boyd et al (1971) suggested two explanations fer the contrasting
results obtained by anatomical and electrophysiological studies Of

the commissural connections between the somatosensory cortical areas.

13
They suggested that either a synapse was interposed between the granular
(acallosal) and agranular (callosally connected) areas, or that
anatomical techniques failed to detect the commissural fibers and
terminals in the acallosal zones (Boyd et al., 1971). The study
by Akers and Killackey (1978) supports the fermer explanation. This
data showed that neurons in the granular cortex of rats project
intracortically to the surrounding agranular cortex (Akers and
Killackey, 1978). Presumably, the intracortical fibers terminate on
callosally projecting cells which then transmit the infOrmation through

the corpus callosum to the contralateral somatosensory areas.

Summary

Investigators used the split brain approach to localize the site

of learning and.memory within one hemisphere. The visual and somatic

sensory areas were capable of learning, respectively, brightness and
tactile discriminations.

The corpus callosum mediated the interhemispheric transfer of
learning. In cats and.monkeys, localization of visual and somatic
sensory functions were observed in the corpus callosum.

The somatic sensory projection areas contained at least two electro-
physiologically defined short latency representations of the receptors
on the animal's body surface. There are cytoarchitectural areas in
SI and SII related to those areas which receive projections from the
densely innervated regions on the animal's body surface and those that
are interconnected with the contralateral SI and SII cortical regions.
Granular areas in the SI and SII cortical regions are those areas which
contain a relatively higher concentration of neurons with stellate

shaped cell bodies whereas agranular areas in the SI and SII cortical

14

regions are those areas which contain a relatively higher concentration
of neurons with pyramidal shaped cell bodies:

Anatomically and electrophysiologically, the intrahemispheric
and commissural afferent and efferent connections in SI and SII can
be characterized in the following manner: (a) homotopic connections
are connections between cortical areas that receive projections from
the same or very similar peripheral body parts, and (b) heterotopic
connections are connections between cortical areas that do not receive
projections from the same or very similar peripheral body parts, in
other words, connections between cortical areas which receive project—
ions from very different peripheral body parts. Heterotopic connections
can also be defined as nonhomotopic connections.

The granular areas of SI receive projections from the densely
innervated regions of the body and, consequently, heavy thalamic input
from its referent specific thalamic nucleus. The agranular areas of
SI and SII agranular cortices were reciprocally and homotopically
connected with respectively, the contralateral SI and SII agranular
cortices. SI sends a somatotopically organized projection to SII as
well.

In monkeys, the cell bodies of commissural projecting neurons in
SI are located in layer IIIB. Intracortical afferents originated from
layer IIIA in SI and layers III, IV, and V in SII. In nonprimates,
intracortical afferents originated from all layers except layer I.

In rats, small lesions in the granular cortex of SI resulted in
degenerated fibers and terminals in the surrounding agranular cortex.

Electrophysiological studies, in contrast to anatomical studies,
show that all areas of SI and SII are homotopically connected. These

studies also showed that some points on the cerebral neocortex project

15
to heterotopic sites.

Recordings from single fibers in the corpus callosum Showed that
the callosal projecting units had the same electrophysiological
characteristics as those observed for units in the granular areas.
However, these axons terminated on very different type of cells:
cells with unusually large and bilateral receptive fields.

Behaviorally in cats, ablation of SI blocked the interhemispheric
transfer of learning from the damaged to the normal hemisphere.
Ablation of SI did not block the transfer of learning from the normal
to the damaged hemisphere. Ablation of SII blocked the transfer of

learning to, as well as from, the damaged hemisphere.

The rationale fer this study»

 

Potential sources of confusion in the study of interhemispheric
transfer of learning are the contrasting results of electrophysiological

and anatomical studies: electrophysiological studies of commissural

 

projections Show that all symmetrical cortical areas in SI and SII are

connected whereas anatomical studies indicate the granular cortices are

 

devoid of commissural connections. This discrepancy between the
electrophysiological and anatomical studies regarding commissural
connections can be resolved by understanding the intrahemispheric and
commissural circuitry which allows fur synaptic interaction of agranular
(Commissurally connected) and granular cortices of SI and SII. One
could postulate a shema of organization which shows that, in addition

to the intrahemispheric axons which connect those cortical fOci in SI

and SII that receive projections from related parts of the periphery,

16
intrahemispheric axons also connect cortical foci that receive
projections from unrelated parts of the periphery. Therefore,
infermation from the granular cortices (i.e. the noncommissurally
connected regions of SI and SII) destined fer the contralateral
homotopic areas is first relayed via intrahemispheric connections
to agranular cortex. The information is then transmitted to the
contralateral hemisphere via commissural connections and then to the
homotopic granular area by intrahemispheric connections (Fig. 1).

As a first step in testing this schema, the purpose of this
study was to establish the cells of origin of the intrahemispheric
and commissural connections in the granular and agranular reigons of
SI and SII in raccoons. Horseradish peroxidase and autoradiographic
techniques were used to determine; (1) the intrahemispheric afferents
and efferents of neurons in two sites of the granular cortex of SI,
the 4th and 5th digital area, (20 the intrahemispheric and commissural
afferents and efferents of neurons in one site of the agranular
cortex of SI, the trunk region, (3) the intrahemispheric afferents
and efferents of neurons in the granular cortex of SII, and (4) the
intracortical afferents and efferents of neurons in the agranular
cortex of SII.

In a pilot study using raccoons, the functional significance of
these connections of SI and SII in the interhemispheric transfer of
learning were determined by bilaterally ablating either SI or SII and

testing for transfer of tactual and temperature discrimination learning.

17

Midllne

-——————o—————————.—--—‘-——-—

 

 

 

   

Figure 1: Schematic diagram of postulated intrahemispheric
and commissural connections between Si and SII.
G, granular cortex, AG, agranular cortex.

18

The subjects used in this study

 

The questions proposed above can best be investigated in animals
such as the raccoon which exhibit a neural specialization of its
sensory system that correspond well with its behavior specialization
(Welker and Campos, 1963; Johnson 1979 fer review). The adaptive life-
style of an animal and its predecessors may select for the outstanding
development of the somatic sensory system in an animal relative to the
development Of other sensory systems in the same animal. The raccoon,
which makes extensive use of its forepaw in the manipulation and
tactile exploration of its environment, has a somatic sensory system
that exhibits both a specialized anatomical and physiological development.
The SI and SII cortical regions are dominated by their extensive fOrepaw
projections. According to Welker and Seidenstein (1959), SI can be
discretely separated into individual "digit" and "foot pad" gyri.

These projections are 60% of the total SI area in the raccoon compared
to only 20% and 30% fOrepaw projection in the SI cortical region Of the
dog and cat, respectively, related carnivores (Welker and Seidenstein,
1959). Similar differential patterns of peripheral projections are
Observed in SII of the raccoon where fOrepaw projection are 70% of the
tactile SII cortical area (Herron, 1978). By studying the anatomical,
physiological, and behavioral characteristics of such a sensory system,
properties are manifested which otherwise may not be noticed (Welker

and Seidenstein, 1959).

METHODS

In 17 adolescent and adult raccoons, the origin and termination
Of intracortical and commissural connections to the SI and SII cor-
tical areas were investigated by the horseradish peroxidase, auto-
radiographic and anterograde degeneration techniques.

The first part of this presentation of anatomical methods will
discuss the procedures used in the horseradish peroxidase and auto-
radiographic experiments and the second part will discuss the procedures

used in the anterograde degeneration experiments.

Anatomical Experiments: Intracellular Transport of Horseradish

Peroxidase and Tritiated Amino Acids. The brains of 17 raccoons were

 

used fer this investigation. The raccoons were trapped in the wooded
areas surrounding the Michigan State University campus.

The animals were anesthetized with chloralose (initial dosage,
17 mg/kg) or sodium pentobarbital (initial dosage, 37 mg/kg). The head
was placed in a stereotaxic apparatus and the cranium exposed. Small
holes approximately 2 mm in diameter were drilled in the skull above
the area of experimental interest and a surface recording electrode
placed on the dura to determine, electrophysiologically, the area's
general location with regard to the somatotopic map. Small incisions
were made in the dura of the drilled sites chosen fer further investig-
ation and a microelectrode was lowered into the cortex to determine the
detailed receptive field properties. The electrophysiological infbrmation
along with the gyral patterns were used to determine the injection site.

Horseradish peroxidase (HRP) and tritiated amino acids (TAA)
19

20

(1:1 mixture of L-leucine [4, 5 3H] and L-proline [3H], Schwarz/Mann)
were the tracers injected. The injection procedure is a modification
of the pressure injection procedures developed by Droz (1975) and
Price et al (1977) and the iontophoretic procedure developed by
Graybiel and Devor (1974). Without introducing any air bubbles,
beveled pipette electrodes, tip diameter of 60-120u, were sealed onto
the tip of a 1 ul Hamilton syringe with wax. The injection apparatus
consisted of two interconnected B-D Yale Syringes (6 ml and 20 ml)
which transmitted the driving force of a Harvard Apparatus infusion
pump (Figure 2). The two syringes, the micropipette and all the
tubing were filled with paraffin oil. An electrical lead fer ionto-
phoresis was attached to an outlet of the syringe needle. HRP was
then injected by applying both pressure and current simultaneously.

Two types of HRP solutions were injected into the same site.
Firstly, HRP solution A was injected via pressure and current. Solution
A was a 30-40% HRP solution which consisted of equal amounts of Sigma
type VI and type IX, Werthington and Miles HRP powder or crystals and
1% poly-l-ornithine dissolved in tris buffer with 0.2 - 1.0 M
potassium chloride.

Secondly, solution B was injected by pressure alone. Solution B
contained both HRP and TAA. The TAA mixture was dehydrated by passing
a slow stream of nitrogen gas over it and reconstituted with an HRP
solution which contained water as the solvent instead of tris buffer
and potassium chloride.

The pressure injection rate was lul/l.2-l.6 hours and 1-3 micro-
amps were used (Midguard High Voltage Precision current source). These
methods of injection of the HRP and then the HRP and TAA combined allowed

fer better labeling of terminals and cell bodies without increasing the

21

size of the injection site. The range of injection site sizes are
discussed in the RESULTS section.

After survival periods of 12-72 hours, the animals were perfused
and the brain removed, the location of the injection site marked on a
photograph and the brain processed according to the protocol developed
by Mesulam and Rosene (1977). The perfusion solution contained 1%
paraformaldehyde and 1.5% glutaraldehyde in 0.1 M phosphate buffer.
Frozen sections 40 um thick were cut in the coronal plane and stored
fer either autoradiography or HRP histochemistry.

The HRP was visualized by incubating the tissue in a solution
which contained tetramethylbenzidine (TMB) or dihydrochlorobenzidine
(DCB) in the presence of hydrogen peroxide (Mesulam and Rosene, 1977).
The sections were then counterstained in buffered 1% neutral red and
cover—slipped.

The sections fer autoradiography were dehydrated and dipped in a
1:1 mixture of water and NTB-2 Kodak emulsion. These sections were
stored in a light-proof container in the refrigerator at 4°C for
5-20 weeks. The sections were then developed in D-19 at 12-140 fer
3 minutes and 15 seconds followed by fixation of the emulsion and

counterstaining of the tissue in 1% thionine.

‘Anterograde'DegenerationTechnique

 

The brains of 2 raccoons were used fer this investigation. An
opening approximately 1 cm in diameter was made in the skull above the
cortical area of interest. The dura was incised in 4 directions, then
peeled away, and with the aid of a dissecting microscope, the site of
the lesion in the cortical area of interest was determined. The
lesion was made with a small pipette attached to a suction pump with

tygon tubing.

Figure 2:

22

 

 

 

 

 

 

~
’0,

 

Schematic diagram Of the injection apparatus. The
apparatus consisted of two syringes (6 ml and 20 ml)
connected together by tygon tubing filled with paraffin
oil. The syringes transmitted the driving fOrce of an
infusion pump. The apparatus permitted both a pressure
and ionotophoretic injections simultaneously. A. 1 ul
syringe inside syringe holder. A. Syringe whose plunger
drove the plunger of the 1 ul syringe. C, 20 ml syringe.
D. Outlet fur electrical lead for iontophoresis.

23

Following a 48 hr survival time, the animals were perfused intra-
cardially and the brain processed according to the protocol developed
by De Olmos (1960). The perfusion solution contained 4% paraformaldehyde,
4% sucrose and .067 M sodium cacodylate at a ph of 7.2-7.4. The brain
was embedded in gelatin and frozen sections, 40 pm thick, were cut
in the coronal plane. Some of the sections were stored fer cupric
silver staining and others were stored fer thionine staining. The
sections were incubated in a copper silver solution for 5 days and then
stained with silver nitrate.

The sections were reduced in a solution which contained 12 ml of
10% commercial fOrmalin, 7 ml 1% citric acid and 100 ml of 95% ethanol
in 881 ml of distilled water.

The sections were mounted out of creosote or acetate buffer
Cmodification by Robert Switzer, personal communication) and cover

slipped.

Analysis of Data

 

In all HRP, autoradiographic and lesion experiments, the brains
were blocked in a standard plane perpendicular to the ventral base of
the brain resting on a horizontal surface and sectioned at 40 pm. In
the HRP experiments, adjacent sections, taken at 200 um intervals
through the brain, were stained with TMB and DCB. The HRP, auto-
radiographic and cupric silver sections were examined microscopically
and, respectively, the foci of labeled cell bodies, silver grains, and
degenerated fibers and terminals were charted on projected tracings of
the histological sections. The distribution and approximate density
of labeled cell bodies in each section was indicated by placing small

dots in comparable locations in the tracing. In the tracings the

24

blackened area indicates the central core and the stippled area
indicates the diffusion of the reaction product in the injection
site.

The approximate density of the silver grains or degenerated
fibers and terminals was indicated in each tracing by very small

dots in places comparable to those observed in the histological

section.

RESULTS

Features of the injectiOn site. Horseradish peroxidase injection

 

sites exhibited several distinctive features. A prominent feature

of each TMB or DCB injection site was the differential concentration
of the HRP reaction product in the injection site. Under the light
microscope, the injection sites of DCB and TMB consisted of three
zones. Each zone was representative of a different concentration of
HRP reaction product. These zones of concentrations observed in the
injection sites of DCB and TMB are very similar to those described fer
diaminobenzidine-tetrahydrochloride (DAB) (Vanegas et al., 1978).

Zone 1 was the area in the center of the injection site and
surrounded the needle track. When DCB was used as the chromogen, zone
1 was characterized by a very dark blue staining background (Figure 3).
The dense concentration of the HRP reaction product in the background
prevented the identification of individual neural elements. The
relative density of the staining in zone 1 in several experiments
appeared to be a function of the injection rate: a given quantity of
HRP injected over a longer period of time resulted in denser con-
centration of the reaction product.

Zone II, the area of the injection site surrounding zone 1, was
characterized by a lesser concentration of the reaction product in
the background than that Observed in zone 1 (Figure 3). Zone II
contained the profiles of densely filled cell bodies and dendrites.

In zone III of a DCB injection site, the background was clear of
the reaction product. Many of the cell bodies and dendrites were

densely filled with granulated HRP (Figure 3).

25

Figure 3:

26

Photomicrographs of the differential concentration
of HRP reaction product in experiment 78593.

A. Photomicrograph of a coronal section through the
HRP injection site. B. Higher magnification of an
area in the injection site indicated approximately
by the small rectangle in A. Note the differential
concentration of HRP reaction in zones I, II and
III. C and D. Higher magnification of, respectively,
zones II and III show the relative difference in the
amount of reaction product in the background of the
labeled neurons. B. Photomicrograph of a cell body
with diffused HRP. F. Photomicrograph of cell
bodies filled with granulated HRP.

27

Figure 3

 

50 um

 

10um

28

The relative size of each zone in an injection site was a
function of the postinjection survival time. Zones II and III were
relatively larger fer shorter survival times. Similar to the results
of Vanegas et al., (1978), it was Observed in these experiments that
zone 1 is relatively larger with longer survival times.

The injection site in a given experiment was larger in TMB
stained tissue than that Observed in the adjacent section stained with
DCB. In most, but not all Of the experiments, the labeling of terminals
and cell bodies in the thalamic nuclei were most extensive in TMB
stained tissue than that observed in the adjacent section stained
with DCB. The visualization of terminal labeling was enhanced by
shorter survival times.

The difficulties in accurately defining the zones which are
effective in labeling afferent and efferent processes are now well
recognized. Some investigators consider the central core to be the
only zone effective in labeling the afferent and efferent processes
in the injection site (Jones et al., 1977; Vanegas et al., 1978). In
these experiments, the relationship between labeling in the ventro-
basal Or ventroposterior inferior thalamic nuclei and zone 1 were the
most consistent indicator of the effective region of the injection

site.

Nature of Stainingp- horseradish peroxidase. Under the light microscope,
HRP labeling of cell bodies were seen as coloured particles when using
bright field or as brilliant points Of light when using dark field
illumination. Occasionally the reaction product was homogeneous
diffused throughout the cytoplasm of the cell body. It is widely
believed that only cell bodies and dendrites with a granular HRP

pattern indicate the presence of retrogradely transported HRP.

29
Diffusely filled neurons are known to be the result of injury to
the axons in the injection site (Jones et al., 1974, Vanegas et al.,
1978). The cell bodies of injured neurons may also contain granulated
HRP in a manner similar to that of physiologically labeled neurons.

The criterion fer distinguishing an injured population of labeled
cell bodies from that of a physiologically labeled population was the
presence of diffusely filled cell bodies. In zone III of the injection
site, fOci of labeled cell bodies containing a few cell bodies with
diffused reaction product and other cell bodies with granulated reaction
product. It is probably that many of the cell bodies with granulated
reaction product are the result of physiological uptake and transport.
However, the suspected presence of injured neurons whose cell bodies
contained granulated reaction product makes it impossible to determine
accurately which of the cell bodies are the result of physiologically
transported HRP and which labeled cell bodies are the result of injury.
For the purpose of this study, only those fOci of labeled neurons
which contained only cell bodies with granulated HRP were interpreted
to be the result of physiological uptake and transport and therefbre
relevant data.

Those regions of the brain which are reciprocally connected with
the site of injection produced an intricate and varied pattern of labeling.
Often, terminals and cell bodies were labeled in these sites. The inter-
pretation of terminal labeling distinguishable from soma and dendritic
labeling was particularly difficult in lightly counterstained material.

In densely labeled regions, under the light microscope, labeled terminals
were an irregular distribution Of HRP granules in the neuropil surrounding

various cell types.

3O

Nature'of‘staining‘a antOradiOgraphy. Substantial labeling of the

 

somata in the central core of the injection site is held to be
effective fer transported label to be identified at a distance. The
surrounding zone of mainly neuropil labeling is held to be ineffective
in labeling terminals of neurons of this region.

Since tritium particles travel approximately lum, the activation
Of the silver halide crystals results from radioactivity in only the
superficial 1 pm of the 40 um frozen sections.

The labeling of fibers exhibited features different from that
of labeled terminals (see figure 22). Labeled fibers are character-
ized by straight chains of silver grains whereas terminals fields
are characterized by an irregular and random distribtion of silver
grains.

Topography of intrahemispheric and commissural connections. The

 

intracortical and commissural connections of SI and SII in the raccoon
formed a complicated and varied pattern. .In the description of the
results, the location of the injection site and the distribution of
the afferent sources and the efferent target areas will be related
to the cortical maps derived using electrophysiological mapping
techniques. The maps of the raccoon's SI OWelker and Seidenstein,
1959) and SII (Herron, 1978) cortical areas are particularly useful
fer determining the topography of intrahemispheric connections.

The topography of the cell bodies of afferent neurons was
related to the Site of each injection in the following manner:
(1) intrahemispheric non-homotopic afferent neurons (INA) - the cell
bodies of afferents were in an intrahemispheric locus that receives
projections from peripheral body parts which are unrelated to the

body parts that project to the site of injection, (2) intrahemispheric

31

homotopic afferent neurons (IHA) - the cell bodies Of these afferents
were located in a cortical area that received projections from
peripheral body parts which also project to the site of the injection,
and (3) commissural afferents (CA) - the cell bodies of afferents
from the contralateral homotopic cortex. The topography of labeled
or degenerated fibers and terminals were similarly related to the
site of, respectively, injection or lesion.

Table I is a summary of the injection sites and the topographic
distribution of labeled cell bodies within SI and SII cortical region
(also see figure 4). The results of selected experiments are
described below in greater detail. Results from SII injections are
presented first, fOllowed by those of SI injections.

Afferents of the SII forepaw area. The results of two experiments will

 

be used to describe the topography of the cell bodies of INA and IHA
that resulted from injections in the SII forepaw region. In experiment
78500, a combined injection of HRP and tritiated leucine and proline
was made in an area that yielded a high amplitude evoked potential
after manual stimulation of the contralateral middle digits of the
forepaw. The diffusion of the reaction product from the injection site
was approximately 2 mm in diameter.

The cell bodies of a large number of INA were labeled as a result
of this injection. In transverse sections, caudal to the injection
site on the inferior bank of the suprasylvian sulcus, labeled cell
bodies were organized into distinct clusters. Figure 5 is a recon-
struction of a series of transverse sections through the region of
labeled cell bodies and shows that the clusters were part of three
rostrocaudally oriented strips of labeled cell bodies. The strips
of labeled cells were separated by gaps of fairly constant width where
few or no cell bodies were labeled. The labeled cell bodies were

localized in the hindpaw and trunk region of the somatotopically

32

Table 1. Summary of the experiments and results of this study

 

 

 

 

 

 

Animal # HRP Survival

Injection site time INA/E IHA/E . CA/E
77606 3rd 6 4th digit 24 hrs. X X

SI ferepaw
77604 4th digit 24 hrs. X X

SI forepaw
77574 4th digit 36 hrs. X

SI forepaw
77597 SI fbrepaw 30 hrs. X
77559 SI hindpaw 30 hrs. X X
78565 SI hindpaw 30 hrs. X X
77563 SI hindpaw 24 hrs. X
78584 SII forepaw 24 hrs. X
78593 SII hindpaw 45 hrs. X X X
78516 SII hindpaw 39 hrs. X X
78511 SII ferepaw

8 hindpaw
Animal # TAA Survival

Injection site time INE IHE CE
77561 SI hindpaw 40 hrs X
78586 SI trunk 48 hrs X

G hindlimb
Animal # Lesion site Survival INE IHE CE

' time

77608 Gyral crown of 48 hrs. X

4th digit area

SI

77609 SI hindpaw 48 hrs. x

33

Table 1 (contd.)

 

 

Animal # HRP/TAA Survival
Injection site time INA/E IHA/E CA/E
78500 SII forepaw 40 hrs. INA X
78508 SI hindpaw 64 hrs. INA X CA
Abbreviations: CA - Commissural afferents
CA/E - Commissural afferents or efferents
CE - Commissural efferents
IHA/E - Intrahemispheric homotopic afferents or efferents
IHA - Intrahemispheric homotopic efferents
INA - Intrahemispheric nonhomotopic afferents

INA/E

Intrahemispheric nonhomotopic afferents or
efferents
INE - Intrahemispheric nonhomotopic efferents

Figure 4:

34

Schematic diagram of the injection sites listed
in table 1. A. The SI and SII cortical regions
are shown on the cerebral hemispheres with all
the sulci removed except those in SI and SII to
emphasize the relationship of SI and SII. The
stippled areas in SI and SII indicate the
granular cortices and the darkened areas indicate
the agranular areas of SI and SII.

B. Diagram of the injection sites in the granular
and agranular cortices of SI and SII. Many of the
injections covered the same area in the fbrepaw,
hindlimb and trunk representation areas of SI

and SII.

35

   

Figure 4

7756! -{3’3’221 775 63
. xxx

 

 

36

of cell bodies with granulated reaction product suggested physio-
logical uptake and retrograde transport by this focus of neurons.

The strips of labeled cell bodies consisted of both pyramidal
and non-pyramidal shaped neurons. HRP positive cell bodies were
in all layers of the cortex except layer I. The bulk of the HRP
positive cell bodies were in layers II, III, IV and V. Fewer
labeled cell bodies were observed in layer VI.

The cell bodies of IHA in SI were also labeled as a result of
experiment 78500. In transverse sections, the labeled cell bodies
were organized into clusters in the sulcal cortex of the 2nd, 3rd and
4th digital representation areas (figure 6 and 7). Each fucus of
labeled cell bodies fermed a rostrocaudally oriented strip which
began in the anteriormost region of SI and extended caudally fer l
to 2 mm. Occasionally, HRP positive cell bodies were fbund in the
cortex of the gyral crown.

In experiment 78500 the terminals of intrahemispheric homotopic
efferent neurons in the SII forepaw area were demonstrated in auto-
radiographic processed sections that were adjacent to the HRP
sections. Silver grains were observed above fibers and terminals in
the 2nd, 3rd and 4th digital representation areas of the SI fbrepaw
area. In transverse sections, the silver grains above terminals were
distributed in patches. The topography of the patches was the same
or very similar to the topography of clusters of labeled cell bodies
Observed in the HRP stained tissue.

In experiment 78584, a smaller injection of HRP was made in a zone
of SII which yielded a high amplitude evoked response after manual
stimulation of the second digit. Labeled cell bodies of IHA were
fbund in the 2nd digital representation area of SI. A reconstruction
of the tracing of a series of transverse sections shows that the

labeled cell bodies form rostrocaudal oriented strips in the medial and

37

mwmceo mu

aro memeevaHwoe om Exp chowoa ooHH oomwom we «do sweavwz eoeeomoeewewoe weow om mHH moHHozwam w:
wagonnwos we dam moeoewz weow om mHH w: oxvoewaode ummoo. >. moroawewo mwwmewa om ewo ooeoceww
:oawmrroeom awe: wHH ero mcHOw wen meew eoao<om oxnove dramo we mH no oawrwmwuo «so eonewoemrww

om mH wen mHH.1 ero awewodoa weow we ewo moeovwz eomwoe om mHH waawowdom duo wemoonwo= mweo wen ”so
aoem wemwoweo ero wveeOXwaweo memeewdcdwos om ”so chou a noHH dogwom w: mHH. w. > eewowam om «so
Home noeoceww roawmwwoeo om w :mewsnwem: yew»: awe: ”so woveoxwaweo Hoowewozm om nro new=m<oemo
mooewoam eoooemeecoeom w: n. n. > moewom om new=m<oemo mooewosm «reocmr duo eomwo: om Hwoowom

ooHH comwom w: mHH :wemvwz eomwOB. ero monm eoveomose ero woveoxwaweo modmwee om Hwoowom ooHH comwom
w: ewo moonwoem. moonwo: H wm w eewdm<oemo mooewo: ereocmr ero wsuoonwo: mweo. aro awexodoa

weow wdmwnwdom duo noeeeww noeo om ero wemooewos mweo. ero mrwmoa weow wuawoweom duo mwmmcmwo: om
«so eownewos weomaoe weocsm ewo nonmeww noeo om ero wsuooewos mweo. mooewo= N em w newdm<oemo mooewoq
ereocmr duo domwobwsm om w moocm om deowom noHH eoawom w: nro :wdmvwz eomwos om mHH wan ereocm: nro
weow om wawaca vaowwom om ooHH dogwom w: ero <odeewH vomeoewoe wsmoewoe scoHocm om ewo erwpwacm.
m<vHv. wdmwoweom erwe ero wowooewoe two we mHH won wen we mm mesoo so kuoH zwm ovmoe<om w: owem
oxeoesw wen uwem weocwew om duo erwwwewn <o=eeocwme ooawHox m<ov Amoee05. Howey. >n wxwww come
eoveomoaewewoe weow om mH" N. u won a” men. men won an: mwmwe eoveomodnwewos weowm om me m"

mwoo eoweomosnwewo= weow om mH.

38

 

9 1mm

Figure 6:

39

The distribution of HRP labeled cell bodies in the forepaw
region of SI following an injection in the ferepaw region
of SII A. Schematic diagram Of the cerebral hemispheres
with all the sulci and gyri removed except those in SI to
emphasize the relative situation of SI and SII. The
darkened arrow indicates the injection site and the locat-
ion of labeled cell bodies in SI. B. A tracing of the left
cerebral hemisphere of a "standard" brain with the
approximate locations of the transverse sections through
the region of labeled cell bodies in SI fOrepaw region.

The dots represent the approximate density of labeled cell
bodies in the sections. The darkened area indicates the
central core of the injection site. The Shaded region
surrounding the darkened area indicates the diffusion of
the reaction product around the central core in the
injection site. Section 11 is through the largest extent
of the injection site and section 12 is through the area
of maximum labeling of cell bodies in VPI (Herron, 1979).
Note that the locations of foci of labeled cell bodies

are more related to cortex in sulci than that of gyral crowns.
l, 2, 3, and 4: representation areas of digits 1, 2, 3,
and 4: representation areas of digits 1, 2, 3 and 4;

H: hindlimb; MI: primary motor cortex; Vb: pars externa of
the thalamic ventrobasal complex.

40

Figure 6

Exp 78500

 

 

 

Figure 7:

41

Photomicrograph of the cell bodies of origin of the SI
to SII projection. A. Low magnification photomicro-
graph of the clusters of HRP labeled cell bodies
observed in experiment 78500 (5X). B. Higher magnific-
ation of the cluster of labeled cell bodies in the
dorsal part of A (50X) taken from a transverse section
at the level of section 1 in figure 4.

Figure 7

42

 

 

 

43

lateral walls of the second digital representation area (figure 8).
The topography of the two rostrocaudal strips Of labeled cell
bodies on the medial and lateral wall of the gryal crown was
similar to those resulting from a larger injection in the SII fere-
paw area. The contralateral homotypic cortex was searched thoroughly
for HRP positive cell bodies but none were fOund.

Typically, the HRP positive cell bodies were pyramidal shaped
neurons in which the somata and the proximal and basal dendrites
were labeled. The cell bodies of INA were primarily confined to
layers II and III. The labeled cell bodies were among the largest
observed in layers II and III of the fOrepaw area of SI. A light con-
centration of labeled cell bodies was sprinkled throughout the layers

IV, V, and VI.

The intrahemispheric and commissural afferents of the SII hindpaw

 

and trunk region. In experiment 78593, an injection of HRP was made

 

in the electrophysiologically identified hindpaw and trunk region Of
SII. The cell bodies of INA, IHA and CA neurons were labeled as a
result of this injection.

Figure 9 is a reconstruction Of a series Of transverse sections
through the regions which contain the labeled cell bodies of INA
neurons. In a series of transverse sections anterior to the injection
site (sections 1-5 in figure 9), two loosely organized strips of labeled
cell bodies were observed in the cortical region surrounding the depth
of the suprasylvian sulcus. This cortical area corresponds to
boundary region between the face regions of SI and SII. In the same
series of transverse sections, a third and shorter rostrocaudally
oriented strip of labeled cell bodies of INA were observed in the SII

forepaw region (Section 4 in figure 9).

Figure 8:

44

The distribution of HRP labeled cell bodies of IHA
fellowing an injection in the 2nd digit represent-
ation area of SII in experiment 78584. A. Schematic
diagram of the cerebral hemispheres with all the

sulci and gyri removed except those in SI to emphasize
the relationship of SI and SII. The darkened arrow
indicates the locations of the injection site and the
region of labeled cell bodies. B. A tracing of the
left cerebral hemisphere of a "standard" brain with
the approximate locations of the transverse sections
reconstructed in C. C. A series of transverse sections
through the region of labeled cell bodies in the 2nd
digit representation of SI. The dots represent the
approximate density of labeled cell bodies in the
sections. The darkened area indicates the central
core of the injection site. The shaded region
surrounding the darkened area indicates the diffusion

‘of the reaction product around the central core of the

injection site. Section 5 is through the largest

extent of the injection Site and section 6 is through

the area of maximum labeling of cell bodies and terminals
in VPI. Note that the location of foci of labeled cell
bodies in SI are more related to sulcal cortex than that
of the gyral crown. l, 2, 3 and 4: representation areas
of digits 1, 2, 3, and 4; H: Hindlimb; MI: primary
motor cortex; Vb: pars externa of the thalamic ventro-
basal complex.

45

Figure 8

Exp. 78584

 

 

 

 

Figure 9:

46

The distribution of HRP labeled cell bodie511f INA in SI and
SII following an injection in the hindlimb and trunk
regions of SII in experiment 78593. A. Schematic

diagram of the cerebral hemispheres with all the sulci

and gyri removed except those in SI to emphasize the
relationship of SI and SII. The darkened area in the
hindlimb and trunk region of SII indicates the injection
Site and the dots indicate the approximate distribution

of labeled cell bodies in SI and SII. B. A tracing of

the left cerebral hemisphere of a "standard" brain

with the approximate locations of the transverse sections
reconstructed in C. C. A series of transverse sections
through the region of labeled cell bodies in SI and SII.
The dots represent the approximate density of labeled

cell bodies in the sections. The darkened area indicates
the central core of the injection Site. The Shaded region
surrounding the darkened area indicates the diffusion of
the reaction product around the central core. Section 9
is a transverse section through both the injection site
and the area of maximum labeling of cell bodies and
terminals in VPI. Note that the locations of the labeled
cell bodies are nonhomotopic to that of the injection
site. Two foci of labeled cell bodies are observed. One
focus is localized in the junctional region between SI and
SII. Section 4 contains labeled cell bodies in SII. A
second focus of labeled cell bodies occupies the occiput
representation area of SI.

 

47

48

The bulk of the labeled cell bodies in this focus of labeled
neurons were in layers II, III and V. Many labeled cell bodies were
also observed in layers IV and VI.

A second focus of labeled cell bodies of INA were observed in
a region posterior to the first fOcus and medial to the injection
site. The labeled cell bodies were distributed on the superior bank
of the suprasylvian sulcus (sections 6-9 of figure 59). This cortex
corresponds to the shoulder and occiput representation areas in SI.
The fOci of labeled cell bodies were well outside the zone of diffusion
and all the labeled cell bodies were labeled in a granulated pattern;
therefore, the labeled cell bodies are interpreted to be the result of
physiological uptake by the terminals and retrograde transport by the
axons of the labeled neurons.

The posterior strip of labeled cell bodies Of INA was highly
laminated. Labeled cell bodies were confined almost exclusively to
layers II, III and V. Occasionally, small bridges of labeled cell
bodies were observed in layer IV between those in layers III and V
(section 7 of figure 9).

In experiment 78593, the cell bodies of IHA were found in a
region of SI which corresponds to the trunk and hindlimb regions. Figure
10 is a reconstruction of transverse sections through the region of
labeled cell bodies of IHA in SI and shows that the HRP positive cell
bodies are organized into rostrocaudally oriented strips. Similar
to the topography of the strips of labeled cell bodies observed in SI
forepaw region fbllowing an injection in the furepaw region of SII,
the strips of labeled cell bodies were located in the sulcal cortex

(figure 10).

49

.mwmceo Ho"

awo newnewocewoe om awe deowom ooHH comwom om Hm> we nro wvmwpweoeww rwemywso wen necex eomwoem
om mH moHHozwem w: wagondwoe wo «wo swampwao wan necew eomwosm om mHH w: oxvoewsoen ummom. ,
>. moroawewn mwwmewa om ero ooeoceww woawmwwoeom awe: wHH ero mcHow wen «we» eoao<oa oxoowe exemo
we mH no oavwwmwuo ewo eowwewonmwww om mH won mHH. ero weeoz waawoweom ero wagonewon mwno wow
«so Honwewoo om kuowom ooHH vomwom. w. > eewowem om ero Home ooeodeww :oawmvsoeo om w
:mewsawem: cewwe awe: ewo wereoxwaweo Hoowewoem om ero eewbm<oemo mooewo=m eoooemeeconom w: n.
n. > moewom om newem<oemo mooewosm areocmw ero eomwo: om vaowom ooHH vomwom we mH. Ado mono
eoweomose ero wvweoXWBweo mosmwew om Hweowom ooHH comwom w: ero monew05m. ero mwewoeom weow
wsmwoweom ero nosnewH noeo om ero wagooewoe mweo. aro mswaom eomwos meeeocbawdm nro mwewooom
weow wdawoweom ero mwmmmeoa om ero eowoewoe reagenn weocsm ero ooueewp ooeo. moonwos m wm w
monewos ”recon: dear nro wouooewo: mweo wen ero weow om Bwaaca chouwsm om nowu vomwom w: <vH.
zoeo nrwn ero meewp neozdm weo meoo om vaowom ooHH comwom. m” reamwwao eoveomodewewos weow“
a" eecbw eooeomodewnwos weow“ <d" wwem oxeoezw om «So <o=neocwme nosrwox" wan <vH" <o=eewH
demeoewoe wsmoewoe scopocm om ero erwuwacm.

SO

mwmceo Ho

 

 

51

The cell bodies of IHA were concentrated primarily in the
middle layers. In some instances, labeled cell bodies of IHA were
found only in layers III and V.

In experiment 78593, the cell bodies of CA were observed in
the contralateral homotopic cortices of SI and SII. In the contra-
lateral SII region, the strips of labeled cell bodies surrounded a
small cortical region which was free of labeled cell bodies. The
island of cortex free of labeled cell bodies contained a marked
increase in stellate shaped cell bodies and a lesser concentration of
pyramidal shaped cell bodies than that of the cortex which contained
labeled cell bodies. The island that was free of labeled cell
bodies corresponds to the hindpaw region of SII.

The density of labeled cell bodies of CA in SI were light compared
to the density of labeled cell bodies of CA in SII. Figure 11 is a
reconstruction of a series of transverse sections through the region
of labeled cell bodies in SI and SII. It shows that the HRP positive
cell bodies in SI and SII are loosely organized into rostrocaudally
oriented strips.

The labeled cell bodies of commissurally projecting neurons were
found in all layers except layer 1. Most of the HRP positive cell
bodies were found in layers II, III and V. Fewer labeled cell bodies
were fOund in layer IV.

Measurements were made of various parameters of the clusters of
labeled cell bodies in experiment 78593 to better understand the
organization of the diverse afferent sources. Measurements were made
of the diameter of clusters and intercluster distances in order to
determine if the spatial relationships of clusters in one functional
region were consistent with those in another functional region. These

results showed no consistent relationships between clusters in one

Figure 11:

52

The distribution of HRP labeled cell bodies in the
contralateral SI and SII region following an injection

in the hindlimb and trunk regions of SIIin experiment

78593. A. Schematic diagram of the cerebral hemisphere

with all the sulci and gyri removed except those in SI to
emphasize the relationship of SI and SII. The darkened area
in the hindlimb and trunk regions of SII indicates the
injection site and the arrows indicate the region of labeled
cell bodies in the contralateral hindlimb and trunk regions
of a "standard" brain with the approximate locations of the
transverse sections reconstructed in C. C. A series of
transverse sections through the region of labeled cell bodies
in SI and SII. The dots represent the approximate density of
the labeled cell bodies in the sections. In section 5, the
darkened area indicates the central core of the injection site
and the shaded area indicates the diffusion of the reaction
product around the central core. Section 5 is also through the
area of maximum labeling of cell bodies in VPI. Note the
distribution of labeling of cell bodies in section 3 in the
contralateral SII and the axial and trunk representation areas
in SI. A: axial body representation area; T: trunk represent-
ation area; VPI: ventral posterior inferior nucleus; and Vb:
pars externa of the ventrobasal complex.

53

Figure 11

 

54

functional region or between clusters in different functional regions.

The diameter of the clusters of labeled cell bodies of INA in the
boundary region between SI and SII ranged between 200 to 700 um. The
cell bodies of INA afferents in the hindlimb and trunk regions of SI
were slightly larger (300-800 um).

The intercluster distances varied widely within each functional
region. Clusters were closer together in SII than they were in SI. In
SI, as seen in transverse sections, the intercluster distances ranged
between 70 to 1000 um. Generally in SI, the clusters were in the sulcal
cortex of adjacent sulci and, therefOre, the intercluster distances
were determined by the width of the gyral crown. The intercluster
distances of labeled cell bodies in SI were typically around 1000 um.
In the loosely organized clusters of labeled cell bodies of CA in the
SII hindlimb and trunk regions, the diameter of clusters were generally
larger (500 um - 1000 um) than the clusters in the ipsilateral cortex
but the intercluster distances were shorter (60 - 200 um).

In experiment 78511, a large injection of HRP was made in the
SII region. The reaction product in the injection sites covered much
Of the somatotopically organized region of SII. In contrast to the
lresults of other injections in SII, labeled cell bodies in IHA were
found in the cortex of the gyral crown of hindlimb representation
area of SI. A thin layer of HRP positive pyramidal shaped cell bodies
in layer V were distributed between two clusters of labeled cell bodies
in the sulcal cortices (figure 12). The labeled cell bodies were among

the largest in the SI hindlimb and trunk region.

Figure 12:

55

Labeled cell bodies Of the SII hindlimb to SI hindlimb
projection. A. Low magnification of labeled cell bodies
in SI hindlimb regions following an injection in the

SII hindlimb region (50X). Higher magnification of
pyramidal neurons in layer V of photomicrograph A
(250X).

56

Figure 12

    

 

 

 

 

 

 

 

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Figure 12:

55

Labeled cell bodies of the SII hindlimb to SI hindlimb
projection. A. Low magnification of labeled cell bodies
in SI hindlimb regions fbllowing an injection in the

SII hindlimb region (50X). Higher magnification of
pyramidal neurons in layer V of photomicrograph A

(250X).

56

Figure 12

 

 

 

S7

The intrahemiSPheric afferents of the SI forepaw region. Experiment

 

77606 exemplified the intrahemispheric afferents of the 3rd and 4th
digit projection areas in SI. Two small injections were made in
these digit representation areas to determine if corresponding pairs
of fOci of labeled cell bodies of intrahemispheric afferents would
be produced. One injection was in the anterior gyral crown of digit
3 representation and a slightly smaller injection was posterior to
the first injection in the gyral crown of digit 4 representation area.
Small foci of labeled cell bodies were observed in the 3rd and 4th
digital representation areas of Vb.

Two fOci of labeled cell bodies of IHA were feund in the SII
region. One focus of labeled cell bodies were located medial and
posterior to the other fOcus on the inferior bank of the suprasylvian
sulcus. The fOcus of labeled cell bodies were in a region which
corresponds to the 3rd digit representation area (figure 13). The
second fOcus of labeled cell bodies was anterolateral to those of the
first fOcus and corresponds to a more proximal representation of the
4th digit. The area between the two foci of labeled cell bodies was
largely free of HRP positive cell bodies. The distance between the
foci of labeled cell bodies was approximately the same as that of
the injection sites. The cell bodies of IHA in SII were located in
all layers except layer I. The largest percentage of labeled cell
bodies was fOund in layer III and the majority of the remainder were
feund in layer V.

The cell bodies of INA were located in the adjacent digital and
proximal volar surface representation areas in SI. Figure 14 is a
reconstruction of a series of transverse sections through the region

of the labeled cell bodies of INA observed in the experiment 77606.

Figure 13:

58

The distribution of HRP labeled cell bodies in the fore—
paw region of SII fOllowing an injection in the 3rd

and 4th digital representation areas of SI. A. Schematic
diagram of the cerebral hemispheres with all the sulci

and gyri removed except those in SI to emphasize the
relationship of SI and SII. The two arrows indicate the
injection sites and the locations of the labeled cell
bodies in SII. B. A tracing of the left cerebral
hemisphere of a "standard" brain with the approximate
locations of the transverse sections reconstructed in C.
C. A series of transverse sections through the region of
labeled cell bodies in the SII fOrepaw region. The dots
represent the approximate density of labeled cell bodies
in the sections. The darkened area indicates the central
core of the injection site. The Shaded region surrounding
the darkened area indicates the diffusion of the reaction
product around the central core of the injection site.
Section 12 is through the area of maximum labeling of cell
bodies in Vb. Note the two fOci of labeled cell bodies

in SII that correspond to the two sites of HRP injections.
1, 2, 3, 4 and 5: the digital representation areas of SI;
H: hindlimb representation area, P: palm representation
area; F: face representation area; Vb: pars externa of
thalamic ventrobasal complex; VPI: ventral posterior inferior
nucleus of the thalamus.

59

Figure 13

 

Figure 14:

60

The distribution of HRP labeled cell bodies in SI following
injections in the 3rd and 4th digit representation areas
of SI in experiment 77606. A. Schematic diagram of the
cerebral hemispheres with all the sulci and gyri removed
except those in 81 to emphasize the relationship of SI

and SII. B. A tracing of the left cerebral hemisphere of
a "standard" brain with the approximate locations of the
transverse sections reconstructed in C. C. A series of
transverse sections through the injection sites and the
area of labeled cell bodies in S1. The dots represent the
approximate density of labeled cell bodies in the sections.
The darkened area indicates the central core of the
injection site. The shaded region surrounding the darken—
ed areas indicate the diffusion of the reaction product
around the central core. Section 6 shows the two foci of
labeled cell bodies in Vb. Note the labeled cell bodies
posterior to the injection site in the proximal volar
representation area of digit 3 in SI.

61

Figure 14

 

62
The topography of the labeled cell bodies are more related to
sulcal cortex than with the cortex of the gyral crown.

The labeled cell bodies of INA were limited almost entirely
to the supragranular layers. Must of the HRP positive cell
bodies were pyramidal shaped.

No HRP positive cell bodies were found in the homotopic or
heterotopic areas of the contralateral SI cortex despite thorough

searches.

Intrahemispheric distribution of terminals from the SI forepaw

 

regign, The terminals of intrahemispheric homotopic efferents (IHE)
were indicated by the results of experiment 77604. A short post-
injection survival time (20 hrs.) enhanced the visualization of
terminals. The injection covered the representation areas of palm
and proximal region of the 5th digit in the SI forepaw region. The
terminals were located in the SII region on the inferior bank of the
suprasylvian sulcus. The terminals were distributed over layers 11,
III, IV and V (figure 15).

In experiment 77608, the distribution of terminals of neurons
in the 4th digit representation of SI area was determined by using
anterograde degeneration technique. Following a small ablation (3mm
in diameter) of the gyral cortex in the 4th digit representation area
of SI, degenerated fibers and terminals were homogenously distributed
in layers II, III, IV and o\FII’ngigure 16). In contrast to the organiz-
ation of cell bodies of IHA, no patches of degenerated fibers or term-
inals were observed. The medial-lateral width of the SII area which
contained degenerated fibers and terminals was larger than that

typically occupied by labeled cell bodies fOllowing injection of

HRP in the SI digital representation area.

63

mwmceo Hm"

 

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noeodewu :oawmuroeom awn: wHH nro mcwow won ween eoao<om oxoorn nwomo w: mH no oarrwmwno nro
eonnnoomrww om mH woo mHH. aro mwewosom weow won weeoz weowowno nro wagonnwos mwno woo nro
newnewecnwoo om noeawowum we mHH. w. > newowom om nro Homn ooeodeww woawmvwoeo on w
:mnwoawem: dew»: awn: nro wwueoxwawno Honwnwoom om nro newom<oemo moonwoom nweocm: nro eomwo:
om vaopom noeawowpm we nro wwmwwwnoewp mHH eomwos. n. aew=m<oemo moonwoom nreocmw nro
womoonwoo mwno mmoonwoe Hg wow nwo eomwoo om Hweopom noeawowwm w: nro wwmwpwnoeww mHH.

moonwo: N noonwwom nvo weow om Swansea deowwom om noeawowpm we <w. 2ono nrwn nro noeswowpm
weo mwmnewocnom w: nro sweawo Hweoem om mHH.

65

mwmceo Ho”

duo mwmnewucnwoo om aowosoewnom awooem won noeawowwm w: nro wvmwuwnoeww mHH eomwo: mouwozwom
w: wvanwoo om nwo meeww oeoze om nro mn: mwmwnwu eoveomoenwnwoo weow we mm w: oxvoewaoon
uqaom. >. mowoawnwo mwwmews om nro noeodewp :oawmvwoeom awn: wHH nvo mcwow eo5o<om oxooen
nromo w: mH no oawrwmwuo nro eonnwoomrww om mH woo mHH. w. > newowem om nwo Homn noeoceww
woawmwroeo om w :mnwsmwea: cewn: awn: nro woveoxwawno Hoownwoem om nro new=m<oemo moonwoem
nreocmr nro eomwo= om aomosoewnom mwooem won noeawowpm eonoomneconoa w: n. n. > moewom om
newom<oemo moonwoom nreocm: nro eomwo: om momoooewnom mwcoem who noeswswwm w: nwo wvmwwwnoeww
mHH ooenwoww eomwoo. ewo mono eoveomoon nro wvweoxwawno moomwne om nwo aomodoewnom mwvoem
woo noeawswwm ovmoe<oa we nwo wwmnopomwoww moonwoeu. zono nswn nwo Bomwwwuuwnoeww swan:

om nro moocm om momosoewnoa mwooem won noeawdwpm weo 5:07 meownoe nrwb nro somwwunpwnoewa
swan: om mnewwm om chopoo noun coawom moHHonom w: nomoonwo: om mar we nro moeowwz weow om
mH.

67

Intrahemispheric and commissural afferents of SI agranular area.

 

In experiment 78565, a 1 ul injection of HRP was made in an area

that yielded a high amplitude evoked potential after manual stimulat-
ion of the contralateral upper hindlimb. The effective zone of the
injection site, as determined by labeled cell bodies and terminals in
Vb, covered the distal limb and trunk representation areas.

The cell bodies of IHA were found in the hindlimb and trunk
region of SII. Figure 17 is a reconstruction of a series of transverse
sections through the region of labeled cell bodies in the SII region.
These sections showed a loosely organized rostrocaudal oriented strip
of labeled cell bodies. Occasionally, the labeled cell bodies were
subdivided into 2 or 3 discrete clusters.

In experiment 78508, an injection of HRP was made in the trunk
and leg region of SI. The distribution of labeled terminals and
cell bodies in Vb indicated that the central core of the injection
site covered the leg and trunk region (Figure 18). Similar to the
organization of cell bodies in SII fellowing the injection in the
upper leg in experiment 77565, the labeled cell bodies in SII of IHA
farmed one fairly large strip of cell bodies. The strip of labeled
cell bodies on the inferior bank of the suprasylvan sulcus in this
experiment was slightly anteromedial to the strip of labeled cell
bodies resulting from an injection in the hindlimb area of SI in
experiment 77565. I

The cell bodies of IHA were distributed in layers II, III, IV
and V. Typically, the cell bodies were evenly distributed in these
layers. Occasionally, the labeled neurons were only in the supra-

granular layers.

Figure 17:

68

The distribution of HRP labeled cell bodies of IHA in

the ipsilateral SII following an injection in the hind-

limb and trunk region of SI in experiment 78565.

A. Schematic diagram of the cerebral hemispheres with all

the sulci and gyri removed except those in SI to emphasize
the relationship of SI and SII. B. A tracing of the left
cerebral hemisphere of a "standard" brain with the approximate
locations of the transverse sections reconstructed in C.

C. A series of transverse sections through the region of
labeled cell bodies in the hindlimb and trunk region of the
ipsilateral SII region. The dots represent the approximate
density of labeled cell bodies in the sections. The darkened
area indicates the central core of the injection site. The
shaded region surrounding the darkened area indicates the
diffusion of the reaction product around the central core in
the injection site. Section 1 is through the area of maximum
labeling of cell bodies and terminals in Vb. Note that most
of the labeled cell bodies in SII are in layers III and V.

In section 3, the labeled cell bodies in SII form 3 distinct
clusters.

69‘

Figure 17

 

Exn 78565 E3

  

Figure 18:

70

The distribution of labeled cell bodies in the hindlimb
and trunk region of SII following an injection in the
hindlimb and trunk region of SI in experiment 78508.
A. Schematic diagram of the cerebral hemispheres with all
the sulci removed except those in SI to emphasize the
relationship of SI and SII. B. A tracing of the left
cerebral hemisphere of a "standard" brain with the approx-
imate locations of the transverse sections reconstructed
in C. C. A series of transverse sections through the
region of labeled cell bodies in the ipsilateral SII region.
The dots represent the approximate density of labeled cell
bodies in the sections. The darkened area indicates the
central core of the injection site. The shaded region
surrounding the darkened area indicate the diffusion of the
reaction product around the central core. Section 1 is a
transverse section through both the injection site and the
area of maximum labeling of cell bodies and terminals in Vb.
Note the formation of the labeled cell bodies in the
ipsilateral SII hindlimb and trunk region into a rostrocaudal
oriented strip. Vb: pars externa of ventrobasal complex; and
VPI: ventral posterior inferior nucleus of the thalamus.

71

18

Figure

 

 

8
nu
5
8
v:
p
x
E

 

72

In experiment 77559, multiple small injections (.025 total
amount injected) were made in a stepped vertical penetration
through a region of cortex responsive to manual stimulation of the
trunk. The central core of the injection site was less than 1 mm
in diameter in all the cortical layers.

The injection labeled a discrete group of cell bodies in the
trunk representation area of Vb. Labeled fibers exited below the
injection site where some entered the internal capsule, some were
observed in the corpus callosum, and others were directed laterally
(Figure 19). Despite a thorough search, no labeled cell bodies were
observed in the ipsilateral SII region.

In transverse sections, the labeled cell bodies of CA were
distributed in the contralateral homotopic cortex over a 3 mm area
(Figure 20). The diameter of the fOcus of labeled cell bodies was
relatively larger than that of the injection site. These data
suggest that the cortex in the trunk region receives commissural
connections but does not receive intrahemispheric connections. In
addition, the terminals of commissural neurons are convergent in
the contralateral homotopic cortex.

Larger injections of HRP in the upper limb and trunk represent-
ation areas of experiment 77565 resulted in the labeling of two
distinct fOci of cell bodies in the contralateral homotopic cortex.
Figure 21 is a reconstruction of a series of transverse sections through
the region of labeled cell bodies. It shows strips of labeled cell
bodies distributed primarily in the sulcal cortex. The diamter
of each focus of labeled cell bodies was 500 to 1000 um wide. The

two strips of labeled cell bodies were occasionally joined by a thin

73

 

t
te.

mu
mn
r0
8.1
mt
C
86
..J
nn
.1.1
86
th
.It
5
nm
01
.um
C
es
..Jr
me
im
Pf
ma
8
81
an
8
f1
08
hh
t
e
t
0
N

omicrograp

Phot
77559.

Figure 19

Figure 20:

74

The distribution of HRP labeled cell bodies in the contra-
lateral homotopic cortex following an injection in the
trunk region of SI in experiment 77559. A. Schematic
diagram of the cerebral hemispheres with all the sulci and
gyri removed except those in SI to emphasize the relation—
ship of SI and SII. The arrow in A indicates the injection
site and the location of labeled cell bodies. B. A tracing
of the left cerebral hemisphere of a "standard" brain with
the approximate locations of the transverse sections recon-
structed in C. C. A series of transverse sections through
the region of labeled cell bodies in the contralateral
homotopic SI cortex. The dots represent the approximate
density of labeled cell bodies in the sections. The darkened
area indicates the central core of the injection site. The
shaded region surrounding the darkened area indicates the
diffusion of the reaction product around the central core.
Section 5 is through the area of maximum labeling of cell
bodies in Vb. Note that the distribution of labeled cell
bodies in the contralateral cortex is spread over an area
much greater than that of the injection Site. T, trunk
representation area, S, shoulder representation area.

Vb: pars externa of the ventrobasal complex; and VPI: ventral
posterior inferior nucleus of the thalamus-

75

Figure 20

 

Exp. 77559

 

I {a} 5

Figure 21:

76

The distribution of HRP labeled cell bodies of CA in the
hindpaw and trunk region of SI following an injection in

the contralateral SI hindpaw and trunk regions.

A. Schematic diagram of the cerebral hemispheres with all

the sulci and gyri removed except those in S1 to emphasize
the relationship of SI and SII. The darkened arrow indicates
the injection site and the location of the labeled cell bodies
of CA. B. A tracing of the left cerebral hemisphere of a
"standard" brain with the approximate locations of the trans-
verse sections reconstructed in C. C. A series of transverse
sections through the region of labeled cell bodies of CA in
the hindpaw and trunk regions. The dots represent the
approximate density of labeled cell bodies in the sections.
The darkened area indicates the central core of the injection
site.. The shaded region surrounding the darkened area
indicates the diffusion of the reaction product around the
central core in the injection site. Section 11 is also
through the region of maximum labeling of cell bodies in Vb.
Note the rostrocaudal oriented strips of labeled cell bodies.
In section 3, a thin lamina of labeled cell bodies connects
the two clusters of labeled cell bodies. H: hindlimb repres-
entation area; T: trunk representation area; Vb: pars externa
of the ventrobasal complex; and VPI: ventral posterior
inferior nucleus of the thalamus.

77

Figure 21

 

Exp 78565

\V
\ \r L.
‘P‘
I jhre.
7 .—)~/

 

 

 

 

 

 

 

 

 

78

layer of labeled cell bodies in layer V.

In experiments 77565 and 78508, the density of labeled cell
bodies of CA was comparable to that INA and IHA. The majority of
the labeled neurons had pyramidal shaped cell bodies. The laminar
organization of cell bodies of CA were distributed primarily in

layers II, III and V.

IntracOrtical and commissural efferents of SI agranular certex.

 

In experiment 77586, tritiated leucine and proline was injected

in the middle of a zone responsive to manual stimulation of the
trunk. A very dense concentration of grains was Observed above
fibers and terminals in the trunk and upper leg representation areas
of the Vb nucleus in the thalamus.

Silver grains characteristic of fibers and terminals were
observed in the ipsilateral SII cortex on the inferior bank of the
suprasylvan sulcus. The grains were distributed in patterns
characteristic of fibers above the white matter and sixth layer of
the cortex. A random distribution of Silver grains indicative of
terminals was observed in layers V, IV, III and II. The heaviest
concentration of grains was above terminals in layers V, III, and
II (figure 22 and 23).

A dense concentration of grains was observed above fibers in the
corpus callosum. No grain patterns characteristic of terminals were

observed in the contralateral SI homotopic cortex.

Summary of Results. The results of this series of experiments can be

 

summarized by the observation that the intrahemispheric and commissural
connections fall into three categories. These categories are:

(a) intrahemispheric homotopic connections (IHA), (b) intrahemispheric

Figure 22:

79

Distribution of fibers and terminals originating from
SI trunk region. A. Darkfield photomicrograph of
silver grains above fibers which exited below the
injection site. Note that the fibers exited below the
injection site in two main bundles in which some of
the fibers are directed laterally (left in the photo-
micrograph) and some of the fibers are directed medially
toward the corpus callosum. B. Darkfield photomicro-
graph of straight chaiHSof.silver grains that are
indicative of fibers in the corpus callosum. C. Dark-
field photomicrograph of a patch of irregular
arrangement of silvergrains that are indicative of
terminals in the ipsilateral SII cortical region.

80

Figure 22

 

81

mwmweo mm“

ado mwmnewvcnwoo om mewwom woo<o mwaoem who noeawowwm w: nro wvmwuwnoewp mHH ooenwoww eomwoo
moHHozwom w: wagoonwos om newnwwnoa Hocowoo woo weonoo we nwo necew eomwoo mm.

>. moroawnwo awwmews om nro.ooeocewH roawmwwoeom zwnw wHH nro mcwow eoso<oa oxoown nromo

w: mH no oarrwmwuo nwo eonnwoomrwe om mH weo mHH. w. > newnwdm om nwo Homn ooeovoeww roawm-
wroeo om w :mnwamwem: vewww awn: nro woveoXWBwno Hoownwodm om nro newom<oemo moonwoom
eoooomneconom w: n. n. > uoewom om newom<oemo moonwowm nreocm: nro eomwoo om waouoa
noeawswwm w: nwo wvmwuwnoeww noenox. duo mawHH monm eoweomown nwo newnewccnwoo om mewwdm
woo<o mwdoem wen noeawowwm w: nro wwmwwwnoewp mHH eomwoo. aro mwewooom weow wsmwnwnom nwo

oosnewp ooeo om nvo womoonwoe mwno. moonwoo m wm nseocmv nro weow om anwaca chopwom we
<v. :. swamwwac. a. necow.

 

83
nonhomotopic connections (INA), (c) commissural connections (CA)
(see table 1).

These results show that a given representation area of the peri-
Fhery in SI is connected with a similar representation area of the
periphery in SII.

The topography and density of cell bodies of intrahemispheric
nonhomotopic afferents was varied and complex. The labeled cell
bodies of intrahemispheric nonhomotopic afferents resulting from an
injection of HRP in the hindlimb and trunk regions of SII are the
most complex. Injections in this region labeled the cell bodies of
INA in the fOrepaw region of SII, the anterolateral face region and
the junctional area between the face regions of SI and SII.

Labeled cell bodies were found in the contralateral homotopic
cortex fOllowing injections of HRP in the hindlimb and trunk regions
of SI and SII, but not after injections in the ferepaw regions of SI
or SII.

Three dimensional reconstructions Of a series of transverse
sections revealed that labeled neurons are organized into rostro-
caudally oriented strips. Most of the strips of labeled cell bodies
of INA, IHA, and CA were lOcated in the sulcal cortex, and relatively
few labeled cell bodies were observed in the cortex of the gyral crowns.

Most of the labeled neurons had pyramidal shaped cell bodies.
The laminar distribution of the labeled cell bodies of INA, IHA, and
CA were uniquely related to the functional region of the injection site.
The cell bodies of the intrahemispheric projecting neurons in the fere-

paw arersof SI were restricted to the supragranular layers whereas

84
the cell bodies of intrahemispheric projecting neurons in the
ferepaw area of SII were in all layers except layer I. The bulk
of labeled cell bodies were in layers II, III, and V. The
arrangements of cell bodies of afferent neurons in the trunk
and hindlimb regions of SI and SII were variations of that de-

cribed for the ferepaw regions of SI and SII.

DISCUSSION

Utilizing the tracers HRP and tritiated amino acids, the
intrahemispheric and commissural circuitry of SI and SII areas was
investigated. Figure 24 is a summary of the connections observed in
this series of experiments. Similar to the investigations in the rat
(White and DeAmicis, 1977), and monkey (Jones and Wise, 1977), it
shows that neurons in the trunk, hindlimb and fOrepaw representation
areas in SI and SII are reciprocally connected. The figure also
shows that the results of these experiments support the hypothesis
that there is synaptic interaction between the granular and agranular
regions of SI and SII. Neurons in the granular region of SII or SI
(the ferepaw region) receive afferents from neurons whose cell bodies
are located in the agranular region of SII or SI (the trunk and hind-
limb region). Neurons in the agranular regions of SI or SII receive
afferents from neurons whose cell bodies are located in the granular
regions of SI or SII. In addition, neurons in the boundary area between
the face regions of SI and SII project to SII to the hindlimb and trunk
regions of SII.

Similar to the observations made in the rat, cat, and monkey,
neurons in the trunk region of SI receive afferents from the homotopic
area in the contralateral hemisphere. Neurons in the SII hindlimb and
trunk regions receive afferents from the contralateral homotopic area
in SI and homotopic areas in SI.

- These results together with those in the rat (Akers and Killackey,
1978; White and DeAmicis, 1977) and monkey (Jones and Wise, 1977)
suggest two principles of organization of intrahemispheric and

commissural connections.

Figure 24:

86

Summary of the connections Observed in this series of
experiments. The reciprocal connections between the
ferepaw regions of SI and SII and the trunk and hind-
limb regions of SI and SII indicate one principle or
organization: this circuitry is related to the electro-
physiologically observed projection of peripheral
receptors. The reciprocal connections between the trunk
and hindlimb regions within SI and the fOrepaw and
hindlimb regions within SII illustrate a second principle
of organization: this circuitry is related to something
other than the electrophysiological projection of
peripheral receptors to the cortical surface. The
reciprocal callosal connections are related to the second
principle of organization. In this proposed schema,
callosal connections transmit information accrued by the
intrahemispheric nonhomotopic connections.

88

One principle is illustrated by the intrahemispheric homotopic
reciprocal connections. The topography of these connections is
intimately related to the electrophysiological projections of
peripheral receptors to the SI and SII cortical regions. This study
and other anatomical studies in the rat (Akers and Killackey, 1978)
and monkey (Jones and Wise, 1977) have shown that neurons of each
cortical sector of SI receive projections from a cortical sector in
SII which receives projection from peripheral receptors in the same or
very similar body parts. These connections are invariant between SI and
SII and appear in all mammals investigated.

The presence of nonhomotopic connections illustrated a second
principle of organization. In this study and in the rat (Akers and
Killackey, 1978), connections have been demonstrated between neurons
in the granular cortex and those in the agranular cortex. The topo-
graphy of the cell bodies of these connections is unrelated to the
topography of specific thalamocortical afferents. Hewever, the topo-
graphy of the cell bodies of INA appears to be related to the
distribution of the cell bodies of callosal projecting neurons.

The topography of callosal connections is also unrelated to the
topography of specific thalamocortical afferents. Jones et a1 (1975)
suggested that, in the monkey, callosal neurons terminated on homo-
logous neurons in the contralateral hemisphere. Akers and Killackey
(1978) demonstrated in the rat that callosal and specific thalamo-
cortical afferents terminated in adjacent but nonoverlapping areas in
the face region of SI.

These anatomical results are corroborated by the electrophysiol-
ogical studies. In the rat, Welker (1976) showed that zones of callosal

termination were unresponsive to peripheral stimulation of specific

89

regions of the body. In the cat, Innocenti et al (1974) have

shown that 90% of the callosal projecting neurons terminate on
neurons with wide and bilateral receptive fields and are not somato—
topically organized.

Innocenti et a1 (1972) feund that single fibers in the corpus
callosum had small localized receptive fields from all parts of the
body. Those regions of SI and SII which are devoid of anatomical
connections transmit electrophysiological infOrmation in a manner
similar to those regions in which anatomical callosal connections
exist. These data indicate that, electrophysiologically, callosal
neurons are able to transmit precise topographical infOrmation,
although the neurons themselves are not driven by stimulation of
receptive fields that are precise and restricted. It is probable,
therefore, that tactile infbrmation from the densely innervated regions
destined for the contralateral hemisphere is first relayed to the
callosal neurons via the nonhomotopic connections, then to the homo-
topic region in the contralateral hemisphere, and then to the homotopic
area via symmetrical connections.

Future studies will be needed to determine if and how these
connections combine to mediate the physiological pathway fer sensory
infermation between the noncommissurally connected regions in SI and

SII.

Laminar Organization and the Formation of Stripg, The laminar distrib-

 

ution of the cell bodies of efferent neurons in SI and SII displays a

variety of patterns. The laminar organization of the cell bodies of

90
efferent neurons in some subdivisions exhibits a pattern of laminar
organization that is characteristic of monkeys whereas that of
other subdivisions are characteristic of nonprimates. In monkeys,
the cell bodies of origin in the SI to SII projection are located
in layer IIIB (Jones and Wise, 1977). In this study, the cell bodies
of efferent neurons in the SI to SII projection are confined primarily
to layers II and III (figure 25).

The laminar distribution of cell bodies of intrahemispheric
efferent neurons in the SI trunk, SII forepaw and SII hindpaw regions
was typical of that observed in other nonprimates. In mice (White and
De Amicis, 1977) and cats (Jacobson and Trojanowski, 1974), and in
this study, the cell bodies of origin in the SII to SI projection
were in all layers except layer I. The largest concentration of cell
bodies were localized in layers III and V with the majority of the
remainder in layer VI.

The bulk of the cell bodies of commissural efferents were located
in layers III and V. The cell bodies of commissural efferents in SII,
however, were more loosely organized than those in SI.

The cell bodies of fiber systems studied in SI and SII were
further organized into strips oriented in the rostrocaudal direction.
The organization of the cell bodies in SI and SII into distinct strips
has not been described in other nonprimates. An apparent clustering of
the cell bodies of commissural efferent neurons ("waxing and waning")
was reported by Jacobson and Trojanowski (1974).

The orientation of the strips of labeled cell bodies in the raccoon
is different from that Observed in the monkey. In the monkey, the strips

of cell bodies of origin of the intrahemispheric and commissural fiber

91

 

 

 

 

 

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. O
U
a . ‘
. g ‘ g. .
. . 4'
I
~ - ' a.» ..-
.‘ ’V? L " ‘t‘.
it’ ‘ . 1 ‘E633
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. , ,IL.‘
3. '. .5 ‘
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5005a! 100um

 

Figure 25: Pyramidal cell bodies of origin of the SI fOrepaw
to SII ferepaw projection. A. Only pyramidal cell
bodies in layer II were labeled in this cluster of
cell bodies. B. Higher magnification of the cluster

of labeled cell bodies shown in A.

 

92

systems are oriented in a medial-lateral direction.

In the raccoon, similar to the observations made in the monkey,
the diameter of the clusters of labeled cell bodies on intrahemispheric
and commissural efferents ranged between 200 and 1000 um. Typically,
many neurons in a column were labeled and neurons in adjacent columns
of neurons were labeled. The density of labeled cell bodies in a
fOcus of labeled neurons indicates that most, if not all, the neurons
were labeled. This suggests that the neurons of each fiber system are
not intermixed. In support Of this hypothesis are results of experiment
77559. In this experiment, a small injection in the SI trunk region
labeled the cell bodies only of commissural afferents. The cell bodies
of intrahemispheric afferents from the ipsilateral SIIregion were not
fOund. Since a regular series of sections was processed for the histo-
chemical reaction in this experiment, the explanation fur the absence
of labeled cell bodies may be explained as either: (1) the region in
the SI trunk region which receivesafferents from the contralateral
homotopic cortex does not also receive afferents from the ipsilateral
SII, or (2) the fucus of labeled cell bodies in the ipsilateral SII
is much smaller than the fOcus in the contralateral cortex and, con-
sequently, was contained in the 200 um interval of tissue not
histochemically processed. The latter explanation is unlikely since,
in other experiments, the lengthsof the rostrocaudal oriented strips
in the ipsilateral cortex are comparable to those in the contralateral
cortex.

These data suggest that, in SI and SII, the cell bodies of
efferents are organized into interdigitating strips. The degree to
which the cell bodies of one efferent strip interact with the cell bodies

of an adjacent, but different, efferent strip was undetermined.

93
In raccoons, the density of the cell bodies of efferents to the
motor cortex is comparable to that of intrahemispheric and
commissural efferents (Sakai and Herron, 1979). This suggests

that the cell bodies of these fiber systems are mutually exclusive.

Behavior Procedure

Seven raccoons, 4 to 6 months old, were used in this study.
Suckling infants were obtained from the Michigan Department of
Natural Resources and raised in the laboratory. Young raccoons
trapped in the wild were uncooperative in these behavioral experi-
ments.

At the outset, each animal was placed in the testing cage for
15-30 minutes each day to familiarize them with the behavioral
environment. The weight and food deprivation of each animal was
maintained at a level in which the animal would closely pursue food
placed within reaching distance. The raccoons were taught to extend
their forepaw through a portal in the front end of the testing cage
to obtain peanuts in a fOod well occluded from their sight. The
portals in the testing cage were arranged such that the animal could
only use his left forepaw on the left Side of the testing cage and
right ferepaw on the right side of the cage. After the animals had
acquired the "peanut reaching" behavior, they were tested to determine
the amount of time required to obtain one peanut from the food well.
Each animal was tested ten times a day until the amount of time it
took to retrieve the peanut was stabilized at 2.2 to 2.4 seconds.
Following surgery, the animals were then trained on a tactual roughness

discrimination task.

Surgical Procedure Surgical operations were perfOrmed on six animals.

 

Of these six animals, sham lesions were perfOrmed on two, ablation of

94

95
the SI forepaw area was perfOrmed in two animals and partial or
complete ablation of the SI or SII region in two others. Intraperitoneal
injection of chloralose (initial dosage, 17 mg/kg) was used to produce
general anesthesia. The hair on the dorsal surface of the head was
clipped and the dorsal surface washed with Betadine surgical scrub.
In an aseptic environment, the skin was incised along the midline and
the muscle and fascia were retracted. A large free bone flap was removed
over the area of interest and the dura widely retracted. The ablation
was carried out using a glass pipette and low vacuum suction. The
ablations in their entirely were carried out under visual control aided
by an operating microscope. The animals were ready for training after a

two week recovery period.

TestigggApparatus. The testing apparatus was a small box 4 inches wide,

 

5 inches high and 6.5 inches long (see figure 26). The apparatus had
a circular opening (diameter, 1.75 inches) at each end. For each trial
the circular opening was aligned with one of the testing cage portals.
A small door attached inside of the box covered “the circular opening at
each end. The doors were held in place by a mild spring tension.

The animals were taught to reach through the portal of the testing
cage, push the small door backward and into the apparatus to obtain
a peanut butter mixture. After the animals had acquired this behavior with
both forepaws, they were ready for training on a tactual rouanessdiscrim-
ination task. "Coarse" sandpaper was glued to one door and "fine"
sandpaper glued to the other door (Production Sand-Pak, 3M Company).
The "coarse" door was designated the positive rewarding stimulus of the
pair and the order of the doors presentation was according to a chance

sequence. After the animals had reached a criterion of 32 correct

Figure 26:

96

 

 

UI

 

 

 

 

 

 

 

_._’_.—.—_fi. A.

Schematic of the outside and the inside of one end of
the testing apparatus. A. Response counter.

B. Electrical outlets fer response counter. C. The
opening in which the animal could reach through to obtain
fOod. The discriminants were attached to a door which
covered the opening. The raccoon had to learn which was
the - and + reward doors. D. Access to the fOod well.

E. Inside view of the door covering the opening to one
end of the apparatus.

97
responses in 40 stimulus presentations, the other ferepaw was tested
to determine if transfer of learning had occurred. The temperature
discrimination learning task was conducted in a manner similar to the
tactile discrimination task; a hot plate (37°C) was attached to one
apparatus door and designated the negative rewarding stimulus and
another plate (24°C) was attached to the other door and designated the
positive rewarding stimulus.
Controls The odor of the peanut butter mixture was masked by having ten
times the amount used on each reward trial sandwiched between two pieces
of 1/4 inch plywood in the bottom of the apparatus. Stimulus
presentation was occluded from the raccoon's view by covering the front
on the testing cage and not presenting the stimulus until the raccoon
extended his forepaw to the portal in the testing cage.

Figure 27 is a diagram of the extent of the bilateral lesions in
the SI and SII cortical areas. In one animal, the gyral cortices of
the face representation areas were bilaterally removed (part A of
figure 27).

In another animal, the ablation removed part of the ferepaw
representation area of SII and lateral-most face representation area of
SI in the left hemisphere and the gyral cortex of the face representation
area of SI in the right hemisphere (SII fbrepaw + SI face animal) (part
B of figure 27).

In two additional animals, the ferepaw representation areas of SI
were bilaterally removed. The bilateral ablations were very similar in
the two animals. The ablations removed.most of the fbrepaw representat-
ion areas bilaterally and occasionally extended into the underlying
white matter (part C of figure 27).

The control group for the rough vs. smooth task were two normal
animals and one sham operated animal. The control group fer the

temperature task was one normal and one sham operated animal.

98

mwmceo No”

mnwoawnwo mwwmewa om nro oxnosn weo Hoownwo: om owpwnoewu Homwoam we nso mH woo mHH noenwowu weowm.
>. new” moemonnoewH <woz om nro Homn voawmeroeo om w ewoooos weww: awn: unsom no waawowno nro
woveOXWBwno Hoownwoom om nro newsm<oemo moonwowm nreocmr nro mwno om Homwoo nrwn wm mroza vowoz.
wonnoau nreoo new=m<oemo moonwoom no womwowno nro oxnosn om nro ewwwnoeww Homeowm w: nro mH noenwowp
mwno eoweomoonwnwowm. a. How" aoemonnoewH <wo£ om nro Homn roanmvroeo om w ewoooo: dewno awn:
<oenwowH Hweom no wsmwowno nwo wereoxwawno Hoownwoom om nwo newbm<oemo moonwoom copes. wonnoa"
nreoo new=m<oemo moonwoom no womwowno nwo powwow w: nro mwoo eoveomoonwnwos weow om mH won nSo
moeoewz weow om mHH no nro Homn woawmvroeo woo nso meewu ooenox om nro mwno eoveomoonwnwo: weow om
mH w: enmrn roawmwSoeo flmHH moeowwz + mH mwoov. a. doe" aoemonnoewH <woz om nro Homn roawmvroeo
om w ewnooo: oewwo awn: Hwoom no womwnwno nro wvweoxwawno Hoownwoom om nro newom<oemo moonwoom ores:
oowoz. wonnoa” nweoo newom<oemo moonwoam nreocm: nro mwno om nwo cwwwnoeww Homeowm om nro mH moeowwz
weowm.

99

 

 

[Z aln31d

  

____,

100
The animals were required to learn the tactile and temperature
discrimination tasks with one fOrepaw and subsequently tested for
saving in the intermanual transfer of the discrimination learning to
the second fbrepaw. The saving score was calculated as:

Learning score with lst hand - learning score with 2nd hand

 

X 100
Learning score with lst hand + learning score with 2nd hand .

RESULTS

The animals which had bilateral ablations of the ferepaw
representation areas in SI showed severe impairment of reflex
hopping and placing reactions. They retained the "reaching"
behavior and were therefore able to perform the gross motor
activities required fer performing the tasks. However, they were
unable to pick up the food in the rewarded trials, and therefOre
became uninterested after a few trials. They were unable to learn
the tactile and temperature discriminations using the above proced-
ures (see Table 2).

Reflex hopping and placing reactions were found to be
unchanged fer the animals with bilateral ablations of the SII fore-
paw + SI face animal and the bilateral SI face animal during the two
week recovery period. The speed and accuracy with which they could
retrieve peanuts from a food well occluded from view were comparable
to that observed befbre the ablations.(see Table 2).

Discrimination PerfOrmance and Transfer of the Rough vs SmOOth Task
Shown in figure 28 are the individual performance curves for each
forepaw of a normal animal, the bilateral SI face animal, the
bilateral SII forepaw + SI face animal and the sham animal. The
animals were trained on a rough vs. smooth discrimination using one
ferepaw to a criterion of 80% correct (32 correct responses in 40
consecutive trials). The normal and sham controls required at least
as many trials to reach criterion with the second forepaw as they

did with the first forepaw.
101

ewcpo Nu vomnuomwoo vuwowow won rovwwom cosw<woe wow nvo mw<w=m mooeom w: woeooonwmom contooo
woncwmwnnow newwwm won newommoe nomn.

102

 

>wwaww e romwow mwno vomnuwomwos wwwowom won awonwwo Hoawoewnceo
rooowwmlcoww<woe Unmoewawownwoo Unmoewawawnwow

«omen zoeawp zoeawu um.o mq.m
qmmmm mrwa zerwH ou.o mm.u
ummmu wwwwnoeww zoeaww mm.o um.m

mH mwoo
ummmn mHH moeovwz zoeawH Nm.o mu.m

+ mH mwoo
qmmmo wwwwnoeww Harwweoa zoso zooo

mH moeowwz
ummmu wnwwnoewu Harwweoa zoom zooo

mH moeovw:

103

Pier? .26}

‘0

----—--- ---—------- -

CORRECT RESPONSES
is

N
U

 

 

 

40 E 1% 1 00 75—156—
Trdfng (RM) Testhq (Loft)

Correct responses 'n 40 Ind Meets (or round raccoon on he rum lsnoofh
c'amun task the Ion pmeI «am the common vote for the up!
forepaw and the mg" ml sham the losing (or Irmslev In"! "I It" forever

p_—-—----. _———-——— -—--

CORRECT RESPONSES

 

 

 

V , If
‘20 H I «1) “0 ‘0 no ‘20 ‘0
Training Rich) Tuthg (Lott)

TRIALS

Correct m ’n 40 mm blocks Ian 0 raccoon nth a mutual SLSI'SII
(blotch on the «xvi/smooth discrmimhon task The It" pmel sham IN
acouwm rote for the urn taepau at! the my“ part shun "- Ming '0!
mm with It. In" torqu-

 

 

 

40‘
a:
u
m
E III---- --—-&—d—————Z——_
E ’° / \
E V

20

L.._.1 ‘
500 720 790 ”3 ~40 or, :0
Trdlho (R5011) Tosfng (Loft)

TRIALS

Correct m n 40 trio! blocks (or o mccoon with o hdotevol SI Ioce
micron m the (mgr/smooth earthworm task The left pave! she»: the
mansion rm Ia the up! tempo: and the “W we: aim the feslnq Ia
haste! II"! the left forepa-

p-———- ---_—__/_——

 

 

 

I20 60 «I go ,2.

I) .
Tm (RM) Twhq I Left)

40

CamtmhwmhhcnfamWoMmommtmwl
WWIMmmTNMImmo-shmtmroufam
rm famummmmmmtmca tractor with".
hfltorepm.

104
The subjects with bilateral ablation of the SI face region
and the SII fOrepaw + SI face showed intermanual transfer of the
rough vs smooth discrimination learning. The bilateral SI face
animal and the SII forepaw + SI face animal required as many trials
to acquire the discrimination learning with the first hand as the
controls. The sham operated animal had a moderate saving (63%)

while the SI face animal showed the greatest saving (85%).

Discrimination Performance and Transfer of the Temperature Task

 

One normal, the sham operated animal, the bilateral SI face
animal and the SII forepaw + SI face animal received training and
intermanual transfer testing with the temperature discrimination
task (37°C vs. 24°C). The animals were trained on the temperature
discrimination task to a criterion of 80% and given 40 overtraining
trials in a counterbalanced design.

The acquisition of the temperature discrimination learning did
not differ for the ablated animals and the controls (figure 29).
The SII ferepaw + SI face animal and the bilateral SI face animal
as well as the control animals showed large intermanual transfer of

learning scores (figure 29).

CORRECT RESPONSES

40

20

CORRECT RESPONSES
8
\

.----____/__...._-____-_.___

 

105

/

_—-—-—— —-uh————-'_-l*—-—-

ml ./

"20 "60 I200 Q40 40 80 20 '60

Train (R t) Testl (Left)
m I9" TRIALS no

 

 

 

Correct responses in 40 tnol blocks for a sham operated raccoon on o
hot/cold discrmnoton toslr The left panel shows the ocquvsmon rote for the
n¢tl forepaw me the non pmel shows the ICSIIDQ for transfer wuth the
left forepaw,

 

 

680 720 760 DOC 40 80 I20 160 200 2 40 280

Trolnlng (Right) Testing (Left)
TRIALS

Correct responses In 40 tnol blocks for o raccoon with o bilateral SI foce
deletion on a hot/cold discnmnotion task The left panel shows the ocouxsihon
role for the right forepaw aid the rich pmeI shows the testunq for transfer
with the left forepaw.

--—————— —-———————-y——

f
#50 /
8
5

 

 

 

20 » .\o’ ‘
88A: 920 960 m0 ‘0 I) 12C IGO
Trolnhg (R ) Test (Left)
W TRIALS '0

Correct responses in 40 tnol blocks for o raccoon with o bilateral 51 WW '5‘?“
(blot-on on o hot/cold discmhoton task The left pcneI shows the ocmisitm

rate for left forepaw and the run pmel stone the testnq for traisfer with

the rigut forepaw

DISCUSSION

The results of this pilot study support the hypothesis that
the bilateral removal of the SI forepaw, SI face or the SII forepaw
and SI face region differentially impairs the intermanual transfer
of discrimination learning in raccoons. These results, however, are
inconsistent with those of Teitelbaum et al (1968) who feund thatthe
removal of the SI forepaw or SII cortical region impaired cats'
ability to intermanually transfer discrimination learning. There
are several explanations for the differences in the results of these
experiments and those of Teitelbaum et al (1968).

Firstly, following the removal of SI forepaw area, there appears
to be a very strong species difference between the tactile behavior
of raccoons and the tactile behavior of cats and monkeys. The removal
of SI in monkeys (Kruger and Porter, 1958; Orbach and Chow,1959), or
SI forepaw area in cats (Teitelbaum et al., 1968) did not severely
impair the ability of these animals to learn tactile discriminations.
In this study, the SI furepaw region has been shown to be essential
for raccoons to learn tactile discrimination.

The impairment appeared to be primarily a sensory deficit. The
animals were not paralyzed, as they could grip objects, climb up cage
bars, and palpate the surfaces in their environment. Although they
could see familiar fOod parcels on the floor of their cage they were
rarely able to manipulate it into their mouth with their fbrepaw
because of clumsiness. In this respect, the animals behaved in a

manner that supports Kornhuber's (1974) hypothesis which suggests

106

107

that one of the functions of the SI cortical region is to provide
guidance fer voluntary motor activities.

Secondly, it is possible that the bilateral removal of SII
forepaw + SI face or SI face regions impairs the ability of
raccoons to intermanually transfer tactile discrimination learning.
The animals used in this study were not pretested fer their ability
to intermanually transfer tactile discrimination learning. Other
studies pretested their subjects to select only those subjects that
did well on intermanual transfer of discrimination learning tasks
(Teitelbaum et al., 1968). Thus a more homogeneous population was
used and the deficits encountered as a result of cortical ablations
were more obvious. The small number of available and trainable
raccoons prevented the selection process in this study. The way to
circumvent this particular problem in future studies is to use
reversible cooling of the cortical areas in the raccoon so that each

animal can serve as its own control.

Summagy. Control and experimental subjects were trained to
discriminate rough vs. smooth and temperature tasks in one fOrepaw
and subsequently tested with the other forepaw to determine if saving
had occurred. ‘The animals with ablation of the
fOrepaw region in SI were unable to learn the tactile or temperature
discrimination. There were no differences between the results of

the controls and those of the experimental animals,«other than this.

 

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