THE ORGAMZAUON OF SDMATDTOPlC PROJECHONS T0
SH CEREBRAL NEOCORTEX 1N THE RACCOON

(PROCYON LOTOR)

Thesis fer the Degree of M. A.
WCHIGAN STATE UNWERSHY
PAUL HERRUN

1975

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ABSTRACT

THE ORGANIZATION OF SOMATOTOPIC PROJECTIONS
TO 311 CEREBRAL NEOCORTEX IN THE
RACCOON (PROCYON LOTOR)

By*

Paul Herron

The pattern of projections of peripheral receptors
at the level of the neocortex in the secondary somesthetic
receiving area (811) was mapped. The purpose was to deter-
mine if the projection of peripheral receptors to the fore-
paw area in the 811 region are commensurate with projections
to the forepaw area in SI. An ancillary portion of the
study dealt with the orientation of the 811 somatotOpic
map on the $11 cortical surface.

Tungsten microelectrode mapping procedures were
used to explore thoroughly the inferior wall of the
suprasylvian sulcus, for regions responsive to mechanical
stimulation of peripheral receptors.

The results show that:

1. The forepaw area in the 811 cortical region shows
an enlargement commensurate with that found in the

SI cortical region.

Paul Herron

2. The somatotOpic organization of mechanoreceptive
fields of raccoon SII cortical region is reversed
from the way in which the postcranial regions have
previously been portrayed. Axial structures lie
medial and apical structures lie laterally along
the inferior bank of the suprasylvian sulcus.

This suggest that--in evolutionary terms--those
factors that are selective for tactile acuity of the

raccoon forepaw were Operating in the evolution of 811 as

they were in SI.

THE ORGANIZATION OF SOMATOTOPIC PROJECTIONS
TO 511 CEREBRAL NEOCORTEX IN THE

RACCOON (PROCYON LOTOR)

BY

Paul Herron

A THESIS

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

MASTER OF ARTS

Department of Psychology

1975

ACKNOWLEDGMENTS

I wish to express my appreciation to the following
people for their assistance during the course of this
project: Michael J. Harteau, Steven J. Warach, Charles R. R.
Watson, Prue Watson, Harry Scheline, and Jacqueline
Schreck for their help in preparing the animal for
recording, collecting the data, and the histological
processing of the raccoon brains; and Neal BrOphy for doing
the photography.

Further, my gratitude to the members of my thesis
committee: Dr. John I. Johnson, who was instrumental in
providing me with the chance to pursue this project, and
who has provided encouragement throughout my undergraduate
and graduate career; Dr. James L. Zacks for his assistance
and support; and Dr. Glenn I. Hatton for the use of his
equipment and assistance. Finally, I wish to express my
deep appreciation to my girlfriend, Janice Peterson, for
her moral support and encouragement.

This was supported by NIH training Grant STOl and

NSF GB 4346.

ii

TABLE OF CONTENTS

LIST OF TABLES . . . . . . . . . . .
LIST OF FIGURES. . . . . . . . . . .
INTRODUCTION. . . . . . . . . . . .
Historical. . . . . . . . . . . .
SomatotOpic Organization . . . . . . .

Behavior . . . . . . . .
Phylogeny of SI and. SII . . . . .

Specific Problems Concerning SII in This Study.

MTERIAL AIqD METHODS O O O O O O O O .

Subjects . . . . . . . . . . . .
Preparation . . . . . . . . . . .
Recording Apparatus. . . . . . . . .
Data Collection . . . . . . .
Reconstruction of Recording Sites . . . .
Quantitative Neuroanatomical Measurements .
SII Region Considered in This Study . . .

RESULTS 0 O O O O O O O O O O O 0
Location of the SII Cortical Region . . .

SomatotOpic Organization . . . . . . .
Enlarged Forepaw Representation. . . .

Receptive Field Properties of SII Mechanoreceptive

units 0 O O O O O O 0 O O O O O
Stimuli Modalities . . .
Anesthetic Effects Upon SII Mechanoreceptive
units 0 O O O O O O O O O 0 O 0

DISCUSSION . . . . . . . . . . . .
Similarities of SI and SII . . . . . .
SomatotOpic Organization of SII. . . . .
Bilaterality . . . . . . . . . . .
Summary. . . . . . . . . . . . .

REFERENCES 0 O O O O O O O O O O 0

iii

Page

iv

35
36

38

4O

LIST OF TABLES

Table Page

1. The total volume of the SII region (excluding
cranial representation) and the relative
volume of the forepaw area in the SII
cortical region . . . . . . . . . . 31

iv

LIST OF FIGURES

Figure Page

1. Organization of SI and SII in two placental
mamrnals O O O O O O O O O O O O O 4

2. Single and multi-unit response . . . . . . l6

3. Location of SII region in the raccoon from
two subjects . . . . . . . . . . . 23

4. Reconstruction of three coronal rows of
penetration at three different planes in
the anterOpostior extent of the
mechanoreceptive portion of SII in
raccoon 75515 . . . . . . . . . . . 26

5. Reconstruction of a coronal row of
penetrations in Subject 75515. . . . . . 28

6.. Reconstruction of a coronal row of
penetrations in Subject 75515. . . . . . 30

INTRODUCTION

Historical

 

The "dual nature of neOpallium" was first described
in monotremes by Abbie1 and a short time later by Adrian2
in placentals. Adrian found that somatic peripheral
receptors were represented in two separate and distinct
areas on the cortical surface. Subsequent electrOphysiolo-
gical experiments revealed double and sometimes triple
representation of somatic receptors on the cortical surface.
Double representations were found in a variety of mammals.
For example, double representation has been found in the
Virginia opossum,15 hedgehog,17 raccoon,36 and squirrel
monkey.3 The primary sensorimotor area (SI) received the
bulk of the attention for two primary reasons: (1)
cortical area is larger than the secondary sensorimotor
area (SII), and (2) SI is more accessible for electro—
physiological recording than SII.

The SI region, in all mammals investigates, lies
on the rostrosmedial area of the parietal cortex. Most of
SI projection area is exposed on the gyral crowns of

gyrencephalic animals whereas most of SII is often buried

inside a sulcus in gyrencephalic animals. Since earlier

electrophysiological experiments used macroelectrodes for
surface recording experiments, they were restricted in the
data they could obtain from SII.

However, the data obtained from the experiments
done with macroelectrodes and subsequently with micro-
electrodes dealt with the functional significance of double
projection areas on the cortical surface. With the exception
of one study that reported a double representation of
peripheral receptors in the ventrobasal complex of the
thalamus of the rat,7 double representation of peripheral
receptors seems to be a cortical phenomenon. Various kinds
of experiments were done to provide insight and information
with regard to somatotopic organization, behavior, and
phylogeny on the two cortical areas. What follows is a

brief review of information gained from these experiments.

Somatotopic Organization

 

SI and SII are somatotOpically organized, as the
somatic receptors are represented on the cortical surface
in a manner that reflects their actual relationships on the
body surface (see Fig. 1). In SI, the projections of the
peripheral receptors on the contralateral cortical surface
are somatotOpically organized such that the projections
from posterior quarters of the body are found lying medially,
often extending into the median sagittal fissure. More
cephalic structures are represented in an increasingly

lateral position on the surface of the parietal cortex.

Figure 1.

Organization of SI and SII in two lacental
mammals. (a) Cat (SI after Rubel2 and
Woolsey,37 SII after Haightlo). (b) Rat (after
C. Welker29r30). Dorsalateral viewf of the
left cerebral hemiSphere are represented with
anterior to the left. The presence or absence
of gyri do not effect the general orientation
or the relative position of SII with respect
to SI in the sensorimotor neocortex. The
orientation of the SII map on cat cortical
surface is different than the orientation 0f
the SII map on the rat cortical surface, as
reported in these studies.

Representations of the limbs and their apices are situated
rostrally, with those from the body axis forming the
posterior limit of the SI receiving areas. The SII region,
in all mammals investigated at this juncture, is situated
laterally to SI with the medial part of the SII repre-
sentation, the face area, in apposition to the face area
of SI. The orientation of SII on the cortical surface,
however, has been found to lie differently in recent
experiments than the orientation reported in earlier
experiments.

Earlier macroelectrode studies showed that SII
somatotopic organization is oriented on the cortical surface
in such a way that the limb apices point medially and the
body axis occupies the most lateral part of SII30'32'33'38.
These experiments were done with macroelectrodies and the
somatotopic map was incomplete.

Recently, microelectrode studies of the SII region
in the cat10 and sheep12 reported the orientation to be the
reverse of those in previous depictions. These studies
indicate that the orientation is such that the axial
structures are situated medially and limb apices are
represented laterally. The orientation of the somatotOpic
map is still confused by the results of the microelectrode

study on the rat31 which support the depictions of the

macroelectrode study.

To determine the importance of SI and/or SII in
behavior, studies tested the ability of the animal to
perform a previously learned tactile discrimination after
ablation of all or part of the sensorimotor cortex. Studies
on the cat shown that bilateral ablation of the SII region
caused a large deficit in previously learned tactile dis-
crimination tests and that these animals were unable to
relearn the tactile discrimination. Bilateral ablation of
SI in these animals (cats) caused only a temporary deficit
and ablation of both the SI and SII areas resulted in the
same deficit as that achieved by the ablation of SII alone.8
These experiments suggest that SII is of major importance
for tactile discrimination in the cat. With monkeys,
tactile discrimination was more severely affected when SI
was removed than when SII was removed.21 In rats and cats,
results in conflict with those obtained by Glassman suggest
there is only a temporary impairment when SI or SII is
removed and that the rat, but not the cat, can overcome the
impairment with some difficulty after the removal of both
areas I and II.45

The results of ablation studies seem to vary
between different species and different experimenters on
the same Species. It is often very difficult if not
impossible for different investigators to remove the same
area and same amount of cortical tissue in ablation

experiments. C. Welker suggests that the area that Zubek44

removed as being only SII in his ablation experiments
included areas of the cortex besides the electrophysiologi-
cally defined SII region. Discrete albations or lesions
have not been very successful in assessing the behavioral

significance of SI and SII.

Phylogeny of SI and SII

 

Some attention has been directed toward the
evolution of the two cortical areas to determine the
significance this may have in the functioning of the dual
sensory projections. The SII region is generally thought
to be phylogenetically older than SI. There is anatomical
and physiological data in support of this hypothesis.

Sanides speculated about the evolution of the
sensorimotor areas on the cortical surface of the slow

loris.29

He suggested that the sensorimotor cortex evolved
from the insular cortex, derivative of the paleocortex. He
found a stepwise increase in the concentration of granular
cells of cortex from the insular cortex, where there are no
granular cells, to the SI cortical region, where the
granular cells are the most concentrated. Sanides described
the stepwise granularization as differential trends or
concentrically developing growth rings, each successive

ring representing a more specialized cortex. Abbie noted
similar trends in monotremes and marsupials in which he

described "successive waves of circumferential differ-

entiation" away from both the archicortex and the

paleocortex.l Sanides traced these trends in the sensori-
motor region away from the insular cortex. The trend
begins in the anterior rhinal sulcus, the borderline of

the paleocortex (olfactory cortex); a two-cell strata is
encountered with a rather blank "lamina dissecans" in
between. In the region just medial to the paleocrotex and
lateral to the neocortex that he calls the proisorcortex,
lamina dissecans disappears and the granular cells of layer
IV appear. Medial to this region, there is a concentration
of granular cells in layers II, III, and IV. Sanides calls
this region prokoniocortex, which means before-the-powder
(i.e., granular) cortex. More medially, the next stage in
the trend shows an even greater emphasis on granularization
of the cortex, with a heavier concentration of granular
cells in layers II, III, and IV, a region he appropriately
called koniocortex.

This cytoarchitectonic study was accompanied by a
microelectrode recording study on the prokonio- and
konicocortex of the slow loris. The electrophysiological
study revealed that "the prokoniocortex, which appears as
an intermediate step in differential trends from the insular
proisocortex to the koniocortex, was consistent with the
so-called second somatic sensory representation, a much less
detailed representation of the whole body . . . this
somatic area was partly responsive to auditory stimuli,
too, an indication of the limited specialization compared

with the primary somatic area."29 In support of this

hypothesis, investigators have shown that the SII region in

4’5 Woolsey and

the cat overlaps with the auditory area.
Fairman, in a series of experiments, recorded evoked
potentials from the sensorimotor region in pig, sheep, and
other mammals and found that in SII, the spatial differ-
entiation of perpheral receptive fields increases from
rabbit to monkey, but that the spatial differentiation is
much less than the increasing differentiation found within
SI--that is, it does not reflect the specialization of
receptor surface as does SI. Woolsey and Fairman conclude,
"The position of somatic and auditory areas II between the
rhinencephalon and insula on the one hand and the more
highly differentiated areas I on the other hand suggest
that the "second" areas may be phylogenetically more
ancient and primitive."42
Experiments on a variety of mammals have demon-
strated a relationship in SI between the degree of receptor
specialization and the degree of cortical elaboration.
The raccoon, which makes extensive use of its forepaws in
the manipulation and tactile exploration of its environ-
ment, manifests an enlarged SI hand area when compared to

33,36

the hand area of other carnivores. Similarly, the

spider monkey, with its prehensile tail, shows a marked

increase in the SI cortical area devoted to the tail,

25

compared to other primates. Rodents and lagomorphs

manifest an enlarged face area in the SI cortical area

31,44

compared to primates and carnivores. On the other

10

hand, the cortical forelimb area in the SI region of
primates and carnivores is much larger than corresponding

areas in rodents and lagomorphs.42

Anatomical techniques,
combined with electrophysiological methods, have demon-
strated a rather unique functional specialization in the SI
region of the rat. The rat possesses an architectonic unit
referred to as the "barrel" in layer IV. An excellent
study by C. Welker has shown that each barrel is the
morphological counterpart of the cortical representation

of a single vibrissa. These barrels have also been found
in marsupials.37 Specialized cellular aggregates have not
been found in the SII of these animals.

Over all, these anatomical and physiological data
have been interpreted to indicate that SI constitutes a more
"recent" or "specialized" stage in the evolution of cerebral
neocortex, when compared with SII. To summarize: (1) The
anatomical location of SII between SI and the rhinencephalon
may indicate it is more primitive than SI. (2) The con-
centration of granular cells in SI cortex is greater than
the concentration of granular cells in the SII cortical
region--also thought to be indicative of "newer" cortex.

(3) Electrophysiological data suggest that the SII cortical
region is responsive to auditory as well as mechanosensory
stimulation, whereas the SI cortical region is responsive
only to mechanosensory stimulation, and (4) The relation-
ship in SI cortical region between the degree of receptor

specialization and the degree of cortical elaboration of

11

that receptor surface does not exist in the SII cortical

region.

Specific Problems Concerning SII in This Study

 

I have electrOphysiologically recorded units and
clusters of unit activity in the SII region. The study
dealt with the following questions:

1. Does the SII cortical region in the raccoon show an
enlargement in its hand region commensurate with
that found in SI cortical region?

2. What is the detailed somatotOpic organization of
mechanoreceptive projection to raccoon SII?

The rationale for choosing the raccoon deserves
some mention. The SI region in the raccoon has been mapped
and an extensive part of the SI cortical region receives
projections from the forepaw. The forepaw projections are
60% of the total sensorimotor area in the raccoon, compared
to only 20% and 30% forepavarojections respectively in the
SI region of dog and cat, closely related carnivores.36
Mapping the raccoon SII cortical region allows direct
comparison of the projection patterns of SI and SII in the
same animal.

In addition, a partial map of the SII region was

done with macroelectrodes.36

The somatotopic map obtained
in this study is an improvement over the previous map

afforded by the increased precision of microelectrodes.

MATERIAL AND METHODS

Subjects

Twelve raccoons of both sexes were used in the
study. The raccoons were trapped in wooded areas near
Michigan State University and cared for in university
facilities. As a consequence, their life histories and
exact ages could not be determined. The animals appeared
to be in good health with no obvious signs of disease.

All animals were either young adults or adults.

Preparation

 

General anesthesia was induced in eight animals by
intraperitoneal (IP) injections of chloralose (initial
dosage, 17 mg/kg). Four subjects were anesthetized with
Dial-urethane buffered with NaOH (initial dosage, 70 mg/kg
dial-lybarbituric acid and 288 mg/kg urethane). In order
to eliminate nociceptive reflexes, usually after six to
eight hours, an additional one-quarter of the original dose
was administered. In all cases the trachea was cannulated.v
To maintain body fluids and nutrients, saline and 5%
dextrose were administered IP alternatively at four-hour

intervals.

12

13

The head of the animal was securely fixed by means
of screws placed in the skull which were fastened with
dental acrylic to bars of a specially designed headholder.
The body was suspended on a frame which passed under the
axillae and inguinae of the limbs on either side of the
abdomen and thorax, leaving the limbs, sternum and abdomen
available for stimulation. Over one side of the anterior
neocortex the cranium was removed and the brain exposed by
excising the dura mater. The exposed surface was kept warm
and moist by constructing an acrylic dam around the skull
Opening and filling it was warm mineral oil (38°C). This
exposed surface was photographed through the mineral oil,
and an enlarged print was made for recording the sites of
electrode placements during the experiment. In some
experiments, the mineral oil was replaced with warm saline-

agar to reduce cortical pulsations.

Recordinngpparatus

 

Glass insulated, tungsten microelectrodes with
exposed conical tips having base diameters of 30 to 40 um
and altitudes of 25 to 40 um were used to record from single
and cluster cortical units. The tungsten electrodes
recorded the potentials with respect to a stainless steel
wire which served as a differential electrode inserted
through an exposed muscle of the head or neck. Signals
were initially amplified with a Tektronix 122 preamplifier

with a low frequency cut off at 80 cycles and high

l4

frequencies cut off at 40 Kcycles. Signals were then
transmitted to a Tektronix 565 dual-beam oscillosc0pe for
visual display and a Grass model AM-S audio monitor. The
signals were recorded on magnetic tape using a Magnecord
1028 recorder, while a second tape channel was used for

synchronized voice commentary.

Data Collection

 

Electrode penetrations were in a series of regularly
spaced rows, usually .5mm apart with penetrations .2 or
.5mm apart. This spacing was maintained at all times,
except where surface blood vessels lay in the path of a
proposed penetration. Since most of SII is located on the
inferior bank of the suprasylvian sulcus, the microelectrode
angle of entry was such that many initial penetrations were
through the superior bank of the suprasylvian sulcus.
Using a mechanical microdrive, the electrode was then passed
through the sulcus, distinguished by the silence of
activities heard over the audio-monitor, and driven through
the SII cortex. Every 75-looum the electrode was stOpped
and the entire body of the animal was mechanically stimu-
lated. When "drivable" unit activity was encountered, the
peripheral receptive field was carefully delineated. The
receptive field was defined as that area of the body
surface which, with minimal mechanical stimulation, reliably

evoked a cortical response.

15

Stimulation was performed manually with wooden rods
1 to 2mm in diameter. For finer stimulation, the finger of
the experimenter was placed in contact with the raccoon's
hair or skin with a pressure just sufficient to cross the
experimenter's tactile threshold. All stimuli were at
room temperature (20-24C).

"Drivable" unit activity, as seen on the oscillo-
sc0pe screen, was most commonly a series of spikes riding
upon a positive going slow wave (this slow wave is often
called the gross evoked potential, and is the response
recorded with macroelectrodes). The spikes were all of the
same amplitude and fairly evenly spaced in time (see
Fig. 2). These trains contained from one to as many as
ten or twelve spikes, and were considered to result from
single unit activity. In approximately 75% of the cases,
several cortical units were firing within the receiving
area of the electrode tip; Spikes of different amplitudes
were seen riding the slow wave on the oscillosc0pe screen.
Neural reSponse was qualitatively categorized by the most
effective stimulus as follows:

1. Cutaneous

a. Light skin response. Slight deformation of

the skin on a glabrous portion of the body
evoked a reSponse.

b. Hair response. Movement of the hairs on the

animal's body without deformation of the skin

evoked the response.

Figure 2.

16

Single and multi-unit response. A. Single
unit example from subject 75515. The unit
responded with a single Spike to light
pressure applied to the third digit.
Calibration: 20 mV & 10 mSec. B. Multi unit
response from subject 75515. This response
consists of a cluster of units firing together
in response to light mechanical stimulation

of the palm of the forepaw. Calibration:

20 mV & 10 mSec.

Figure 2

 

A __J20 mV

IO
mSec

 

 

.I‘l‘ [I ‘1 'III III . A

18

c. Deep pressure or normal skin response. A
pronounced deformation of the hairy or non-
hairy skin of the body was necessary to evoke
a response.

Samples of the response activity were recorded on
magnetic tape along with verbal descriptions of the
receptive field and the electrode coordinates. Written
protocols were kept throughout the experiments, describing
the category of the response, the depth of the electrode
where the response was encountered, and the focus of the
peripheral receptive field. The peripheral receptive field
was also drawn onto a photograph of the apprOpriate area of
the body. The penetration, with reSponding units of
interest, were marked by withdrawing the electrode tip,
immersing it in India ink, and lowering the electrode tip

to the depth of the response and retrieving the response.

Reconstruction of Recording Sites

The plane of electrode penetrations was preserved
at the conclusion of each experiment by replacing the
microelectrode attached to the micrometer with pieces of
hypodermic tubing and inserting them at the boundaries of
the investigated area.

The animal was then given an additional dose of
anesthesia and was perfused intracardially with 0.9% saline
solution followed by 10% formOlsaline. The head was

removed and stored in formol-saline for at least one week

19

after which the brain was removed, photographed and the
neocortex of interest was removed by cutting along the
plane of the inserted hypodermic tubing. The block was
embedded in celloidin and sectioned at 30 um intervals in
the plane of rows of electrode tracks. Alternate sections
were stained for cell bodies (thionin and myelinated fibers
(Weil and Sanides-Heidenhain technique). Sections were
examined microscopically and the electrode tracks were
identified using the data logged during the recording

sessions.

Quantitative Neuroanatomical Measurements

 

The absolute and relative enlargement of the forepaw
cortical area in the SII cortical region was measured
following the procedure described by Dornfield, Slater, and
Scheffe.7 The measurements of sections with penetrations
that encountered responses were plotted on a graph whose
abscissa represents the distance between those sections,
and whose ordinate is the responsive area within each
section. The points were then connected with a continuous
line with zero reading at either end and the volume deter-

mined by measuring the area under the curve with a plani-

meter.

SII Region Considered in This Study
The secondary sensorimotor receiving area was

penetrated 351 times in the twelve subjects, yielding 161

20

responding loci. A large number of penetrations were made
to demarcate the boundaries of the SII cortical region.
Penetration of the SII region required penetra-
tions of the SI face cortical region. This created a
difficulty in distinguishing SI and SII head regions, since
they may meet, or even overlap at the depths of the supra-
sylvian sulcus. Therefore, the cranial areas were excluded

from consideration in this study.

RESULTS

Location of the SII Cortical Region

Approximately 80-90% of the SII cortical area is
buried on the inferior bank of the suprasylvian sulcus.
Ten to 20% lies on the lateral edge of the suprasylvian
bank. The amount of SII cortical region inside the sulcus
remained fairly constant throughout this series of experi-
ments. Physiological boundaries of SII were defined by the
location of microelectrode penetrations in which no responses
could be elicited by mechanical stimulatiOn. The antero-
medial and posteriomedial SII cortical regions are bounded
by the cranial and shoulder cortical areas, respectively,
of SI in the fundus of the suprasylvian sulcus. The anterior
and lateral regions of SII are bounded by "silent" areas
(unresponsive to mechanical stimulation of the body
surface) and posterior region is bounded by the auditory
cortical area. Unit activity driven by mechanical stimu-
lation of the forelimb was recorded from the fundus of the

suprasylvian sulcus (see Fig. 5 and description).

Somatotopic Organization

 

Figure 3 illustrates the general relationships of

projections from peripheral receptive fields. The general

21

Figure 3.

22

Location of SII region in the raccoon from two
subjects. A. Dorsolateral view of the left
hemiSphere, with anterior to the left. Shaded
region indicate the coronal gyrus which must be
removed to visualize the cortical surface of the
SII region on the inferior bank of the supra—
sylvian sulcus. B. Diagram of the SII region

on the inferior bank of suprasysvian sulcus with
the superior bank partially removed, from
experiment 75515. Shaded line represents the
cortex surface where the coronal gyrus has been
removed. Locations where electrodes penetrated
the cortical surface are indicated by dots.

All penetrations containing units which
responded to stimulation of a given body area are
closed within a line. Thus all "forepaw"
responses are enclosed within the area labeled
forepaw. C. Composite diagram of experiments
74502 and 75519. Note that the trunk is
represented medial to the hindlimb and the fore-
paw anterior to leg and hind paw. D. and B.
Data from B. and C. respectively, replotted to
show the locations of projections from the
digits (1, 2, 3, 4, and 5) and palm of the
forepaw.

— ____— Amp—'-

Figure 3

 

 

B

   
  
 

Posterior

Forearm

W Ivian sums

A

Lower

755:5 Forearm

 

Palm 8
C Digits

Posterior
Anterior

 

755|9
74502

Lateral

 

24

organization is similar to that found in SII and SI of
other mammals. The tail and posterior part of the trunk
lie on the exposed bank of the suprasylvian sulcus.
Projections from the trunk are anterior to projections from
the tail (see Fig. 4). The plantar surface projections are
medial to the projections from the posterior trunk, lateral
to the projections from the leg and anterior to the pro-
jections from the trunk (see Fig. 5 and 6). The digits are
in somatotOpic order, digit 1 occupying the most anterior
position and digits 2, 3, 4, and 5 occupying progressively
a more posterior position on the cortical surface. Axial
body structures lie along the fundus of the suprasylvian
sulcus. Overall, the somatic afferents to SII in raccoon
are represented on the cortical surface in a pattern which
reflects their actual relationships on the raccoon's body

surface.

Enlarged Forepaw Representation

 

Volumetric determinations were made of the SII
region in one animal to obtain quantitative measures of
the relative develOpment of the forepaw and the rest of the
body. In experiment 75519, the emphasis was to define the
physiological boundaries of the SII cortical region and to
define the boundaries of the forepaw area within the SII
cortical region.

An enlarged projection of forepaw receptors was

found represented on the SII cortical surface of this

Figure 4.

25

Reconstruction of three coronal rows of
penetration at three different planes in the
anterOpostior extent of the mechanoreceptive
portion of SII in raccoon 75515. Upper right:
tracings of the left cerebral hemisphere of this
animal with the orientation of the three rows

of penetrations shown by a small line. Pro-
jecting to the inferior bank of the suprasylvian
sulcus in an anteroposterior direction are the
lower arm and forepaw, hindleg and trunk, and
tail. The lines in the diagram represent the
electrode tracks and the shaded areas represent
the activities receptive fields on the surface
of the body.

 

_— — —- -—._—-—-—__ ———-_——— ‘

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Figure 5.

27

Reconstruction of a coronal row of penetrations
in Subject 75515. At upper right is a tracing
of the left cerebral hemisphere of this animal
with the orientation of the puncture row shown
by a dotted line. This section lies near the
anteriormost extent of the mechanoreceptive'
portion of SII. Tactile receptive fields are
indicated in the schematic brain section at
approximately the level within the row of pene-
trations that they are found. Note that the

distal part of the digits are represented on the

lateral surface of the inferior bank of the

suprasylvian sulcus and, that responses from the
lower forearm is found in the medial-most region

of the sulcus. The lines in the diagram
represent the electrode tracks and the shaded

areas represents the activating receptive fields

on the surface of the body.

-..._.——-——,-""—9——"-‘

u—h ‘1-_——“ ._——_-__

#>M

 

L4—

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

\iii

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Figure 6.

29

Reconstruction of a coronal row of penetrations
in Subject 75515. Upper right: a tracing of the
left cerebral hemisphere of this animal with the
orientation of the puncture row shown by a line.
This section lines near the posteriormost extent
of the mechanoreceptive portion of the SII
region. Tactile receptive fields are indicated
in the schematic brain section at approximately
the level at which they are found within the

row of penetrations. Note that the distal part
of the hindleg is represented on the lateral
surface of the inferior bank of the supra-
sylvian sulcus and the trunk and hip region of
the body are represented in the medialmost area
of the sulcus. The lines in the diagram
represent the electrode tracks and the shaded
area represent the activating receptive fields
on the surface of the body.

H
_—_—_‘h*—_‘——__HFH__—__l*m

 

 

 

 

 

lmm

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

31

animal (Table l). The forepaw volume is three-fourths of
the total volume of the SII region. The anterior-posterior
length of the SII cortical region in two experiments were
9.81 mm in experiment 75519 and 11.37 in experiment 75515.
Table l.--The total volume of the SII region (excluding

cranial representation) and the relative volume
of the forepaw area in the SII cortical region.

 

 

Total Forepaw Body, Hindlimb,
Volume Volume and Tail Volume Percent
Animal # (mm3) (mm3) (mm3) Forepaw
75519 515 390 124 76

 

Approximately 90-95% of these afferents are from
the ventral surface of the glabrous palms and digits. The
remaining 5-10% of the afferents originated from the dorsal
surface of the forepaw and lower forearm.

Receptive Field PrOperties of SII
Mechanoreceptive Units

 

 

The best stimulus for delineating the receptive
fields on the forepaw were probes with tip diamter of l to
2mm. Individual digits are discretely represented on the
cortical surface. For instance, a cortical point that was
most responsive to stimulation of one digit reSponds much
less or not at all to stimulation of the four other digits.
If the exploring electrode is moved to another point on the
cortical surface, the receptive field that maximally stimu-

lates that cortical point is also shifted.

32

The receptive field size decreases progressively
from axial to distal body areas, very similar to the
receptive field gradations found in SI. The smallest
receptive fields were found on the forepaw with the largest
occupying the trunk and upper limbs. The receptive fields
were constant and did not vary over time.

Bilateral units or clusters of units were rare.

Of the 161 mechanoreceptive responses, only nine had
bilateral receptive fields, and these receptive fields were
restricted to the hind quarters and axial body structures.
The bilateral receptive fields often extended across the
midline and had symmetrical receptive fields. The
ipsilateral component of the bilaterally reSponding clusters
was generally lower in amplitude than the contralateral
component. There were never any responses encountered with

bilateral receptive fields on the forepaws.

Stimulus Modalities

 

Of the 161 foci, 154 were mechanosensory units or
clusters whose receptive fields were responsive to light
pressure. Slight depression of the glabrous Skin or light
stroking of the surface hair were adequate stimuli. Six
units had receptive fields that were driven by heavier
pressure or a pronounced indentation of the skin. These
units were later localized in the fibers of the white
matter underlying cortex by correlating their position in

the penetration with the histological location of the

33

electrode track. With the exception of one unit cluster
which included responses to both auditory (clicks) and
pressure stimulation, all the mechanosensory units and
clusters were responsive to light pressure. There were no
units inside the SII region that responded to auditory
stimuli; the exceptional cluster mentioned above was on the
posterior boundary of SII.

Anesthetic Effects Upon SII
Mechanoreceptive Units

 

 

Of the twelve animals used in this study, eight
were anesthetized with chloralose and four with dial
urethane. The somatotopic organization was not altered by

the type of anesthesia used.

DISSCUSSION

Utilizing microelectrodes, fine grain mapping of
the secondary sensorimotor region in the raccoon supports
the hypothesis that the behavior specialization of the
animals--the degree to which the raccoon uses its forepaw--
is reflected in the proportion of SII cortical area
devoted to the forepaw. The data suggests that the
pr0portion of cortical area devoted to the forepaw in SII
is approximately comparable to the prOportion of cortical
area devoted to the forepaw in SI. Similar results have
been obtained at subcortical levels in the raccoon. In
the medulla, forepaw projections are 42% of the dorsal
column projection.35 At the next level of somatic sensory
integration, the ventrobasal complax of the thalamus,
forepaw projections increase significantly to 66% of the
total volume of the somatic projections from the peripheral
receptive fields. In the two projection areas of the
cortex, the forepaw projections are greater than 50%.

Thus, Specialization is seen throughout the
raccoon's somatic sensory system. Specialization of sub—

cortical levels similar to that which occurs in the raccoon

34

35

have been demonstrated in a variety of animals. But in the

albino rat, the elaboration of projections from the

20 17

thalamic,
32

mystacial vibrissae and face to the medulla,

31

and SI cortex are not found in the SII region.

Similarities of SI and SII

 

Differences commonly found between SI and SII are
absent in the raccoon. The Similarities of the two areas
in the raccoon are many. For example, investigation of the
cat sensory areas have shown that SI reSponds to movement
of joints while SII does not. In the raccoon, no responses

were found to movement of joints in $136

or the present
study of SII. The receptors which project to SI and SII are
reSponsive to light mechanical deformation of hairs and
skin. Previous studies have indicated that the tOpographic
organization of SII is less precise than that of 81.43
This requires some elaboration.

Although the responsiveness of single cells in
homologous regions of SI and SII has not been studied, one
would expect the receptive fields of units in SII to be
somewhat larger than they are in SI. There are more cells
in SI, thus the number of cells subserving the same area
are less in SII, an receptive fields would be larger. This
does not mean that the receptive fields of SI are more
discrete than they are in SII, but smaller. Welker and

Seidenstein found that the digits of the forepaw are dis-

cretely and individually represented on the SI cortical

36

surface with no overlap of the projection regions whereas
the digits of the hindpaw are not discretely and individually
represented on the cortical surface. Comparable data from
this study was also found for the digits of fore and hind-
paw in SII: regions responsive to only one digit were
localized in the forepaw representation, in the hindpaw
projections receptive fields always included the whole
glabrous surface of the paw including all digits. Welker
and Seidenstein noted that when comparing the SI of some
mammals that the degree of localization, intensity of evoked
response, and volume of neural tissue appear to vary
directly with the innervation density of the peripheral
sense organs, while the degree of overlap within the somatic
area appears to vary inversely with innervation density.
They also noted that "such evidence suggests that this
elaboration or specialization results in lowered thresholds
for certain types of stimuli as well as in greater sensory
acuity" (33, pp. 492-93). This suggests that--in evolu-
tionary terms--those factors that are selective for tactile
acuity of the raccoon forepaw were operating in the

evolution of SII as they were in SI.

Somatotopic Organization of SII
It was suggested by Welker and Seidenstein36 that
the orientation of the somatotopic representation of body

structures on the SII cortical surface is such that axial

structures are represented laterally on the inferior bank

37

of the suprasylvian sulcus with distal body parts pointing
medially into the suprasylvian sulcus. The results
obtained in this study indicate that the somatotOpic
organization orientation on the cortical surface agrees

with recent results obtained in the cat10 12

and sheep.
These results show that the orientation is reversed
to that of previous assumptions. The orientation
of the somatotOpic organization on the SII cortical surface
of racc00ns is such that the distal structures lie laterally

with axial body parts lying medially in the suprasylvian

sulcus in agreement with results from cat and sheep.

Bilaterality

 

Functionally, the SII cortical region in the cat10

and rhesus monkey38 is divided into two cortical fields, a
rostral and caudal field. The rostral field of the SII
cortical region have receptive fields that are somato-
topically organized, discrete, and modality specific. The
caudal field of the SII cortical region have receptive
fields that are not somatotopically organized, discrete,
and modality Specific. The receptive fields of the caudal
field are often bilateral, responsive to auditory stimuli.
C. Welker32 was unable to find the caudal field in the rat
and it was not encountered in the present study.

There is some disagreement regarding bilaterality
in the rostral field of the SII cortical region. In

barbiturate anesthetized cats,5 bilaterality is minimal.

38

Haight recorded from both anesthetized and slightly
anesthetized (nitrous oxide) subjects and found a minimal
of bilaterality using either anesthetic states. In
contrast, 90% of the units of awake rhesus monkey are
bilateral. Bilaterlity was also minimal in the present
study in which the anesthetics used were chloralose and
Dial-urethane. The differences observed in the bi-
laterality of these animals may be Species differences
rather than suppression of the ipsilateral component
thought to occur in barbituate anesthetized animals.38
However, comprehensive single unit investigations of a
variety of awake animals are needed to determine if there

are species differences in the bilaterality of the rostral

field of the SII cortical region.

Summary

1. The afferent connections to the cerebral cortex
in raccoons were mapped using microelectrodes.

2. The SII region show an enlargement of the forepaw
area commensurate with that found in SI.

3. The afferents project onto the SII region in a
manner which reflects (although distorted in size
and shape) their actual peripheral relationships.

4. The tactile interest of the raccoon's SII region
appears to be light mechanical stimulation of

peripheral receptors.

39

The somatotopic organization of mechanoreceptive
fields in raccoon SII is reversed from the way in
which postcrainial regions have previously been
portrayed. Axial structures lie medial and apical
structures lie laterally along the inferior bank
of the suprasylvian sulcus.

Bilateral receptive fields are minimal in the SII

cortical region of the raccoon.

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