DEVELOPMENT OF ViSUAL ACUITY {N TWO
SPECiES' OF PEROMYSCUS (RODENI'IA)

The‘sis for the Degree «of PhD
MICHIGAN STATE UNIVERSITY
BEDFORD MATH ER VESIAL *

1970.

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LIB R A R Y
Michigan 3:3 re
University *-

This is to certify that the

I
I
I
I

thesis entitled

DEVELOPMENT OF VISUAL ACUITY IN TWO
SPECIES or PEROMYSCUS (RODENTIA)

presented by

Bedford Mather Vestal

has been accepted towards fulfillment
of the requirements for

ilk—D'— degree in M

Date May 6, 1970

0-169

 

 

 

 

 

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LIB RA R Y
Michigan State
University

  

This is to certify that the

thesis entitled

DEVELOPMENT OF VISUAL ACUITY IN TWO
SPECIES OF PEROMYSCUS (RODENTIA)

 

presented by

Bedford Mather Vestal

has been accepted towards fulfillment
of the requirements for

Ph-D- degree mm

Date May 6, 1970 I

0-169

 

 

ABSTRACT

DEVELOPMENT OF VISUAL ACUITY IN TWO
SPECIES OF PEROMYSCUS (RODENTIA)

By
Bedford Mather Vestal

Peromyscus maniculatus bairdi, a terrestrial grass-
land rodent, and 2. leuconus noveboracensis, a semi-
arboreal form, were used as eXperimental subjects to:

1) describe visual acuity and ontogeny of vision in a
nocturnal rodent; 2) determine whether evolutionary
adaptation to different habitats has led to differences
in visual development: and 3) determine the effect of
stimulus distance and ambient illuminance on visual
acuity. Visual acuity, the resolving power of the visual
system, is the resultant of several environmental and
morphological factors and was used as an indicator of
visual maturation.

The mice were restrained on a platform within a rotating
drum which could be lined with equal black and white
stripes of various widths. The minimum separable visual
angle was the measure of acuity. If the stripes were large
enough to be seen, an optokinetic nystagmus response was
exhibited by the mice. A maximum of eight trials of 15
seconds duration were given for each stripe width. The

angle subtended by the smallest stripe eliciting a response

Bedford Mather Vestal

in each direction of drum rotation was the visual angle for
that subject. Stripes differed by 7' (minutes of arc) in-
crements. A cross-sectional design was used, with age
after eye opening, stimulus distance (10 cm, 20 cm, and 40
cm), and light intensities (4.3 lux, 86.1 lux, and 861.1
lux) as the main variables. Two-hundred forty-eight mice
were tested. The smallest stimulus stripe sizes available
at each distance (35' at 10 cm, 21' at 20 cm, and l#' at

40 cm) limited determination of the minimum thresholds of
acuity for some mice.

Both species had average acuities of 18.2' visual angle
at 40 cm, 8 days after eye opening. Individuals reSponded
to lh' stripes as early as # days after eye opening. These
values represent the smallest visual angle reported for any
rodent. At 20 cm stimulus distance the mean visual angle
of leucopus drOpped significantly one day before that of
maniculatus. At 40 cm maniculatus' mean decreased one day
before leucopus'. The develOpmental patterns of the two
species were otherwise similar. Acuity improved signifi-
cantly with age. The pattern of results during develop-
ment was significantly affected by stimulus distance. The
limits of stripe size were seen by all mice on the day of
eye Opening at 10 cm (35'). by 95% of the mice at two days
after eye opening at 20 cm (21'), and by 85% of the mice at
six days after eye opening at no em (14'). Threshold visual

angles at comparable ages were significantly smaller at

Bedford Mather Vestal

20 cm than at #0 cm. The illuminance levels used had no
significant effect on visual acuity. Size of visual angle
was significantly and negatively correlated with body
weight and age at the time of testing.

There was no consistent relationship between species'
habitat and deve10pmental pattern. The visual system
matured rapidly, and vision was more acute than in other

rodents which have been studied.

DEVELOPMENT OF VISUAL ACUITY
IN TWO SPECIES OF PEROMYSCUS
(RODENTIA)

By

Bedford Mather Vestal

A THESIS

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

DOCTOR OF PHILOSOPHY

Department of Zoology

1970

ACKNOWLEDGEMENTS

I wish to thank the members of my guidance committee,
Dr. John A. King, Dr. Martin Balaban, Dr. J.I. Johnson, Dr.
Glenn Hatton, and Dr. Rollin Baker for their critical
reading of this manuscript. Dr. King has been very help-
ful as an advisor in the planning and execution of this
project. I especially appreciated his habit of providing
help and advice when requested and leaving me alone the
rest of the time. Dr. Balaban's critical comments were
also beneficial during this research. Dr. Johnson pro-
vided photographic facilities for constructing the test
stimuli. I thank Dr. Dominic Zerbolio, Jr. for his advice
on statistical analysis and the use of a computer program.
Special thanks are due my wife Carolyn for her many hours
of help in building apparatus and editing and typing the
manuscript.

I was supported while carrying out this project by a
graduate traineeship under Training Grant TOl—GM 1751 from
the National Institute of General Medicine. Research sup-
port was supplied by the above grant and by grant 5-R01-
EYOOHU7 from the National Eye Institute to Dr. John A. King.

ii

TABLE OF CONTENTS

Abstract
IntrOdUCtion 00000000000000000000000000000000000000000 1
Literature Review

Definition and Methods of Measurement ............. 4
FaCtorS Governing Visual ACUity 0000000000000000000 7
Species Differences in Visual Acuity ..............11
Development of Vision and Visual Acuity ...........lb
The Experimental Animal, Peromyscus 00000000000000017
Aims Of This StUdy 0000000000000000000000000000000023

Materials and Methods

SUbjeCtS 00000000000000000000000000000000000000000027
Apparatus 0000000000000000000000000000000000000000027
Procedures 000000000000000000000000000000000000000031
StatiStical AnalySiS 00000000000000000000000000000035

Results
Pattern Of Development 000000000000000000000000000036
EffeCt Of StimUlUS DiStance 00000000000000000000000u2
EffeCt Of Light IUtenSity 000000000000000000000000049
Other Variables 0000000000000000000000000000000000049
Behavioral Observations 00000000000000000000000000051
DiSCUSSion 00000000000000000000000000000000000000000005“
Summary and COHClUSiOUS 00000000000000000000000000000062

Bibliography 0000000000000000000000000000000000000000065

Appendix 10 Width Of TBSt Stripes in MM 000000000000071

iii

Table
Table
Table
Table

Table

(2"me

U1

Table 6

Table

Table
Table

Table

Table

Table
Table

10

ll

12
13

LIST OF TABLES

Visual Acuity and Visual Distance in
Age in Days At Eye Opening
Development of Visual Angle at 20 cm

Analysis of Variance of Visual Angle
Distance

Development of Visual Angle at 40 cm

Analysis of Variance of Visual Angle
Distance

Peromyscus 13

Distance

at 20 cm

Distance

at #0 cm

Species and Day Differences in Mean Visual

Angle, #0 cm Distance

Effect of Distance on Visual Angle

Effect of Distance on Visual Angle, 2.

maniculatus

Effect of Distance on Visual Angle, P.

leucopus

Effect of Illuminance on Visual Angle at

Three Days After Eye Opening
Days of Age at Testing
Weight (g) at Time of Testing

Appendix 1 Width of Test Stripes in MM

iv

32
37
39

not
“3

44

46
47

#8

50

52
53

71

Figure 1

Figure 2

Figure 3

Figure U

LIST OF FIGURES

Mice on Platform in Testing Apparatus: t0p - 30
half-cylinder covering subject: bottom -
half-cylinder removed

Development of Visual Acuity, 20 cm Distance 38
DevelOpment of Visual Acuity, 40 cm Distance #1

Weight at Time of Testing, #0 cm Developmental #5.

INTRODUCTION

The age of an animal when it encounters various types of
stimuli can contribute to its adult behavior. Early expe-
rience variables are related to the developmental state of
an animal's sensory systems at the time it receives the
stimuli. The resolving power of a sensory system can
affect the quality and quantity of stimulus input and thus
determine the quality of early experience which may shape
adult behavior. Species differences in behavior may be
partly due to differential patterns of sensory development
(King, 1961a).

Many adult behavior patterns are visually mediated, and
since early visual experience affects later behavior, it is
necessary to know the developmental pattern of visual acuity
(the resolving power of the visual system) in relation to
the develOpment of behavior.

The morphology of the visual system, which varies between
Species and with developmental state, can affect visual
acuity (Rahmann, 1967). The distance of the stimulus from
the eye also affects acuity because of limitations on accom-
modation and depth of focus imposed by eye structure (Walls,
1967). Since vision is based on light, acuity may be lim-
ited by the ambient illuminance (Riggs, 1965) and the light
gathering power of the eye (Walls, 1967). A comparative

deve10pmenta1 study of visual acuity, which includes the

manipulation of stimulus distance and ambient illuminance,
was needed to determine the relationship of these factors
to each other.

Comprehensive studies of this type have not been re-
ported. Most comparative studies utilize only adult sub-
jects and are made across broad phyletic lines (Rahmann,
1967). Comparisons of relatively closely related species
are needed in studying the evolutionary effects of various
ecological factors on vision and its development. The
single comparative develOpmental study to date (Ordy,
Latanick, Samorajski, and Massopust, 196A) only used small
numbers of animals from several primate genera. Their
study had the additional disadvantages of a longitudinal
type of design (which may confuse testing experience with
develOpment) and lack of any indication of variability in
the reSponses. Weymouth (1963) points out the need for
indications of variability in visual acuity and statistical
analysis of the data for evaluating the vision of a group
or species. While most animals lack visual accommodative
mechanisms (Walls, 1967), no work on the development of
visual range in this type of animal has been reported. The
effects of illuminance levels on visual acuity in human
beings and other diurnal animals have been well shown
(Rahmann, 1967), but only two studies have been done on noc-
turnal animals (Rahmann, Rahmann, and King, 1968; Neuweiler,

1962).

The primary aim of this study was to describe the visual
acuity and development of acuity in two relatively closely
related Species of nocturnal rodents and to experimentally
determine the effect of stimulus distance and illuminance
on visual acuity in the develOping animals. By using a
cross-sectional design, measuring acuity with relative pre-
cision, and indicating the variability of response, this
experiment was meant to provide a more accurate analysis of

development of visual acuity than was previously available.

LITERATURE REVIEW

Definition and Methods of Measurement

Visual acuity is the capacity to resolve details of
objects in the visual field, specified in terms of some
critical measurement of the stimulus objects. Acuity is
the reciprocal of the angle (in minutes of arc) subtended
at the eye by this critical measurement (Riggs, 1965).

Four major types of visual tasks are used to measure
visual acuity. For humans these are described as:

1. detection - detection of a test object in the visual
field: 2. recognition - name test object or name or spe-
cify some critical aspect of it; 3. localization (or
vernier acuity) - discrimination of small displacements of
one part of the test object with respect to other parts:
a. resolution (or simple discrimination) - response to a
separation between elements of a pattern (Riggs, 1965).
The resolution task has been used most often to test
visual acuity of non-human animals because it can gener-
ally be determined more easily by objective behavioral
responses.

Tasks 1, 2, and 3 provide a measurement of the minimum
visible, the smallest single object or feature which can
be seen. Resolution provides the minimum separable, the

minimal distance between two visual objects (i.e. two points

or lines) which can be discriminated as separate. In
both cases the angle subtended at the eye by the critical
measurement is defined as the minimum visual angle (or
visual angle) in degrees, minutes or seconds of are. It
is a measure of the maximal resolving power of the eye
being tested (Rahmann, 1967). In most cases minimum
visible angles are smaller, indicating better acuity for
these types of tasks, than minimum separable angles.

Four objective behavioral measures of visual acuity
have been described: 1. Visual cliff (Walk, 1965):
2. Visual preference or fixation (Fantz, Ordy, and Udelf,
1962); 3. Simultaneous discrimination (Lashley, 1930;
Rahmann, 1966); A. Optokinetic response (Warkentin and
Smith, 1937: Reinecke and Cogan, 1958; Suthers, 1966).
The visual cliff and discrimination methods require ambu-
latory abilities which are often poorly deve10ped in young
animals. Discrimination also can confound sensory deve1-
Opment with discrimination learning. Visual fixation
requires close restraint of the animal, a method of deter-
mining pupil position, and relatively high arousal or
attention levels, all of which make the method difficult
to use in many Species.

The Optokinetic response is a reflex visual response
to a moving visual field. The nystagmus consists of two

phases: 1. a slow or pursuit phase in the direction of

stimulus movement: 2. a fast or return phase opposite in
direction to stimulus movement. The eyes, head and body
may exhibit the response (Smith and Bojar, 1938).

The Optokinetic response was chosen for this study be-
cause it involves a discrete motor response which is well
deve10ped at the age when vision becomes functional (Ordy,
Massopust and Wolin, 1962; Vestal and King, 1968). It has
been used in other developmental studies of visual acuity
(Warkentin and Smith. 1937: Ordy gt a1, 1962; Ordy gt a1,
1964). Results from human beings indicate a high correla-‘
tion between acuity values found by the Optokinetic method
and values from standard Snellen tests. However, the Opto-
kinetic visual angles were consistently larger than results
from Snellen tests (Reinecke and Cogan, 1958). Wolin and
Dillman (196A) used a different Optokinetic method with
human adults and also found a high correlation with the
Snellen method. Their results showed relatively smaller
Optokinetic visual angles for subjects with poorer acuity.
Fantz gt_a1 (1962) compared visual fixation and Optokinetic
tests in human infants. The results corresponded closely
at most ages with lower Optokinetic thresholds at one to
two months of age.

The principal objection to the use of this response as
a test for acuity is that in animals with foveate retinas,
the periphery of the retina contributes more to the response

than the foveal area. Tests of peripheral vision will show

a lower value of acuity than tests involving primarily the
fovea (Riesen, 1960; Riggs, 1965; Rahmann, 1967). The above
comparisons suggest that this is not a valid criticism.

This problem can be avoided by testing subjects without
foveate retinas. Although the Optokinetic response can pro-
vide the minimum visible angle (Smith and Warkentin, 1939),
it is usually used, as in this study, to find the minimum

separable angle (Smith and Bojar, 1938).

Factors Governing Visual Acuity

Various factors affecting visual acuity are reviewed for
human beings by Riggs (1965) and Lit (1968) and on a compar-
ative basis by Walls (1967). Three of these factors, mor-
phological structure, stimulus distance, and light inten-
sity, will be discussed here, primarily as they have been
studied in rodents and as they apply to the present study.

Morphological structure may limit the maximal visual
acuity of a species. The fineness of the retinal mosaic,
both in size and density of visual receptor cells and in
degree of nervous summation, may in many species be the
ultimate limiting factor (Rahmann, 1967). Acuity should
be best in that part of the visual field where the density
of receptors is highest and/or where there is less sum-
mation of receptors on ganglion cells and Optic nerve

fibers. Although rats and mice do not have retinal foveas,

there is a decrease in the ratio of rod nuclei per ganglion
cell (decrease in summation) from periphery to center in
the rat retina (Lashley, 1932). This would indicate the
possibility of higher acuity for images projected on the
central part of the retina and would explain the eye move-
ments seen in visual fixation in rats (Lashley, 1932).
With a homogeneous retinal mosaic there would be no need
of fixation movements. Retinal summation appears to be
greater in mice (63-89 rod nuclei per ganglion cell)
(Menner, 1929; Bucciante and DeLarenz, 1929, as cited in
Lashley, 1932) than rats which have ratios varying from
27:1 at the approximate center to 78:1 at the periphery.
Although the part of the retina from which mouse cell
counts were taken was not given, Lashley (1932) indicates
that on the basis of these counts visual acuity in the
house mouse must be poorer than in the rat.

Quality of the visual image is further affected by the
cornea, pupil Opening and lens. Walls (1967) discusses
the adaptation of mouse and rat eyes for nocturnal life.
Their almost Spherical lenses, along with the large cornea
and pupil, act to maximally brighten the retinal image in
dim light. Walls feels that this arrangement along with a
rather homogeneous retinal mosaic obviates the need for
eye movements by providing a wide field Of vision, although
rats and deermice exhibit distinct eye movements (Lashley,

1932: personal Observation).

I F

 

The morphology of the cornea and lens systems affect
visual image quality by focusing the image on the retina.
Shape and size of the lens, as well as its ability to accom-
modate, determine the range Of distances at which objects
will be seen most sharply (Rahmann, 1967). Mice have degen-
erate ciliary muscles indicating that they have probably
lost the ability to accommodate. They apparently have a
nearby focal point, and everything is in focus from there
to the eye (Walls, 1967). Lashley (1932) found Norway rats
to be very myOpic, with the sharpest focus of objects at
7.5 to 8 cm from the cornea. However, he felt that in such
a small diOptric system with relatively large functional
units in the retina there is considerable depth of focus
which permits nearly equal detail vision over a wide dis-
tance range, even without accommodation. Lashley could
view objects ranging from 15 mm up to 20 meters away in
some detail through the excised eye of an albino rat.
Rahmann, Rahmann and King (1968) indicate Optimal visual
ranges (a behavioral measure of focal length) for several
species Of deermice ranging from h.0 to 11.0 cm. However,
their method involved increasing stimulus distance without
corresponding increase in stimulus size. At greater dis-
tances the stimulus objects would be relatively smaller.
Thus their measure of visual range would be strongly af-
fected by the visual acuity Of the Species (Graham, McVean,
and Farrer, 1968) and is probably not a good measure of

actual Optimal focal length. The values should be larger

10

than those reported. All of the above evidence indicates
that nocturnal rodents such as rats and mice are rather
myOpic.

The range of detail vision can be tested by using sti-
muli subtending corresponding Visual angles at different
distances. Only a few species have been tested in this
way. Human infants accommodate very well from 5 to 20
inches distance (Fantz gt a1, 1962). Primates, such as the
rhesus monkey, have good accommodation and exhibit no dif-
ferences in acuity at 3 feet and 20 feet (Graham g3_al,
1968). Two cats tested by Smith (1936) had higher acuity
at 75 cm distance than at 50 or 100 cm. Walls (1967) indi-
cates that among mammals the extent of accommodation is
poor except in primates. Lashley (1932) was not able to
accurately determine the change in resolving power with
changes in stimulus distance in excised albino rat eyes.

Visual acuity is generally better under higher than
lower light intensities. In animals with mixed rod-cone
retinas, acuity plotted as a function of the logarithm of
light intensity generally follows a rising sigmoid curve.
The lower leg of the curve indicates rod function; the
rising portion and level part represent increasing stimu-
lation of cones. Rahmann(1967) reviews these results in
vertebrates. However, in the only acuity test of a noctur-
nal animal with an all rod retina (flying fox bat) where
light intensity was systematically varied, acuity merely

leveled off at the higher light levels used (Neuweiler,

11

1962). Results with deermice indicated that acuity was
somewhat better at the highest of 3 levels of illuminance
tested (Rahmann gt g1, 1968). In a nocturnal animal there
could be a possibility of dazzlement and consequent loss

of acuity. However, the human pupil appears to adapt to
Optimum apertures for acuity at different light intensities
(Campbell and Gregory, 1960) and since the rat has a good
pupillary reflex (Lashley, 1932), this effect could probably
be ruled out. The pupillary reflex in mice has not been
studied. The enlarged pupil at low intensities increases
optical abberations in the human eye (Riggs, 1965), but

the effect of this factor in eyes which have evolved for

function at low illuminance levels is not known.

Species Differences In Visual Acuity

Species differences in adult visual acuity have been
reviewed by Rahmann (1967) over a wide variety of verte-
brates. Polyak (1957) and Walls (1967) compared the visual
systems of vertebrates and discussed structural and func-
tional differences in visual equipment which may be the
basis of acuity differences. These structural and func-
tional differences have presumably evolved as the result
of different environmental demands on the animals, and
comparative studies of visual acuity can perhaps point out

some of these environmental demands. A primary reason for

12

doing comparative studies of vision is to help point out
the genetic basis for visual behavior. A major problem of
comparative studies has been with the use of widely diver-
gent phyletic groups which may obscure genetic factors
(King, 1968a). In recent years a few workers have begun
comparing rather similar forms and attempting to relate the
results to the life history of the animals. Cowey and Ellis
(1967) attempted this with rhesus and squirrel monkeys.
Suthers (1966) obtained approximate visual acuity scores
for 8 genera of bats but his results should be carried fur-
ther using much smaller stimuli. Comparative studies of I
rodents have not been extensive. Rahmann (1966) compared
the acuity Obtained by discrimination learning in 2 genera
Of lemmings. The best score for mountain lemmings (Lemmus
lemmus) was 36' of are at 6 cm distance and that of wood
lemmings (Myopus schisticolor) was 71' at 4 cm. Lashley
(1938) used a jumping stand discrimination test to Obtain
visual acuity values of 2A-35' for pigmented laboratory
rats (Rattus norvegicus) and 10 10' - 1° 20' for albinos.
Rahmann gt al's (1968) paper on adult deermice is the only
study to date on visual acuity of several closely related
species of mammals (see Table l for their results). The
results are not strictly comparable to those of the present
study because they used a discrimination learning technique.

They sometimes used the same stripe width at different

distances to Obtain different angles for testing. This

13

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procedure may confuse visual acuity with ability to accom-
modate (Graham gt a1, 1968). The four comparative studies
of visual acuity in rodents all used discrimination learning

techniques, and all tested only adult animals.

Development of Vision and Visual Acuity

Just as species differences in visual equipment affect
visual performance so does the stage Of development. The
ontogeny of visual parameters such as depth perception
(Walk, 1965b), visual preference (Fantz, 1965), sensori-
motor coordination (Hein and Held, 1967) and morphological
development (Samorajski, Keefe, and Ordy, 1965) have been
studied in some species (see also Riesen, 1960 for a review).
Visual acuity and the range of optimal vision should also
improve during development as the eye increases in size and
the neuromuscular systems mature (Rahmann, 1967).

Baerends, Bennema, and Vogelzang (1960) found a smooth
decrease in the minimum resolvable visual angle during the
development of the cichlid fish Aeguidens. However, devel-
opment may have been confused with learning in the discrim-
ination technique used. Warkentin and Smith (1937)
elicited Optokinetic responses to four sizes of stimulus
angles to demonstrate the gradual development of visual
acuity in kittens. The kittens required an average of
11.2 days after eye opening to develop a response to the

smallest angle tested, 11' of arc. Development of acuity

15

in rabbits seems to occur saltatorily rather than gradually
as in kittens. First appearance of the Optokinetic response
occurred at about the same time the cornea and lens became
transparent (Warkentin, 1937). Ordy gt g1 (1962) found that
in rhesus monkey infants visual acuity (Optokinetic test)
matured much more rapidly than did postnatal retinal dif-
ferentiation as determined by fundoscopic examination. Four
stimulus angles were used in the acuity test. Further
studies indicated that the rhesus reached adult levels of
acuity (1' of arc, discrimination technique) by 2 months of
age but again only four stimulus angles were used (Ordy gt I
g1, 1965). Morphological studies of the retina showed

that peripheral cones had completed ultra-structural devel-
opment at birth while foveal cones were structurally mature
by 2 months of age (Samorajski gt a1, 1965). The peripheral
develOpment apparently is correlated with maturity of the
Optokinetic response while foveal maturation would allow
adult performance in the discrimination test. Develop—
mental studies Of acuity in 4 genera of primate infants

and human infants indicated that rhesus and baboons matured
faster than a gibbon and an orangutan, and they all matured
faster than human infants. The data are not presented in a
form which can be compared readily to other studies (Ordy
gt a1, 196A). Some data on the development of acuity in
human infants and children are also available (Slataper,

1950: Fantz gt a1, 1962; Weymouth, 1963). Weymouth

l6

emphasized that good measures of variability are missing
from the data available on human beings, largely because
many of the data have been derived from various clinical
tests. The overall review of the visual acuity develOpment
studies found that they shared common problems. They gener-
ally involved very few subjects. Few stimulus angles were
used for testing, and they were of such sizes as to pre-
clude statistical analysis of the data. In addition, infor-
mation was not available for many important groups of
animals such as the rodents.

Little information is available on other aSpects Of
visual development in mice. DeRobertis (1956) has done
anatomical studies of rod ultra-structural develOpment

in Mus musculus. Dapson (1968) found develOpmental changes

 

in lens proteins of Mg§_which slowed or reversed at about
seven months of age. In several strains of Mug the eyes
Opened at 11-13 days of age, and a visual placing response
was first elicited reliably at 14 to 15 days (Fox, 1965).
Lens weight in Peromyscus leucopus increased rather
rapidly until about 25 days of age, but growth was not
measured past 30 days of age (King, 1965). While in rats
the iris and lens are reported to be cloudy at eye Opening
but clear in 2-3 days (Turner, 1935), no iris clouding has
been observed in deermice. Vestal and King (1968) found
that infant Peromyscus can exhibit an Optokinetic response

as soon as their eyes Open, indicating vision is functional

17

at that time. Clark's (1967) study on the vestibular sys-
tem is the only one available on another sensory system in
deermice. Young Peromyscus leucopus first exhibited nys-
tagmus responses to rotation at 11 days of age. There was
a 50% increase in number Of animals responding at 15 days

of age, and the response was mature at 23 days.

The Experimental Animal, Peromyscus

Two species of Peromyscus (deermice) were the subjects
of this study. The genus contains mice of varying degrees
of genetic relationship living in practically all types of
terrestrial habitats in North America. There are 57 species,
two of the most widely distributed being g. leucopus and 2.
maniculatus (Hall and Kelson, 1955; HOOper, 1968). Closely
related forms often differ markedly in morphology, behavior,
develOpmental pattern and natural history. This diversity
provides a basis for a comparative study of the development
of visual acuity. Peromyscus is nocturnal, with an all-
rod retina (Moody, 1929) and no fovea (Walls, 1967). The
large body of background information available on Peromyscus
enables this study to be related to other aspects of the
animal's biology (King, 1968b). Finally, large numbers Of
these animals are available for testing, allowing an esti-
mate of the population variability of this sensory char-
acteristic.

The experimental subjects were Peromyscus maniculatus

18

bairdi, the prairie deermouse, and E. leucopus noveboracensis
the white-footed mouse. Both are classified in the subgenus
Peromyscus, with maniculatus in the maniculatus species
group and leucopus in the leucopus species group (HOOper,
1968).
P. m. bairdi inhabits the Midwestern grasslands, prima-
rily well drained areas with rather sparse grass plant
cover. They apparently prefer more open habitats than those
with denser grass growth (Howard, 1959) and are rarely if
ever trapped in woodlands (Blair, 1940: Nicholson, 1941). P.
m, bairdi is primarily terrestrial in its habits (Howard,
1949). Horner (1954) found bairdi to perform like other
terrestrial forms in tests for semi-arboreal adaptations.
3.‘1. noveboracensis, although rather versatile in its
habitats, primarily inhabits upland mixed hardwood forests
of hickory and oak (Nicholson, 1941). It may range into low-
land forests in the absence of competing species and also
occurs in brushy areas (McCarley, 1963) and areas of rocky
outcrops (Rainey, 1955). Blair (1940) sometimes found

noveboracensis in the edges of fields around woodlots, and

 

Nicholson (1941) indicates that they prefer nest sites near
the edges of woods. ‘2. leucOpus tends to nest more often in
elevated than in ground level nest boxes (Nicholson, 1941:
Taylor and McCarley, 1963). This nesting tendency plus the
semi-arboreal types of behavior found by Horner (1954) indi-

cates that they are more arboreal in their behavior than P.

19

m. bairdi. Vision appears to be important to a scansorial
animal in negotiating its environment.

Morphologically bairdi is smaller than noveboracensis.
Adult bairdi range from 119 to 156 mm in total length and
10 to 24 g in weight (Burt, l957)(male mean 18.0 g, female
16.5 g, King, 1965). Adult noveboracensis range from 141-
195 mm long and weigh 12-31 g (Burt, l957)(male mean 22.9 g,
female 19.7 g, King, 1965). The eye lenses of adult
noveboracensis are much heavier (female mean 27.6 mg) than
those Of bairdi (female mean 18.2 mg) indicating a larger
lens (King, 1965). The E. m. bairdi lens is almost spher-
ical with a ratio of minimum/maximum diameter of 0.843, and
the total eye bulb weight is approximately 49 mg (from
Rahmann gt g1, 1968). NO lens shape data are available for
noveboracensis. The size and shape of the eye and lens are
important factors in visual acuity (Rahmann, 1967, Walls,
1967).

The two species resemble each other in their morpho-
logical develOpment. Ages at eye Opening in the mice used
in this study averaged almost the same for each species (12.8
:_1.1 days for noveboracensis and 12.9 :_1.1 days for bairdi).
Other workers have reported average eye opening ages in days
for noveboracensis of 13.0 (Layne, 1968) and 13.4 (Svihla,
1932) and for bairdi 12.1 (King, 1958 ), 13.0 (Vestal and
Huff, unpublished data) and 13.7 (Svihla, 1932). Weaning

age of bairdi can be early as 18 days (King, Deshaies and

20

Webster, 1963) while noveboracensis can be weaned by 19 days
of age (Layne, 1968). They are normally weaned by the
mother sometime after 22 days of age (Svihla, 1932). Layne
(1968) summarized growth data from several sources on these
two species. He found that in terms Of percentage of mature
weight at weekly intervals the two species are equal at one
week and four weeks of age with noveboracensis slightly
higher at two and three weeks. In noveboracensis body
weight is still increasing when lens growth levels off at
25 days of age (King, 1965).

The above data indicate a strong similarity in morpho-
logical growth in the two species during the ages covered
in this study. Morphological growth may affect vision by
its effect on the condition of the eye (Rahmann, 1967).

Layne (1968) reviews behavioral development in Pergmyscus,
and in such behaviors as righting, nipple clinging and vocal-
izations the two species have Very similar developmental
patterns. The young of the two species closely resemble
each other in morphological and behavioral development,
while the adult ecology and behavior patterns are very dif-
ferent. This indicates that the young mice may also have
similar patterns of sensory development which may become
different after the age of weaning and before the mice
reach sexual maturity.

Data on the eyes and vision of Peromyscus are rather

scarce. Some have been presented above. The eye balls are

21

almost spherical with wide corneas and almost spherical
lenses (Moody, 1929; Rahmann gt gt, 1968). Moody found the
ciliary process to be weakly deve10ped and apparently poorly
deve10ped iris muscles. He considered the eye to be of
seemingly fixed focus with only slight accommodation for
distance. Rods are the only visual elements in the retina Of
E. maniculatus racilis, and this is presumably the case for
other Peromyscus species. The short focal length indicates
that Peromyscus should be myopic (Moody, 1929). The reti-
nal composition of all rods is believed by Walls (1967) to
be designed more for sensitivity than acuity and to india I
cate that the mice should have relatively poor acuity.

Rahmann gt gt (1968) have the only study of visual acuity
in this genus. Some criticisms of their methods have been
noted above, and their results are shown in Table l. The
results do indicate the relative range of distance vision
and acuity for their testing situation. While 2. t.

noveboracensis was not tested, the other semi-arboreal

 

forms (2. californicus and E. m. gracilig have slightly
longer visual ranges than the more terrestrial forms(£. g.
bairdi, 3. floridanus, and E. polionotus). The best mini-
mum separable visual angle for the bairdi was 54' at all
three light intensities tested. Because Of the small num-
bers and methods of manipulation, no firm conclusions can
be drawn concerning the effect of distance and light inten-
sity on size of visual angle. The two semi-arboreal groups

had slightly better acuity than the terrestrial forms.

22

Horner (1954) in studying the climbing behavior of several
Peromyscus Species trained the mice to jump from one 0.7 cm
diameter rod to another under dim light. Using 0.7 cm as
the target size her best results would indicate a minimum
visible angle of 62' at 39 cm for 2. g, bairdi and 40' at

60 cm for E. t. noveboracensis. This experiment was not
designed to test vision, and the ranges are primarily the
result of jumping ability. While her mice did use kines-
thetic cues to some extent, it seems safe to assume the mice
cOuld see at least to the other rod. 0n the basis of
Rahmann gt_gt (1968) and Horner's (1954) results and the
assumption that a scansorial animal would need good acuity
at longer distances in negotiating its habitat, it could be
predicted that adult 2. t. noveboracensis would show better
acuity at longer stimulus distances than 2, m, bairdi. How-
ever, this difference may not be evident during early devel-
opment.

Peromyscus Species are also reSponsive to light inten-

 

sity, as indicated in discrimination tests by Moody (1929)
and King and Weisman (1966), and activity tests (Blair,
1943; Kavanau, 1967). The mice in Blair's test became
inactive when ambient illuminance was increased to 0.26 ft.
candles (2.8 lux) which is very dim for human eyes. Kavanau
(1967) found that activity onset and cutoff intensities
usually range from 0.129 lux to 2.5 lux for mice confined to

a running wheel. In Rahmann gt gt's (1968) eXperiment the

23

acuity Of the more terrestrial forms was either not affected
(3, m. bairdi) or was Slightly improved (2. polionotus) by
decreasing illuminance. The semi-arboreal P. californicus
and P. m. gracilis had better scores at higher than at lower
intensities (Table 1). The values Of Rahmann gt gt (1968)
are best individual results from the mice tested, and no
definite quantitative relationship to light intensity can

be determined. Presumably light levels would be higher in
the grassland where P. m. bairdi is found than in forests
where leaf cover is dense most of the year. For this reason
a forest species such as B. leucopus should be less affected
by low illuminance, but in view of Rahmann gt gt's (1968)

results the Opposite relationship could be predicted.

Aims of This Study

The general aim of this study is to describe the behav-
ioral develOpment of visual acuity in two ecologically dif-
ferent species of a common wild rodent. It is meant to be
an improvement over previous comparative and develOpmental
studies in several ways. Comparative studies of vision are
usually made across broad phyletic lines (Rahmann, 1967).
By comparing relatively closely related species which dif-
fer in their habitat utilization we may gain data which
will be useful in studying the evolutionary effects Of

habitat pressures on vision.

24

There have been problems in the measurement and
presentation of data in most developmental and comparative
studies of visual acuity. The visual acuity of a species
or group is Often given as the minimal angle or best indi-
vidual performance from the group tested, with no indica-
tion of the variation in the measure (Weymouth, 1963).

Some more recent studies with small numbers of animals do
indicate the variability in the response. This can be cor-
rected by using large numbers of animals Of varied parent-
age to provide a realistic sampling of the species being
studied. Another problem Of previous developmental studies‘
(Warkentin and Smith, 1937: Ordy gt gt, 1965) is the exclu-
sive use of longitudinal eXperimental design in which the
effects Of experience and develOpment are confounded. A
cross-sectional experimental design can eliminate the effect
of experience in the testing situation and provides data
more amenable to statistical analysis.

In most studies, both developmental and comparative, the
stimulus Sizes and gradation intervals are those that are
most readily available commercially (i.e. measured in fourths
or eighths of an inch). This practice has the effect Of
both limiting the precision Of measurement because there
are large differences in stimulus size and Of creating a
measurement scale with unequal divisions. In addition, the

same stimulus size may be used at different distances to

25

provide different stimulus angles, which confuses accom-
modation ability with acuity. By making the differences in
stimulus angles sufficiently small and of equal magnitude
over most of the range, and by making comparable stimulus
angles for each stimulus distance, the visual angle can be
measured separately. All of these changes will allow sta-
tistical analysis of the data. Finally, by controlled mani-
pulation of Species, age, distance and light intensity in
the same experiment, it will be possible to Show the rela-
tionships of these variables with each other.
The specific aims of this study were:
1. To describe the pattern of develOpment of visual

acuity in P. t. noveboracensis and P. m, bairdi. The adults

 

of the two species differ in morphology and ecology, but
their young are very similar in morphological and behavior
development. This study will help determine if there are
differences in sensory development or at what time during
ontogeny the Species may begin to differ.

2. To experimentally determine the effect of stimulus
distance on acuity during development. Peromyscus are ap-
parently very myopic so that acuity should be better at the
shorter distances. During early development the young mice
are apparently eXploring their immediate environment at
short range. The short range acuity Should be better

earlier than the long range acuity. The leucopus are more

26

arboreal in their habits than the maniculatus and may need
Sharper distance vision in scansorial behavior. If there is
a species difference in develOpment, leucopus should have
sharper vision than maniculatus at the longer distances.

3. To determine how the acuity of these nocturnal ro-
dents is affected by the ambient level of illuminance.
The available data is ambivalent. Because they are noc-
turnal animals with very sensitive eyes, it could be ex-
pected that their acuity would not be lessened signifi-
cantly by testing at low light levels where they can still
be observed by the eXperimenter. They may Show some daz~
zlement and loss of acuity at higher levels. If there is
a Species difference, leucopus Should have more acute vision
at lower light levels, in part because of larger absolute

eye size (determined by lens weight).

MATERIALS AND METHODS
Subjects

All mice used in this study were born and raised in the
breeding colony of the Michigan State University animal
behavior laboratory. All were recent descendants (first
to fourth generation) of animals wild-trapped in the vicin-
ity of East Lansing, Michigan.

One-hundred nineteen P. leucopus noveboracensis and 129
P. maniculatus bairdi were tested. Eleven of the leucopus
and one maniculatus were used in 2 eXperimental conditions,'
all others being used in only one. The ranking of the
scores of the second tests of these 12 mice Showed no
observable effect of previous testing so the results were
considered independent. The total number of independent
scores for each Species used in the statistical analysis
is 130.

The mice were housed in 6 X 6 X 11 inch long clear plastic
cages with wood chips and cotton bedding. Water and food
(Purina mouse breeder chow) were provided gg libitum.
Subjects were kept with their parents until weaning (21
days of age) and housed as a litter afterward until test-

ing was completed.
Apparatus

The Optokinetic device used to elicit the visual

27

28

response consisted of rotatable one-meter diameter wooden
disc powered through belt drive by a 1/8 horsepower rever-
sible, variable speed electric motor (Bodine Electric
Company). Concentric circular grooves were cut in the
wooden disc to hold upright sheet aluminum cylinders, 51 cm
high, of various diameters. The cylinders were interchange-
able to permit presentation of the various stimuli at dif-
ferent distances. Drums of radii 20 cm and 40 cm were used
primarily, with some preliminary tests run with a drum of

10 cm radius. The floor of the drum was painted flat black.

Illumination was provided by an incandescent lamp
mounted in a metal reflector above the center of the drum.
The light was diffused by Sheets of white bond paper.

Three light intensities were used: 0.4 foot-candles = 4.3
lux; 8.0 foot-candles = 86.1 lux: 80 foot-candles = 861.1
lux (conversion factor 10.764 lux = l foot-candle (Riggs,
1965). Illuminance levels were measured by placing the
probe of a light meter (Gossen Tri-Lux Foot Candle Meter,

P. Gossen Co., Erlangen, Germany) facing the light source

on the subject platform in the center of the apparatus.
Distance of light source, bulb wattage, and number of sheets
of paper used as filters were varied to provide the desired
light intensities.

The visual stimuli were interchangeable striped panels
lining the metal cylinder. Twenty-six X thirty-three cm
long photographs of vertical black and white stripes of
equal width glued to the top portion of a 51 cm wide Sheet

29

of heavy Kraft paper formed the panels. A panel of appro-
priate stripe width was constructed for each visual angle
tested at each distance. The angle subtended by each stripe
was calculated from the tangent formed by the distance of
the stripe from the center of the drum and width of the
stripe. Stripes for the 10 cm drum ranged from 35' of arc
to 126' of arc in 7' increments. For the 20 cm drums
stripes were used which ranged from 21' of arc to 140' in
7' increments and additional stripes subtending 231', 280'
and 326' of arc. Stripes for the 40 cm drum ranged from 14'
to 140' of arc in 7' increments and additional stripes of
203' and 266' of arc (Appendix 1). The lower limit in
stimulus angle at each distance was determined by the smal-
lest size of stripe which could be printed and mounted ac-
curately. A gray paper panel was used in control trials.
Subjects were restrained on a 12.5 X 10.8 cm gray wooden
platform mounted on a central shaft in the apparatus, inde-
pendent of cylinder motion (Figure 1). The platform was
30.5 cm above the floor of the drum during the 20 cm dis-
tance tests and 20 cm above the floor for 40 cm tests.
These heights enabled ready observation and insured that a
sufficiently large amount of the mouse's visual field was
filled with moving stripes to elicit a reSponse. Narrow
stripes 2.4 mm apart were glued on the platform to provide
a ruled background against which movements of the subject's

head could be viewed. The responses were recorded visually

30

 

Figure l. Mice on Platform in Testing Apparatus:
Top - half-cylinder covering subject:
Bottom - half-cylinder removed.

31

because the small Size of the animals precluded using
electronic recording apparatus.

Each mouse was restrained by taping its tail to a flat
piece of lead. Lateral and vertical movement was restricted
by a half-cylinder of lead placed over the body and resting
on the platform. The head and forequarters were free to
move. The center of the mouse's head between the eyes was
placed over the center of the drum. However, lateral move-
ments could carry the eyes 1-2 cm to either side of the cen-

ter.

Procedures

Mice from litters of 3 to 5 young were used. Where neces-
sary, litters were reduced to 5 young at birth. Beginning
at 10 days of age litters were checked once daily for eye-
lid separation by applying gentle pressure to the eyelids.
0n the day of eye Opening each mouse was toe-clipped for
identification and weighed to the nearest one-tenth gram.
No more than two mice from any litter were used in any
experimental cell: and if two were used, they were of Oppo-
site sexes.

At the time Of eye Opening each litter and mouse were
assigned a code number. Testing was scheduled only by code
number to avoid eXperimenter bias. Average age at eye
Opening for each experimental cell is shown in Table 2,

which also illustrates the overall design of the eXperiment.

32

 

nanomefl 2M u Hm

OSPOHSOAOOB am I am

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So o:

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M0

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Hm

so
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N0 N0
m.NH H.ma
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m.NH n.NH
m. n.
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M0 M0
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N0 N0
n.ma m.na
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33

At the time of testing mice were removed from the home
cage, weighed, restrained and placed in the apparatus. The
mice were given 1 - 2 minutes to adapt to the light inten-
sity. Testing began with stripes of the largest width for
the distance being tested. Rotation of the drum began when
the subjects were motionless or only moderately active, but
apparently alert. There was no fixed inter-trial interval
because it was essential to begin the trial when the mice
appeared attentive. Direction of rotation was reversed
for each trial. The mice responded to a wide range of
rotational speeds. If subjects did not respond during
the early trials, rotational Speed was sometimes changed
in an attempt to allow elicitation of the response.

Subjects were given eight trials of 15 seconds duration
with one stripe width unless they responded earlier. An
Optokinetic response was recorded for either: 1. one Clear
head movement in the direction of drum rotation (slow phase)
in which the head crossed 2 of the lines on the platform: or
2. two clear eye responses (slow and fast phases). The cri-
terion of response to a given stripe width was an Opto-
kinetic response during at least one trial in each direction.
This criterion was used to reduce effects of possible ob-
server error.

If a mouse reSponded to the larger stripes, smaller
stripes were inserted until the subject failed to reach

criterion. Stripe size was decreased in decrements of 14'

34

to 28' of arc. Once the mouse failed to reSpond, stripe
size was increased in increments of 7' Of arc until the
mouse responded again. The smallest stripe width to which
a subject responded was designated as its minimum visual
angle for the experimental condition.

Mice were observed during the intertrial intervals for
head waving movements which resembled Optokinetic responses.
If these were seen, the subject was discarded. Mice which
struggled constantly, failed to keep their eyes open,
"froze" and remained immobile, or failed to reSpond to the
largest stripes at the distance being tested were also
discarded.

Six mice were tested as controls with a solid gray drum
at 20 cm distance. Control tests for both maniculatus and
leuCOpus consisted of obtaining two clear reSponseS with
a striped drum, presenting 8 trials with the gray drum,
and again obtaining 2 responses with the stripes. Two
observers conducted these eXperiments. All control mice
responded to the stripes but none reSponded to the gray
panels. The control results, the reversibility of the
response, and the fact that there was a limit in the stripe
size below which a reSponse could not be elicited (a
threshold) indicate that the mice were responding pri-
marily to the experimental stimuli.

Observer reliability was calculated by the percentage
of agreement between two independent observers on presence

or absence of response during a trial. On 327 fifteen

35

second trials with 15 mice, there was 92.7% agreement

between observers.

Statistical Analysis

Each experimental cell contained results from 10 sub-
jects, 5 males and 5 females. Differences between results
of experimental cells were determined by the analysis of
variance and Duncan's New Multiple Range test (Li, 1964).
Most data met the assumptions for these tests, except in
some cases of lack of homogeneity of variance (F max-min
test, Bruning and Kintz, 1968). In these cases the data
were transformed to common logarithms before analysis,
serving to make the results approach homogeneity of var-
iance. Violation of this assumption would make the test
more conservative by increasing acceptance of the null
hypothesis (Li, 1964). Boneau (1960) finds that if sample
sizes are equal, meeting the assumption of variance homo-
geneity is not crucial to the results of the F-test of
the analysis of variance. The "t" test (Li, 1964) was
used to determine the age at which 40 cm results became
no different from the limit at 20 cm. Correlations of age
and weight at testing with visual angle were found by the
Pearson product moment correlation (Li, 1964).

The stimulus test angles were printed in intervals of
7' of are. For the analysis the visual angles were divided

by 7 to aid in calculation.

RESULTS
Pattern of Development

Preliminary tests at 10 cm stimulus distance indi-
cated that mice of all ages consistently responded to the
smallest stripe width available for that distance (35') from
the day of eye Opening. Accordingly, only 20 cm and 40 cm
radius drums were used for the other experiments.

At 20 cm distance 95% of the mice of both species res-
ponded to the smallest stripe width presented (21') by two
days after eye Opening (Table 3, Figure 2). Testing was
terminated at that time. The two species were not statisti-
cally different in their responses on day 0 but on day l
leucopus' mean visual angle was significantly smaller than
maniculatus'. Visual angle decreased significantly with age
(analysis of variance, Table 4). 2. leucogus' visual angle
decreased Significantly between days 0 and 1, and scores on
days 1 and 2 were not different (t-test, p>I0.05). 2.
maniculatus' scores did not decrease significantly until
between days 1 and 2 (t-test, p¢;0.05). Mice of both species
tested at 20 cm from 2 days to 6 days post eye Opening con-
sistently reSponded to 21' stripes.

At 40 cm distance 85% of the mice responded at the lower
limit of measurement (14') on day 6, and 90% responded on

day 8. The develOpmental patterns were Similar for the two

Species (Table 5, Figure 3) except that maniculatus had a

36

37

TABLE 3 DEVELOPMENT OF VISUAL ANGLE AT 20 CM DISTANCE

Days After Eye Opening

 

O 1 2
P. maniculatus mean 63.7 60.9 21.7
SE 6.5 11.8 0.7
P. leucopus mean 70.7 29.4 21.0
SE 11.1 7.6 0.0

a Scores in minutes of are

n = 10 per cell

38

8H1 -——- E; maniculatus - MeaniSE
77- ---- P;_leucopus - MeaniSE

 

 

 

Limit of Measurement

Visual Angle in Minutes of Arc

”I

7—

 

 

' I I

0 l 2
Days After Eye Opening

Figure 2. Development of Visual Acuity, 20 cm Distance

39

TABLE 4 ANALYSIS OF VARIANCE OF VISUAL ANGLE
AT 20 CM DISTANCE

Source DF MSS F

Day 1 99.281 4.88 p<0.05
Species 1 30.6 1.50

Day X Species 1 12.7 <1.

Error 36 20.3

Total 39

a Scores in visual angle in minutes/7

 

 

Species P.1eucogus P.maniculatus P.maniculatus 2,1eucopus
Days After
Eye Opening 0 0 l 1

Mean in minutes
of arc 29.7a 63.2 60.9 29.4

a Means not connected by common underline are different
at pI<0.05, Duncan's New Multiple Range Test.

no

N.:
N.mH
N.#
N.wH

0.: 0.0 0.5 m.m H.m 2.35
0.0a 0.0m 5.05 0.55 0.Hm «.05H

0.0 5.0 0.0 0.~ ms.s H.0H
s.- s.0m ~.mm 5.50 0.05 5.55
O m 0 m m H

wcwcomo ohm nopm< when

Moz<BmHQ So 03 B¢_mgoz< H<DMH> mo ezmzmoam>mm

one mo novscfis ca uohoom O

HHOO pom OH I c

m.mH mm
m.H- ewes mmmmmmmw 2M

0.0H mm
mo.nma ewes uifldflflflflfldflzm
o

m mam<e

41

 

\
\
\
‘~ I
\‘ -———- P. maniculatus
\
\ ----- P. leucopus

 

Limit Of Measurement

 

2u5

1

210-

140.

70.

63-

.§ 55-

49-
L...
O

m u2-
Q)
S

c 35‘
-H
E

c 28-
-a
(I)
H
00

E 21-
H
I'D
:3
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'H

> 1n

‘3 -I
M
(1)
2
b0
0
,_]

7

 

I I I I r I

0 1 2 3 u 5 6 7 ' 8
Days After Eye Opening

Figure 3. Development of Visual Acuity, 40 cm Distance

42

significant decrease in visual angle between days 0 and 1
while leucopus' scores first decreased Significantly one
day later (Tables 6 and 7). This relationship is the re-
verse of the results at 20 cm. There were significant
decreases between days 4 and 5 and between days 5 and 6 in
both species. The increase in weight of the experimental
animals (Figure 4) was not comparable to the 9 to 12-fold

decrease in mean visual angle.

Effect of Stimulus Distance

Stimulus distance had a strong effect on acuity scores
in both species as indicated by the above results (Table 8).
Because of the rapid decrease in visual angle to the limit
of measurement at 20 cm, only results from days 0 and l
were compared statistically between the two distances. The
maniculatus 40 cm - 0 day group had a Significantly larger
visual angle than the other three maniculatus groups (Table
9; analysis of variance and new multiple range test, p<0.005).

The maniculatus 40 cm - 5 day group had significantly lar-

 

ger visual angles than the 20 cm limit of 21' (t-test,
p<I0.05), but the 40 cm - 6 day group was not Significantly
different (t-test, p>'0.05). Nine of the ten mice in the
20 cm - 2 day group reached the limit of 21'.

Mean visual angles of leucopus at 20 cm - days 0 and l
were significantly smaller than the 40 cm scores (Table

10: analysis of variance and new multiple range test,

43

TABLE 6 ANALYSIS OF VARIANCE OF VISUAL ANGLE
AT 40 CM DISTANCE

Source DF MSS F

Days 7 2.8223 74.263 p< 0.001
Species 1 0.280 7.368 p< 0.001
Day X Species 7 0.090 2.368 p< 0.001
Error 144 0.038

Total 159

a Scores in loglo of visual angle/7

44

TABLE 7 SPECIES AND DAY DIFFERENCES IN
MEAN VISUAL ANGLE, 40 CM DISTANCE

 

 

Species Days Post Mean
Eye Opening
P1a 0 1.493b'c
P1 1 1.363
Pm 0 1.348
P1 2 1.059
pl 3 1.032
Pm 1 0.998
Pm 2 0.991
pm 3 0.984
P1 4 0.964
Pm 4 0.831
Pm 5 0.649
P1 5 0.612
Pm 6 0.419
P1 6 0.366
Pm 8 0.361
P1 8 0.361

 

a P1 = P. leucogus: Pm = E, maniculatus
b Scores in loglo of visual angle/7

0 Means not connected by common line are different at
p< 0.05, Duncan's New Multiple Range Test

45

-—- P. maniculatus - MeaniSE

 

-1"- P. leucopus - MeantSE

 

 

11.0 ‘
1000 '1 I
9.0,
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55
go 8.0-J
C‘.
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12
00 7.0..
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(D
3
>5
8
m 6.0 -
:1
5.0

 

I l I T l r I l T

0 l 2 3 4 S 6 7 8
Days After Eye Opening

Figure 4. Weight at Time of Testing, 40cm Developmental

TABLE 8

Distance

2. maniculatus

 

20
40

P. leucogus

20
4O

46

EFFECT OF DISTANCE ON VISUAL ANGLE

cm

cm

cm

cm

Days After

0
63.7 i‘. 6.63 60.9
163.0 116.6 77.7

70.7 3111.1 29.4
221.8 113.5 179.2

a Mean t_S.E. in minutes of are

1'!

10 per cell

Eye Opening

[—4

t 11.8
+ 10.1

I; 7.6
124.4

21.7
70.0

21.0
81.9

0.7
4.4

0.0
5.1

47

TABLE 9 EFFECT OF DISTANCE ON VISUAL ANGLE, _E. maniculatus

Analysis of Variance

Source DF MSS F

Distance 1 396.981 13.9 p < 0.005
Days 1 688.9 24.1 p< 0.005
Distance X Days 1 348.1 12.2 p < 0.005
Error 36 28.6

Total 39

a Scores in visual angle/7

Distance and Day After Eye Opening

20 cm-Day l 20 cm-Day 0 40 cm-Day l 40 cm-Day 0
60.98"b 63.7 77:2 163.0

a Mean in minutes of arc

b Means not connected by underline are significantly dif-
ferent at p<0.05, Duncan's New Multiple Range test.

TABLE 10 EFFECT OF DISTANCE ON VISUAL ANGLE, E. leucopus

Analysis of Variance

Source DF
Distance 1
Day 1
Day X Distance 1
Error 36
Total 39

a Scores in visual angle/7

Distance and Day After Eye Opening

20 cm-Day 1 20 cm-Day O
29.481:b 704

a Mean in minutes of arc

mss F
3605 7.4 p<0.01
4623 94.4 p< 0.01
0 <1
49

4O cm-Day 1 40 cm-Day 0
179.2 221.9

b Means not connected by common underline are significantly
different at p<L0.05, Duncan's New Multiple Range Test.

49
p<.0.01). The leucogus 40 cm-4 day group mean was Signi-
ficantly larger than the 20 cm limit of 21' (t-test,
p<:0.05) but the 40 cm—5 day mean was not significantly
different (t-test, p>’0.05). All the leucopus at 20 cm-

2 days reached 21'.

Effect of Light Intensity

The three light intensities used in this study had no
effect on mean visual angles (Table ll)(ana1ysis of vari-
ance, p>'0.05). Illuminance levels lower than 4.3 lux

could not be used because responses were visually recorded.‘

Other Variables

Because detail vision is not possible before the eyes
open, the age in days after eye opening was used as the
controlled variable for maturation. However, visual angle
was also correlated to the chronological age at testing
and weight at testing. For maniculatus the correlation
was r= -0.6924 and for leucopus r= -0.8240 with chronolo-
gical age (p<L0.001, Pearson Product Moment Correlation).
The correlation with weight at time of testing was
r= -0.6203 (pICO.OOl) for maniculatus and r= -0.4059
(p<:0.01) in leucopus. The negative correlations corres-
pond to the decrease in minimum visual angle with maturation.

Mean values of age at testing and weight at testing for

50

TABLE 11 EFFECT OF ILLUMINANCE ON VISUAL ANGLE
AT THREE DAYS AFTER EYE OPENING

 

Illuminance P. maniculatus P. leucopus
(lux) mean SE mean SE
4.3 70.78 3.4 63.7 6.3
86.1 67.9b 2.6 77.0b 6.3

861.1 60.9 7.7 74.9 2.1

a Visual angle in minutes of arc
b Same data as 40 cm developmental

n=10 per cell

51
each experimental cell are given in Tables 12 and 13 res-

pectively.

Behavioral Observations

The experimental situation appeared to be noxious to
many of the mice in that it involved restricting their
movements and placing them in an eXposed situation on top
of a lighted platform. Approximately 13% of all the
maniculatus and 6% of all the leucopus placed in the
situation struggled so violently that testing was impos-
sible for them. Of all the maniculatus placed in the
apparatus 17% exhibited an immobile or"freezing" response
while only 4% of the leucopus did so. While in this state
the mice had their eyes open but were limp and unresponsive
to such stimuli as shaking, loud noises, light flashes and
electric shock. When replaced in the home cage they immedi-
ately returned to apparently normal behavior. 3.

maniculatus showed an increasing incidence of this response

 

with age, ranging from 18% at 4 days up to 62% at 8 days

after eye opening.

52

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DISCUSSION

Both Species had an unexpectedly small visual angle at
a relatively early age. The mean of 18.9' of arc of leucogus
at 6 days and the mean of 18.2' of both species at 8 days is
smaller than any visual angle yet reported for a rodent
(Rahmann, 1967). Nine of 10 mice of both leucopus and
maniculatus responded to 14' angles at 8 days after eye
opening. Since the Species values in the literature are
usually the best result of any individual of that species,
the 14' value indicates much better acuity than other rodents.
An alternative explanation is that this testing method is
more sensitive than others which have been used. Because
almost all of the mice in the terminal age groups reSponded
at the equipment limits of 21' at 20 cm and 14' at 40 cm, it
seems safe to postulate that the adult threshold visual
angle of these two species is smaller than 14'.

One of the criticisms of the Optokinetic method has been
its relative insensitivity for animals with retinal foveas.
Part of this criticism may be justified but much of it may
be due to the labor and difficulty involved in constructing
suitable test stimuli for this response. This method ap-
pears to be at least more sensitive than the simultaneous
discrimination method of Rahmann gt_gt(l968) for Peromyscus.
This is in spite of the indication that at least in human
beings, acuity is lower for single moving objects than for

non-moving stimuli (Ludvigh, 1948). Peromyscus appear to

54

55

be very responsive to movement. Perhaps because of their
sensitivity to movement the mice were more attentive to the
moving stimulus. In addition, the Optokinetic response is
reflexive while discrimination requires a more general vol-
untary body response. By eliminating the factors associated
with the more general response, a closer approximation of
the threshold of acuity may be reached.

The effect of stimulus distance was great enough to
produce a different pattern for each distance. At 10 cm
both species responded to the smallest stripe available (35')
from the day of eye opening. In the 20 cm tests both spe-
cies reached the limit of 21' by 2 days after eye opening.l
There was a significant decrease in leucopus' mean visual
angle between day 0 and day 1, one day earlier than for

maniculatus. At 40 cm the first significant decrease in

 

scores occurred at the same time, but maniculatus' decreased
one day earlier than leucOpus'. From day 2 the curves were
essentially parallel, and corresponding days were not sig-
nificantly different through 8 days after eye Opening. The
difference in order of decrease at the two distances on day
1 may possibly be explained by slight differences in the
relative ages and weights at testing of the four groups in-
volved (Tables 12 and 13). The Species groups with smaller
visual angles were Slightly heavier and slightly older than
the groups with larger visual angles. Determination of the

threshold of minimum separable acuity at maturity in these

56
species may contribute to the understanding of the effect
of environmental selection on the pattern of visual acuity
develOpment.

The overall developmental pattern for these two species
is that of more rapid development of acuity for nearby
stimulus objects than for those farther away. At 10 cm dis-
tance mice of all ages could see 35' stripes. At an aver-
age of 13 days of age (day of eye Opening) the mice averaged
visual thresholds of 63' to 70' at 20 cm and on 2 days after
eye opening (average 14 days of age) 19 of 20 responded to
21' stripes. The 40 cm group of maniculatus averaged 163'
and leucopus averaged 222' thresholds at 13 days of age
(day of eye opening). The pattern of change at 40 cm Shows
a rapid decline in mean angle from 1 to 2 days after eye
Opening (14 to 15 days of age), a leveling off period from
3 to 4 days (16 to 17 days of age) and then a further rapid
decline in size. By 5 days after eye opening (17.6 days of
age) the 40 cm leu00pus average angle is not different from
the day 2 average at 20 cm (21' limit), while the maniculatus
40 cm - 6 day group (18.7 days) is not different. This
indicates that development of acuity at 40 cm is at least
3 to 4 days behind that for 20 cm. By 19 to 21 days of
age most of the individuals of both Species respond to the
14' stripe limit at 40 cm.

The adult threshold acuity values at all distances are

undoubtedly better than the limiting values imposed by the

57

equipment limits of this experiment. Almost all mice in
the terminal age groups reSponded to the smallest stimulus
stripes available. In addition, morphological and sensory
develOpment is still going on after 19 to 21 days of age.
The young mice are not normally weaned by the mother until
22 to 30 days (Svihla, 1932) and leave the home area even
later (Howard, 1949). Lens weight in leucogus increases
rapidly until about 25 days (King, 1965). Post-rotatory
nystagmus, a response indicating vestibular system function,
is mature at 23 days of age in leuOOpus. Adult-like habitu-
ation of this response develOpS even later (Clark, 1967).
ngomyscus leucopus and P. maniculatus should reach the
adult threshold of visual acuity by 25 to 30 days of age.
The 9 to 12 fold improvement in mean visual angle with
age at 40 cm is almost certainly not due to the development
of an accommodation mechanism. According to Moody (1929),
Lashley (1932) and Walls (1967), rats and mice have very
poorly developed ciliary muscles and fibers which would
be necessary for accommodation. Walls (1967) states that
small lenses have a short focal length and great depth of
focus. In addition, the receptor cells are the same Size
as in larger eyes. This means that there will be rela-
tively less lateral and longitudinal movement of the reti-
nal image of a moving object than in a larger eye. Thus
small-eyed animals have less need of accommodation because

objects will be in focus over a longer distance. The change

58
in Peromyscus visual response to stimulus distance can
perhaps be explained by developmental changes in eye mor-
phology. There may be a flattening of the shape of the lens,
so that the commencement point or far point of fine focus
moves out from the eye. There may be a change in the Shape
of the eyeball so that the focal point within the eyeball
changes. A third possibility is that morphogenesis of the
rods may be going on during this developmental period.
DeRobertis (1956) finds that differentiation of retinal rods
in white mice (Mus musculus) was complete by 12 to 16 days
of age while the eyelids Opened at 12 to 13 days. In his
mice reorientation of the rod sacs to the adult form began
in the middle of the outer rod segment and Spread to either
end. Tokuyasu and Yamada (1959) found that in kittens rod
differentiation included elongation of the primitive rod
cells followed by appearance of the primitive rod sacs
first at the distal end of the cell and later development
in the proximal end. If this rod elongation and differen-
tiation is going on in Peromyscus at the ages studied in
this eXperiment, it might cause a change in the thickness of
the sensitive part of the retina. This could be a partial
explanation for the change in depth of fine focus. The
total effect of the interacting changes in eye morphology
could account in large part for the change in depth of
focus.

The distances of optimal acuity reported for rodents

59
range from 4 to 11 cm (Lashley, 1932; Rahmann, 1966:
Rahmann gt gt, 1968). The visual angles of young Peromyscus
at 20 cm and 40 cm are smaller than those of adult animals
in the above studies. Systematic determination of adult
acuity thresholds over several stimulus distances will be
necessary to accurately delineate the range of fine focus
in Peromyscus.

To determine the effects of light intensity, mice were
tested at three days after eye opening because a true aver-
age threshold of acuity could be found at that age. The
results can best be compared to Rahmann gt_gt (1968) who
used intensities of 1.08, 10.8, and 107.6 lux (see Liter-
ature Review). I used here levels of 4.3, 86, and 861 lux.
The two eXperiments together cover a range of intensities
from 1 to 861 lux but Show no statistically reliable dif-
ferences in response at different illuminance levels. This
indicates a wide range of adaptability to light level in
these nocturnal animals. We have not developed methods of
adequately recording Optokinetic reSponseS when the illumi-
nance is very low such as that under moon light (0.13 lux
to 0.25 lux, Kavanau, 1967). Laboratory studies indicate
that Peromyscus is most active under these very low illumi-
nance levels (Blair, 1943; Kavanau, 1967) so that these are
the light intensities under which detail vision might
normally be used.

The use of days after eye Opening as the indicator of

60

visual maturation seems well justified by the results.

Age at time of testing and weight at testing are also signi-
ficantly correlated with visual angle. Since all three
factors are measures Of maturation, this is not unexpected.
Because the age at eye opening is variable and the mice can-
not see before eye opening, days after eye opening still
appears to be the best indicator of visual maturity for use
with young mice.

The striking change in the percentage of immobility
("freezing") reSponses in P. m, bairdi coincides with the
significant decreases in visual angle at 4 to 8 days after
eye opening (17 to 21 days of age). The tendency to I
"freeze" in strange or noxious situations appears to be a
definite subspecific characteristic of P, m. bairdi and has
been noted in other eXperiments (King, 1961b: King, Price
and Weber, 1968). King gt gt (1968) also note a tendency
for adult P. leucogus to remain immobile in strange Situ-
ations. Since the young 3. leucopus in this eXperiment
showed a low incidence of this response, the characteristic
must develop later than in P, m. bairdi.

Several types of further research are suggested by the
results of these eXperiments. The use of very narrow
Single lines for finding minimum visible acuity with an
Optokinetic device offers a means of determining the adult
threshold of response and tracing the full pattern of

visual acuity development in Peromyscus.

61

The visual system of Peromyscus is functional at eye
Opening but there is definite improvement in acuity and
compensation for distance with increasing age. What are
the relative contributions of visual eXperience and physical
maturation to this improvement ? Vestal and King's (1968)
results with the first Optokinetic responses in an early
eye Opening strain of P. m, bairdi indicate that the oppor-
tunity for visual experience did not Speed up the first
appearance of the response. Once the visual system is func-
tional however, practice may play a more important role in
perceptual develOpment. Two types of studies would bear on.
this problem. One is the use of deprivation experiments
after eye Opening to determine the effect of eXperience.
Another is an anatomical study of development of the size
and shape of the eye bulb, cornea, lens and retinal micro-
and ultra-structure. The patterns of relative morphological
change during the developmental period may provide the basis
for the changes in acuity and visual range.

P. leucopus and E, maniculatus develop relatively good
acuity at an early age. We do not yet know the age at
which the mice begin to visually explore their surround-
ings and actually venture out of the nest. Determination
of the develOpment of early locomotory and exploratory
behavior may allow predictions of the possible usefulness

of this acute vision to the young mouse in its particular

environment.

SUMMARY AND CONCLUSIONS

1. The best visual acuity value measured for individual
3. leucopus and P. maniculatus was a minimum separable
visual angle of 14' of are at 40 cm stimulus distance.

One individual of each species reached this value by four
days after eye opening. The best average acuity for each
species was a visual angle of 18.2' of are at 40 cm, 8
days after eye Opening. The 14' stimulus stripes were the
smallest available for testing. Peromyscus has the smal-
lest visual angle of any rodent studied to date. This
result may be due to greater sensitivity of the testing
method used in this experiment.

2. P. leuCOQus had a significant decrease in visual
angle one day earlier than maniculatus at 20 cm. P.
maniculatus' average decreased one day earlier at 40 cm.
The differences may possibly be explained by age and
weight differences between the eXperimental groups. The
groups with smaller visual angles were slightly older and
heavier than the comparable groups with larger visual
angles.

3. Visual acuity improved significantly with age. The
mean visual angle of maniculatus at 40 cm decreased approxi-
mately 9-fold between the day of eye Opening and eight days
afterward while leucopus' mean decreased approximately 12-
fold. This sensory system matures at a faster rate than

body weight.

62

63

4. The pattern of results during development was sig-
nificantly affected by stimulus distance. At 10 cm dis-
tance all mice responded to the smallest stimulus of 35'
of are on the day of eye opening. At 20 cm 19 of 20 mice
reached the 21' limit by 2 days post eye Opening. At 40
cm 17 of 20 individuals reached the limit of 14' by 6
days after eye Opening. Acuity for stimuli at 20 cm
develops earlier than for stimuli at 40 cm.

5. Mean visual angles of both Species at 3 days after
eye Opening were not significantly different under illumi-
nance levels of 4.3 lux, 86.1 lux and 861.1 lux. All
developmental tests were conducted under 86.1 lux. These
nocturnal animals exhibit a wide range of adaptability
to light intensity level.

6. Size of visual angle was significantly and nega-
tively correlated with body weight at time Of testing and
chronological age at the time of testing in both species.
The number of days since eye Opening still appears to be
the best indicator of maturation for studies of visual
develOpment in young mice.

7. Elicitation of the Optokinetic reSponse is suitable
for developmental studies of visual acuity in rodents.
Use of the minimum separable task appears to be limited to
very early ages, and another acuity task must be used to
determine adult thresholds.

8. The frequency Of occurrence of the "immobility"

64

response by maniculatus in the experimental situation
increased with age after eye opening. 2. leucopus did
not exhibit this response as often as maniculatus. The
response appears to mature later in leucopus than in

maniculatus.

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APPENDIX

71

APPENDIX 1

WIDTH OF TEST STRIPES IN MM

Visual Angle Stimulus Distance

10 cm 20 cm 40 cm
14' X X 1.6
21' X 1.2 2.4
28' X 1.6 3.2
35' 1.0 2.0 4.0
42' 1.2 2.4 4.8
49' 1.4 2.8 5.6
56' 1.6 3.2 6.4
63' 1.8 3.6 7.2
70' 2.0 4.0 8.0
77' 2.2 4.4 8.8
84' 2.4 4.8 9.6
91' 2.6 5.2 10.4
98' 2.8 5.6 11.2
105' 3.0 6.0 12.0
112' 3.2 6.4 12.8
119' 3.4 6.8 13.6
126' 3.6 7.2 14.4
133' X 7.6 15.2
140' X 8.0 16.0

203' X X 23.2

72

APPENDIX 1 ( cont'd )

231' X 11.2 X
266' X X 30.2
280' X 16.0 X
326' X 19.0 X

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