Visual acuity and ERG-CFF in relation to the morphologic organization of the retina among diurnal and nocturnal primates

Vision

Rcr.

Vol.

8. pp.

1205-1225.

I’ergamon

I’rcrs

1968.

Prinlcd in Great Rrilain.

VlSUAL ACUlTY AND ERG-CFF IN RELATION TO THE MORPHOLOGIC ORGANIZATION OF THE RETINA AMONG DIURNAL AND NOCTURNAL PRIMATES’ J. M. OI~DYand T. Cleveland

Psychiatric

SAMORAJSKI

Institute and School of Medicine. Western Reserve University, Cleveland, Ohio (Received 29 May 1967; it1 revised form 12 March 1968) INTRODUCTION

ADULT human subjects have a minimum separable visual acuity of 1 min of arc, usually

designated as 20/20 in the Snellen notation (DUKE-ELDER,1962). Studies with chimpanzees (SPENCEand FULTON, 1936), rhesus monkeys (WEINSTEINand GRETHER,1940; KL~~VER, 1933; WEISKRANTZ and COWEY, 1963; ORDY ef al., 1965) and with cebusrnonkeys(W~~~~, 1942) have shown that higher diurnal primates have acuity thresholds ranging from 0.21 to 1.95 min, making them comparable to human subjects. However, within the primate order, data on acuity and visual learning capacity in relation to the morphologic organization of the retina and visual pathways and centers of the brain are particularly fragmentary for tree shrews, lemurs, galagos and marmosets (ROHEN,1964; v. CASTENHOLZ, 1965). Since acuity and the organization of receptive fields within the retina have not been examined in greater detail in lower nocturnal primates, comparative studies have simply implied that high acuity and color vision in diurnal primates are most clbsely associated with cones and the differentiation of a fovea (WOLLARD,1927; KOLMER,1930, 1936; DETWILER,1939, 1943; POLYAK,1957). Although ERG responses have not been related to acuity or specific regions of the retina, a widely applied technique for segregating the temporal response characteristics of photopic, scotopic, and mixed photoreceptor systems among diurnal and nocturnal species has been the ERG critical flicker frequency (ERG-CFF). Depending on the light intensity and the rod to cone ratio of the retina, the ERG-CFF has been estimated from 3 lo 143 fl/sec among vertebrates (DODT and WIRTH, 1953; DODT, 1954). It has been proposed that an avascular region in the temporal retina may be associated with the development of high acuity among primates (POLYAK,1957; CLARK, 1960; WEALE, 1966). However, knowledge on retinal topography of the temporal region of the eye among lower primates is still fragmentary. Since physiological studies have suggested that many functions attributed previously to photorcccptors may bc more closely associated with the neural network of the retina (GLEZER, 1965), more recent observations on the morphology of the retina have been directed toward the description of synaptic linkages of photoreceptors to bipolar and ganglion cells (COHEN, 1965; DOWLINGand Boycon, 1 Part of these experimental findings were prescntcd at the “Fine Structure of the Retina, U.S.-Japan Seminar”, Sept. 8-10, 1966, at Fukuoka, Japan, sponsored by the National Science Foundation, U.S.A., and the Japan Society for the Promotion of Science. This research has been supported by NIH grants NB-04393 and GRS-05563. 1205

I206

J. M. OWY

ANI)

‘I’. SAMORhJShl

1966). Howcvcr, most of the observations on visual acuity have been made on man or higher diurnal primates (WLXIIEIMLR, 1965), whereas studies of the structural organization of photoreceptors and the retina have been made predominantly on lower vertcbratcs (COHEN, 1963). Consequently, comparative studies of visual acuity and Icarning capacity

in relation to the organization of the retina and visual pathways and ccntcrs in different primates appear particularly relevant for a more comprehensive understanding of vision in man (POLYAK, 1957). The present multidisciplinary investigation was undertaken to compare visual acuity among 6 lower primate spccics in relation to the morphologic organization of photcreceptors and the retina. Specific aims wcrc as follows: (1) to establish minimum separable visual acuity by behavioral discrimination procedures in 6 lower primates, (2) to determine differences in their visual learning capacity, (3) to compare ERG-CFF thresholds after light and dark adaptation for electrophysiological differentiation of photopic, scotopic, and duplex photoreceptor systems among the 6 species, (4) to establish retinal topography, light reflexes and patterns of pigmentation in temporal region by fundus photography, (5) to study the distribution of rod and cone populations in relation to bipolar and ganglion cells in the temporal region of the retina by histologic procedures, and (6) to examine with the electron microscope the ultrastructural features of single photoreceptors in relation to the pigment epithelium and to bipolars at the level of the receptor basal processes identified with the light microscope as rod spherules and cone pedicles. MATERIALS AND METILODS Subjects A total of 36 monkeys from 6 different primate species was used in the prcscnt invcstigation. The 6 primate species included the diurnal squirrel monkey, Sabniri sciureus; the diurnal marmoset, Cdidwis jucchs; the South American night or owl monkey, A&us trivirgntus; the diurnal Icmur, Lwur catta; the nocturnal bush baby, Galago crussicuudutus; and the diurnal tree shrew, Tupuiu glis. Four animals from each species were included in the behavioral acuity tests and the remaining two subjects were used for the electrophysiological and morphological evaluations. Behavioral ncuity tesls

The behavioral discrimination apparatus consisted of a longitudinally divided straight alley runway 24 in. high, 20 in. wide, and 72 in. long. The start and goal compartments were located at the opposite ends of the runway. The acuity test cards were located in the 2 goal compartments and illuminated by a 60 W pearl bulb with the light diffused by a translucent plastic screen. The luminosity of the field was 100 mL measured by an SEI photomcler and was the same for all 6 primate species. Six sets of test patterns were used for testing. Each set consisted of two 8 x 8 in. cards covered with $ in., + in., rb in., 3’2in., l/64 in., and l/l28 in. black and white striae of equal width printed on non-gloss white paper. At the testing distance of 4 ft they subtended 16, 8, 4, 2, 1, and 0.5 min of visual angle. For establishing acuity threshold, 2 cards from the 6 test patterns wcrc placed randomly in a vertical and horizontal orientation and the subjects were trained to discriminate between the horizontal and vertical striae by obtaining differential food reinforcement located beneath the test cards. For each training and testing trial, an opaque and then a plexiglas door were removed at the start compartment and the subject selected

Acuity mJ the Retina

1207

one of the 2 test cards located at a distance of 4 ft in the 2 goal compartmcnls. A noncorrection method of training and a modified method of limits for testing were used to determine the acuity thresholds. Minimum separable binocular acuity thresholds were established by 20 correct discriminations out of 25 trials for 3 consecutive days of testing with each pair of the test patterns. For the behavioral testing, at least 4 subjects from each of the 6 selected species were trained with the discrimination procedure,for establishing acuity thresholds. However, only 2 lemurs were available for the behavioral testing. The behavioral findings obtained from 22 subjects of the 6 species wcrc included in the statistical evaluations of visual acuity thresholds and visual learning capacity. Electrophysiology The ERG-CFP thresholds were dctcrmincd at the same lcvcl of light intensity in 2 animals from each species after 20 min of light and 20 min of dark adaptation for a possible electrophysiologic differentiation of photopic, scotopic, and duplex photoreceptor systems among the 6 species. Each subject was lightly anesthetized with Serotol, positioned in a stereotaxic head holder, and tested with an electrically shielded enclosure. The right upper lid was rctraclcd and the pupil was dilated with a 1 per cent solution of cyclopentolate hydrochloride. The left eye was covered with an eye patch. A properly fitted contact lens was positioned on the cornea of the eye. The contact lens contained an electrode which made contact with the cornea through a 2 per cent methyl cellulose and O-9 per cent saline solution. A reference electrode from the scalp was grounded. The potential difference between the cornea1 and reference electrode was passed through a shielded cable for recording with an Offner 8-channel EEG polygraph. The ERG responses were elicited by a Grass PS-2C photostimulator with a 10 psec-fl at 8.5 x 106 Lux. The responses of a photocell monitor for the light flashes were recorded simultaneously with the ERG responses. The distance from the eye to the light source was 12 in. The retinal area illuminated was approximately 30 deg of visual angle. Comparisons of light and dark adapted ERG-CFF thresholds among the 6 species were based on the amplitude and rate of the b or x components of the ERG responses obtained at the same light intensity within a range of IO-100 tlashcs per second. Fundus photography

The objectives in the photography of the fundus were to establish retinal topography, light reflexes and patterns of pigmentation in the temporal region of the eye in the 6 primate species. Photographs of the retina were obtained by a Zeiss Fundus Camera in conjunction with the body of Contax 1IA camera. Kodachrome K135 color reversal film was used for all fundus photographs. The camera produced a flat 22 mm image -of a fundus area of approximately 30 deg. Histolog),

For the histologic examinations, whole eyes were fixed briefly in a 1 :I :8 mixture of formalin, acetic acid, and methyl alcohol (DAVID et al., 1960). Within a few hours after initial fixation, the eyes were cut along the equator and the posterior half of each eye was again immersed in fixative for an additional 24 hr. After fixation, the retinal tissue was further dissected into smaller pieces containing the optic disc as well as segments from central and peripheral portions of the eye. These sections were then processed for F

embedding in paraffin. Sections cut at 8 ILwere stained with hcmatoxylin and cosin. For orientation of photoreceptors in relation to other retinal layers, tissues embedded in Maraglas for electron microscopy were cut at 1 p, stained with Azure II (Jeon, 1965) and examined with the light microscope. Electroll microscopy

The clcctron microscopic observations wcrc made on sclcctcd scgmcnts of retinal tissue fixed for 12 hr at 4°C in 4 per cent glutaraldehyde buffered to pH 7.2 with O-2 M cacodylate buffer. After initial fixation, tissues from the central and peripheral portions of the eye were trimmed under a dissecting microscope into smaller pieces (l-2 mm) which wcrc then further fixed at 4°C in 1 per cent osmium tctroxide in O-2 M cacodylatc buffer for 2 hr. After dehydration in solutions of cold ethyl alcohol, tissue segments were embedded in Maraglas. Thin sections cut with an LKB Ultratome set at 200-400 b; were mounted on carbonized grids, stained with lead citrate (Venable and Coggeshall, 1965) and examined in a Siemens Elmiskop I electron microscope at 60 kV.

RESULTS

Sensory acuity thresholds arc generally defined statistically as the stimulus value at which a subject responds correctly at least 75 per cent of the time in a series of trials since a 50 per cent correct response level in a 2 choice learning problem represents only chance discrimination. Binocular minimum separable visual acuity thresholds were established in all 22 subjects of the 6 species by 20 correct responses out of 25 trials for 3 consccutivc days of testing. The more stringent criterion of 20 correct choices out of 25 trials (80 per cent) for 3 consecutive days with each acuity test pattern was used in this study to compare acuity thresholds as well as to determine possible differences in visual learning, positive transfer of training, and retention or memory capacity among the 6 primate species. Visual acuity

thrcsskolil~

A modified method of limits with descending series was used to define the acuity threshold by using the largest test card of 16’ from the onset of training followed by the next smaller test striations until the threshold value was established for each subject. The successively smaller test patterns were introduced only when each preceding acuity test pattern had been discriminated to the criterion of 20 correct responses out of 25 trials for 3 consecutive days of testing. The threshold value was then estimated by the interval between the larger test pattern discriminated above 80 per cent correctly and the next smaller test pattern that elicited only chance level responses on 3 consecutive days of testing. Table 1 shows the binocular minimum separable visual acuity thresholds exprcsscd in minutes of arc for each of the 22 subjects from the 6 primate species. All 4 squirrel monkeys as well as the 4 marmosets responded above the 80 per cent threshold to the 16’, 8’, 4’, and 2’ acuity test striations. Only 1 of the 4 squirrel monkeys and only 2 of the 4 marmosets discriminated the 1’ test card to the 80 per cent criterion. None of the 8 subjects from these 2 species discriminated the 0.5’ test cards above chance. If it is assumed that the acuity results obtained with the sample of 4 subjects from each of the 2 species are representative of the species, it may be concluded that the acuity thresholds

Acuity T~are

1.

Acuity

test cards:

Species

‘&MPARlSON

OF MINIMUM

SEPARADLE

16’

ss

T1

VISUAL

ACUITY

8’

_f %2

T

I2OY

end the Retina THRESHOLDS

AMONG

THE SIX PRIMATE

2’

4’

x’“/,

T

.?%

T

0.5’

1’

2%

T

2%

564 425 425 375

80 93 92 84

XOY 500 500 450

85 91 96 91

1184 625 600 575

‘)I 85 87 91

1334 900 700 675

83 88 93 85

1412 1100 925 775

52 76 60 83

4

494 225 500 485

91 91 93 92

584 300 625 560

87 85 92 91

675 375 700 735

93 93 84 88

750 450 825 1235

85 85 88 80

825 525 900 1410

84 84 71 71

2 3 4

875 700 700 850

84 92 88 84

1100 815 800 1150

87 85 84 84

1425 1050 1150 1375

81 85 63 63

1725 1275 ---

60 63

-----

Lemur Catta

275 300

87 91

522 650

88 81

1173 1200

81 81

1350 1425

81 80

1650 1725

Galago

796 825 800 850

81 85 88 85

963 1025 975 950

85 87 80 85

1113 1225 1475 1675

81 65 52 60

1313 ----

53

-----

919 900 925 875

81 85 81 84

1732 1600 1325 1400

83 80 80 85

1957 2000 1425 1600

85 81 83 81

2107 2200 1525 1675

84 81 84 80

2307 2450 1675 1800

Squirrel Monkey

Marmoset

I

3” AOLUS

Tree Shrew

2 3 4

SPECltS

Tax 1175 --

56

850

53

90060 600 56 -------

83 84

1725 1925

52 60

----84 81 60 72

2382 2650 ---

56 56

t T Cumulative number of trials for each successive acuity test pattern. 2 _? Mean percent correct choices of 3 successive days for each acuity test pattern.

for these 2 diurnal primate species range from 05’ to 15’ of visual angle. Similarly, all 4 nocturnal aotus monkeys and all 4 nocturnal galagos responded above the 80 per cent threshold to the larger 16’ and 8’ acuity test striations. However, only 3 out of the 8 subjects from these 2 nocturnal species responded above threshold to the 4’ acuity pattern. From these behavioral findings, it can also be inferred that the acuity thresholds for these 2 nocturnal species may range from 3.5’ to 8’ of visual angle. All 4 tree shrews and both lemurs responded above 80 per cent to the 16’, 8’, 4’, and 2’ acuity test cards. Only 2 of the 4 tree shrews, but both lemurs responded above the 80 per cent threshold to the 1’ striations. However, none of the 6 subjects from these 2 species responded above chance to the O-5’ test cards. Consequently, if the results from the sample of 4 and 2 subjects are presumed to bc representative of the 2 species, it can also be concluded that the acuity thresholds may range fron O-5’ to l-5’ of arc in these 2 lower diurnal species. Visual learning capacity

The visual discrimination training included at least 4 animals in 5 of the 6 spccics. Since all 20 subjects responded above threshold to the larger 16’ and 8’ acuity test cards, combined and separate statistical analyses of variance were made to evaluate possible differences in overall visual learning, positive transfer of training, and retention or memory

Ill0

J. M. ORDY AND T. SAMORAJSKI

capacity among the 5 primate species (WINER, 1962). Figure 1 shows a combined array of the minimum separable visual acuity for each of the 6 species expressed in terms of the mean percent and range of correct choices for the successively smaller acuity patterns, and the mean and range of the number of Icarning trials for the 5 acuity test striations.

SPECIES

COMFAHISON OF MINIMUM

ACUITY

1

MARMOSET

CAROS:.

(N=4)

16’

0 8’

SEPARABLE VISUAL ACUITY

A 4’

A 2’

m I’

Cl 0.5’

-+

r

AOTUS

(N=4)

t _________________

t -------

1

LEMUA

CATTA

__-_

-

_-_--

-

-+

_____+__-___---____---___-

/______-----__--2

1

-‘L---L--

(MS21

I

GALAGO

T

(N ~41

-+_-_-____-_--___ --+=c;;f;;___--_

TREE

StiREW

IN=41

h I 0

500 MEAN

1000 AND RANGE OFSPECIES

I

I

1500

2000

LEARNING

I 2500

TRIALS

FIG. 1. A combined array of the minimum separable visual acuity threshold of each of the 6 species, the mean percent and range of correct choices for the successively smaller acuity test patterns, and the mean and range of the cumulative number of learning trials for the acuity test striations.

In considering possible species differences in visual learning, the overall analysis of variance of the total number of trials to reach the 3 day criterion of 80 per cent for the 16’ and 8’ acuity test cards indicated significant differences in visual learning capacity among the 5 species (F=37*30; df=4/30; P<04001). The more specific statistical multiple

Acuity

and the Retina

1211

range test for identifying and ranking means and evaluating the significance of differences among combinations of the 5 species’ group means indicated that the marmosets and squirrel monkeys learned the 2 larger sets of discrimination problems in significantly fewer trials than the other 3 species (P~0.01). The aotus and the galago monkeys ranked intcrmediatcly, whereas the tree shrews rcquircd the highest number of learning trials to attain the 3 day criterion performance levels (P-CO-01). Positive transfer of learning is generally inferred from increases or similarities in performance under 2 different test conditions. There was a highly significant decrease in the number of trials to reach the 3 day crilerion from the 16’ to the 8’ test patterns (F=22596; df= l/30; P
J. M. ORDY ANI) T. SAMORAJSKI

1212

comparative evaluation presented in Table 1 and in Fig. 2. Although they were excluded from the analysis of variance, it seems interesting to note by inspection of Table 1 and Fig. 2 that the 2 lemurs reached the threshold criterion for the largest 16’ acuity cards in significantly fewer trials than the diurnal squirrel monkeys or marmosets. However, their subsequent discrimination learning of successively finer test striations was slower and more comparable to the discrimination learning of the diurnal tree shrews. ERG critical flicker jiisiott (CFF) thresholds

The highest flicker frequency of 90-100 c/s after both light and dark adaptation was recorded from the retina of the predominantly cone eye of the diurnal tree shrew. The ERG-CFF from the diurnal squirrel monkey and marmoset was lower at 50-60 c/s after 20 min of light or dark adaptation. The ERG-CFF thresholds of the nocturnal aotus and galago were the lowest at 10-30 c/s, depending on the state of adaptation. The ERG-CFF thresholds of the 2 diurnal lemurs was at 50-60 c/s after light or dark adaptation and in general agreement with their high acuity and diurnal habits. Table 2 shows a quantitative comparison of the ERG-CFF thresholds among the 6 primate species. TABLE 2. COMPAKISINOF ERG-CFF

THRESHOLDS AMONGTHE SIX PRIMATESPECIES

Range of flash/xc1 20 mins of light (L) or dark (D) adaptation

(10)

(100)

(L)

(D)

1

60

60

2

60

60

Marmoset

1 2

60 60

50 60

Aotusz

1 2

30 25

20 20

Lemur Catta

1 2

60 50

50 50

Galago*

1 2

30 25

20 20

Tree Shrew

1 2

90 100

90 100

Squirrel Monkey

ss

1 Strobe= 10 psec, flash at 8.5 x 106 Lux. 2 Note decrease in ERG-CFF after dark adaptation and Galago.

in Aotus

In general, the ERG-CFF responses were not altered significantly by the state of adaptation in the 4 diurnal species. In the 2 nocturnal species, dark adaptation resulted in a highly significant increase in the amplitude of the b-wave of the first ERG response after dark adaptation. This increase in rod sensitivity brought about a change in rate of recovery and decrease in the ERG-CFF thresholds. Comparisons of the different ERG-CFF thresholds among the 6 species are shown after 20 min of light adaptation (Fig. 2) and after 20 min of dark adaptation (Fig. 3).

1213

Acuity and the Retina

LIGHTADAPTED FLICKER ERGTHRESHOLD aTRoBE i lop SEC-FLATa.5 YId LUX

7. ___.

:__. _..-._.-.. .-. _,___. ___,.-_. ._...._^... _._._:_._.-

~

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++

;s :

A-LL...

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:

1,:

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: P------l __ ._.:

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FIG.2. Comparison of the different ERG-CFF thresholdsamong the 6 speciesafter 20 min of light adaptation. The 6 sets of tracings on the left side of the figure illustrate ERG responses to JO R/xc after 20 min of light adaptation. The 6 tracings on right side of figure illustrate ERG responses at the criticalflickerfrequencyin A/set alter 20 min otlight adaptation. The ERG responses are the tracings on top and the light flash tracings are presented on the bottom for each species. Voltage and time constants for recording ERG responses are includedseparatelyfor each species, The light source was a strobe = 10 psec-fl at & 5 x 106 Lux.

Fu~dus photogmphy

Plate 1 represents a cotnposite of 6 color photographs and illustrates the ophthalmologically observable funduscopic organization in the temporal region of the eye among the 6 selected species. The typical diurnal primate fundus specialization with an area centralis containing fovea1 light reflexes can be seen in the duplex retinae of the squirrel monkey and marmoset. However, no demarcation of a fovea1 region is discernible in the eye of the diurnal lemur or the nocturnal aotus or galago. However, the arching blood vessels in the temporal

1214

J. M. ORDY AND T. SAMORAJSKI DARK ADAPTED FLICKER ERG THRESHOLDS STWOI)E ’ IOr SEC-FL

AT 8.5 X IO@ LUX

SCUIKRCL MCUKLY

FIG. 3. Comparison of the different ERG-CFF thresholds among the 6 species after 20 min of dark adaptation.

between the optic disc and the raph4 suggest an area centralis in the diurnal lemur as well as in the 2 nocturnal species. The eye of the tree shrew represents the most undifferentiated appearance since only a radial distribution of the retinal blood vessels can be observed in the temporal half of the retina. In general, these comparative funduscopic observations suggest that there is a trend above the transitional tree shrew among nocturnal as well as among the lower diurnal primates toward a differentiation or specialization of an avascular area coinciding with the fovea of the diurnal primate eye. retina

Although various central factors in the visual pathways and centers of the brain are known to be involved in visual acuity, flicker fusion, and other visual functions, two of

Acuity and the Retina

1215

the more significant morphologic features of the retina involved in visual acuity as well as in sensitivity to light have generally been associated with the type, size and distribution of photoreceptors, and more recently with the receptive fields based on the convergence of receptors on ganglion cells. Functionally, an increase in visual resolution in diurnal species has been associated with greater density of both rod and cone photoreceptors and a decreased receptor to ganglion cell convergence. In contrast, an increase in the threshold sensitivity to light in nocturnal species is generally associated with retinal mechanisms of summation or greater receptor to ganglion cell convergence. Plate 2 shows a light micrograph of a histologic section with the typical fovea1 depression in the duplex retina of the diurnal squirrel monkey. Plate 3 shows a light micrograph with the fovea1 depression in the duplex retina of the diurnal marmoset. In general, a more detailed comparison of the histologic findings presented in Plates 2 and 3 indicates a typical diurnal retinal neural network, a well differentiated central area with the characteristic fovea1 depression, and the 2 types of photoreceptors in these 2 diurnal species. Also, the rod inner segments are approximately of the same diameter as their much longer outer segments and the rod nuclei are smaller, more dense, spherical, and located considerably more internal to the outer limiting membrane than the cone nuclei. Outside of the fovea, the cone inner segments are considerably thicker. In both of these diurnal species, the ganglion cell layer increases from 5 to 7 rows in the clivus around the fovea1 depression. Plate 4 shows a light micrograph of a histologic section from the area centralis of the nocturnal aotus without the typical fovea1 depression of the duplex primate retina. Only the characteristic nocturnal neural network of 8-10 dense layers of receptor nuclei, 2-4

PLATE I. Fundus photographs of the temporal retina illustrating differences in the ophthalmologic appearance of the eye among the 6 primate species. Top row: left, squirrel monkey, right, marmoset. Middle row: left, aotus, right, lemur, Bottom row: left, bush baby, right, tree shrew. PLATE2. Vertical histologic section through macula and fovea of the diurnal squirrel monkey retina. Main morphologic features observable in the duplex retina include sclera, choroid, dense pigment epithelium, photoreceptors, as well as the bipolar and ganglion cell layers around the fovea1 depression. Hematoxylin and eosin. x 375. PLATE3. Vertical histologic section through the macula and fovea of the diurnal marmoset retina. Hematoxylin and eosin. x 375. PLATE4. Vertical histologic section through area centralis of the predominantly rod retina of the nocturnal aotus. Note characteristic nocturnal neural network of the retina. Although not observable in this section, the ganglion cells increase from 1 to 2 rows in the area centralis of the aotus. Hematoxylin and eosin. x 250. PLATE5. Vertical histologic section through area centralis of the retina of the diurnal lemur catta. The ganglion cells increase from 2 to 5 rows in the area centralis of the retina in this diurnal lemur. Hematoxylin and eosin. x 200. PLATE 6. Vertical histologic section through the area centralis of the all rod retina of the nocturnal galago. The ganglion cells are closer together in the central region of the retina. Hematoxylin and eosin. x 200. PLATE7. Vertical histologic section through the area centralis of the all cone retina of the diurnal tree shrew. The ganglion cell layer increases from 2 to 4 rows in the area centralis. Hematoxylin and eosin. x 320.

1216

J. M. ORUY AND T.

SAMORAJSKI

PLATE 8. Electron micrograph of choroid (C) and pigment epithelium (Pe) also showing the envelopment of the receptor outer segments by elongated and spherical pigment bodies in the parafoveal region of the retina of the diurnal squirrel monkey. x 7,500. PLATE 9.

Electron micrograph of rod outer segment (OS), the narrow connecting cilium or junction (arrow) to the inner segment (Is), and a portion of the receptor inner segment with several elongated mitochondria (M). The rod is from the central region of the retina of the diurnal squirrel monkey. x 22,000.

PLATE 10. Electron micrograph of cone outer segment (OS), the narrow connecting cilium (arrow) to the inner segment (Is), and a portion of the inner segment containing numerous elongated mitochondria (M). The cone is also from the central region of the retina of the diurnal squirrel monkey. x 22,000. PLAIT 11. Electron micrograph of a cross section through the ellipsoid portion of the cone showing the connecting cilium (arrow) with the characteristic ciliary filaments linking the inner and outer segments of the receptor. The connecting cilium appears surrounded by a clear chamber at the junction between the inner and outer segment. x 35,000. PLATE 12. Electron micrograph of receptor basal processes showing rod (Rs) and cone (Cp) synaptic endings in close proximity to bipolar cells and their dendrites (Bd) in the central region of the squirrel monkey retina. x 3,500. PLATE 13.

Electron

and rod spherule

micrograph of receptor basal processes showing a cone pedicle (Cp) (Rs) in relation to bipolar dendrites (Bd) in the central region of the squirrel monkey retina. x 18,000.

PLATE 14. Electron micrograph ofchoroid (C), portion of pigment epithelial cell with nucleus

(N), mitochondria (M), endoplasmic reticulum (Er), dense bodies (D), and cell fringes cnvcloping the outer segments (0s) of two rods in central region of the retina of the nocturnal galago. x 10,000. PLATE 15.

Electron

microgroph

with higher magnification

of chorio-epithelial

junction

in relation to Bruch’s membrane (B). Note close proximity of blood vessel wall (Bv) to infoldings of the basal portion of the epithelial cell. x 24,000. PLATE 16. Electron micrograph of three extremely long and slender rod outer segments (OS), the connecting cilium (arrows) and portion of a rod inner segment (Is) with mitochondria (M) in central region of the retina of the nocturnal galago. x 16,000. PLATE 17. Electron micrograph

of cross section through the ellipsoid portion of two adjacent

rods showing the connecting cilium with the typical ciliary filaments linking the receptor inner and outer segments. x 32,000. PLATE 18. Electron micrograph of rod spherule showing synaptic endings with a synaptic ribbon (arrow), synaptic vesicles, and bipolar dendrites (Bd) in central region of the galago retina. X 21,600. PLATE 19. Electron micrograph of a cone and adjacent cell of the pigment epithelium in the central region of the retina in the diurnal tree shrew. The micrograph illustrates Bruch’s membrane (B), a cell nucleus (N), mitochondria (M), pigment granules (P) as well as a cone outer segment (OS) and inner segment (Is) with unusually large mitochondria (ML). x 9,000. PLATE 20.

Electron

micrograph

of cone nucleus (N), the cone pedicle containing

numerous

vesicles (V), and the bipolar dendrite-s (Bd) in the central region of the tree shrew retina. x 9,000. PLATE 21. Electron micrograph of cone basal processes showing synaptic endings with tubular profiles in close proximity to a synaptic ribbon (arrow), and bipolar dendrites (Bd) in the central region of the tree shrew retina. x 24,000.

[See

plate on facing page

[/icing

puge 12 I 6

Acuity and the Retina

1217

layers of bipolars, and a single layer of ganglion cells can be observed throughout the retina. However, in even more central histologic sections, the ganglion cells increase from 1 to 2 rows suggesting an area centralis in the aotus. Plate 5 shows a light micrograph of a histologic section from the area centralis of the diurnal lemur. With the exception of the thicker ganglion cell layer in the area centralis, almost all of the other major morphologic characteristics of a nocturnal neural network can be observed in the retina of this diurnal lemur. However, it seems interesting to note that the ganglion cells increased considerably from 2 to 5 rows in the area centralis of the predominantly rod eye of this diurnal lemur. As in the higher diurnal primates, the smaller proportion of cones appear to be concentrated primarily in the area centralis of this atypical diurnal lemur. Plate 6 shows a light micrograph of a histologic section through the temporal retina of the nocturnal galago. All photoreceptors are slender rods with extremely long outer segments. The outer nuclear layer consists of 8-10 rows, the inner nuclear layer is composed of 3-4 rows, and the ganglion layer contains only a single row of cells. Although the ganglion cells appear closer together in the central region, no significant increase can bc observed in the thickness of the inner nuclear layer or in the ganglion cell layer in the temporal region of the galago eye. Plate 7, a light micrograph, illustrates that only a single layer of short and thick cones extends uniformly across the entire retina in the eye of the diurnal tree shrew. The inner nuclear layer consists of 5-8 rows of closely packed nuclei, whereas the ganglion layer increases from 2-4 rows in the area centralis. The cone inner and outer segments in the retina of the tree shrew contain some unique morphologic characteristics for a primate photoreceptor. The inner segments are quite uniform and cylindrical, whereas the outer segments are characterized by their great uniformity in size, thick shape, and their complete envelopment by cell processes of the pigment epithelium. Plate 7 also illustrates the single row of short and thick cone receptors in relation to the pigment epithelium and in relation to the external limiting membrane in the retina of the diurnal tree shrew. Electrorl microscopy

Since it was not feasible to examine the ultrastructural features of the photoreceptors within the retina in all 6 primate species, the ultrastructural evaluations were restricted to specific regions of the pigment epithelium, the outer, inner, and connecting segments of the photoreceptors, and to receptor basal processes in the duplex retina of the diurnal squirrel monkey (Plates 8-13), the rod retina of the nocturnal galago (Plates 14-18), and the cone retina of the diurnal tree shrew (Plates 19-21). These 3 species were selected as representative examples of duplex, scotopic, and photopic photoreceptor systems among lower primates. Photoreceptors of diurnd squirrel monkey

Composite Plates 8-13 illustrate in a series of electron micrographs the ultrastructural organization and contact relationships between receptor outer segments and the pigment epithelium, the connecting cilia, the receptor inner segments, and the basal synaptic processes of a rod spherule and adjacent cone pedicle in the duplex retina of the diurnal squirrel monkey. Although fovea1 cones appear structurally more like rods in gross histologic sections of the squirrel monkey duplex retina as well as in other diurnal primates, the cones may

J. M. ORDY

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be distinguished from the more peripheral rods by differences in their envelopment by apical cell processes of the pigment epithelium and by several distinguishing features in the fine structure of the receptor inner and outer segments. The pigment epithelium of the entire retina as well as in the fovea1 region in the eye of the squirrel monkey is formed by a dense layer of rectangular cells containing spherical nuclei, numerous elongated and oval pigment bodies, some scattered mitochondria, and an agranular endoplasmic reticulum (Plate 8). The outer segments of the fovea1 cones are invested almost entirely by pigment granules, whereas only the tips of the outer segments of the peripheral rods are invested by oval pigments of more variable electron density. 1‘11~ outer segments of both rods and cones contain the typical array of discs or sacs (Plate 8). The intra-disc spaces frequently appear greater in the rods than in the cones, whcrcus the inter-disc spaces seem considerably smaller. In both rods (Plate 9) and cones (Plate 10) the receptor inner segments arc connected to the outer segments by the typical cilia (Plate 11) which occupy an eccentric position to the ellipsoid of the inner segments and the edge of the outer segments. The inner segments of both rods (Plate 9) and cones (Plate 10) contain only elongated mitochondria in the outer ellipsoid portion. The oval cone nuclei are located closely adjacent to the external limiting membrane. The conducting fibrcs of the cones terminate in the cone pedicles (Plates 12-13). In contrast, the round and smaller rod nuclei are located at variable distances from the external limiting membrane and the cytoplasmic stalks of the rod receptors end in the spherule terminals (Plates 12-13). Morphologically, it seems interesting to note that both types of receptors basal processes are in ciosc proximity to bipolar cells and their dendrites as well as in close contiguity with basal processes of other adjacent receptors. Photoreceptors

ofnocturnal

&ago

Composite Plates 14-18 illustrate in a series of electron micrographs the ultrastructural organization and contact relationships between receptor outer segments and the pigment epithelium, the connecting cilia, the receptor inner segments, and the basal synaptic processes of a rod spherule in relation to bipolar dendrites in the rod retina of the nocturnal galago. The pigment epithelium of the entire retina of the galago is formed by a single layer of rectangular cells containing spherical nuclei, only very few oval pigments localized near the ora serrata, some scattered mitochondria, rough and smooth endoplasmic reticulum, and small clusters of ribosomes (Plate 14). The outer segments of the rods appear to be invested at the tips only near the ora serrata by a very small number of oval dense bodies (Plate 14). The slender outer segments are also extremely long and contain the regularly disposed arrays of double-membraned discs which do not appear to be in contact with the surrounding plasma membrane (Plate 16). The inner segments of the rods are connected to the outer segments by the typical cilia (Plate 17) which also occupy an eccentric position to the ellipsoid of the inner segments and the edge of the outer segments. The inner segments of the rods contain only a few mitochondria characterized by their elongated configuration (Plate 17). The cytoplasmic stalks of the rod end in the spherule terminals with their synaptic lamellae located in close proximity to bipolar dendrites (Plate 18). Photoreceptors of diurnal tree shrew

Composite Plates 19-21 illustrate in a series of electron micrographs the ultrastructural

Acuity and the Retina

1219

organization and contact relationships between receptor outer segments and the pigment epithelium, the connecting cilia, the receptor inner segments, and the basal synaptic processes of a cone pedicle in relation to bipolar dendrites in the cone retina of the diurnal tree shrew. In contrast to the lack of pigmentation in the retina of the nocturnal galago, the pigment epithelial cells in the retina of the diurnal tree shrew contain numerous oval as well as elongated pigment granules, mitochondria, and masses of smooth endoplasmic reticulum. Numerous cell processes filled with elongated pigments envelop each cone outer segment (Plate 19). The relatively short and thick cone outer segments contain the characteristic double-membraned saccules which may be in contact with the plasma membrane along some portions of the outer segment. The ellipsoid portion of each cone inner segment contains extraordinarily large mitochondria. These mitochondria contain some unique patterns of concentric cristae arranged in rings of membrane whorls. An examination of several receptors indicated a close continuity between the inner andouter segments rather than the narrow constriction. The cone nuclei are large, oval, and arranged in a radial orientation to the external limiting membrane. The short and thick cytoplasmic stalks of the cones terminate in the cone pedicles which are in close proximity to the dendrites of the bipolar cells (Plates 20 and 21). DISCUSSION

Acuity and the ntorphologic organization of the retina

The behavioral results of the present study indicate that the minimum separable acuity thresholds of the diurnal squirrel monkey, marmoset, lemur, and tree shrew range from 05’ to 1.5’ of arc and that they are comparable to higher diurnal monkeys, anthropoids, and man. The acuity thresholds of the nocturnal aotus and galago range from 3.5’ to 8.0’ corresponding more closely to the human rod monochromat (HECHT et al., 1948) and the optokinetic acuity of 5’ reported for the predominantly rod retina of the cat (SMITH, 1938). Although quantitative comparisons of acuity and receptor or ganglion layer thickness or cell density in relation to retina1 eccentricity were not undertaken in the present study, the comparative histologic findings suggested that in the temporal retina, the convergence of receptors on ganglion cells, rather than receptor type or density, provided one of the more consistent anatomical features of the retina associated with acuity among the 6 primate species. A maximum number of ganglion cells was observed in the clivus around the fovea in the squirrel monkey and marmoset, as well as in the area centralis of the lemur and tree shrew. The increases in ganglion layer thickness observed in the area centralis of the lemur and the tree shrew have been reported previously (v. CASTENHOLZ, 1965; ROHEN and v. CASTENHOLZ,1967). Similar increases in ganglion layer thickness have been observed in the retina of the aotus (JONES, 1965). Increases in ganglion cell density in the area centralis have also been reported for the bush baby (DARTNALLet al., 1965; ROHENand v. CASTENHOLZ,1967). Acuity and ERG-CFF

rhreslrolds

Although the ERG-CFF rcsponscs are known to represent only mass retinal action potentials, previous findings with human subjects have suggested that radial gradients of “eccentricity” can be associated with decreasing acuity and decreasing ERG-CFF from the fovea to the periphery (PIRENNE,1962; WOLFand VINCENT,1963). For interpreting

1220

J. M. ORDY

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T. SAMORAJSKI

the differences in minimum separable acuity and ERG-CFF thresholds obscrvcd among the 6 primate species in the present study, a number of experimental findings on radial gradients of acuity and psychophysical CFF thresholds from the fovea to the periphery of human subjects can serve as possible points of reference. In man, it is well established that visual acuity decreases sharply from the fovcn to the periphery (WERTHEIM,1894). Previously, this decrease has been closely identilicd with the decrease in cone density from the fovea to the periphery (~STERUERG,1935; POLYAK,1957). More recently, decreases in acuity have been correlated statistically with decreases in cone density as well as with retinal eccentricity of ganglion cells from the clivus of the fovea to the periphery (WEYMOUTH,1958). According to thcsc correlations, spatial thresholds of the photopic human eye appear to be linear functions of retinal eccentricity, whereas the acuity functions of the dark adapted eye and those of intensity and critical flicker frequency in the light or dark adapted duplex eye are nonlinear. These correlations suggest that the radial gradients of ganglion cells, rather than receptor size or density, provide a more reliable anatomical basis for both spatial and intensity thresholds. More direct evidence has also been presented for the relationship between acuity, critical flicker frequency and eccentricity by experimental observations on rod monochromatic human subjects (KOENIG, 1897; HECH~ et al., 1948). It was found that the acuity of the rod monochromat subtended a visual angle of 6’ of arc. The relationship between acuity and luminance was similar to that of normal humans of scotopic levels. Acuity did not increase at higher levels of luminance as it does in normal subjects. The CFF threshold was 20 rather than 55-65 c/s, generally observed in the normal human eye under similar test conditions (PIRENNE,1962). ln the present study, the most significant differences in the temporal aspects of the ERG-CFF was the fast recovery of the evoked responses to successive light flashes of the cone dominated eye of the tree shrew in contrast to the slower recovery in duplex or rod dominated eyes of the other species. Among the 6 species, the highest flicker frequency of 90-100 c/s after both light and dark adaptation was recorded from the tree shrew. A considerably higher flicker frequency of 140 c/s has been reported previously for the all cone retina of the pigeon (DODT and WIRTH, 1953). The ERG-CFF thresholds of the nocturnal aotus and galago were the lowest at lo-30 c/s, depending on the state of adaptation. The comparative electrophysiological findings of this study are in general agreement with observations reported previously for the aotus (JONESand JACOBS,1963), galago (DARTNALLet al., 1965; SILVER,1966) and the tree shrew (TIGGESet al., 1967). Fundus photography

The topography of the temporal retina in lower primates has not been cxplorcd in detail previously. The only comparative colored drawings of the fundus of several species of subhuman primates were published in 1901 (JOHNSON,1901) and reproduced in 1957 (POLYAK,1957; ORDY cf al., 1962). More recently, it has been established experimentally that in the region of the visual axis, the area of highest acuity is characterized by a pattern of detouring blood vessels and optic nerve fibers, suggesting a more effective transmission of light by reducing the scatter of light transmitted to the photoreceptors (WEALE, 1966). Since the retinal neural layers do not appear to interfere with visual acuity, it has been proposed that the internal retinal blood vessels could interfere with visual acuity by scattering the light in the fovea or area centralis. The relatively constant diameter of the human avascular area of 0*42*0-1 mm has also been used in support of the hypothesis

Acuity and the

Retina

1221

that the avascular area must play a critical role in visual acuity (WEALE,1966). The comparative funduscopic observations of the present study suggest that there is a trend above the transitional tree shrew among nocturnal as well as among the lower diurnal primates toward a differentiation of an avascular area coinciding with the fovea of the duplex primate eye. Ekwron microscopy

Previously reported studies with the electron microscope have examined similarities and differences in the ultrastructural organization of photoreceptors and synaptic contacts to bipolar and ganglion cells (SJ~STRAND,1961; PEDLERand TILLY, 1965; COHEN, 1965; DOWLINGand Bo~corr, 1966). Earlier studies emphasized some universal similarities in the photoreceptor outer segments among vertebrates. More recent studies have reported some interesting variations in rod and cone ultrastructure among primates (DOWLING, 1965; PEDLERand TILLY, 1965; COIJEN,1965). In the present study, fovea1 cones appeared structurally more like rods in gross histologic sections of the diurnal squirrel monkey and marmoset. However, these cones can be distinguished from peripheral rods by their cnvclopment by apical cell processes of the pigment epithelium and by several other differences in the fine structure of the receptor inner and outer segments. In nocturnal eyes, the outer segments of the rods in the galago are slender and also extremely long but contain the typical arrays of double-membraned discs which do not appear to be in contact with the surrounding plasma membrane. The relatively short and thick cone outer segments in the diurnal tree shrew also contain the characteristic double-membranes saccules which may be in contact with the plasma membrane along some portions of the outer segment. Within the inner segments, one of the more striking observations in the present study was the extraordinarily large mitochondria with some unique patterns of concentric cristae arranged in rings of membranous whorls in tree shrew cones (SAMORAJSKI et al., 1966). Although these large and complex mitochondria in the inner segment would appear to be unique in primates, some unusually large mitochondria have also been observed in the ellipsoid portion of the inner segment in cones of the diurnal gecko (PEDLERand TANSLEY, 1963). It seems possible that the extremely high ERG-CFF responses of the cone dominated eye of the tree shrew can be associated with the photochemistry of visual pigment and the unique milochondria in the receptor inner segments. The basal processes of both rods and cones appear as relatively dense club-shaped expansions filled with synaptic vesicle;. Their synaptic lamellae are generally located in close proximity to the bipolar dendrites. Although the basal membrane contacts with the basal processes of other adjacent photoreceptors suggest a structural basis for some possible interreceptor synaptic transmission, physiological evidence would be essential to establish the possibility of receptor interaction and the role of such an interaction in visual acuity and other visual functions (COHEN, 1965; DOWLINGand Bo~co-rr, 1966). Visual acuily ad learning capacity

Surprisingly few studies have been reported on visual acuity in relation to the projections of the retina to the striate and prestriate cortex in primates (KL~~vER, 1941; SPENCEand FULTON, 1936; WEISKRANTZand COWEY, 1963; DOTYet al., 1964; COWEY,1964). Experiments on minimum separable acuity before and after bilateral lesions of the striate cortex have indicated a postoperative reduction of 51 per cent in the acuity of rhesus monkeys

1222

J. hl. ORDY AND T. SAMORAJSKI

(WEISKRANYZ and COWEY, 1963). The subjects with the greatest reduction in acuity had the most extensive lesions in the macular projections to the striate cortex. In a behavioral study on the effects of cortical lesions on critical flicker frequency in monkeys, an initial loss and gradual improvement was observed after 1 year of postoperative testing (MISHKIN and WEISKRANTZ, 1959). More recent comparisons of striate and retinal lesions on visual acuity in the rhesus monkey have also indicated that macular lesions can produce a significantly greater reduction of acuity than striate cortex lesions (WEISKRANTZ and Cowtu, 1967). These findings seem to have cast some uncertainty on “point-to-point” retinocortical projection theories of acuity. In considering species differences in visual learning capacity in the prcscnt study, the anatomically expanded occipital lobes in relation to the size of the superior colliculi and

lateral geniculates in the tree shrew suggest great reliance on vision even in this transitional primate (POLYAK, 1957; NOUACKand Mostcowrrz, 1963; ROHEN, 1964; TIGGES, 1964). However, the significant differences in learning, positive transfer and retention among the 6 species indicate that various structural as well as functional differences must exist in the size and complexity of the retino-cortical projection and association areas of the brain. In summary, the multidisciplinary findings suggest that there is a close relationship between acuity and the convergence of receptors on ganglion cells of the retina. However, the significance of horizontal or amacrine cells for lateral interaction within the neural network of the retina must yet be explored among these 6 primate species. The observations with the electron microscope indicate vast possibilities of interaction even at the level of adjacent photoreceptors and bipolar cells. Finally, whereas the role of the visual pathways and centers of the brain in acuity and visual learning capacity cannot be neglected, it seems reasonable to assume that the visual system at any higher level cannot resolve and utilize stimulus characteristics unless they are first encoded in differential inputs within the retina and then transmitted through the optic nerve as some temporal or spatial code sequences (BARLOW, 1964; OGDEN and MILLER, 1966). Acknowledgnlenfs-Grateful acknowledgments are made to the numerous professional and technical staff members of a multidisciplinary group in the Laboratory of Neurochemistry at the Cleveland Psychiatric Institute that have made this combined research program on the primate visual system possible.

REFERENCES BARLOW,H. B. (1964). In Photophysiology II, edited by A. GIESE, pp. 163-202, Acadcrnic Press, New York. CLARK, W. E. (1960). The A!rlecedenfs of Man, pp. 266-286, Quadrangle Books, Chicago. COHEN, A. I. (1963). Vertebrate retinal cells and their organization. Biol. Rev. 38, 427-459. COHEN, A. I. (1964). In Conference 011 the Physiological Basis for Form Discrirninariorz. pp. 1-7, Brown

University. COHEN, A. I. (1965). Some electron microscopic observations on inter-receptor contacts in the human and macaque retinae. J. Anal. 99, 595-610. COWEY, A. (1964). Projection of the retina on to striate and prcstriate cortex in the squirrel monkey, Saimiri Sciurcus. J. Neurophysiof. 27, 366-393. DARTNALL,H. J. A., ARDEN, G. B., IKEDA, H., LUCK, C. P., ROSENBERG,M. E., PEDLLR, C. M. and TANSLEY,K. (1965). Anatomical, ciectrophysiological and pigmcntary aspects of vision in the bush baby: An intcrprctative study. Vision Res. 5, 399-424. DAVID, G. B., MALLION, K. B. and BROWN, A. W. A method of silvering the ‘Golgi apparatus’ (Nissl network) in paraffin sections of the central nervous system of vertebrates. Q. J. Mirrosc. Sri. 101, 207-22 1. DETWILER,S. IX. (1939). Comparative studies upon the eyes of nocturnal lemuroids, monkeys and man. Anat. Rec. 74, 129-146. DETWLER, S. R. (1943). Vertebra/e Photoreceptors,

MacMillan Co., New York. DODT, E. (1954). Ergebnisse der Flimmer-Elektroretinographie. Experienria 8, 330-333.

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PEDLER,C. and TILLY, R. (1965). Ultrastructural variations in the photoreceptors of the macaque. fi@i Eve Res.4.370-373. P~REN&,M. H. (IY62). 77re Eye, Vol. 2, The Visual Process, edited by H. DAVSON,Academic Press, New York. POLYAK,S. (1957). The Vertebrate Visual System, University of Chicago Press, Chicago. ROHEN,J. W. (I 964). Handbuch der Mikroskopischen Aaatomie des Menschen, Springer-Verlag, Heidelberg. ROHEN,J. W. and VONCA~TENHOLZ. . E. (1967). _ Uber die Zentralisation der Retina bei Primaten. Folia P&at.

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SAMORAISKI, T., ORDY, J. M. and KEEFE,J. R. (1966). Structural organization of the retina in the tree shrew (Tuvaia Glisl. J. Ceil Biof. 28.489-504. SILVER,P.‘H,-(1966). $ectraI sensitivity of a trained bush baby. Vision Res. 6, 153-162. SJ~STRAND,F. S. (1961). Ekxtron microscopy OJ’the retina. The structure of the eye, edited by G. K. SMELSER, pp. l-28, Academic Press, New York. SMITH,K. U. (1938). Visual discrimination in the cat: VI, The relation between pattern vision and visual acuity and the optic projection centers of the nervous system. J. genet. Psychof. 53, 231-272. SPENCE, K, W. and FULT~N, J. F. (1936). The effects of occipital lobcctomy on vision in chimpanzee. Brain 59,35-50.

TIGGES,J. (1964). On visual learning capacity, rctcntion and memory in Tupaia Glis Diard 1820. F&u Printot. 2, 232-245.

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VON C&srrNItot_z, Ii. (1965). ijbcr die Struktur dcr Nctzhautmittc bci Primatcn. Z. Zcllforsch. 65, 646-66 1. WALLS, G. L. (1942). Tlte Vertebrate Eye ad 11s Atlaptirc Radiation. Cranbrook Inst. Sci., Bloomticld Hills, Michigan. WEALE,R. A. (1966). Why does the human retina possess a fovea? Na/ure, Lord 212, 255-256. WEINSTEIN,B. and GRETHER,W. F. (1940). A comparison of visual acuity in the rhesus monkey and man. J. camp. P.~ycbol. 30, 187-l 95. WUSKRANTZ, L. and COWEY, A. (1963). Striate cortex lesions and visual acuity of the rhesus monkey. J. corup. Physiol. P.~ycbol. 56, 225-23 I. WEISKRANTZ,L. and COWEY,A. (1967). Comparison of the clfccts of striate cortex and retinal lesions on visual acuity in the monkey. Scieucc, N. Y. 155, 104-106. WERTHEIM,T. (1894). ileber die indirekte Sehscharfe. Z. Psyclrol. Physiol. Simresorg. 7, 172-180. WESTBEIMER,G. (1965). Visual acuity. &n. Rev. Psychol. 16, 359-450. WEYMOUTH.F. W. (1958). Visual scnsorv units and the minimal angle of resolution. A/t?. J. Oohrhal. 46. WINER, B. J. (1962). Statistical Primp/es irr Experimcrrtal &SI$II, McGraw-Hill, New York. WOLF, E. and VINCENT,R. 1. (1963). Effect of target size on critical flicker frequency in flicker perimctry. Vision Rex 3, 523-530.

WOLLARD,H. H. (1927). The differentiation

of the retina in the primates.

Proc. Zoo/.

Sm.,

Lad.

1, l-17.

Abstract-Visual acuity and ERG critical tlickcr frequency (CFF) of 4 diurnal and 2 nocturnal primate species wcrc related to the morphologic organization of photoreceptors and the retina. Acuity thresholds of the diurnal squirrel monkey, marmoset, lemur and tree shrew ranged from 0.5 to 1.5’ and of the nocturnal aotus and galago from 3.5 to 80’ of visual angle. Species differences in ERG-CFF included high response rates and fast recovery of cone dominated in contrast to duplex or rod dominated eyes. In the temporal retina, there was a trend toward a diffcrcntation of an avascular area coinciding with the fovea of the duplex primate cyc. Rods, cones and fovea were observed in the squirrel monkey and marmoset. Mostly rods and an area centralis were found in the aotus and gaiago. Cones were observed predominantly in the tree shrew. The maximum number of ganglion cells was located around the fovea and the area centralis. The. electron microscope indicated similarities in ultrastructure of receptor outer segments. Species differences were found in the inner segments and synaptic contacts of photoreceptors. Significant differences wcrc also observed in visual discrimination learning capacity. From the multidisciplinary comparisons it was concluded that similarities in acuity were associated with the convergence of receptors on ganglion cells, whcrcas visual learning capacity was associated with differences in visual projection and association areas in the brain. R&sum&-Chcz quatre cspeccs diurnes ct dcux cs+es nocturnes dc primates, on etudic I’acuite visuelle ct la fr&quence critique dc fusion (CFF) dans I’ERG, en relation avec la morphologie de.s photorecepteurs et de I’organisation retinienne. Lea seuils d’acuitt des esp&es diurnes (singe saimiri, ouistiti, lemurien et tupala) varient entre 0,5 et 1,5’ tandis que pour les esp&es nocturnes (aotus et galago) ils varient entre 3,5 et 8.0’. Les differences entre esp&es pour le CFF consistent en taux Clevb de reponses et recuperation rapide dans lo cas des yeux ou dominent les cones, en opposition avec les r&tines mixtes ou a domination de batonnets. Dans la retine temporale, il existe une tendance a la differentiation de l’aire avasculaire qui coincide avec la fovea dc I’oeil mixte de primate. On observe des bitonnets, dcs cBnes et une fovea chcz le sai’miri et lc ouistiti; surtout des bitonnets et une area centralis chez aotus et galago; enfin les cones predominent chez le tupaia. Le nombre maximum de cellules ganglionnaires est situe autour de la fovea et de I’area centralis. Le microscope Clcctronique indique des ressemblances dans I’ultrastructure des segments externes des recepteurs. Entre Its especes on trouve des ditferences dans les segments internes et les contacts synaptiques des photorecepteurs. On observe aussi des differences significatives dans I’apprcntissage a la discrimination visuellc. Les comparaisons entre disciplines diverses permcttent de conclurc quc les rcsscmblances en acuite sont Ii& a la convergence dcs receptcurs sur Ies cellultx ganglionnaires, tandis que I’apprcntissagc cst lie a des differcnccs dans la projection visucllc ct Its aircs d’association dans Ic cerveau.

Acuity and the Retina Zusammcnfassung--Die SchschIrfc und die FIimmcrvcrschInclrungsfrcq~lcnz (CFF) vu11 4 Tag- und 2 Nachtprimatenattcn wurden in Zusammenhang mit dcr morphologischcn Organisation der Photorczcptoren und der Netzhaut gcbracht. Die SchschB;rfcschwellen dcs amcrikanischen Flughiirnchenaffen Saimiri sciurcus, vom KrallcnHffchen Callithrix jacchus, der Lemure Lemur catta und dcr Baumratte Tupaia glis, variierten von 0,s’ bis l,5’ und beim stidamerikanischcn Nachtoder Eulenaffen Actus trivirgatus und der afrikanischcn Langohrlcmure Galago eras sicaudatus von 3,5’ bis 8.0’ Gcsichtsfcldwinkcl. Die Untcrschi de dcr einzelnen Arten bei dcr ERG-CFF crgaben hohc Antwortfrcqucnzcn und kurzc Erholzeiten bei Augcn mit Zapfendominanz im Gcgensatz zu Duplexaugen odcr Augcn mit StPbchendominanz. In der temporalen Netzhaut gab es cinen Trend zur Ditfcrentiation cincs gcf&Rlosen Gcbietcs, das mit der Fovea dcs Duplexauges bcim Primatcn tibereinstimmtc. Stiibchen, Zapfen und Fovea wurdcn bcim amerikanischen Flughijrnchenaffcn und bcim Kralleniffchcn beobachtet. Beim siidamerikanischcn Eulenaffcn und bei dcr afrikanischcn Langohrlcmure wurden hauptsitchlich Stlbchcn und tine Area centralis gefundcn. Zapfcn wurdcn tiberwiegend in der Baumratte gefunden. Die gr6l3te Anzahl von Ganglienzellen befand sich un die Fovea und die Area centralis. Durch das Elektronenmikroskop wurde auf Similaritlten in der Ultrafeinstruktur der luBeren Segmente der Rezeptoren hingewiesen. Artbedingte Unterschiede ergaben sich in den inncren Segmenten und den synaptischcn Kontaktcn der Photorezeptoren. AuRcrd wurden signifikante Unterschicdc in der Lcrnftihigkeit, in Bczug auf das visuelle Untcrscheidungsverm&en, fcstgcstellt. Mit Hilfe multidiszipliniircr Vergleichc wurde gcschlosscn, daR die Ahnlichkciten bei der Sehschlrfc mit der Konvergcnz der Rezeptorcn auf die Ganglienzellcn zusammenhlngt, wlhrend die visuclle Lernfithigkcit mit Untcrschicdcn in visuellen Projektions- und Assoziationsgcbictcn dcr Hirnrinde zusammenhlngt. PC3lOMC - OCTpOTa 3l>eHun u KpuTu'leCKaSl YPCTOTa CBeTOBblX MCnbKaliUii I33Pr (KYM) 6blnu COOTHeCeHbl K htop@onorRrecKoii opraliu3auIII~ 4oTopeueniopoe II CeTYaTOK Boo6Lue y 4 LZHeBHblX u 2 HO'lHblX BUnOB IlpUMaTOB. flOpOr& OCTpOTbl 3peliuPlJIHeBHblX:CIuMupu, M~pTblUlKu,neMypa UTyllaiiu6blnu BllpeLWlaXOT0.S~O 1,5',a HoYHblx MupuKuHbI u ranaro B npenenax 0T 3,5 no 8,0’ 3pHTenbHoro yrna. BnnoBblCOCO6eHHOCTH B KYM-3Pl-np0~~~1nnltCb BblCOKOfiCKOpOCTbKI pCaKUUu II6bIcTpbIM BOCCTal~OBJ?elueM NISI rna3 c IIpCO6naAaHuCM Kon6oVeK, B OTnuYue OT ma3 rat npmanl4poBanu rIanoYKu tinu 6blnu Te u npyrtie. B eltcoqi*ofi 06nacTu CCTY~LTKU HMenaCb TeHAeHLluII K AU&#SpeHUUaLtUu aDaCKyJl5lpHOtl30Hb1, COOTBCTCTByKIl.U&i~ ~OB~~ByXCucTeMHOrOrna3~~puMaTOB.~anOYKu,Kon6oYKuu~0Be;lH36n~)A3nuCb y CauMupu If MapTbIUlKu. n0 llpe4iMylI.@CTBynanOYKu u LleHTpaJJbHaSl3OHa 6bmu HatiAeHbIy MupuKuHbI u raJlar0.npeuMylWCTBeHH0 Kon6oYKu 6blnu 06UapyHteHbly TynaBu. Has6onburee wm-10 raHrnu03tiblx KneToK 6blno pacnonoxeuo BoKpyr 4ollea U lleHTpaJlbuO& 30Hbl. 3neKTpOHHaR MuKpOCKOllWl yKa3blBaeT Ha CXOLICTBO B ynbTpaCTpyKType HapyXHblX CerMeHTOB pel.lenTopoB. BIl~OBble pa3nnrun 6bmu IiatiAeHbIBO BHyTpeHHUX CerMeHTaX U CUHallTUYeCKUX KOHTaKTaX ~OTO~UellTOpOB. 3tlaYUTeJlbHble pa3nUYUSl 6bmu Ha6nlOnaeMbl TaKxe B cnoco6HocTu HayYeHurr 3pUTWlbHOMy pa3JlUYeHUW. Ha OcHOBaHuu MHOP~CTO~OHHUX CpaBueHuii 6blno CDZJlaHO3aKJIlOYeHHe, YTOCXOACTBOBOCTpOTe3pi?HUII 6blno CBSl3aHOCKOHBCprCUuU&i peXWTOpOB Ha I-aHI-JIU03HbIe KSXTKU, B TO BpeM5I KBK CllOCO6HOCTb K SpUTWIbUOMy 06yYemo 6bIna cBR3aua c pa3nuYunMu B 3puTenbHoR npoelcuuu u accouuauuotuiofi o6nacTu B M03ry.

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