Brain Research, 104 (1976) 233-241 © Elsevier ScientificPublishing Company, Amsterdam - Printed in The Netherlands
233
D E V E L O P M E N T OF VISUOMOTOR BEHAVIOR IN N O R M A L A N D D A R K R E A R E D CATS
J. VAN H O F - V A N D U I N
Department of Physiology, Erasmus University Rotterdam, P.O. Box 1738, Rotterdam (The Nether-
lands)
(Accepted August 16th, 1975)
SUMMARY
The development of visuomotor coordination in light-deprived cats was compared with that of newborn animals, raised under normal circumstances, using behavioral tests. Two groups of light-deprived cats were studied: one of which was dark-reared for 4 months, the other for 7 months. After dark-rearing the cats were kept in animal rooms which were illuminated for 12 h each day. All cats spent at ieast 4 h each day in a big playroom, where toys were available. Obstacle avoidance, tracking of' moving objects, optokinetic nystagmus, visually triggered extension, visually guided placing, visual cliff behavior and jumping were tested. All lightdeprived cats revealed a complete recovery of visuomotor behavior; the 7-months deprived cats recovered within 10 weeks and the 4-months deprived ones within 7 weeks. The time period in which the various responses in both groups of lightdeprived cats developed after dark-rearing was found to be roughly in accordance with that of normally visually inexperienced kittens after birth.
INTRODUCTION
It is generally accepted that binocular light deprivation leads to visuomotor deficits which are less severe than those found after monocular deprivation. However, although agreement exists on the fact that early after deprivation binocularly deprived (BD) cats demonstrate profound behavioral defects, there is a diversity of opinion as to the permanence of these deprivation effects1,4-6,1a-a6,z2,2a. Whereas in BD cats Wiesel and Hube123 reported little recovery one year after the deprivation time, Baxter 1 described recovery in 5 behavioral tests in 30 days. No behavioral abnormalities could be determined by Chow and Stewart 4 6-10 months after the deprivation period. Neither Wiesel and Hubel, nor Chow and Stewart mentioned results of
234 specific tests in judging the long-term behavioral effects of deprivation. Therefore the discrepancies could be due to the different nature of the tests used in the investigations, and to differences in specific visual training after the deprivation period. As part of a long-term study on deprivation, which includes the behavioral effects of monocular deprivation, the present study is confined to the behavioral effects of binocular deprivation. In order to get a better understanding of the longterm effects of binocular deprivation, a relatively large number of behavioral tests (obstacle avoidance, tracking of moving objects, optokinetic nystagmus, tactile placing response, visually triggered extension, visually guided reaching, visual cliff and jumping behavior) was regularly applied to dark-reared cats for a period of at least 6 months after the deprivation time. The duration o f the recovery period in each of those tests was determined. To achieve optimal motor development the animals were allowed to stay in large playrooms for at least 4 h each day. Since the properties of visual cortex neurons found in BD cats (less than half of the cells being normally responsive, the other cells being sluggish, unpredictable and either responsive to visual stimuli but not selective for orientation, or not responsive to visual stimulation at all) are comparable with those found in visually inexperienced kittens, the term 'immaturity' has been introduced to describe the situation in the visual cortex of BD cats 2,14. If this qualification applies to the visuomotor system in general, one would expect the behavioral recovery after light deprivation to be a replica of the visuomotor development in newborn kittens raised under normal circumstances. Therefore, in the present report, by using the aforementioned tests, the behavioral development of newborn kittens raised under normal circumstances was determined and compared with that of BD cats after dark-rearing. MATERIAL
Dark-reared cats
All kittens were born and kept in complete darkness. Weaning took place two months after birth. Then one group of 5 kittens from two separate litters was kept in darkness for another two months; a second group consisting of 16 kittens from 5 separate litters was kept in darkness until the cats were 7 months old. In darkness the cats were housed in large cages in groups of 2-4 cats per cage where they were handled daily. When the cats were 4 or 7 months old they were housed in large cages in the animal room, which was illuminated with artificial light for 12 h each day. After 4-7 days they were allowed to play 4-6 h each day in a large playroom where toys, stepchairs etc. were available. During the first 4 weeks all dark-reared cats were tested each day, and later on twice a week. In spite of the daily handling 6 of the 7-months dark-reared cats became aggressive and were not co-operative in some of the behavioral tests. Normal cats
Development was followed in 15 kittens from 4 separate litters born in the
235 laboratory. After weaning, which also took place two months after birth, the animals were housed in large cages in groups of 2-4 kittens per cage. The animal room was illuminated by artificial light for 12 h each day. In turn groups of these cats were also allowed to play for 4-6 h each day in large playrooms. Seven kittens from two litters were tested three times per week from the second week of age; 8 kittens from two other litters were tested once or twice a week from the fourth week on. METHODS
(1) Obstacle avoidance. In animals walking freely around in an area enclosed by a thin iron wire fence, bumping against the enclosure was scored. Also the reactions were studied, when objects were placed in front of their heads unexpectedly. (2) Tracking of moving objects above and around the animal's head was tested in a well-lit r o o m with the aid of objects (of several sizes and colors) hanging from an iron wire. (3) Optokinetic nystagmus was studied by looking at the cat's eyes while observer and cat were sitting inside a rotating drum. The radius of the drum was 60 cm, the height 120 cm. The cat's head was held in the center of the drum. The pattern consisted of black and white vertical stripes, each 9 cm wide. In this way the width of one stripe as seen from the center of the drum amounted to 8.57 ° (or the frequency of the square wave grating was 0.058 cycles/degree). D r u m rates used in the experiments were 1, 2, 3.5 or 6 rotations/min. Testing was done with clockwise as well as with counterclockwise rotations. (4) To test the presence of the tactile placing response a cat was held in such a way that its head and forelegs were free to move. While both eyes were covered the animal was slowly carried downwards towards the edge of a table. The dorsa of its front paws were then brought into contact with the vertical edge of the table. In case of a positive response the cat will stretch its claws and place its paws on the table. (5) Visually triggered extension was assessed by carrying an animal slowly downwards towards a broad surface. The reaction was scored as positive if, in approaching the surface, the cat showed an extension of the forelegs. (6) Visually guided reaching was tested with the aid of an interrupted surface as described by Hein and Held 7. The apparatus consisted of a board with 7.5 cm cutouts spaced to form 20 cm long, parallel prongs (of 2.5 cm each). The cat was carried downwards with one forelimb restrained. Ten trials were given with each forelimb. The ratio between the number of prong contacts and failures was determined. (7) The visual cliff consisted of a narrow platform raised 8 cm above the center of a large piece of plate glass. On one side of the platform a checker-board cloth was fixed directly to the underside of the glass. The same pattern was placed 40 cm below the glass on the other side o f the platform. Both surfaces were of equal brightness. The cat was placed on the platform ten times per session. The ratio was determined between descents to the optically shallow and the optically deep surface. (8) Jumping behavior was studied by observing the cats after placing them on top of
236 a 60 cm high stepchair. If the cats did not jump spontaneously, they were helped by folding out two steps. A distinction was made between 'uncertain' and 'practised' jumping. In 'uncertain' jumping the cats felt their way first and when they finally jumped, they gave at the knees. 'Practised' jumping was seen when the animals were able to judge distances and showed a normal landing behavior. RESULTS
Dark-reared cats (a) 7-months dark-reared After removal from the dark-room each cat remained in an enclosure of some 10 sq.m for 30-60 min. In two out of 16 cats convulsive movements occurred immediately after exposure to light. These animals fell down, but recovered within 1 or 2 min. In the course of the investigation their behavioral pattern became indistinguishable from that of the other cats. All cats sniffed frequently and walked in a peculiar way: they moved slowly and cautiously with bended forelegs, the abdomen almost touching the floor. The animals bumped into objects and made the impression of being blind. They were startled when touched by the observer. The pupils, which wele not dilated, showed some reaction to light. Most cats showed a marked divergent strabismus. Ophthalmoscopic examination revealed no abnormalities. The tactile placing response was positive and all visuomotor tests were negative. After 7 days tracking TABLE I DEVELOPMENT OF VISUOMOTOR RESPONSES IN CATS
Numbers indicate days of age in normal kittens and days after dark-rearing in light-deprived cats. Except for obstacle avoidance in each group for each test the time is given of the earliest and that of the latest positive response. In obstacle avoidance the numbers indicate the time in which all cats no longer bumped into objects.
Obstacle avoidance (bumping) Tracking Optokinetic nystagmus (a) drumrate 3½ and 6 rot/min (b) drumrate 1 and 2 rot/min Tactile placing response Visual placing response (a) visually triggered extension (b) visually guided reaching Visual cliff Uncertain jumping Practised jumping
Normal (n ~ 15)
4-months dark-reared (n--5)
7-months dark-reared ( n ~ 16)
26 24-42
13 1- 8
14 7-13
26-31 31-38 31-35
5-- 9 9-19 0
19-27 27-35 0
28-33 35-69 28-35 33-56 56-70
13-21 22-29 8-20 5-33 33~9
14-23 42-54 49-56 13-42 42 70
237
tracking
optokinetic nystagmus tactile
placing response visual placing response a. extension b.visually
guided reaching visual cliff
uncertain jumping
practised jumping 1
2
3
4
5
6
7
8
9 10 weeks
Fig. 1. Development of visuomotor responses. Horizontal bars indicate the periods in which the responses became positive: white, range of days after birth in normal cats; black, range of days after dark rearing in 7-months light-deprived cats; hatched, range of days after dark rearing in 4-months light-deprived cats. movements began to appear. At first the head and eyes followed large objects (for instance a white towel), but within a few days smaller objects (a ball of 5 cm diameter) could also be tracked (Table I, Fig. 1). After 14 days, the cats did not bump into objects anymore. At this time the visually triggered extension response appeared and uncertain jumping behavior developed. In the third week the optokinetic nystagmus could be elicited with 3.5 or 6 drum rotations/min, whereas in the fourth week this reaction was also apparent with 1 or 2 rotations/min (rot./min, Table I). The other tests became positive also, but required a markedly longer time for development. After some 6 weeks the cats showed adequate visually guided reaching. At that time they developed the normal preference to the shallow side in the visual cliff test. The jumping behavior varied considerably among the animals. Some cats were able to make normally balanced jumps, both up and down after 6 weeks. In other cats this development took some 9 or 10 weeks. As mentioned before, 6 out of 16 of the 7-months dark-reared cats were extremely shy after leaving the dark room. Four of these cats became more and more aggressive and had to be killed after 7-9 weeks. All other cats were, and remained, friendly and cooperative.
(b) 4-months dark-reared At first the 4-months dark-reared cats showed, in general, the same behavior
238 as the 7-months dark-reared ones. However, these animals seemed to improve already from the second day on. At that time the animals were able to follow large objects which were moved above or around their head. Normal tracking was seen after about 8 days. As can be seen in Fig. 1 and Table I, all other tests also developed at an earlier time than in the 7-months dark-reared cats. N o r m a l cats
The visuomotor coordination of visually inexperienced normal kittens developed completely in the course of about 10 weeks after birth. The details are given in Table I and Fig. 1. There is a loose similarity of the time periods in which the reactions appeared in normal development and during recovery after light deprivation. DISCUSSION
In the present study all light-deprived cats revealed a complete recovery of their visuomotor behavior within 10 weeks after the deprivation time. This confirms the results of Baxter 1, as far as obstacle avoidance, tracking, visually triggered extension and jumping from a 15 cm high surface (comparable with our uncertain jumping) is concerned. However in Baxter's study, which covered a post-deprivation period of about 30 days, complicated visuomotor coordination was not tested. Baxter emphasized the importance of the visual experience by showing that the time necessary to achieve a certain degree of recovery amounted to 10 days in cats kept at home, and more than 30 days in cats who were confined to cages. In spite of the fact that our animals played in large rooms for at least 4 h daily, recovery in visually guided reaching, visual cliff behavior and practised jumping required a much longer time (some 6-10 weeks) (Table I, Fig. 1). This is in agreement with the findings of Fitch 5 who described that impairment of more complicated tests like the visual cliff behavior were still present 20 days following light deprivation. The results of Walk and Gibson 20 and Held and Hein s seem to be contradictory. They found in BD cats, by using the visual cliff, a recovery in depth discrimination after, respectively, 7 days and 30 h of normal environment. However, in both studies the kittens were raised in darkness for a comparatively short period, namely 26 days in Walk and Gibson's study and 8-11 weeks in the case of Held and Hein, which in both cases is within the critical period as described by Hubel and Wiese111 for monocularly deprived cats. Since, according to Blakemore and Van Sluyters 3 the effects of monocular deprivation are reversible within this period, i.e. between 5 weeks and 4 months of age, the effects of short lasting binocular deprivation cannot be compared with that of binocular deprivation continuing for at least 4 months from birth. Wiesel and Hube122, 2a reported that animals deprived binocularly by lid suturing during the first 3 months of life showed profound visual deficits which demonstrated little recovery when one deprived eye had been opened for as long as 14 months after the deprivation period. Only one BD cat was studied in this way, and specific tests are not mentioned. Chow and Stewart a repeated these experiments in 4 BD cats and described that
239 following opening of one eye for 4--14 months, 'the animals could be distinguished from normal cats, only by an overly reactive startle response to sudden stimulation'. However, 'they still moved with exceptional caution when in novel environments'. So apparently these animals were still handicapped. Striated pattern discrimination tests could be mastered, but no other behavioral data are given. These findings are not controversial to that of the present report, since monocular exposure after binocular deprivation is not comparable with binocular exposure. As can be gathered from the electrophysiological findings in the visual cortex by both Hubel and Wiesel and by Chow and Stewart, monocular exposure after binocular deprivation may be compared with monocular deprivation. So the behavioral changes found in both studies may be considered as long-term effects of monocular deprivation. Sherman 13 described permanent changes in interocular alignment after binocular deprivation. In agreement with this some degree of strabismus was observed in all animals described in the present report. Apparently the visual field defects found in perimetry testing as described by Sherman 15,16, as well as the strabismus, do not interfere with visuomotor coordination. Hoffmann and Cynader1°, in studying one of our 4-months dark-reared cats electrophysiologically, demonstrated that the behavioral recovery after BD seems to be attended by a reversal of the changes in lateral geniculate nucleus cells as found early after deprivation. All apparently controversial effects of binocular deprivation can be explained if certain prerequisites are made. Binocular deprivation must be continued from birth for a period of at least 4 months; the subsequent recovery period must be extended for at least 10 weeks, in which period the animals must be allowed to get visual (and motor) experience by way of both eyes; behavioral recovery can only be judged if several behavioral tests are used and carried out in novel environments. Except for minor discrepancies, probably due to technical differences, the development of the visuomotor behavior in normal cats was generally in good agreement with previous descriptions: obstacle avoidancel~; visually placing response12,18,21; depth perception in the visual cliff12; trackinglZ, z4. (Compared to Norton's results the appearance of tracking in our cats seems to be late, but whereas Norton was looking for the first sign of a following response, in our cats tracking was called positive only if consistent following was observed in both directions.) One exception concerns the optokinetic nystagmus. Using a similar method, Warkentin and Smith 21 already observed an optokinetic nystagmus in normal kittens from the fifteenth to the nineteenth day after birth, whereas in our experiments a nystagmus could not be observed until the twenty-sixth day. A possible explanation for this discrepancy may be due to differing drum rates. In BD cats Fitch 5 and Vital-Durand and co-workers T M could elicit an optokinetic nystagmus immediately after light deprivation. However, in these studies an electro-oculographic method was used, which is quite likely a more sensitive method than ours, Since in studying the development of normal kittens optokinetic nystagmus had to be tested daily from the time of natural eye opening, which is 7-10 days after birth,
240 in our study oculographic testing was discarded to avoid possible interference with normal development. Consequently, to compare recovery after early deprivation with normal development, the same method had to be used. Our method, as such, seems to be justified by the similarity of the responses seen in the 3 groups of animals (15 normal, five 4-months dark-reared, and sixteen 7-months dark-reared cats). Fig. 1 shows the time periods in which the various responses developed after dark-rearing in both groups of light-deprived cats to be roughly in accordance with those found in normally visually inexperienced kittens. It seems reasonable to assume that those reactions, which appear relatively late, are the ones which require a more elaborate neuronal circuitry. Since the response of a neuronal network depends on the nervous elements and on the topology of the interneuronal connections, it may not be concluded that the underlying processes are identical. Recovery after dark-rearing seems to a large extent due to synapse activation in innately determined networks 9,19, whereas during postnatal development the growth of the wiring diagram is more likely of greater importance. As long as this problem has not been solved, the similarities of the time duration as found in newborn kittens and in 7-months light-deprived cats should be considered a coincidence. The more so since those periods are shorter in the 4-months light-deprived cats. The fact that complete recovery took place, even following dark-rearing for 7 months, shows that the plasticity of the cat's visuomotor system is not limited to the early postnatal period. ACKNOWLEDGEMENTS
The author is greatly indebted to Dr. James M. Sprague for reading the manuscript and to Dr. Marius W. van Hof for his help and encouragement during this project.
REFERENCES 1 BAXTER,B. L., Effect of visual deprivation during postnatal maturation on the electroencephalo-
gram of the cat, Exp. Neurol., 14 (1966) 224-237. 2 BLAKEMORE, C., Development of functional connexions in the mammalian visual system, Brit.
Med. Bull., 30 (1974) 152-157. 3 BLAKEMORE,C., AND VAN SLUYTERS,R. C., Reversal of the physiological effects of monocular deprivation in kittens: further evidence for a sensitive period, J. Physiol. (Lond.), 237 (1974) 195216. 4 CHOW,K. L., AND STEWART, n . L., Reversal of structural and functional effects of long-term visual deprivation in cats, Exp. Neurol., 34 (1972) 409-433. 5 FITCH,M. H., Development of Visuomotor Behaviorsfollowing Monocular andBinocular Patterned Visual Deprivation in the Cat, Thesis, University of California at Riverside, 1971. 6 GANZ,L., HIRSCH,H. V. B., ANDTIEMAN,S. B., The nature of perceptual deficits in visually deprived cats, Brain Research, 44 (1972) 547-568. 7 HEIN, A., AND HELD, R., Dissociations of the visual placing response into elicited and guided components, Science, 158 (1967) 390-392. 8 HELD,R., ANDHEIN,A.~ Movement produced stimulation in the development of visually guided behavior, J. comp. physiol. PsychoL, 56 (1963) 872-876.
241 9 VAN HOF, M. W., Retinal input and early development of the visual system, Xlth I.S.C.E.R.G. Symposium, Doc. Ophthalmol. Proc. Set., 4 0974) 495-501. 10 HOFFMANN,K.-P., ANt) CYNAt)ER,M., Recovery in the LGN of the cat after early visual deprivation, Brain Research, 85 (1975) 179. 11 HUBEL, D. H., AND WIESEL,T. N., The period of susceptibility to the physiological effects of unilateral eye closure in kittens, J. Physiol. (Lond.), 206 (1970) 419-436. 12 NORTON, T. T., Receptive field properties of superior coUiculus cells and development of visua. behavior in kittens, J. Neurophysiol., 37 (1974) 674-691. 13 SHERMAN,S. M., Development of interocular alignment in cats, Brain Research, 37 (1972) 187203. 14 SHERMAN,S. M., Visual development in cats, Invest. Ophthalmol., 11 (1972) 394-402. 15 SHERMAN,S. M., Visual field defects in monocularly and binocularly deprived cats, Brain Research, 49 (1973) 25-45. 16 SHERMAN, S. M., Permanence of visual perimetry deficits in monocularly and binocularly deprived cats, Brain Research, 73 (1974) 491-501. 17 VITAL-DURAND,F., PUTKONEN, P. T. S., AND JEANNEROD,M., Letter to the editor. Motion detection and optokinetic responses in dark-reared kittens, Vision Res., 14 (1974) 141-142. 18 VITAL-DURAND,F., AND JEANNEROD,M., Maturation of the optokinetic response: genetic and environmental factors, Brain Research, 71 (1974) 249-257. 19 VRENSEN,G., AND DE GROOT, D., The effect of dark rearing and its recovery on synaptic terminals in the visual cortex of rabbits. A quantitative electron microscopic study, Brain Research, 78 (1974) 263-279. 20 WALK,R. D., AND GIaSON, E. J., A comparative and analytical study of depth perception, Psychol. Monogr., 75 0961) 15 (No. 519). 21 WARKENTIN,J., ANt) SMITH,K. U., The development of visual acuity in the cat, J. genet. Psychol., 50 (1937) 371-399. 22 WIESEL,T. N., AND HUBEL,D. H., Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens, J. Neurophysiol., 28 (1965) 1029-1040. 23 WIESEL,T. N., AND HUBEL, O. H., Extent of recovery from the effects of visual deprivation in kittens, J. Neurophysiol., 28 0965) 1060-1072. 24 WINDLE,W. F., Normal behavioral reactions in kittens correlated with the postnatal development of nerve-fiber density in the spinal gray matter, J. comp. Neurol., 50 (1930) 479-503.
233
D E V E L O P M E N T OF VISUOMOTOR BEHAVIOR IN N O R M A L A N D D A R K R E A R E D CATS
J. VAN H O F - V A N D U I N
Department of Physiology, Erasmus University Rotterdam, P.O. Box 1738, Rotterdam (The Nether-
lands)
(Accepted August 16th, 1975)
SUMMARY
The development of visuomotor coordination in light-deprived cats was compared with that of newborn animals, raised under normal circumstances, using behavioral tests. Two groups of light-deprived cats were studied: one of which was dark-reared for 4 months, the other for 7 months. After dark-rearing the cats were kept in animal rooms which were illuminated for 12 h each day. All cats spent at ieast 4 h each day in a big playroom, where toys were available. Obstacle avoidance, tracking of' moving objects, optokinetic nystagmus, visually triggered extension, visually guided placing, visual cliff behavior and jumping were tested. All lightdeprived cats revealed a complete recovery of visuomotor behavior; the 7-months deprived cats recovered within 10 weeks and the 4-months deprived ones within 7 weeks. The time period in which the various responses in both groups of lightdeprived cats developed after dark-rearing was found to be roughly in accordance with that of normally visually inexperienced kittens after birth.
INTRODUCTION
It is generally accepted that binocular light deprivation leads to visuomotor deficits which are less severe than those found after monocular deprivation. However, although agreement exists on the fact that early after deprivation binocularly deprived (BD) cats demonstrate profound behavioral defects, there is a diversity of opinion as to the permanence of these deprivation effects1,4-6,1a-a6,z2,2a. Whereas in BD cats Wiesel and Hube123 reported little recovery one year after the deprivation time, Baxter 1 described recovery in 5 behavioral tests in 30 days. No behavioral abnormalities could be determined by Chow and Stewart 4 6-10 months after the deprivation period. Neither Wiesel and Hubel, nor Chow and Stewart mentioned results of
234 specific tests in judging the long-term behavioral effects of deprivation. Therefore the discrepancies could be due to the different nature of the tests used in the investigations, and to differences in specific visual training after the deprivation period. As part of a long-term study on deprivation, which includes the behavioral effects of monocular deprivation, the present study is confined to the behavioral effects of binocular deprivation. In order to get a better understanding of the longterm effects of binocular deprivation, a relatively large number of behavioral tests (obstacle avoidance, tracking of moving objects, optokinetic nystagmus, tactile placing response, visually triggered extension, visually guided reaching, visual cliff and jumping behavior) was regularly applied to dark-reared cats for a period of at least 6 months after the deprivation time. The duration o f the recovery period in each of those tests was determined. To achieve optimal motor development the animals were allowed to stay in large playrooms for at least 4 h each day. Since the properties of visual cortex neurons found in BD cats (less than half of the cells being normally responsive, the other cells being sluggish, unpredictable and either responsive to visual stimuli but not selective for orientation, or not responsive to visual stimulation at all) are comparable with those found in visually inexperienced kittens, the term 'immaturity' has been introduced to describe the situation in the visual cortex of BD cats 2,14. If this qualification applies to the visuomotor system in general, one would expect the behavioral recovery after light deprivation to be a replica of the visuomotor development in newborn kittens raised under normal circumstances. Therefore, in the present report, by using the aforementioned tests, the behavioral development of newborn kittens raised under normal circumstances was determined and compared with that of BD cats after dark-rearing. MATERIAL
Dark-reared cats
All kittens were born and kept in complete darkness. Weaning took place two months after birth. Then one group of 5 kittens from two separate litters was kept in darkness for another two months; a second group consisting of 16 kittens from 5 separate litters was kept in darkness until the cats were 7 months old. In darkness the cats were housed in large cages in groups of 2-4 cats per cage where they were handled daily. When the cats were 4 or 7 months old they were housed in large cages in the animal room, which was illuminated with artificial light for 12 h each day. After 4-7 days they were allowed to play 4-6 h each day in a large playroom where toys, stepchairs etc. were available. During the first 4 weeks all dark-reared cats were tested each day, and later on twice a week. In spite of the daily handling 6 of the 7-months dark-reared cats became aggressive and were not co-operative in some of the behavioral tests. Normal cats
Development was followed in 15 kittens from 4 separate litters born in the
235 laboratory. After weaning, which also took place two months after birth, the animals were housed in large cages in groups of 2-4 kittens per cage. The animal room was illuminated by artificial light for 12 h each day. In turn groups of these cats were also allowed to play for 4-6 h each day in large playrooms. Seven kittens from two litters were tested three times per week from the second week of age; 8 kittens from two other litters were tested once or twice a week from the fourth week on. METHODS
(1) Obstacle avoidance. In animals walking freely around in an area enclosed by a thin iron wire fence, bumping against the enclosure was scored. Also the reactions were studied, when objects were placed in front of their heads unexpectedly. (2) Tracking of moving objects above and around the animal's head was tested in a well-lit r o o m with the aid of objects (of several sizes and colors) hanging from an iron wire. (3) Optokinetic nystagmus was studied by looking at the cat's eyes while observer and cat were sitting inside a rotating drum. The radius of the drum was 60 cm, the height 120 cm. The cat's head was held in the center of the drum. The pattern consisted of black and white vertical stripes, each 9 cm wide. In this way the width of one stripe as seen from the center of the drum amounted to 8.57 ° (or the frequency of the square wave grating was 0.058 cycles/degree). D r u m rates used in the experiments were 1, 2, 3.5 or 6 rotations/min. Testing was done with clockwise as well as with counterclockwise rotations. (4) To test the presence of the tactile placing response a cat was held in such a way that its head and forelegs were free to move. While both eyes were covered the animal was slowly carried downwards towards the edge of a table. The dorsa of its front paws were then brought into contact with the vertical edge of the table. In case of a positive response the cat will stretch its claws and place its paws on the table. (5) Visually triggered extension was assessed by carrying an animal slowly downwards towards a broad surface. The reaction was scored as positive if, in approaching the surface, the cat showed an extension of the forelegs. (6) Visually guided reaching was tested with the aid of an interrupted surface as described by Hein and Held 7. The apparatus consisted of a board with 7.5 cm cutouts spaced to form 20 cm long, parallel prongs (of 2.5 cm each). The cat was carried downwards with one forelimb restrained. Ten trials were given with each forelimb. The ratio between the number of prong contacts and failures was determined. (7) The visual cliff consisted of a narrow platform raised 8 cm above the center of a large piece of plate glass. On one side of the platform a checker-board cloth was fixed directly to the underside of the glass. The same pattern was placed 40 cm below the glass on the other side o f the platform. Both surfaces were of equal brightness. The cat was placed on the platform ten times per session. The ratio was determined between descents to the optically shallow and the optically deep surface. (8) Jumping behavior was studied by observing the cats after placing them on top of
236 a 60 cm high stepchair. If the cats did not jump spontaneously, they were helped by folding out two steps. A distinction was made between 'uncertain' and 'practised' jumping. In 'uncertain' jumping the cats felt their way first and when they finally jumped, they gave at the knees. 'Practised' jumping was seen when the animals were able to judge distances and showed a normal landing behavior. RESULTS
Dark-reared cats (a) 7-months dark-reared After removal from the dark-room each cat remained in an enclosure of some 10 sq.m for 30-60 min. In two out of 16 cats convulsive movements occurred immediately after exposure to light. These animals fell down, but recovered within 1 or 2 min. In the course of the investigation their behavioral pattern became indistinguishable from that of the other cats. All cats sniffed frequently and walked in a peculiar way: they moved slowly and cautiously with bended forelegs, the abdomen almost touching the floor. The animals bumped into objects and made the impression of being blind. They were startled when touched by the observer. The pupils, which wele not dilated, showed some reaction to light. Most cats showed a marked divergent strabismus. Ophthalmoscopic examination revealed no abnormalities. The tactile placing response was positive and all visuomotor tests were negative. After 7 days tracking TABLE I DEVELOPMENT OF VISUOMOTOR RESPONSES IN CATS
Numbers indicate days of age in normal kittens and days after dark-rearing in light-deprived cats. Except for obstacle avoidance in each group for each test the time is given of the earliest and that of the latest positive response. In obstacle avoidance the numbers indicate the time in which all cats no longer bumped into objects.
Obstacle avoidance (bumping) Tracking Optokinetic nystagmus (a) drumrate 3½ and 6 rot/min (b) drumrate 1 and 2 rot/min Tactile placing response Visual placing response (a) visually triggered extension (b) visually guided reaching Visual cliff Uncertain jumping Practised jumping
Normal (n ~ 15)
4-months dark-reared (n--5)
7-months dark-reared ( n ~ 16)
26 24-42
13 1- 8
14 7-13
26-31 31-38 31-35
5-- 9 9-19 0
19-27 27-35 0
28-33 35-69 28-35 33-56 56-70
13-21 22-29 8-20 5-33 33~9
14-23 42-54 49-56 13-42 42 70
237
tracking
optokinetic nystagmus tactile
placing response visual placing response a. extension b.visually
guided reaching visual cliff
uncertain jumping
practised jumping 1
2
3
4
5
6
7
8
9 10 weeks
Fig. 1. Development of visuomotor responses. Horizontal bars indicate the periods in which the responses became positive: white, range of days after birth in normal cats; black, range of days after dark rearing in 7-months light-deprived cats; hatched, range of days after dark rearing in 4-months light-deprived cats. movements began to appear. At first the head and eyes followed large objects (for instance a white towel), but within a few days smaller objects (a ball of 5 cm diameter) could also be tracked (Table I, Fig. 1). After 14 days, the cats did not bump into objects anymore. At this time the visually triggered extension response appeared and uncertain jumping behavior developed. In the third week the optokinetic nystagmus could be elicited with 3.5 or 6 drum rotations/min, whereas in the fourth week this reaction was also apparent with 1 or 2 rotations/min (rot./min, Table I). The other tests became positive also, but required a markedly longer time for development. After some 6 weeks the cats showed adequate visually guided reaching. At that time they developed the normal preference to the shallow side in the visual cliff test. The jumping behavior varied considerably among the animals. Some cats were able to make normally balanced jumps, both up and down after 6 weeks. In other cats this development took some 9 or 10 weeks. As mentioned before, 6 out of 16 of the 7-months dark-reared cats were extremely shy after leaving the dark room. Four of these cats became more and more aggressive and had to be killed after 7-9 weeks. All other cats were, and remained, friendly and cooperative.
(b) 4-months dark-reared At first the 4-months dark-reared cats showed, in general, the same behavior
238 as the 7-months dark-reared ones. However, these animals seemed to improve already from the second day on. At that time the animals were able to follow large objects which were moved above or around their head. Normal tracking was seen after about 8 days. As can be seen in Fig. 1 and Table I, all other tests also developed at an earlier time than in the 7-months dark-reared cats. N o r m a l cats
The visuomotor coordination of visually inexperienced normal kittens developed completely in the course of about 10 weeks after birth. The details are given in Table I and Fig. 1. There is a loose similarity of the time periods in which the reactions appeared in normal development and during recovery after light deprivation. DISCUSSION
In the present study all light-deprived cats revealed a complete recovery of their visuomotor behavior within 10 weeks after the deprivation time. This confirms the results of Baxter 1, as far as obstacle avoidance, tracking, visually triggered extension and jumping from a 15 cm high surface (comparable with our uncertain jumping) is concerned. However in Baxter's study, which covered a post-deprivation period of about 30 days, complicated visuomotor coordination was not tested. Baxter emphasized the importance of the visual experience by showing that the time necessary to achieve a certain degree of recovery amounted to 10 days in cats kept at home, and more than 30 days in cats who were confined to cages. In spite of the fact that our animals played in large rooms for at least 4 h daily, recovery in visually guided reaching, visual cliff behavior and practised jumping required a much longer time (some 6-10 weeks) (Table I, Fig. 1). This is in agreement with the findings of Fitch 5 who described that impairment of more complicated tests like the visual cliff behavior were still present 20 days following light deprivation. The results of Walk and Gibson 20 and Held and Hein s seem to be contradictory. They found in BD cats, by using the visual cliff, a recovery in depth discrimination after, respectively, 7 days and 30 h of normal environment. However, in both studies the kittens were raised in darkness for a comparatively short period, namely 26 days in Walk and Gibson's study and 8-11 weeks in the case of Held and Hein, which in both cases is within the critical period as described by Hubel and Wiese111 for monocularly deprived cats. Since, according to Blakemore and Van Sluyters 3 the effects of monocular deprivation are reversible within this period, i.e. between 5 weeks and 4 months of age, the effects of short lasting binocular deprivation cannot be compared with that of binocular deprivation continuing for at least 4 months from birth. Wiesel and Hube122, 2a reported that animals deprived binocularly by lid suturing during the first 3 months of life showed profound visual deficits which demonstrated little recovery when one deprived eye had been opened for as long as 14 months after the deprivation period. Only one BD cat was studied in this way, and specific tests are not mentioned. Chow and Stewart a repeated these experiments in 4 BD cats and described that
239 following opening of one eye for 4--14 months, 'the animals could be distinguished from normal cats, only by an overly reactive startle response to sudden stimulation'. However, 'they still moved with exceptional caution when in novel environments'. So apparently these animals were still handicapped. Striated pattern discrimination tests could be mastered, but no other behavioral data are given. These findings are not controversial to that of the present report, since monocular exposure after binocular deprivation is not comparable with binocular exposure. As can be gathered from the electrophysiological findings in the visual cortex by both Hubel and Wiesel and by Chow and Stewart, monocular exposure after binocular deprivation may be compared with monocular deprivation. So the behavioral changes found in both studies may be considered as long-term effects of monocular deprivation. Sherman 13 described permanent changes in interocular alignment after binocular deprivation. In agreement with this some degree of strabismus was observed in all animals described in the present report. Apparently the visual field defects found in perimetry testing as described by Sherman 15,16, as well as the strabismus, do not interfere with visuomotor coordination. Hoffmann and Cynader1°, in studying one of our 4-months dark-reared cats electrophysiologically, demonstrated that the behavioral recovery after BD seems to be attended by a reversal of the changes in lateral geniculate nucleus cells as found early after deprivation. All apparently controversial effects of binocular deprivation can be explained if certain prerequisites are made. Binocular deprivation must be continued from birth for a period of at least 4 months; the subsequent recovery period must be extended for at least 10 weeks, in which period the animals must be allowed to get visual (and motor) experience by way of both eyes; behavioral recovery can only be judged if several behavioral tests are used and carried out in novel environments. Except for minor discrepancies, probably due to technical differences, the development of the visuomotor behavior in normal cats was generally in good agreement with previous descriptions: obstacle avoidancel~; visually placing response12,18,21; depth perception in the visual cliff12; trackinglZ, z4. (Compared to Norton's results the appearance of tracking in our cats seems to be late, but whereas Norton was looking for the first sign of a following response, in our cats tracking was called positive only if consistent following was observed in both directions.) One exception concerns the optokinetic nystagmus. Using a similar method, Warkentin and Smith 21 already observed an optokinetic nystagmus in normal kittens from the fifteenth to the nineteenth day after birth, whereas in our experiments a nystagmus could not be observed until the twenty-sixth day. A possible explanation for this discrepancy may be due to differing drum rates. In BD cats Fitch 5 and Vital-Durand and co-workers T M could elicit an optokinetic nystagmus immediately after light deprivation. However, in these studies an electro-oculographic method was used, which is quite likely a more sensitive method than ours, Since in studying the development of normal kittens optokinetic nystagmus had to be tested daily from the time of natural eye opening, which is 7-10 days after birth,
240 in our study oculographic testing was discarded to avoid possible interference with normal development. Consequently, to compare recovery after early deprivation with normal development, the same method had to be used. Our method, as such, seems to be justified by the similarity of the responses seen in the 3 groups of animals (15 normal, five 4-months dark-reared, and sixteen 7-months dark-reared cats). Fig. 1 shows the time periods in which the various responses developed after dark-rearing in both groups of light-deprived cats to be roughly in accordance with those found in normally visually inexperienced kittens. It seems reasonable to assume that those reactions, which appear relatively late, are the ones which require a more elaborate neuronal circuitry. Since the response of a neuronal network depends on the nervous elements and on the topology of the interneuronal connections, it may not be concluded that the underlying processes are identical. Recovery after dark-rearing seems to a large extent due to synapse activation in innately determined networks 9,19, whereas during postnatal development the growth of the wiring diagram is more likely of greater importance. As long as this problem has not been solved, the similarities of the time duration as found in newborn kittens and in 7-months light-deprived cats should be considered a coincidence. The more so since those periods are shorter in the 4-months light-deprived cats. The fact that complete recovery took place, even following dark-rearing for 7 months, shows that the plasticity of the cat's visuomotor system is not limited to the early postnatal period. ACKNOWLEDGEMENTS
The author is greatly indebted to Dr. James M. Sprague for reading the manuscript and to Dr. Marius W. van Hof for his help and encouragement during this project.
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