Effects of the Duration of Dark Rearing on Visually Guided Behavior in the Kitten JOHN W. CRABTREE AUSTIN H. RIESEN Department of Psychology University of California Riverside, California
Fortyeight kittens were dark reared or light reared from birth for 1 to 8 months and formed 6 age groups. Following rearing the kittens were examined daily in several tasks of visually guided behavior. Compared to younger dark-reared groups of kittens, older deprived groups showed longer acquisition times for visual placing to a surface, visual tracking, visually guided reaching to a serrated edge and moving object, and visually guided locomotion on elevated platforms. After dark rearing durations of 3 months or longer, deprived groups displayed overall deficiencies in obstacle avoidance during their 1st postdeprivation month. The older dark-reared groups gave some indication of a direct relationship between duration of dark rearing and both delay in acquisition times for the visually guided behaviors and deficiency in obstacle avoidance. One interpretation of the results is that during dark rearing the kitten may acquire nonvisual behaviors which could interfere with and prolong its development of visually guided behavior subsequent to deprivation.
Kittens which are dark reared from birth appear behaviorally blind when first placed in a patterned light environment. Such kittens initially perform poorly in tasks which require visual guidance in response to obstacles, surfaces, moving objects, and depths (Baxter, 1966; Held & Hein, 1963; Riesen & Aarons, 1959; Riesen, Kurke, & Mellinger, 1953; Riesen & Mellinger, 1956; Van Hof-Van Duin, 1976; Vital-Durand, Putkonen, & Jeannerod, 1974; Walk & Gibson, 1961). This initial deficiency in visual guidance is transient, however, and dark-reared kittens can develop visually guided behaviors during subsequent postdeprivation periods. The postdeprivation time to acquire visually guided behavior varies for kittens with unequal durations of dark rearing from birth. Walk and Gibson (1961) reported that 26-day-old dark-reared kittens required less than 2 weeks after the onset of patterned light exposure to display accuracy in tests of visual placing, visual tracking, depth avoidance, and obstacle avoidance. Using these same tests, Baxter (1966) found that kittens which were deprived of light from birth for 10% months required over 30 days from the onset of patterned light exposure before demonstrating positive responses in Reprint request should be sent to Dr. J. W. Crabtree, Department of Neurology, Stanford University School of Medicine, Stanford, California 94305, U.S.A. Received for publication 25 July 1977 Revised for publication 1 December 1977 Developmental Psychobiology, 12(4):29 1-303 (1979) @ 1979 by John Wiley & Sons, Inc.
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the tests. Recently, Van Hof-Van Duin (1976) reported an increased delay in acquisition of a number of visually guided behaviors in 7-month dark-reared kittens relative to 4-month dark-reared kittens. These studies suggest that with longer durations of dark rearing, postdeprivation acquisition of visually guided behavior is more prolonged in the kitten, but they tell us little, quantitatively, about the kitten’s capacity for visual guidance following dark rearing. The present experiment had a twofold purpose: (1) to examine the relationship between the duration of dark rearing and the initial appearance of several visually guided behaviors in the kitten; and (2) to evaluate the kitten’s postdeprivation ability in visual guidance over days as a function of the duration of dark rearing.
Methods Subjects Forty-eight kittens (Felis domesticus) from 18 litters were born and raised in the laboratory. Litters were randomly assigned to either an experimental or a control condition until 24 subjects were in each condition. The kittens were reared from birth for 1, 2, 3 , 4, 6, or 8 months, establishing 6 age groups for each condition. Each age group included 4 kittens.
Rearing Conditions Shortly after birth, experimental kittens were placed in the darkroom with their mothers. Access to the room was through a double-door, light lock which insured continuous darkness during rearing. Control kittens received patterned light stimulation on a 12-hr light/l2-hr dark cycle, but otherwise their rearing was identicak to that of the experimental kittens. Subjects were weaned at approximately 7 week:$ of age, at which time the mothers were removed from their litters. The kittens were housed in 45 x 45 x 60-cm cages which were occupied by single litters if rearing was for less than 4 months. Animals were placed in separate cages for rearing durations of 4 months or more. Fresh food, water, and bedding were provided for the subjects at regular intervals. Daily handling of the kittens was easily integrated around their routine maintenance. Upon termination of their dark- or light-rearing periods from birth, the kittens were placed in a large room, 3 x 3.5 m, where they lived for the remainder of the experiment. (The kittens’ vibrissae were clipped at this time.) The room was continuously lit and offered a stimulating postrearing environment for the kittenis. Numerous play objects, boxes, and elevated runways were in this environment.
Qualitative Tests of Visually Guided Behavior Apparatus Several implements were employed in qualitative tests of visually guided behavior. These included a red ball, 3 cm in diameter and suspended from a string, a prong apparatus (Hein & Held, 1967) with six 3-cm-wide prongs separated by 6-cm-wide
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Fig. 1. Detail of the rail apparatus showing beam with groove (a), large end platform (b), and smaller, movable platforms (c).
spaces, and a rail apparatus (see Fig. 1). The rail apparatus consisted of a 2.5-m-long, 3-cm-wide beam which was supported at both ends by 1.25-m-high standards. Along the beam, between 3 0 x 40-cm end platforms, 8 x 12-cm platforms were inserted in a 1-cm-wide, 2-cm-deep groove. The smaller platforms could be slid along the groove and could be arranged to create gaps varying from 3 to 20 cm in length. All platform surfaces were 4 cm above the beam.
Procedure Within a few hours following their initial dark-rearing periods, the experimental kittens were administered a battery of visual tests. Thereafter, testing was done daily and was conducted under normal room illumination in the subjects’ postrearing environment. For dark-reared kittens the number of days of postrearing patterned light exposure was recorded when the 1st positive response was demonstrated in each test. Responses were considered positive if they were unambiguously elicited by visual stimuli and were appropriate to the situation. The following tests were given: (1) Visual placing to a surface. The kitten was held by the torso with the forelimbs free and was brought slowly toward a table top. At first dark-reared subjects would extend their limbs in response to simply being lowered. As a control procedure trials were given where no immediate surface was present. A positive response was an outward thrusting of the forelimbs of the kitten when it was lowered only to the table surface. (2) Visual tracking. The red ball was swung slowly (approximately .5 Hz) in front of the subject. At first, orientations to the object were observed and, later, following responses with head and eye movements were recorded. A response was positive if the kitten tracked the ball with head and eye movements for at least several seconds. Care was taken to avoid providing auditory cues while moving the stimulus.
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( 3 ) Visually guided reaching to a serrated edge. One forelimb of the kitten was left free while the kitten was lowered t o the prong apparatus. Placement of the paw on a solid portion of the serrated edge was required. Partial paw placements were not recorded as a positive response. (4) Visually guided reaching to a moving object. The ball was swung in front of the subject. For several days following dark rearing the experimental subjects’ attempts to strike the ball were grossly inaccurate. The kittens would bat vigorously at the ball but would fail to connect with it, Only an accurately guided paw thrust fully striking the object was recorded. (5) Visually guided locomotion on elevated platfomzs. The kitten was placed on one end platform and was required to traverse the rail to a food reward at the other end platform. A baited forceps was sometimes held a short distance in front of the subject at the beginning of a trial. During the early trials the kitten was held under the torso to prevent it from jumping or falling off the apparatus. The kitten’s accuracy in guiding its paws from one platform t o the next was carefully watched and if it made any missteps the trial was considered unsuccessful. The positioning of the platforms was randomly varied from trial to trial, thus changing the gap distances between successive surfaces. Platforms could be added or removed to accommodate the size and reach of the kitten.
Barrier Test of Obstacle Avoidance Apparatus The apparatus was a modification of the maze designed by Fish and Robinson (I97 1). Five barriers, each consisting of fourteen 4-cm-wide vertical slats, interposed and separated six 46 x 46 x 98-cm compartments. The slats were arranged in a row 2 cm apart. When 2 successive slats were removed a 14-cm opening allowed passage between compartments. The barriers were rigidly held in position but slats could be removed and reinserted to change the location of the opening. A start box, 18 x 30 x 40 cm, with a guillotine door was centered in front of the 1st compartment. The interior of the apparatus was flat white and the slats were white on one side and black on the other. The slats were turned SO that their black sides faced the animal as it left the start box. Clear Plexiglas roofing covered each compartment.
Procedure Testing progressed over a 1-month period following the subjects’s initial dark or light rearing. Trials were conducted under normal room lighting which evenly illuminated the barrier apparatus from above. Subjects were first trained to run from the start box to a food dish at the end of the apparatus. The subjects were also maintained on a 22-hr food deprivation schedule. They ate the bulk of their meals, in the end compartment of the apparatus subsequent to completed test trials. Training involved the administration of 3 pretest trials which were given at 24-hr intervals starting on the 1st postrearing day. At this time all slats were removed from the apparatus. Over successive pretest trials the baited food dish was placed at increasing distances from the start box (the center of the 2nd, 4th, and 6th
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compartment, respectively). On each pretest trial the lutten was released from the start box and was required to locate the food dish. To aid the subject in locating the food dish, we provided olfactory cues by holding a baited forceps a short distance in front of the subject between it and the food dish. The barrier slats were reinstated and test trials began on the 4th postrearing day, 24 hr after the last training trial. Testing continued with 1 trial per day for 12 days. Four more trials were given on postrearing Days 25-28. Sixteen trials were administered in all. The kittens were confronted with a different configuration of barrier openings on each trial. The location of each opening could vary over 15 positions. Successive trials required an increasing total distance between openings on a direct path from the start box. All subjects received the same order of trials. Over trials the location of the 1st barrier opening was varied to the left and right of the start box. On Trials 13-16 the slats were reversed so that their white sides faced the subject and the brightness contrast between slats and openings was reduced. Prior to a test trial the subject was placed in the start box. The experimenter initiated the trial by opening the guillotine door by a pulley system. The experimenter was located at the rear and above the apparatus with a full view of the subject’s performance. A mimeographed schema of the maze showing the configuration of barrier openings was used to trace the kitten’s movements during the course of a trial. Only gross movements involving redirection of the entire body were drawn. The tracing was analyzed immediately after the trial. The kitten’s path resembled a continuous series of line segments connecting choice points. The choice points were the start box position and the centers of barrier openings. An orientation was defined by a line segment if the segment resulted from any of the following: (1) a movement from a choice point in a direction other than toward the next choice point; (2) an abrupt change in direction of movement within a compartment; and (3) a movement toward a choice point but without passing beyond that choice point. The number of orientations was counted for the trial and the score was recorded. (In the sample tracings given in Fig. 2A and B, the control and experimental kittens scored 2 and 24 orientations, respectively.) Thus, a kitten could receive a score of 0 orientations, or maximum ability in obstacle avoidance for a test trial, if it moved in a direct path between successive choice points. No subject ever reentered a previously occupied compartment during a trial.
Results
Initial Postrearing Observations All subjects were in good physical condition and remained healthy throughout the experiment. Body weights were comparable among experimental and control kittens of the same age. Upon removal from the darkroom all experimental kittens had a divergent strabismus. For these subjects, pupillary reflexes, both direct and consensual, were present but showed increasing sluggishness with longer deprivation periods. The palpebral reflex was present. Ophthalmoscopic examination revealed clear media and no apparent intraocular abnormalities. When first placed in a light environment all deprived subjects appeared blind,
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A
1 1 I
START
Fig. 2. Tracing of a kitten’s obstacle avoidance performance in the barrier maze on Trial 5 , postrearing Day 8. The continuous line indicates the path taken by the kitten during the trial. The schematic representation of the maze shows the location of the start box, barriers ((squares), and configuration of barrier openings: (A) tracing for an 8-month control kitten; (B) tracing for an 8month experimental kitten.
showing a general neglect for visual cues. As they moved about the environment they did not avoid obstacles and they showed a startle response upon collision with objects. Older dark-reared kittens would move immediately to a wall when placed in an open space and their gait was slow while keeping their torsos in contact with the floor. Most of the deprived kittens appeared easily aroused, exhibiting frequent startle reactions to sudden noises and to tactile stimulation. A seizure occurred in one 8-month deprived subject a few minutes after the onset of light stimulation.
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Qualitative Tests of Visually Guided Behavior For each dark-reared group, positive responses occurred earlier in some tasks than in others. (See Table 1.) Visual placing to a surface always occurred first. This behavior was followed by acquisition of visual tracking and by visually guided reaching to a serrated edge. Positive responses in these 2 tasks generally occurred at the same time or within a few days of each other, and they usually preceded positive responses in visually guided reaching to a moving object. The most difficult task for all experimental groups was visually guided locomotion on elevated platforms. Although for any one behavior the experimental group ranges (in days) overlapped considerably, groups which were deprived for longer durations tended to show longer acquisition times for each behavior. For each visually guided behavior, post hoc rank-sum tests were performed to identify any difference in acquisition times between any 2 experimental groups of consecutive age. The difference in acquisition times between the 2- and 3-month groups was significant for visually guided reaching to both a serrated edge (T’ = 10.5, d f = 4/4, p < .05) and a moving object (T’ = 10.5, d f = 4/4, p < .05). Between the 3- and 4-month groups, the difference in acquisition times was significant for visual tracking (T‘ = 10.0, d f = 4/4, p < .05). For each of the 5 visually guided behaviors, the differewe in acquisition times between the 4- and 6-month groups was significant (T’ = 10.0, d f = 4/4, p < .05). Between the 6- and &month groups, the difference in acquisition times was significant for visually guided reaching to a moving object (T’ = 10.0, d f = 4/4, p < .05) and visually guided locomotion on elevated platforms (T‘ = 10.0, df = 4/4, p < .05).
Barrier Test of Obstacle Avoidance The control kittens showed little difficulty in finding the baited food dish on the 3 pretest trials. They explored the apparatus briefly only on the 1st pretest trial. Compared to the control animals, the experimental subjects moved cautiously during the 1st pretest trial and they explored the apparatus for longer durations before
TABLE 1. Range in Days of Postrearing Patterned Light on which the 1st Positive Response Occurred. Dark-Reared Groups ~
Response Visual placing to a surface Visual tracking Visually guided reaching to a serrated edge Visually guided reaching to a moving object Visually guided locomotion on elevated platforms
~~~
~~~
~
~
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5
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5-8
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< .05)
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4-5
5-6
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8-10
9-13
5-1
6-8
*
10-13
*
14-16
6-9
8-11
*
12-14
*
16-20
3 4-5
2-3 4-5
*
between adjacent groups on rank-sum test.
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locating the baited dish. Their exploratory behavior diminished on the 2nd trial, and by the 3rd pretest trial the experimental subjects readily traversed the length of the apparatus to the food dish. The behavioral strategy employed by the dark-reared subjects in negotiating the maze changed over test days. During the early trials behavior was apparently mediated primarily by somesthetic cues. The I - and 2-month kittens would run straight ahead, bumping into the barriers before turning to one side. Older animals tended to move along the walls and barriers of each compartment. The kittens frequently attempted to force their way through the barriers, and if failing to find an opening innmediately, they would pace back and forth for several seconds. As they paced along the barriers the kittens appeared to be using tactile cues to search for the barrier openings. Running strategy became more visually dominated as trials progressed. Kittens were observed scanning the barrier arrays with head and eye movements and orienting toward barrier openings from a distance. The use of visual cues was apparent within the 1st 4 trials for younger kittens. However, for the 3- through 8-month kittens the use of visual cues did not become obvious until the 2nd postdeprivation week. The mean of the number of orientations (per test day) for all control groups ranged from 1 to 7. The mean scores for the 1-month experimental group fell within the range of mean scores for the 1-month, control group (Fig. 3A). The 2-month experimental group’s mean scores were similar to those of the 2-month control group by the 2nd postrearing week (Fig. 3B). However, for those groups which were dark reared for 3 months and longer, their mean scores did not reach the values of the mean scores for their control groups within the testing period (Fig. 3C-F). The kittens’ orientation scores were entered into a 3-way analysis of variance, with 2 levels of Rearing Condition and 6 levels of Age as between subjects factors and 16 levels of Test Day as a within subjects factor. The orientation scores were treated as repeated measures on the Day factor. The Condition (F = 290.62, df = 1/36, p < .01)
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Fig. 3. Obstacle avoidance performance for matched age groups in the barrier test. Points represent the mean number of orientations of 4 kittens in a group on each designated trial over 16 postrearing days. Performance by the control group is indicated by circles ( 0 ) ; performance by the experimental group is indicated by triangles (A): (A) I-month groups; (B) 2-month groups; (C) 3-month groups; (D)4-month groups; (E) 6-month groups; (F) 8-month groups.
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and Age (F = 17.83, df = 5/36, p < .01) main effects were both significant. The Condition x Age interaction (F = 22.19, df = 5/36, p < .01) was also significant, as were the Day main effect (F = 20.91, df = 15/540, p < .01) and the Condition x Day interaction (F = 10.06, df = 15/540, p < .01). Because the 3 main factors constituted parts of the significant interactions, post hoc comparisons were confined to an analysis of the interactions. The Condition x Age interaction indicated that for the 28-day postrearing period the difference between the overall abilities in obstacle avoidance for dark- and lightreared groups of corresponding age was not the same for all matched age groups. Tukey(a) comparisons were conducted to determine the relative differences among all groups. The total number of orientations over the 16 test days was computed for each group and the differences between these group totals were compared (q = 271, df = 12/36, p = .Ol). The totals for the 1- and 2-month experimental groups and all control
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groups were not significantly different from each other. These same totals, however, were significantly different from the totals of the 3-8-month experimental groups. For the 3-8 month experimental groups, only the totals for the 3-and 8-month groups were significantly different. The results of the Tukey(a) tests showed a deficit in overall obstacle avoidance for those experimental groups which were dark reared for 3 months and longer. Furthermore, this deficit was greater for the 8-month experimental group than for the 3-month experimental group. The Condition x Day interaction signified that the difference between abilities in obstacle avoidance for all dark-reared subjects and for all light-reared subjects was not the same for all test days. Tukey(a) tests were conducted to identify any difference among the day abilities in obstacle avoidance for all dark-reared subjects and for all light-reared subjects. For each test day the total number of orientations was computed for all subjects in each rearing condition. Differences between these day totals were compared (q = 99.29, df = 32/36, p = .Ol). For the light-reared subjects, only the totals for Days 4 and 14 were significantly different. For the dark-reared subjects, the total for Day 4 differed significantly from all other day totals. Totals for Days 5-8 did not differ significantly from one another, nor did the totals for Days 6-15, 8-25, and 9-28. For the dark-reared subjects, the results of the Tukey(a) tests confirmed an improvement in obstacle avoidance over the 4th-9th postrearing days.
Discussion The dark-reared kittens of this study failed t o demonstrate visually guided behavior when first exposed to patterned light. Their initial deficiency in visual guidance was certainly related to their lack of patterned light stimulation but may have been due specifically to their lack of visuomotor reafference. Results from several studies (Hein & Diamond, 1971; Hein, Gower, & Diamond, 1970; Hein & Held, 1967; Held & Hein, 1963; Riesen & Aarons, 1959; Robinson & Fish, 1974) have shown that visuomotor reafference, or visual feedback about one’s limb and body movements, is essential for development of visually guided behavior in the kitten. During dark rearing kittens are prevented from experiencing visuomotor reafference, and until such experience is made available to them, their development of visual guidance is postponed. From the onset of patterned light exposure the deprived groups of kittens required approximately 1-3 weeks to acquire all 5 visually guided behaviors (see Table 1). If the groups were dark reared from birth for at least 3-6 months, acquisition of the visually guided behaviors was prolonged relative to younger deprived groups. Although a direct relationship between the duration of dark rearing and the delay in acquisition of a visually guided behavior was not statistically found, a tendency was evident for such a relationship in the older dark-reared groups. Surprisingly, the dark-reared kittens showed more rapid acquisition of some visually guided behaviors than has been reported for normal-reared kittens. For example, the normally reared kittens first display visual placing to a surface, visual tracking, and visually guided reaching to a serrated edge 2 to 3 weeks after eye-opening (Norton, 1974; Sherman, 1972). For these same behaviors, all deprived groups gave positive responses within 1 or 2 weeks following dark rearing (see Table 1). Sherman (1973) reported similar acquisition times (5 and 17 days) for visually guided behaviors in kittens which were binocularly lid-sutured from birth for 6 and 12 months. However, Van Hof-Van Duin (1976) found that 4- and 7-month dark-reared kittens
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acquired visually guided behaviors within 7-10 postdeprivation weeks, which is considerably longer than the acquisition times found in this study. This discrepancy could be accounted for by differences between the test criteria used and amount of time kittens spent in a stimulating postdeprivation environment. With regard to the latter possibility, Baxter (1966) found faster development of visually guided behaviors in dark-reared kittens which were placed in an ‘‘enriched’’ postdeprivation environment than in those kept in laboratory cages. Furthermore, Konrad and Bagshaw (1970) reported shorter periods of adaptation to a novel environment in normal-reared kittens than in kittens which were reared in confining cages. Summed across test days, obstacle avoidance performance in the barrier maze by the experimental groups tended to become progressively worse with increasing durations of dark rearing. The present findings show that 1-2 months of dark rearing from birth do not appreciably affect the kitten’s ability in obstacle avoidance compared to control group standards. Dark rearing for the 1st 3 postnatal months, however, is sufficient to impair the kitten’s obstacle avoidance, and this impairment becomes more severe with continued dark rearing for several months beyond 3 months of age. The poor obstacle avoidance of the 3-8-month experimental groups is consistent with their prolonged times to acquire visually guided behaviors. The dark-reared kittens’ performance in the barrier maze improved over the 1st 6 days of testing. This initial improvement in obstacle avoidance may be due in part to practice in running the maze, and more generally, it could reflect a developmental period in which the deprived kittens were learning to use visual cues in guiding their behavior. During such a period the dark-reared kittens would come to rely increasingly on visual cues for behavioral guidance and decreasingly on nonvisual cues which they were accustomed to using in their darkroom environment. The dark-reared kittens’ initial improvement in obstacle avoidance is also comparable to that reported for the kitten using an eye which has been deprived of visuomotor reafference (Robinson & Fish, 1974). Dark-reared kittens may acquire habits during deprivation which could subsequently interfere with their development of visually guided behavior (Fox, 1966). The deprived subjects appeared to use, predominantly, tactile cues for guidance in the early trials of the barrier test. This nonvisual guidance in the maze also appeared to persist for more trials for the older dark-reared kittens than for the younger deprived animals. Thus, with longer durations of dark rearing kittens could have become jncreasingly dependent on nonvisual cues for behavioral guidance which in turn would have made development of visually guided behavior more and more difficult subsequent to deprivation. In summary, we found that dark rearing from birth for 3 months or longer prolongs the kitten’s acquisition of visual placing to a surface, visual tracking, visually guided reaching to a serrated edge and moving object, and visually guided locomotion on elevated platforms. The 3-8-month deprived groups provided some evidence for progressively longer delays in acquisition of visually guided behaviors with longer durations of dark rearing. Obstacle avoidance ability was also impaired for those groups which were dark reared from birth for 3 or more months.
Notes This study is based upon data from a dissertation submitted by the 1st author in partial fulfillment of the Ph.D. degree at the University of California, Riverside. This research was
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supported in part by PHS Grant EY00573 to A. H. Riesen. The technical assistance of Steve Bunyak and Garro Fanto is gratefully acknowledged. J. W. C. is now at Department of Neurology, Stanford University School of Medicine, Stanford, California.
References Baxter, B. L. (1966). Effect of visual deprivation during postnatal maturation o n the electroencephalogram of the cat. Exp. Neurot., 14: 224-237. Fish, S. E., and Robinson, J. S. (1971). A new coordination test of visual-motor deprived, visually experienced cats. Psychon. Sci, 22: 28-29. Fox, M. W. (1966). Neuro-behavioral ontogeny. A synthesis of ethological and neurophysiological concepts. Bruin Res., 2: 3-20. Hein, A., and Diamond, R. M. (1971). Contrasting development of visually triggered and guided movements in kittens with respect to interocular and interlimb equivalence. J. Comp. Physiol. Psych ol., 76 2 19-224. Hein, A., Gower, E. C., and Diamond, R. M. (1970). Exposure requirements for developing the triggered component of the visual-placing response. J. Comp. Physiol. Psychol., 73: 188-192. Hein, A., and Held, R. (1967). Dissociation of the visual placing response into elicited and guided components. Science, 158: 390-391. Held, R., and Hein, A. (1963). Movement-produced stimulation in the development of visually guided behavior. J. Comp. Physiol. Psychol., 56: 872-876. Konrad, K. W., and Bagshaw, M. (1970). The effect of novel stimuli o n cats reared in a restricted environment. J. Comp. Physiol. Psychol., 70: 157-164. Norton, T. T. (1974). Receptive-field properties of superior colliculus cells and development of visual behavior in kittens. J. Neurophysiol,, 37: 674-690. Riesen, A. H., and Aarons, L. (1959). Visual movement and intensity discrimination in cats after early deprivation of pattern vision. J. Comp. fhysiol. Psychol., 52: 142-149. Riesen, A. H., Kurke, M. I., and Metlinger, J. C. (1953). Interocular transfer of habits learned monocularly in visually naive and visually experienced cats. J. Comp. Physiol. Psychol., 46: 166-172. Riesen, A. H., and Mellinger, J. C. (1956). Interocular transfer of habits in cats after alternating monocular visual experience. J. Comp. Physiol. Psychol., 49: 5 16-520. Robinson, J. S., and Fish, S. E. (1974). A cat’s form+xperienced but visual-motor deprived eye lacks focal vision. Dev. Psychobiol., 7: 331-342. Sherman, S. M. (1972). Development of interocular alignment in cats. Bruin Res., 37: 187-203. Sherman, S . M, (1973). Visual field defects in monocularly and binocularly deprived cats. Bruin Res., 4 9 : 25-45. Van Hof-Van Duin, J. (1976). Development of visuomotor behavior in normal and dark-reared cats. Brain Res.. 104: 233-241. Vital-Durand, F., Putkonen, P. T. S., and Jeannerod, M. (1974). Motion detection and optokinetic responses in dark-reared kittens. Vision Res., 14: 141-142. Walk, R. D., and Gibson, E. J. (1961). A comparative and analytic study of visual depth perception. fsychot. Monogr., 75: No. 519.
Fortyeight kittens were dark reared or light reared from birth for 1 to 8 months and formed 6 age groups. Following rearing the kittens were examined daily in several tasks of visually guided behavior. Compared to younger dark-reared groups of kittens, older deprived groups showed longer acquisition times for visual placing to a surface, visual tracking, visually guided reaching to a serrated edge and moving object, and visually guided locomotion on elevated platforms. After dark rearing durations of 3 months or longer, deprived groups displayed overall deficiencies in obstacle avoidance during their 1st postdeprivation month. The older dark-reared groups gave some indication of a direct relationship between duration of dark rearing and both delay in acquisition times for the visually guided behaviors and deficiency in obstacle avoidance. One interpretation of the results is that during dark rearing the kitten may acquire nonvisual behaviors which could interfere with and prolong its development of visually guided behavior subsequent to deprivation.
Kittens which are dark reared from birth appear behaviorally blind when first placed in a patterned light environment. Such kittens initially perform poorly in tasks which require visual guidance in response to obstacles, surfaces, moving objects, and depths (Baxter, 1966; Held & Hein, 1963; Riesen & Aarons, 1959; Riesen, Kurke, & Mellinger, 1953; Riesen & Mellinger, 1956; Van Hof-Van Duin, 1976; Vital-Durand, Putkonen, & Jeannerod, 1974; Walk & Gibson, 1961). This initial deficiency in visual guidance is transient, however, and dark-reared kittens can develop visually guided behaviors during subsequent postdeprivation periods. The postdeprivation time to acquire visually guided behavior varies for kittens with unequal durations of dark rearing from birth. Walk and Gibson (1961) reported that 26-day-old dark-reared kittens required less than 2 weeks after the onset of patterned light exposure to display accuracy in tests of visual placing, visual tracking, depth avoidance, and obstacle avoidance. Using these same tests, Baxter (1966) found that kittens which were deprived of light from birth for 10% months required over 30 days from the onset of patterned light exposure before demonstrating positive responses in Reprint request should be sent to Dr. J. W. Crabtree, Department of Neurology, Stanford University School of Medicine, Stanford, California 94305, U.S.A. Received for publication 25 July 1977 Revised for publication 1 December 1977 Developmental Psychobiology, 12(4):29 1-303 (1979) @ 1979 by John Wiley & Sons, Inc.
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the tests. Recently, Van Hof-Van Duin (1976) reported an increased delay in acquisition of a number of visually guided behaviors in 7-month dark-reared kittens relative to 4-month dark-reared kittens. These studies suggest that with longer durations of dark rearing, postdeprivation acquisition of visually guided behavior is more prolonged in the kitten, but they tell us little, quantitatively, about the kitten’s capacity for visual guidance following dark rearing. The present experiment had a twofold purpose: (1) to examine the relationship between the duration of dark rearing and the initial appearance of several visually guided behaviors in the kitten; and (2) to evaluate the kitten’s postdeprivation ability in visual guidance over days as a function of the duration of dark rearing.
Methods Subjects Forty-eight kittens (Felis domesticus) from 18 litters were born and raised in the laboratory. Litters were randomly assigned to either an experimental or a control condition until 24 subjects were in each condition. The kittens were reared from birth for 1, 2, 3 , 4, 6, or 8 months, establishing 6 age groups for each condition. Each age group included 4 kittens.
Rearing Conditions Shortly after birth, experimental kittens were placed in the darkroom with their mothers. Access to the room was through a double-door, light lock which insured continuous darkness during rearing. Control kittens received patterned light stimulation on a 12-hr light/l2-hr dark cycle, but otherwise their rearing was identicak to that of the experimental kittens. Subjects were weaned at approximately 7 week:$ of age, at which time the mothers were removed from their litters. The kittens were housed in 45 x 45 x 60-cm cages which were occupied by single litters if rearing was for less than 4 months. Animals were placed in separate cages for rearing durations of 4 months or more. Fresh food, water, and bedding were provided for the subjects at regular intervals. Daily handling of the kittens was easily integrated around their routine maintenance. Upon termination of their dark- or light-rearing periods from birth, the kittens were placed in a large room, 3 x 3.5 m, where they lived for the remainder of the experiment. (The kittens’ vibrissae were clipped at this time.) The room was continuously lit and offered a stimulating postrearing environment for the kittenis. Numerous play objects, boxes, and elevated runways were in this environment.
Qualitative Tests of Visually Guided Behavior Apparatus Several implements were employed in qualitative tests of visually guided behavior. These included a red ball, 3 cm in diameter and suspended from a string, a prong apparatus (Hein & Held, 1967) with six 3-cm-wide prongs separated by 6-cm-wide
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Fig. 1. Detail of the rail apparatus showing beam with groove (a), large end platform (b), and smaller, movable platforms (c).
spaces, and a rail apparatus (see Fig. 1). The rail apparatus consisted of a 2.5-m-long, 3-cm-wide beam which was supported at both ends by 1.25-m-high standards. Along the beam, between 3 0 x 40-cm end platforms, 8 x 12-cm platforms were inserted in a 1-cm-wide, 2-cm-deep groove. The smaller platforms could be slid along the groove and could be arranged to create gaps varying from 3 to 20 cm in length. All platform surfaces were 4 cm above the beam.
Procedure Within a few hours following their initial dark-rearing periods, the experimental kittens were administered a battery of visual tests. Thereafter, testing was done daily and was conducted under normal room illumination in the subjects’ postrearing environment. For dark-reared kittens the number of days of postrearing patterned light exposure was recorded when the 1st positive response was demonstrated in each test. Responses were considered positive if they were unambiguously elicited by visual stimuli and were appropriate to the situation. The following tests were given: (1) Visual placing to a surface. The kitten was held by the torso with the forelimbs free and was brought slowly toward a table top. At first dark-reared subjects would extend their limbs in response to simply being lowered. As a control procedure trials were given where no immediate surface was present. A positive response was an outward thrusting of the forelimbs of the kitten when it was lowered only to the table surface. (2) Visual tracking. The red ball was swung slowly (approximately .5 Hz) in front of the subject. At first, orientations to the object were observed and, later, following responses with head and eye movements were recorded. A response was positive if the kitten tracked the ball with head and eye movements for at least several seconds. Care was taken to avoid providing auditory cues while moving the stimulus.
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( 3 ) Visually guided reaching to a serrated edge. One forelimb of the kitten was left free while the kitten was lowered t o the prong apparatus. Placement of the paw on a solid portion of the serrated edge was required. Partial paw placements were not recorded as a positive response. (4) Visually guided reaching to a moving object. The ball was swung in front of the subject. For several days following dark rearing the experimental subjects’ attempts to strike the ball were grossly inaccurate. The kittens would bat vigorously at the ball but would fail to connect with it, Only an accurately guided paw thrust fully striking the object was recorded. (5) Visually guided locomotion on elevated platfomzs. The kitten was placed on one end platform and was required to traverse the rail to a food reward at the other end platform. A baited forceps was sometimes held a short distance in front of the subject at the beginning of a trial. During the early trials the kitten was held under the torso to prevent it from jumping or falling off the apparatus. The kitten’s accuracy in guiding its paws from one platform t o the next was carefully watched and if it made any missteps the trial was considered unsuccessful. The positioning of the platforms was randomly varied from trial to trial, thus changing the gap distances between successive surfaces. Platforms could be added or removed to accommodate the size and reach of the kitten.
Barrier Test of Obstacle Avoidance Apparatus The apparatus was a modification of the maze designed by Fish and Robinson (I97 1). Five barriers, each consisting of fourteen 4-cm-wide vertical slats, interposed and separated six 46 x 46 x 98-cm compartments. The slats were arranged in a row 2 cm apart. When 2 successive slats were removed a 14-cm opening allowed passage between compartments. The barriers were rigidly held in position but slats could be removed and reinserted to change the location of the opening. A start box, 18 x 30 x 40 cm, with a guillotine door was centered in front of the 1st compartment. The interior of the apparatus was flat white and the slats were white on one side and black on the other. The slats were turned SO that their black sides faced the animal as it left the start box. Clear Plexiglas roofing covered each compartment.
Procedure Testing progressed over a 1-month period following the subjects’s initial dark or light rearing. Trials were conducted under normal room lighting which evenly illuminated the barrier apparatus from above. Subjects were first trained to run from the start box to a food dish at the end of the apparatus. The subjects were also maintained on a 22-hr food deprivation schedule. They ate the bulk of their meals, in the end compartment of the apparatus subsequent to completed test trials. Training involved the administration of 3 pretest trials which were given at 24-hr intervals starting on the 1st postrearing day. At this time all slats were removed from the apparatus. Over successive pretest trials the baited food dish was placed at increasing distances from the start box (the center of the 2nd, 4th, and 6th
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compartment, respectively). On each pretest trial the lutten was released from the start box and was required to locate the food dish. To aid the subject in locating the food dish, we provided olfactory cues by holding a baited forceps a short distance in front of the subject between it and the food dish. The barrier slats were reinstated and test trials began on the 4th postrearing day, 24 hr after the last training trial. Testing continued with 1 trial per day for 12 days. Four more trials were given on postrearing Days 25-28. Sixteen trials were administered in all. The kittens were confronted with a different configuration of barrier openings on each trial. The location of each opening could vary over 15 positions. Successive trials required an increasing total distance between openings on a direct path from the start box. All subjects received the same order of trials. Over trials the location of the 1st barrier opening was varied to the left and right of the start box. On Trials 13-16 the slats were reversed so that their white sides faced the subject and the brightness contrast between slats and openings was reduced. Prior to a test trial the subject was placed in the start box. The experimenter initiated the trial by opening the guillotine door by a pulley system. The experimenter was located at the rear and above the apparatus with a full view of the subject’s performance. A mimeographed schema of the maze showing the configuration of barrier openings was used to trace the kitten’s movements during the course of a trial. Only gross movements involving redirection of the entire body were drawn. The tracing was analyzed immediately after the trial. The kitten’s path resembled a continuous series of line segments connecting choice points. The choice points were the start box position and the centers of barrier openings. An orientation was defined by a line segment if the segment resulted from any of the following: (1) a movement from a choice point in a direction other than toward the next choice point; (2) an abrupt change in direction of movement within a compartment; and (3) a movement toward a choice point but without passing beyond that choice point. The number of orientations was counted for the trial and the score was recorded. (In the sample tracings given in Fig. 2A and B, the control and experimental kittens scored 2 and 24 orientations, respectively.) Thus, a kitten could receive a score of 0 orientations, or maximum ability in obstacle avoidance for a test trial, if it moved in a direct path between successive choice points. No subject ever reentered a previously occupied compartment during a trial.
Results
Initial Postrearing Observations All subjects were in good physical condition and remained healthy throughout the experiment. Body weights were comparable among experimental and control kittens of the same age. Upon removal from the darkroom all experimental kittens had a divergent strabismus. For these subjects, pupillary reflexes, both direct and consensual, were present but showed increasing sluggishness with longer deprivation periods. The palpebral reflex was present. Ophthalmoscopic examination revealed clear media and no apparent intraocular abnormalities. When first placed in a light environment all deprived subjects appeared blind,
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A
1 1 I
START
Fig. 2. Tracing of a kitten’s obstacle avoidance performance in the barrier maze on Trial 5 , postrearing Day 8. The continuous line indicates the path taken by the kitten during the trial. The schematic representation of the maze shows the location of the start box, barriers ((squares), and configuration of barrier openings: (A) tracing for an 8-month control kitten; (B) tracing for an 8month experimental kitten.
showing a general neglect for visual cues. As they moved about the environment they did not avoid obstacles and they showed a startle response upon collision with objects. Older dark-reared kittens would move immediately to a wall when placed in an open space and their gait was slow while keeping their torsos in contact with the floor. Most of the deprived kittens appeared easily aroused, exhibiting frequent startle reactions to sudden noises and to tactile stimulation. A seizure occurred in one 8-month deprived subject a few minutes after the onset of light stimulation.
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Qualitative Tests of Visually Guided Behavior For each dark-reared group, positive responses occurred earlier in some tasks than in others. (See Table 1.) Visual placing to a surface always occurred first. This behavior was followed by acquisition of visual tracking and by visually guided reaching to a serrated edge. Positive responses in these 2 tasks generally occurred at the same time or within a few days of each other, and they usually preceded positive responses in visually guided reaching to a moving object. The most difficult task for all experimental groups was visually guided locomotion on elevated platforms. Although for any one behavior the experimental group ranges (in days) overlapped considerably, groups which were deprived for longer durations tended to show longer acquisition times for each behavior. For each visually guided behavior, post hoc rank-sum tests were performed to identify any difference in acquisition times between any 2 experimental groups of consecutive age. The difference in acquisition times between the 2- and 3-month groups was significant for visually guided reaching to both a serrated edge (T’ = 10.5, d f = 4/4, p < .05) and a moving object (T’ = 10.5, d f = 4/4, p < .05). Between the 3- and 4-month groups, the difference in acquisition times was significant for visual tracking (T‘ = 10.0, d f = 4/4, p < .05). For each of the 5 visually guided behaviors, the differewe in acquisition times between the 4- and 6-month groups was significant (T’ = 10.0, d f = 4/4, p < .05). Between the 6- and &month groups, the difference in acquisition times was significant for visually guided reaching to a moving object (T’ = 10.0, d f = 4/4, p < .05) and visually guided locomotion on elevated platforms (T‘ = 10.0, df = 4/4, p < .05).
Barrier Test of Obstacle Avoidance The control kittens showed little difficulty in finding the baited food dish on the 3 pretest trials. They explored the apparatus briefly only on the 1st pretest trial. Compared to the control animals, the experimental subjects moved cautiously during the 1st pretest trial and they explored the apparatus for longer durations before
TABLE 1. Range in Days of Postrearing Patterned Light on which the 1st Positive Response Occurred. Dark-Reared Groups ~
Response Visual placing to a surface Visual tracking Visually guided reaching to a serrated edge Visually guided reaching to a moving object Visually guided locomotion on elevated platforms
~~~
~~~
~
~
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< .05)
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8-10
9-13
5-1
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*
10-13
*
14-16
6-9
8-11
*
12-14
*
16-20
3 4-5
2-3 4-5
*
between adjacent groups on rank-sum test.
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locating the baited dish. Their exploratory behavior diminished on the 2nd trial, and by the 3rd pretest trial the experimental subjects readily traversed the length of the apparatus to the food dish. The behavioral strategy employed by the dark-reared subjects in negotiating the maze changed over test days. During the early trials behavior was apparently mediated primarily by somesthetic cues. The I - and 2-month kittens would run straight ahead, bumping into the barriers before turning to one side. Older animals tended to move along the walls and barriers of each compartment. The kittens frequently attempted to force their way through the barriers, and if failing to find an opening innmediately, they would pace back and forth for several seconds. As they paced along the barriers the kittens appeared to be using tactile cues to search for the barrier openings. Running strategy became more visually dominated as trials progressed. Kittens were observed scanning the barrier arrays with head and eye movements and orienting toward barrier openings from a distance. The use of visual cues was apparent within the 1st 4 trials for younger kittens. However, for the 3- through 8-month kittens the use of visual cues did not become obvious until the 2nd postdeprivation week. The mean of the number of orientations (per test day) for all control groups ranged from 1 to 7. The mean scores for the 1-month experimental group fell within the range of mean scores for the 1-month, control group (Fig. 3A). The 2-month experimental group’s mean scores were similar to those of the 2-month control group by the 2nd postrearing week (Fig. 3B). However, for those groups which were dark reared for 3 months and longer, their mean scores did not reach the values of the mean scores for their control groups within the testing period (Fig. 3C-F). The kittens’ orientation scores were entered into a 3-way analysis of variance, with 2 levels of Rearing Condition and 6 levels of Age as between subjects factors and 16 levels of Test Day as a within subjects factor. The orientation scores were treated as repeated measures on the Day factor. The Condition (F = 290.62, df = 1/36, p < .01)
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Fig. 3. Obstacle avoidance performance for matched age groups in the barrier test. Points represent the mean number of orientations of 4 kittens in a group on each designated trial over 16 postrearing days. Performance by the control group is indicated by circles ( 0 ) ; performance by the experimental group is indicated by triangles (A): (A) I-month groups; (B) 2-month groups; (C) 3-month groups; (D)4-month groups; (E) 6-month groups; (F) 8-month groups.
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and Age (F = 17.83, df = 5/36, p < .01) main effects were both significant. The Condition x Age interaction (F = 22.19, df = 5/36, p < .01) was also significant, as were the Day main effect (F = 20.91, df = 15/540, p < .01) and the Condition x Day interaction (F = 10.06, df = 15/540, p < .01). Because the 3 main factors constituted parts of the significant interactions, post hoc comparisons were confined to an analysis of the interactions. The Condition x Age interaction indicated that for the 28-day postrearing period the difference between the overall abilities in obstacle avoidance for dark- and lightreared groups of corresponding age was not the same for all matched age groups. Tukey(a) comparisons were conducted to determine the relative differences among all groups. The total number of orientations over the 16 test days was computed for each group and the differences between these group totals were compared (q = 271, df = 12/36, p = .Ol). The totals for the 1- and 2-month experimental groups and all control
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groups were not significantly different from each other. These same totals, however, were significantly different from the totals of the 3-8-month experimental groups. For the 3-8 month experimental groups, only the totals for the 3-and 8-month groups were significantly different. The results of the Tukey(a) tests showed a deficit in overall obstacle avoidance for those experimental groups which were dark reared for 3 months and longer. Furthermore, this deficit was greater for the 8-month experimental group than for the 3-month experimental group. The Condition x Day interaction signified that the difference between abilities in obstacle avoidance for all dark-reared subjects and for all light-reared subjects was not the same for all test days. Tukey(a) tests were conducted to identify any difference among the day abilities in obstacle avoidance for all dark-reared subjects and for all light-reared subjects. For each test day the total number of orientations was computed for all subjects in each rearing condition. Differences between these day totals were compared (q = 99.29, df = 32/36, p = .Ol). For the light-reared subjects, only the totals for Days 4 and 14 were significantly different. For the dark-reared subjects, the total for Day 4 differed significantly from all other day totals. Totals for Days 5-8 did not differ significantly from one another, nor did the totals for Days 6-15, 8-25, and 9-28. For the dark-reared subjects, the results of the Tukey(a) tests confirmed an improvement in obstacle avoidance over the 4th-9th postrearing days.
Discussion The dark-reared kittens of this study failed t o demonstrate visually guided behavior when first exposed to patterned light. Their initial deficiency in visual guidance was certainly related to their lack of patterned light stimulation but may have been due specifically to their lack of visuomotor reafference. Results from several studies (Hein & Diamond, 1971; Hein, Gower, & Diamond, 1970; Hein & Held, 1967; Held & Hein, 1963; Riesen & Aarons, 1959; Robinson & Fish, 1974) have shown that visuomotor reafference, or visual feedback about one’s limb and body movements, is essential for development of visually guided behavior in the kitten. During dark rearing kittens are prevented from experiencing visuomotor reafference, and until such experience is made available to them, their development of visual guidance is postponed. From the onset of patterned light exposure the deprived groups of kittens required approximately 1-3 weeks to acquire all 5 visually guided behaviors (see Table 1). If the groups were dark reared from birth for at least 3-6 months, acquisition of the visually guided behaviors was prolonged relative to younger deprived groups. Although a direct relationship between the duration of dark rearing and the delay in acquisition of a visually guided behavior was not statistically found, a tendency was evident for such a relationship in the older dark-reared groups. Surprisingly, the dark-reared kittens showed more rapid acquisition of some visually guided behaviors than has been reported for normal-reared kittens. For example, the normally reared kittens first display visual placing to a surface, visual tracking, and visually guided reaching to a serrated edge 2 to 3 weeks after eye-opening (Norton, 1974; Sherman, 1972). For these same behaviors, all deprived groups gave positive responses within 1 or 2 weeks following dark rearing (see Table 1). Sherman (1973) reported similar acquisition times (5 and 17 days) for visually guided behaviors in kittens which were binocularly lid-sutured from birth for 6 and 12 months. However, Van Hof-Van Duin (1976) found that 4- and 7-month dark-reared kittens
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acquired visually guided behaviors within 7-10 postdeprivation weeks, which is considerably longer than the acquisition times found in this study. This discrepancy could be accounted for by differences between the test criteria used and amount of time kittens spent in a stimulating postdeprivation environment. With regard to the latter possibility, Baxter (1966) found faster development of visually guided behaviors in dark-reared kittens which were placed in an ‘‘enriched’’ postdeprivation environment than in those kept in laboratory cages. Furthermore, Konrad and Bagshaw (1970) reported shorter periods of adaptation to a novel environment in normal-reared kittens than in kittens which were reared in confining cages. Summed across test days, obstacle avoidance performance in the barrier maze by the experimental groups tended to become progressively worse with increasing durations of dark rearing. The present findings show that 1-2 months of dark rearing from birth do not appreciably affect the kitten’s ability in obstacle avoidance compared to control group standards. Dark rearing for the 1st 3 postnatal months, however, is sufficient to impair the kitten’s obstacle avoidance, and this impairment becomes more severe with continued dark rearing for several months beyond 3 months of age. The poor obstacle avoidance of the 3-8-month experimental groups is consistent with their prolonged times to acquire visually guided behaviors. The dark-reared kittens’ performance in the barrier maze improved over the 1st 6 days of testing. This initial improvement in obstacle avoidance may be due in part to practice in running the maze, and more generally, it could reflect a developmental period in which the deprived kittens were learning to use visual cues in guiding their behavior. During such a period the dark-reared kittens would come to rely increasingly on visual cues for behavioral guidance and decreasingly on nonvisual cues which they were accustomed to using in their darkroom environment. The dark-reared kittens’ initial improvement in obstacle avoidance is also comparable to that reported for the kitten using an eye which has been deprived of visuomotor reafference (Robinson & Fish, 1974). Dark-reared kittens may acquire habits during deprivation which could subsequently interfere with their development of visually guided behavior (Fox, 1966). The deprived subjects appeared to use, predominantly, tactile cues for guidance in the early trials of the barrier test. This nonvisual guidance in the maze also appeared to persist for more trials for the older dark-reared kittens than for the younger deprived animals. Thus, with longer durations of dark rearing kittens could have become jncreasingly dependent on nonvisual cues for behavioral guidance which in turn would have made development of visually guided behavior more and more difficult subsequent to deprivation. In summary, we found that dark rearing from birth for 3 months or longer prolongs the kitten’s acquisition of visual placing to a surface, visual tracking, visually guided reaching to a serrated edge and moving object, and visually guided locomotion on elevated platforms. The 3-8-month deprived groups provided some evidence for progressively longer delays in acquisition of visually guided behaviors with longer durations of dark rearing. Obstacle avoidance ability was also impaired for those groups which were dark reared from birth for 3 or more months.
Notes This study is based upon data from a dissertation submitted by the 1st author in partial fulfillment of the Ph.D. degree at the University of California, Riverside. This research was
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supported in part by PHS Grant EY00573 to A. H. Riesen. The technical assistance of Steve Bunyak and Garro Fanto is gratefully acknowledged. J. W. C. is now at Department of Neurology, Stanford University School of Medicine, Stanford, California.
References Baxter, B. L. (1966). Effect of visual deprivation during postnatal maturation o n the electroencephalogram of the cat. Exp. Neurot., 14: 224-237. Fish, S. E., and Robinson, J. S. (1971). A new coordination test of visual-motor deprived, visually experienced cats. Psychon. Sci, 22: 28-29. Fox, M. W. (1966). Neuro-behavioral ontogeny. A synthesis of ethological and neurophysiological concepts. Bruin Res., 2: 3-20. Hein, A., and Diamond, R. M. (1971). Contrasting development of visually triggered and guided movements in kittens with respect to interocular and interlimb equivalence. J. Comp. Physiol. Psych ol., 76 2 19-224. Hein, A., Gower, E. C., and Diamond, R. M. (1970). Exposure requirements for developing the triggered component of the visual-placing response. J. Comp. Physiol. Psychol., 73: 188-192. Hein, A., and Held, R. (1967). Dissociation of the visual placing response into elicited and guided components. Science, 158: 390-391. Held, R., and Hein, A. (1963). Movement-produced stimulation in the development of visually guided behavior. J. Comp. Physiol. Psychol., 56: 872-876. Konrad, K. W., and Bagshaw, M. (1970). The effect of novel stimuli o n cats reared in a restricted environment. J. Comp. Physiol. Psychol., 70: 157-164. Norton, T. T. (1974). Receptive-field properties of superior colliculus cells and development of visual behavior in kittens. J. Neurophysiol,, 37: 674-690. Riesen, A. H., and Aarons, L. (1959). Visual movement and intensity discrimination in cats after early deprivation of pattern vision. J. Comp. fhysiol. Psychol., 52: 142-149. Riesen, A. H., Kurke, M. I., and Metlinger, J. C. (1953). Interocular transfer of habits learned monocularly in visually naive and visually experienced cats. J. Comp. Physiol. Psychol., 46: 166-172. Riesen, A. H., and Mellinger, J. C. (1956). Interocular transfer of habits in cats after alternating monocular visual experience. J. Comp. Physiol. Psychol., 49: 5 16-520. Robinson, J. S., and Fish, S. E. (1974). A cat’s form+xperienced but visual-motor deprived eye lacks focal vision. Dev. Psychobiol., 7: 331-342. Sherman, S. M. (1972). Development of interocular alignment in cats. Bruin Res., 37: 187-203. Sherman, S . M, (1973). Visual field defects in monocularly and binocularly deprived cats. Bruin Res., 4 9 : 25-45. Van Hof-Van Duin, J. (1976). Development of visuomotor behavior in normal and dark-reared cats. Brain Res.. 104: 233-241. Vital-Durand, F., Putkonen, P. T. S., and Jeannerod, M. (1974). Motion detection and optokinetic responses in dark-reared kittens. Vision Res., 14: 141-142. Walk, R. D., and Gibson, E. J. (1961). A comparative and analytic study of visual depth perception. fsychot. Monogr., 75: No. 519.
