Subtotal Lesions of the Visual Cortex Impair ... - APA PsycNET

Journal of Comparative and Physiological Psychology 1980, Vol 94, No 2,289-304

Subtotal Lesions of the Visual Cortex Impair Discrimination of Hidden Figures by Cats Paul Cornwell, William Overman, and Alfonso Campbell Pennsylvania State University Cats with partial or nearly total ablation of areas 17, 18, and 19 were assessed on the discrimination of hidden figures and other visually guided behaviors to determine whether such insults produce deficits like those that follow lateral striate lesions in monkeys. Cats with destruction limited to the representation of central vision (Group M) were impaired at discriminating patterns complicated by extraneous cues, but they were less impaired than cats with more complete lesions (Group MS). The deficit was not a general one in visual learning since animals in both Groups M and MS learned simple pattern discriminations as rapidly as controls. It is suggested that the loss of geniculocortical functions representing central vision produces similar deficits m cats and monkeys but that to have this effect in cats, damage must extend beyond area 17.

A number of common features characterize the cortical visual systems of mammals, (a) Most have a core of primary visual koniocortex, with a relatively thick fourth layer (area 17), which is surrounded by one or more belts having a less prominent fourth layer (Gray, 1924; Hall & Diamond, 1968; Kaas, Hall, & Diamond, 1972; Sanides & Hoffmann, 1969). (b) The core cortex is a target of the thalamocortical projections from the dorsal division of the lateral geniculate nucleus (LGNd), and (c) the belt cortex (areas 18 and 19 and other regions) receives projections from the pulvinar and lateral posterior nuclei (Diamond, 1976; Diamond & Hall, 1969; Hughes, 1977; Jones, 1974; M. Wilson, 1978). (d) The pattern of corticofugal projections from core and belt cortex to the thalamus and superior colliculus is similar in most mammals, as are (e)

many corticocortical connections (Jones, 1974; Lund, Henry, MacQueen, & Harvey, 1979). (f) In all mammalian species studied one finds multiple orderly representations of the visual field in both the thalamus and the cortex; there are at least 13 separate representations of the visual field at the cortical level in cats (Tusa, Palmer, & Rosenquist, 1978), and the situation is probably at least as complex in primates (M. Wilson, 1978; Zeki, 1974,1975). Species differ, however, in other aspects of the cortical visual system. A major anatomical difference between monkeys and cats, for example, is in the relation of LGNd to the cerebral cortex. Although LGNd projects to the visual core in both domestic cats and rhesus monkeys, it sends additional projections to widespread areas of the visual belt in cats, but not in monkeys (Garey, 1970; Hollander & Vanegas, 1977; Rosenquist, Edwards, & Palmer, 1974; M. Wilson & This research was supported by Grants MS 04726 and NS 10819 from the U.S Public Health Service. The Cragg, 1967). Thus, the only route to the authors wish to thank Bryan Kolb, Richard Ravizza, belt cortex from LGNd in monkeys is and J. M. Warren for their critical review of the manu- through area 17 (Kuypers, Szwarcbart, script. Parts of this research were reported at the Mishkin, & Rosvold, 1965; Martinez-Millan meeting of the Eastern Psychological Association, & Hollander, 1975; Zeki, 1975). In contrast, Philadelphia, April 1974. William Overman is now at the University of North the belt cortex in cats receives two imputs Carolina at Wilmington, and Alfonso Campbell is now from LGNd, one directly and the other via at the University of Michigan. area 17 (Hubel & Wiesel, 1965; Rosenquist Requests from outside North America for reprints et ah, 1974). should be sent to Paul Cornwell, 130 Moore Building, Physiological experiments yield results Pennsylvania State University, University Park, that are completely consonant with these Pennsylvania 16802. Copyright 1980 by the American Psychological Association, Inc

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P. CORNWELL, W OVERMAN, AND A. CAMPBELL

anatomical differences. Inactivation of area 17 in monkeys abolishes the ability of cells in area 18 to respond to visual stimuli (Schiller & Malpeli, 1977), but such treatments have far less effect on the activity of cells in area 18 in cats (Donaldson & Nash, 1975; Dreher & Cottee, 1975; Sherk, 1978). The primary goal of the present study was to relate these anatomical and physiological differences to differences in the behavioral effects of lesions in the visual cortex of monkeys and cats. One major difference between monkeys and cats in the effects of striate lesions on behavior is already well known. Complete destruction of area 17 greatly impairs the discrimination of visual patterns by monkeys; only with prolonged training do striatectomized monkeys reveal the capacity to discriminate figures that differ in contour but are equal in luminous flux (Humphrey, 1974; Keating, 1975; Kliiver, 1942; Pasik & Pasik, 1971; Weiskrantz, 1963). Cats with lesions confined to area 17, in contrast, are little affected in postoperative tests of pattern vision (Doty, 1971; Sprague, Levy, DiBerardino, & Berlucchi, 1977). However, cats with destruction of the projection fields of LGNd in both core and belt cortices are severely impaired in visually guided behavior (Cornwell, Warren, & Nonneman, 1976; Dalby, Meyer, & Meyer, 1970; Murphy, Mize, & Schechter, 1975; Spear & Braun, 1969; Sprague et al., 1977; Wetzel, 1969; Wetzel, Thompson, Horel, & Meyer, 1965; Wood, Spear, & Braun, 1974). They, like striatectomized monkeys, eventually learn to discriminate simple patterns, but they have serious trouble differentiating shapes of equal luminous flux that are also equal or nearly equal in contour and complexity (Cornwell, Overman, & Ross, in press; Ritchie, Meyer, & Meyer, 1976). The effects of removing all or nearly all of the projection field of LNGd are, therefore, very similar in monkeys and cats, but the relative size of the lesions needed to accomplish this disruption is far greater in cats than in monkeys. The effect of removing only the cortex representing central vision has been examined systematically in rhesus monkeys but not in cats. In monkeys the central 6-8° of the visual field is represented on the lateral

striate (LS) cortex (Daniel & Whitteridge, 1961). Removal of this region does not seriously impair rhesus monkeys on many sorts of pattern discrimination tasks, but monkeys with LS lesions are defective in performance on tasks that require the discrimination of fine differences in visual size (Butter & Doehrman, 1968; W. Wilson & Mishkin, 1959), spatial frequency (Weiskrantz & Cowey, 1963), and flicker rates (Mishkin & Weiskrantz, 1959). Monkeys with LS lesions are also impaired on patterned strings (W. Wilson & Mishkin, 1959) and hidden figures (Butter, 1969,1972,1979) tasks, and the relatively minor decreases in acuity seem insufficient to account for these impairments (Weiskrantz & Cowey, 1963). Nothing is known precisely about the effects of the lesions confined to the cortical representation of the central part of the visual field in cats. Several investigators agree in finding that small remnants of the geniculocortical system can mediate a substantial degree of visual capacity in cats (reviewed by Frommer, 1978). This work is of limited value for comparative purposes, however, since the lesions were not restricted to the representation of central vision and performance of the subjects was not tested on tasks like those used to assess the consequences of LS lesions in monkeys. The specific aim of the present experiment was to ascertain whether the deficits resulting from destruction of the geniculocortical representation of central vision in cats resemble those observed in monkeys with LS lesions. Since LGNd projects both to belt and core cortex in cats, it was necessary to ablate cortex in areas 18 and 19 as well as in area 17 to destroy most of the geniculocortical system representing central vision. This allowed comparisons with behavioral findings with monkeys having LS lesions, in which the total geniculocortical system representing central vision was destroyed by lesions restricted to the striate cortex. Three groups of cats were studied: (a) normal controls, (b) cats with lesions intended to destroy the total projection of LGNd in areas 17, 18, and 19, and (c) cats with lesions restricted to the representation of central vision in areas 17,18, and 19. This

291

VISUAL CORTEX AND HIDDEN FIGURES

design permitted comparison between cats with defects in central vision and monkeys with LS lesions. It also provided the opportunity to compare the performance of cats with definitely subtotal and with nearly complete ablations of the projection field of LGNd. The tasks (Table 1) were chosen to maximize comparability with tests used with monkeys having LS lesions; the major comparison was between performance on conventional tests of pattern vision and performance on tasks that involved spatial masking. The chief finding was that cats with lesions limited to the representation of central vision, like monkeys with LS lesions, were disrupted very little in the conventional tests but were greatly impaired on those that involved spatial masking.

6a

LJ

Method Subjects The 14 adult laboratory-reared mongrel cats had ail served previously in an experiment involving reversals of a probability learning problem with spatial cues (Warren, Note 1), but they had no preoperative training on any visual discrimination task

Apparatus All discrimination training was conducted in a modified Grice box described in detail elsewhere (Cornwell, Overman, & Ross, 1978). In brief, the apparatus consisted of a starting box and a choice compartment which led to two goal boxes that were separated by an opaque partition In each goal box was a vertically mounted stimulus plaque which subtended 9°-25° of visual angle when viewed from the choice point The cat had to go behind one of the plaques to obtain a hidden piece of pork kidney or tuna fish. In all but two of the tasks, the two goal boxes were painted white and the rest of the apparatus was painted gray For two tasks (Tasks 12 and 13) the box was painted gray throughout The visual cliff (Task 3) has been described in detail previously (Cornwell, Overman, Levitsky, Shipley, & Lezynski, 1976) Visual tracking (Task 17) was studied in the home cage with a tassel of brown yarn, 4 cm in diameter, tied to the end of a wand 93 cm long and made of coat-hanger wire

Shape and Pattern Stimuli Hexagonal and hourglass shapes were cut from 2cm-thick lumber, painted black, and mounted vertically on Plexiglas bases (Figure 1) The original training shapes were each 80 cm2; those used to assess shape discrimination in the presence of irrelevant size cues were 80 cm2, 40 cm2, and 20 cm2. L-shapes, each 12.5

Figure 1 Stimuli used for hidden figures test (Tasks 5-6e), simple pattern discrimination (Task 8), and orientation discrimination (Task 9), drawn to scale (Only the L-shapes had a third dimension to them.) X 11 5 cm, were cut from 4-cm-thick lumber and were painted black All pattern stimuli were made from black construction paper mounted on white plywood plaques and are displayed to scale in Figure 1 The stimuli for the landmark discriminations were a pair of vertically oriented gray triangles cut from 2-cm-thick lumber, 10 5 cm in altitude and 12 cm at the base The landmark was a 16 oz Coca Cola bottle, 28 cm high and painted flat black. A silhouette of a cat was cut from black construction paper and is shown in Figure 5, which also shows a control pattern made by rearrangement of fragments of the cat figure. Each silhouette was mounted on a sheet of gray cardboard 70 X 98 cm and placed behind a sheet of nonreflective glass attached to one wall of a room at floor level by a wooden frame The floor of the room was 1.8 X 2 4 m and was marked off into 12 numbered squares.

Procedure Table 1 shows the order of presentation for the 2 preoperative and 15 postoperative tests, along with the number of trials administered per session for each of the tasks. Several of the postoperative tests contained one or more subtests, and these too are listed in Table 1 On all discrimination learning tasks but the final two (Tasks 14 and 15), the criterion for acquisition was 90% or more correct responses. Table 1 indicates, for each task, whether this criterion needed to be met for one or for two consecutive sessions Visual cliff (Task 3) Each cat was given five trials per day on the visual cliff for 4 consecutive days De-

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tails of the testing procedure employed are given elsewhere (Comwell et al., 1976). Visual discrimination training (Tasks 1, 2, and415) Training occurred under 15-24-hr food deprivation and was conducted in a Grice box in which all stimuli were displayed with reflected light. A trial began when the experimenter lifted the opaque door to the starting compartment and, 3 sec later, raised the transparent door to release the cat. The reward was placed behind one of the stimuli, and the other stimulus remained unbaited. A noncorrection procedure was used throughout. The position of the positive stimulus was varied from trial to trial according to a balanced irregular sequence. On those tasks that required the discrimination of form or pattern in the presence of irrelevant variations in the size of the stimuli, each of the three sizes of the reinforced shape was paired with each size of the nonreinforced shape on 4 trials in the 36-tnal session. On Tasks 9-11, the same stimulus of each pair was reinforced for all subjects with the reinforced member of the pairs as follows Task 8, grid; Task 9, right-facing L, Task 10, inverted triangle; and Task 11, oblique line. Many of the discriminations were related to the initial

discrimination of the hexagon versus hourglass acquired preoperatively. Approximately half of the cats in each group were trained with the hexagon positive and the other half with the hourglass positive. On all subsequent tests, the basic shape of the reinforced stimulus remained the same for each cat. Thus, cats with the hexagonal form positive on the initial discrimination were trained with an outline hexagonal positive during testing with stripes superimposed on the patterns (Task 6) and were trained with the circle positive in the task that required the discrimination of a circle from an I (Task 7). During all discrimination training except Task 12, a simultaneous procedure was used, in which both discriminanda were presented on each trial with one reinforced. Task 12 involved the successive discrimination of a circle and an I-pattern and was done in a Grice box with gray goal compartments. Here, a pair of circles was presented on half of the trials, with only responses to the left member of the pair reinforced. On the other half of the trials a pair of Is was present, and only responding to the stimulus on the right was reinforced. The order of stimulus presentation followed a balanced irregular sequence.

Table 1 Order of Presentation of Tasks Pre- and Postoperatively Task

Trials/session

Preoperative 1 Shape 2 Shape: Size irrelevant Postoperative 3 Visual cliff 4. Shape: Size irrelevant 5 Pattern 6. Outline pattern a Outline only b. 2 superimposed stripes c. 4 superimposed stripes d. 6 superimposed stripes e 10 superimposed stripes 7. Pattern: Size irrelevant (circle vs I) 8. Pattern- Grid vs square bulls-eye 9. Orientation: L vs. J 10. Orientation a. Upright vs inverted triangle b. Above triangles surrounded by squares 11. Orientation a. Oblique vs. horizontal line b. Above lines surrounded by lines c. Above lines surrounded by squares 12. Pattern: Successive 13. Outline pattern: Retention 14. Landmark a. Acquisition" b-d. Reversals" 15. Outline patterns: Superimposed stripesb 16. Cat model 17. Visual tracking * Criterion was 90% correct responses in each of two consecutive blocks of 25 trials. b Tested a fixed 200 trials (not to a criterion).

Criterion sessions

25 36

2 2

5 36 25

2 2

25 25 25 25 25 36 25 25

2 2 2 2 2 2 1 1

25 25

1 1

25 25 25 25 25

1 1 1 1 1

50 50 40 2.5 min 8

VISUAL CORTEX AND HIDDEN FIGURES Task 13 was also conducted in the Grice box with solid gray goal compartments. In this retention test, the same outline patterns were employed as were used in Test 6a, but here the white stimulus plaques were presented against a gray background rather than a white one. One subject from Group C and one from Group MS (Subject MS-1) were not tested on this particular task. The procedure in the landmark discrimination (Task 14) was the same as that used previously by Campbell (1978). All testing was conducted in the apparatus with white goal compartments, and all 14 subjects were tested. First, the cat was reinforced for approaching the member of a pair of identical gray triangles that was adjacent to the landmark. Subjects were given 50 trials per day, and the criterion was 90% correct responses in each of two consecutive blocks of 25 trials. When criterion was attained, the cat was required to approach the triangle that did not have the bottle next to it (Reversal 1) Training to approach the stimulus unaccompanied by the landmark continued until the initial criterion was again attained, at which time the cat was once more required to approach the triangle next to the bottle (Reversal 2) A third reversal of the landmark discrimination to the same criterion completed testing on this task. The final test of the discrimination learning series (Task 15) used the outline stimuli with superimposed stripes employed previously (Tasks 6b-6e). Each of the four stimulus pairs (2,4,6, or 10 stripes) was presented on 10 trials of of each 40-tnal session The order ot stimulus presentation was randomized, with the restriction that no stimulus pair could appear more than three times in a row. All cats received a total of 200 trials over five consecutive testing sessions Responses to cat model {Task 16) Testing consisted of three habituation sessions followed by four sessions with test patterns. Each cat was first habituated individually to the small unfamiliar room for 2.5 min per day for 3 consecutive days During this baseline period the cat's behavior was monitored with a time sampling procedure by two observers through a one-way glass window. One observer recorded the position of the cat in the room and the orientation of its head at the end of each 2.5-sec period, marked by a beep audible to both of the observers and to the cat The second observer recorded the behavior of the cat at the end of each 2.5-sec observation period The procedure for classifying the behaviors was the same as that employed previously by Nonneman and Kolb (1974) and consisted of behaviors including piloerection, crouching, and sniffing the region where the cat model appeared. An "interest and affect" score was obtained by taking the sum of the number of intervals during which one or more of these behaviors were.observed. At the start of a trial the cat was placed in the darkened room, and within 2.5 sec the overhead lights were turned on and the observation period was begun. During the initial three sessions the picture frame attached to one wall contained only a blank sheet of gray cardboard. On Sessions 4 and 7 the silhouette of a cat was presented in place of the blank cardboard, and on Sessions 5 and 6 the fragmented cat was presented (Figure 5) Visual tracking (Task 17) Visual orienting and

293

tracking was assessed by moving a tassel of yarn toward the center of the cat's visual field at about 5 rad per second. One observer gained the subject's attention so that its head was at approximately the center of the front of the cage. A second observer then moved the tassel in from one corner of the cage in such a way that the individual strands of yarn jiggled slightly. Performance was rated independently by the two observers on a 5-point scale, with 0 indicating no orientation toward the target and 4 representing immediate, accurate, and smooth tracking of the target Four trials were conducted within a period of about 60 sec, one trial starting from each of the four quadrants. A second block of four trials was administered 15 to 60 min later. The following day another eight trials were given in the same way. Thus, a subject could obtain a maximum score of 64 over the two sessions. The interjudge agreement for the ranking of the total scores was nearlyperfect (p = .99). All nine operated subjects were assessed, but only two of the five controls were available for testing

Surgery All subjects were operated on within 8 days of completing their preoperative training. Cats were assigned to groups so that the median number of errors made during acquisition of the shape discrimination was approximately equal for the three groups. The surgery was conducted under sodium pentobarbital anesthesia (36 mg/kg), with sterile precautions Five cats received control operations which involved only scalp incisions (Group C). In a secondfiveanimals (Group M) the marginal and posterior lateral gyri were removed by subpial aspiration from a point about 1 cm posterior to the ansate sulcus to the ventral limit of the posterior lateral gyrus. For these cats an attempt was made to spare all the cortex along the dorsal bank of the splenial sulcus Thus, the lesions for Group M were designed to spare much of the visual cortex representing the peripheral parts of the visual field (Kalia & Whitteridge, 1973; Tusa et al., 1978). In the four cats in Group MS the surgical procedure was identical to that used for Group M, but in addition, an attempt was made to remove all the cortex on the upper bank of the splenial sulcus. In these cases most of the white matter of the marginal and posterior lateral gyri was also removed. These lesions, then, were intended to remove area 17 completely and to include most of areas 18 and 19 as well (Otsuka & Hassler, 1962; Sanides & Hoffmann, 1969). A 1-mo postoperative recovery period was allowed for all cats before the resumption of behavioral testing.

Histology At the completion of behavioral testing, the operated cats were killed with an overdose of sodium pentobarbital and were perfused intracardially with physiological saline followed by 10% formalin in saline The brains were photographed, dehydrated, embedded in celloidin, and cut in 30-jtm sections. Every 10th coronal section through the lesion and the thalamus was mounted and stained with cresyl violet. The lesions were recon-

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P. CORNWELL, W OVERMAN, AND A. CAMPBELL

structed from the serial sections together with the photographs of the brains, and the posterior region of the thalamus was analyzed for the location and severity of retrograde degeneration

Results Histological Figures 2 and 3 show the smallest and largest lesion in each group and indicate that the dorsal and the lateral extents of the destruction were approximately equal in the two operated groups. As intended, there was far more sparing of the cortex along the splenial sulcus in the cats in Group M than there was in those in Group MS. Indeed, the coronal sections through the lesions and maps of retrograde degeneration in LGNd, represented in Figures 2 and 3, both indicate there was more sparing of the splenial cortex in the cat with the largest lesion in Group M than there was in the cat with the smallest lesion in Group MS. It was difficult to assess from sections through the cortex the amount of sparing in various parts of the visual field because some regions of apparently intact cortex were disconnected by damage to the white matter. For this reason, estimates of the amount and location of sparing of the visual fields were based on the analysis of retrograde degeneration in the thalamus. Cats in Group M had severe retrograde degeneration in the medial zone of the trilaminar part of LGNd. In total, from about 20% to about 70% (Mdn = 50%) of the LGNd

remained relatively intact in the cats in Group M. Regions of LGNd showing severe degeneration and those containing many intact neurons were compared with maps of the retinal projection onto LGNd (Sanderson, 1971) in order to estimate the amount and location of sparing in the visual fields In the cat in Group M with the smallest lesion, almost all of the visual field was apparently intact beyond 5°-10° from the area centralis; in the cat in Group M with the largest lesion, there was sparing beyond about 20° from the area centralis. In Group MS the retrograde degeneration in the medial part of the LGNd was much like that in the cats in Group M, but the lateral region of LGNd, representing the more peripheral parts of the visual field, was also severely but incompletely degenerated. The amount of sparing of the LGNd in cats in Group MS ranged from about 3% to about 10%. For all cats in Group MS there was severe or complete degeneration of the parts of the main lamina of LGNd representing the central 40°-50° of the visual field. There was a variable amount of retrograde degeneration in the medial interlaminar nucleus in cats in both Groups M and MS. but there was very little degeneration in the pulvinar, nucleus lateralis posterior, or elsewhere in the thalamus. Additional details concerning the pattern of retrograde degeneration among all but one of the present subjects (Subject MS-18) can be found in a previous report (Cornwell et al., 1976).

mil Figure 2 Representative coronal sections through the cerebrum and lateral geniculate nucleus (LGNd) for cats in Group M (convexity of marginal and posterior lateral gyri removed) with the smallest and the largest lesions. (Black indicates areas of cortical removal or severe retrograde degeneration; stippling indicates regions of moderate retrograde degeneration Diagrams of LGN adapted from Sanderson, 1971.)

VISUAL CORTEX AND HIDDEN FIGURES

295

MS7 Figure 3 Representative coronal sections through the cerebrum and lateral geniculate nucleus (LGNd) for cats in Group MS with the smallest and the largest lesions (See caption to Figure 2 for key MS lesions included marginal and posterior lateral gyn and cortex on upper bank of splenial sulcus.)

was 57 and the highest by a cat in Group MS was 34. It seems quite clear, however, that Visual tracking. The performance of the the tracking performance of Group MS was three groups on the tracking task is dis- greatly and reliably impaired when it is played in Figure 4, along with that of the compared with the performance of the eight control group reported by Campbell (1978) normal cats studied by Campbell. and tested intercurrently with the cats of the Visual cliff. The performance on the vipresent experiment. Both of the control sual cliff has been reported previously for all subjects that were tested obtained tracking but one of the present subjects (Cornwell et scores near the maximum, and their perfor- al., 1976). In brief, Group MS did not mances were indistinguishable from that of choose the shallow side any more often than the larger group of normal cats reported by chance, whereas both the control group and Campbell. Groups M and MS were sub- Group M chose the shallow side on about stantially impaired. Group M obtained 90% of the trials. The subject not previously tracking scores significantly lower than those reported (Subject MS-18) chose the shallow of Group C (U = 0,p < .05), and Group MS side on only 55% of the trials, a performance in turn had lower scores than Group M (U = level similar to that of other cats with MS 2, p < .05). The numbers of subjects in lesions, below that of any subject in a group Group C and MS were too small for this of 34 controls, and below all but one of the group difference to reach the 5% confidence nine cats in Group M tested in the previously level, although the lowest score by a control reported study (Cornwell et al., 1976). Responses to cat model. Figure 5 shows 64 the performance of the three groups on each of the three measures of reactivity during each of the test sessions. All three measures £48 O yielded essentially the same profile, with the reactivity of Groups C and M peaking during the initial presentation of the cat silhouette H • and that of Group MS remaining fairly O constant and low throughout all seven test 1 16 sessions. The reaction to the cat silhouette by Groups C and M was greatly reduced when the silhouette was introduced for the OL C* M second time on the final session. None of Figure 4 Median tracking scores for Groups C, M, and the groups showed reactivity to the control MS. (The findings from Campbell's, 1978, control [C] silhouette that was appreciably above the subjects are plotted for comparison [asterisk] See baseline. captions to Figures 2 and 3 for identification of When the silhouette of a cat was introgroups.) Behavioral

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IH

2H

3H

4 5P CAT

6P

7 CAT

IH

2H

3H

4 5P CAT

6P

7 CAT

3H

4 5P CAT

6P

7 CAT

SESSIONS Figure 5. Median performance on three measures of salience of a model silhouette cat- orientation toward it, proximity to it, and interest and affect displayed toward it. (H = habituation sessions; P = pseudocat [fragmented control pattern] See captions to Figures 2 and 3 for identification of groups.)

duced, there were dramatic changes in the behavior of most of the cats in Groups C and M. They spent close to half of their time in the vicinity of the cat silhouette, and most of them sniffed it on the nose, the anus, or both. For the combined Groups C and M the scores on the measures of proximity, interest and affect, and orientation were reliably higher on Session 4 than they were on the mean of the three baseline sessions (Wilcoxon's test, all Ts < 2, all ps < .05). In contrast, the performance of Group MS showed little change from that of the baseline period. The control subjects were not reliably different from either of the operated groups during habituation on any of the three measures. However, during habituation Group M showed significantly more interest than Group MS in the region where the silhouette later appeared (U = 0, p < .02) and spent more time in this vicinity (U = 0, p < .02). There were no consistent differences between the orientation scores of these two groups during the habituation period. The mean score on each measure was calculated separately for each cat for the two sessions with the cat silhouette and for the two sessions with the fragmented silhouette. When the cat silhouette was present, the animals in both Group C and Group M had significantly higher scores on all three measures than those in Group MS (U tests, all six possible p values < .05). The only reliable intergroup difference during the periods

with the control silhouette was that the control subjects showed slightly more interest and affect than Group M (U = 2, p < .05). Shape and pattern discrimination Table 2 presents the median number of errors made during the preoperative acquisition of the shape discrimination and indicates the slight, but nonsignificant, bias in favor of the group that later received MS lesions. Preoperatively, all three groups showed excellent transfer, making very fewerrors in the condition with irrelevant size cues. As before, there were no reliable intergroup differences. Postoperatively; the control group showed excellent retention of the object discrimination with irrelevant size cues (Task 4), but Groups M and MS made more errors than they did preoperatively and the overall difference in error scores among the groups was significant (Kruskal-Wallis, H = 10.3, p < .01). Group M made significantly more errors than Group C (U = 2.5, p < .05), and Group MS made more errors than either Group C (U = 0, p < .01) or Group M (U = 0, p < .01). All three groups subsequently made very few errors when two dimensional patterns of equal area were substituted for the stereometric object stimuli of the same shape (Task 5 in Figure 1); there were no reliable intergroup differences on this task. Figure 6 illustrates the number of errors made by each of the three groups in acquir-

297

VISUAL CORTEX AND HIDDEN FIGURES Table 2 .Median Errors to Criterion on Shape and Pattern Discrimination Tasks Group Task I'rooperative 1 Shape 2 Shape Size irrelevant Postoperative 1 Shape' Size irrelevant 5 Pattern 7 Pattern Size irrelevant (circle vs I) 8 Pattern- Grid vs square hulls-eye 9 Orientation. L vs J 12 Pattern Successive 13 Outline pattern. Retention"

C

M

MS

107 14

91 24

80

6 4 11 64 35 64 10

36* 5 31* 78 47 132* 70*

>I81' 2 50* 98 162' 68 112*

" Tested a fixed 200 trials (not to a criterion) • p < 05, significantly different from Group V. 1 p < 05, significanth different from Groups C and M

ing a series of outline discriminations with increasing numbers of superimposed stripes (Task 6). Group MS was impaired under each stimulus condition, but Group M showed a substantial deficit only when there were 10 stripes superimposed on the outline patterns. One-way analyses of variance performed at each condition indicate significant differences among the groups when there were 0 {H = 5.9, p < .05), 4 (H = 6.5, p < .05), 6 (H = 10, p < .01), and 10 (H = 9.6, p < .01) superimposed stripes. With zero and four superimposed stripes, Group MS was significantly impaired relative to both ACQUISITION

RETEST

400-

E 300-

P200-

6

10

STRIPES Figure 6 Left. Median errors to criterion on hexagon versus hourglass discrimination as an outline (0 stripes) and with various numbers of superimposed stripes Right: Median percentage errors in 50 trials with each stimulus pair when pairs were presented in a mixed sequence. (See captions to Figures 2 and 3 for identification of groups )

Group C and Group M (all /7s < 3, all ps < .05), but the number of errors made by Groups M and C did not differ reliably (both Us > 10). With six superimposed stripes each experimental group made significantly more errors than the control group (each U < 3, each p < .05), and Group MS made reliably more errors than Group M (U = 0, p 7.7, each p < .01) but not for the 10-stripes condition. With two, four, and six superimposed stripes both Group M and Group MS made significantly more errors than Group C (each U < 2.5, each p < .05), and with six stripes Group MS made reliably more errors than Group M (U = \,p .05), but on the task involving the orientation of the L, Group MS made significantly more errors than either Group C or Group M (both Us - 2, both ps < .05). Discrimination of an upright from an inverted black triangle required approximately an equal number of errors for each of the three groups (Task 10; Figure 7). However, when these same patterns were subsequently surrounded by a black outline square, dramatic differences appeared among the

groups. The control subjects showed almost perfect positive transfer, but only two of the nine subjects with lesions (both in Group M) showed positive transfer. The overall difference in error scores on the transfer problems was significant (H = 8.1, p < .01). Both Group M and Group MS made significantly more errors than Group C (both L's < 2, both ps < .05), but the difference between Group M and Group MS was not reliable. The right-hand panel in Figure 7 illustrates a similar effect of surrounding lines on discrimination of line orientation (Task 11). The original discrimination of an oblique from a horizontal line was acquired with approximately the same number of errors by the three groups. However, when each line was incompletely framed by four additional lines, only two of the nine operated subjects attained criterion in 1,000 training trials. The overall difference among the groups on this task was significant (H = 8.7, p < .01), and the performance of each of the experimental groups was significantly different from that of the control group (each U < 2, each p < .05). There was no reliable difference between Group M and Group MS. The substantial and reliable effect of the surround at disrupting the discrimination of oblique and horizontal lines was preserved when the surround was subsequently modified to a broken outline square composed of 12 smaller squares (H = 10.0, p < .01). Again, both Group M and Group MS made significantly more errors than Group C (each U < 2, each p < .05), but on this task Group MS was significantly more impaired than Group M((7 = l,p .05), Group M made significantly more errors than Group C (U = 3, p < .05). Clear intergroup differences reappeared when 12 of the 14 cats were retrained on the Figure 7 Median errors to criterion in discriminating the orientation of triangles and lines, without and with outline pattern discrimination in a situation surrounds. (See captions for Figures 2 and 3 for iden- in which the white stimulus plaques appeared against a gray background (Task 13 tification of groups )

VISUAL CORTEX AND HIDDEN FIGURES

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learned to discriminate many uncomplicated forms and patterns as quickly as the control group (Tasks 5,8,9,10a, and lla), but they were mildly impaired when required to discriminate shapes and patterns that varied irrelevantly in size (Tasks 4 and 7) and they were severely impaired when the discriminanda were surrounded by irrelevant lines (Tasks 10b, lib, and lie). Finally, lesions restricted to the cortical representation of central vision caused serious trouble at discriminating outline patterns that were heavily masked with superimposed lines (Task 6e) and at discriminating such patterns when the number of lines superimposed on them varied from trial to trial (Task 15). The cats with relatively complete lesions of the visual cortex (Group MS) were imREVERSALS paired on all tasks in which masking or irFigure 8 Median errors to criterion at acquisition and relevant cues were present, usually more three reversals of "landmark" discrimination (See severely than Group M. Unlike the animals captions for Figures 2 and 3 for identification of in Group M, the cats with MS lesions were groups ) also defective in some discrimination tests in Table 2; H = 6.4, p < .05). The control with little or no masking of the relevant group made significantly fewer errors than features (Tasks 6a, 6c, and 9). In addition, either Group M (U = 2, p < .05) or Group Group MS differed from Group M in maniMS(t/ = 0,p Journal of Anatomy, 1967, 101, 677-692. Wilson, W A , & Mishkin, M Comparison of the effects of inferotemporal and lateral occipital lesions on visually guided behavior in monkeys Journal »/ Comparative and Physiological Psychology, 1959. 52, 10-17. Winans, S. S Visual cues used by normal and visualdecorticate cats to discriminate figures of equal luminous flux Journal of Comparative and Physiological Psychology. 1971,74, 167-178. Wood.C C., Spear, P D,&Braun,J ,1 Effects of sequential lesions of suprasy Ivian gyn and visual cortex on pattern discrimination in the cat Brain Hesearch, 1974,66, 443-466. Zeki.S M Functional organization of a visual area in the posterior bank of the superior temporal sulcus of the rhesus monkey. Journal of Physiology, 1974, 236, 549-573 Zeki, S M The functional organization of projections from striate to prestnate visual cortex in the rhesus monkey Cold Spring Harbor Symposia on Quantitative Biology, 1975, 40, 591-600 Received April 25, 1979