Exp. Brain l~es. 23, 181--201 (1975) 9 by Springer-Verlag 1975

Effects of Visual Cortex Lesions Following Recovery From Monocular Deprivation in the Cat Peter D. Spear and Leo Ganz Department of Psychology, Kansas State University, Manhattan, Kansas (USA) Department of Psychology, Stanford University, Palo Alto, California (USA) Received December 27, 1974 Summary. Six monocularly deprived (MD) and four normal cats were trained monocularly on two-choice form and pattern discriminations. MD cats trained through the initially deprived eye were able to learn the discriminations ; however, they required many more trials than normals. Retention tests showed that MD cats have nearly perfect retention of the discriminations over periods of up to 4 months. With retention intervals of 6 months or longer, there is a tendency for the MD eats to show an initial drop in performance, particularly on more difficult discriminations. However, criterion performance typically was attained with considerable savings, indicating good retention even over these extended intervals. Following the preoperative training and retention testing, the cats received one of three types of visual cortex lesions. Two MD cats received total visual cortex removal (areas 17, 18, and 19). This produced a complete postoperative loss of the discriminations with continued chance performance over 800--1000 trials. Two MD cats and two normal cats received removal of the monocular segment of area 17, with the central visual field projection region of area 17 and all of areas 18 and 19 remaining intact. This produced no loss of the discriminations in either normal or MD cats beyond what is expected on the basis of normal forgetting. Two MD cats and two normal cats received removal of areas 18, 19, and the central 5--10 deg. of the visual field projection in area 17. Postoperative retention was somewhat variable for both normal and MD cats. However, subsequent acquisition of the discriminations by both normal and MD cats was in sharp contrast to the prolonged deficits produced by total visual cortex lesions. These results indicate that one or more of visual cortical areas 17, 18, and 19 are involved in the recovery of visual discrimination capacities in MD cats. However, the monocular segment of striate cortex does not appear to be specially involved in this ability, as has been suggested by previous investigations. Possible mechanisms for the recovered visual capacities in MD eats are considered. Key words : Visual cortex lesions - - Monocular deprivation - - Visual discrimination - - Monocular segment Pattern vision deprivation during development produces a variety of neuroanatomical, neurophysiological, and behavioral abnormalities in both cats and monkeys. Among the effects of monocular deprivation (MD) in cats is a decreased

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responsiveness of cells in the striate cortex to stimulation of the deprived eye. Less than 10~o of these cells can be excited by the deprived eye and virtually none of them have normal receptive field characteristics (Wiesel and Hubel, 1963, 1965 a; Hubel and Wiesel, 1970 ; Blakemore and Van Sluyters, 1974). Monoeularly deprived cats also show marked deficiencies in visually guided behaviors when tested with the deprived eye. A number of investigators report that such cats initially appear blind (Ganz and Fitch, 1968; Dews and Wiesel, 1970; Rizzolatti and Tradardi, 1971 ; Chow and Stewart 1972 ; Ganz et al. 1972 ; Ganz and Haffner 1974). However with extensive training monocularly deprived eats can learn a variety of brightness, form, and pattern discriminations using the eye which was previously deprived during development (Dews and Wiesel, 1970; Rizzolatti and Tradardi, 1971; Chow and Stewart, 1972; Ganz et al., 1972; Ganz and Haffner, 1974). In spite of this behavioral recovery, electrophysiologieal recording in striate cortex of MD cats which have been forced to use the previously deprived eye (via a reverse-suture procedure), or which have received visual training through the deprived eye, indicate that little or no recovery of the single cell response properties occurs (Wiesel and Hubel, 1965b; Ganz et al., 1968; Hubel and Wiesel, 1970; Chow and Stewart, 1972; Blakemore and Van Sluyters, 1974; Ganz and Haffner, 1974). In these cats, still only a small percentage of the striate cortex cells may be driven by the previously deprived eye, and the vast majority of these still have abnormal receptive field properties. These findings raise the question as to the mechanisms by which MD eats are able to recover their ability to perform visually guided behaviors using the deprived eye. Several possibilities may be suggested. First, MD eats may learn to perform the visually guided behaviors on the basis of the remaining abnormal inputs to the small percent of striate cortex cells which continue to respond to stimulation of the deprived eye. This is suggested by studies in cats and monkeys which show that the acquisition of certain learned tasks after various types of monocular or binocular deprivation is related to the percentage of cells in striate cortex which are still driven by the affected eye (Dews and Wiesel, 1970; Ganz et al., 1972 ; Baker et al., 1974 ; Blakemore and Van Sluyters, 1974). A second possibility is that the abnormally responsive visual cortex is no longer involved in performance of the visually guided behaviors, and that the recovery is based on visual information reaching other regions of the brain. For example, Glass (1973) has found that after training through the previously deprived eye, components of visual evoked potentials in preeruciate and suprasylvian cortex show recovery, while those in visual cortex do not. A third possibility is suggested by findings that in some structures of the visual system the morphological and physiological effects of monocular deprivation are absent in the portion of the structure which receives its input flora the peripheral monocular part of the visual field (the monocular segment) (Guillery and Stelzner, 1970; Sherman et al., 1972; Gnillery, 1972, 1973; Garey et al., 1973; Sherman et al., 1974 ; Hoffmann and Sherman, 1974). A behavioral correlate of this result was reported by Sherman (Sherman, 1972a, 1974; Sherman et al., 1974), who found that visual orienting and approach responses in MD cats are deficient for

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stimuli presented to the deprived eye i n the central binocular visual field, while responses to stimuli presented in the peripheral m o n o c u l a r visual field appear normal. These findings suggest t h a t MD cats m a y recover their a b i l i t y to perform visual d i s c r i m i n a t i o n tasks b y learning to employ i n f o r m a t i o n coming from the peripheral m o n o c u l a r segment of the visual field. Indeed, Rizzolatti a n d T r a d a r d i (1971 ) reported t h a t MD eats learning p a t t e r n discriminations t h r o u g h the deprived eye performed large head m o v e m e n t s s c a n n i n g the p a t t e r n s ; m o v e m e n t s which n e v e r occurred when the cats were t r a i n e d t h r o u g h their n o r m a l eye. The present experiments were designed to assess some of these possibilities as to the mechanisms b y which m o n o c u l a r l y deprived cats recover their a b i l i t y to perform visual p a t t e r n discriminations. Cats which had received m o n o c u l a r d e p r i v a t i o n d u r i n g d e v e l o p m e n t were t r a i n e d to discriminate visual p a t t e r n s with their deprived eye. Following recovery, some of the cats were subjected to t o t a l visual cortex lesions (areas 17, 18, a n d 19) a n d retested to determine if visual cortex had been i n v o l v e d in the p a t t e r n d i s c r i m i n a t i o n performance. I n other cats, a n a t t e m p t was m a d e to d e t e r m i n e if the p o r t i o n of striate cortex receiving its i n p u t from the peripheral m o n o c u l a r segment of the visual field played a special role. I n some of these cats, most of the visual cortex except the m o n o c u l a r segment of area 17 was removed, a n d in others only the m o n o c u l a r segment of area 17 was removed. N o r m a l eats received similar lesions for comparison.

Methods Subject8 and Rearing Conditions Ten eats which were born in the laboratory breeding colony were employed. Six were reared with monocular pattern vision deprivation via lid-suture (MD) and four were normal (undeprived). The cats were housed in large group cages. Two of the normal cats (N2 and N3) and all of the ~ D eats were employed in a previous experiment and receivd additional discriminationtesting prior to surgery which is not reported in the present paper (see Ganz and I-Iaffner, 1974). The MD eats had the eyelids of one eye (the initially deprived eye) sutured dosed prior to the time of normal eye opening. Details of the lid-suture procedure have been described elsewhere (Ganz and I-Iaffner, 1974). When the eats were from 14.5 to 17 weeks old the initially deprived eye was opened. For five of the eats She initially experienced eye was sutured dosed at this time (reverse-suture procedure). For the sixth cat (MSL-13) both eyes remained open.

Apparatus and Training A two-choice discrimination apparatus similar to that described by Sperry, myers and Sehrier (1960) was employed for discrimination training. Full details of the training procedure are reported elsewhere (Ganz and Haffner, 1974) and only a brief description will be given here. Two stimuli were mounted on doors at one end of the apparatus. The positions of the stimulus doors were alternated from right to left on each trial according to a Gellerman series (Gcllerman, 1933). On each trial the cats were required to walk from a start-box and press against the door holding the positive stimulus in order to receive a food reward behind it. The door holding the negative stimulus was locked and a correction procedure was employed. Only a trial on which the correct stimulus-door was pushed first was counted as correct. The cats were trained in sessions of 20 trials per day. A discrimination was considered learned to criterion when the cat made 90% or more correct choices in six consecutive blocks of ten trials. No food or water deprivation was employed during training. Two different discrimination tasks were employed for the present experiment. One was a discrimination between horizontal stripes on one stimulus-door and vertical stripes on the other (horizontal-vertical discrimination). Each stimulus was a 12 cm • 12 cm array of alter-

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nating black (3.08 mL) and white (325 mL) stripes, each of which was 12.5 m m wide. The second was a discrimination between a n upright isosceles triangle on one stimulus-door and an inverted isosceles triangle on the other (triangle discrimination). Each triangle was a black (3.08 mL) outline figure, and the thickness of the outline was 12.5 ram. The triangles were 64 m m wide at the base and 82 m m high set against a white (324 mL) background.

Surgery and Histology Surgery was performed under aseptic conditions. The cats were injected with 0.24 mg atropine sulfate intraperitoneally. They were then anesthetized with pentobarbitol sodium administered either intraperitoneally (40 mg/kg) or intravenously to effect. ~cocortieal removal was b y aspiration, after retraction of the overlying meninges. Care was taken to spare all major blood vessels in the area of the intended ablation. Three types of bilateral cortical removals were performed. The first, termed total, was intended to include the lateral gyrus, postero-lateraI gyrus, dorsoposterior genu of the middle suprasylvian gyrus, and suprasplenial and splcnial gyri. This lesion was thus intended to include all of areas 17, 18, and 19, according to the criteria of Otsuka and ttassler (1962). The second type of lesion, termed peripheral, was intended to include the splenial and suprasplenial gyri from the depths of the splenial sulcus to halfway between the suprasplenial suleus and the dorsal edge of the medial wall of the hemisphere. I t was to continue in a narrow b a n d from the postero-ventral tip of the splenial gyrus on the medial wall of the hemisphere around the posterior pole and include the postero-ventrM tip of the postero~la~eral gyrus on the lateral convexity of the hemisphere. This lesion was thus intended to include most or all of the monocular peripheral visual field projection (monocular segment) onto striate cortex according to the maps of T a l b o t and Marshall (1941) and Bilge et al. (1967) (see Fig. 1). I t was intended to spare the projection of the central 5--10 deg. of the visual field onto striate cortex and all of areas 18 and 19 on the lateral convexity of the hemisphere. The third type of lesion, termed central, was intended to be the exact complement of the peripheral lesion. I t was thus intended to include all of areas 19 and 18 on the convexity of the hemisphere in addition to the projection of the central 5--10 dog. of visual field onto area 17. The remainder of striate cortex, including the monocular peripheral visual field projection, was to be left intact. For histological preparation animals were given a lethal dose of pentobarbital sodium and were perfused throlTgh the h e a r t with 0.9% saline followed b y 10% formol-sMine. Brains were then blocked, removed from the skull and stored in 10% formol-saline. After embedding in celloidin, all brains were sectioned a t 30 micra. Every fifteenth section through the cortical lesion and every fifth section through the posterior thalamus was mounted and stained with cresyl violet. The extent of cortical lesions was assessed for each animal using drawings made a t time of sacrifice and b y examination of the serial stained sections. Detailed lesion reconstructions were made from serial sections at 1 m m intervals through the brain on surface maps adapted from the atlas of Reinoso-Suarez (1961), and corrected for the position of the lateral and accessory interlateral sulci of each cat (0tsuka a n d Hassler, 1962). A detailed analysis was made of the extent and p a t t e r n of retrograde degeneration of the dorsal lateral geniculate nuclei (LGD) of each eat.

Procedure Following the initial deprivation period, the MD cats received training on a variety of discrimination and transposition tasks (Ganz and Haffner, 1974) including the horizontalvertical and the triangles discriminations reported in the present paper. For results presented in the present paper, training was monocular via the initially deprived eye for all of the MD eats. This was accomplished for eat MSL-13 b y placing an opaque contact lens occluder over the initially experienced eye during the training sessions, and for the other MD cats b y the reverse-suture procedure already described. The four normal cats were monocularly trained on these tasks b y placing an opaque contact lens occluder over one of the eyes during the training sessions. During training, a variety of procedures was employed to eliminate differential olfactory a n d auditory cues from trial to trial. These are described in detail elsewhere (Ganz a n d Haffner, 1974). I n addition to these controls, the eats received 20 additional training trials with b o t h

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eyes occluded once they h a d reached learning criterion on each discrimination task. This was accomplished b y placing an opaque contact lens occluder over the initially deprived eye for the reverse-sutured cats and over b o t h eyes for cat MSL-13 and for the four normal cats. I n this way, it was possible to test the effectiveness of the contact lens occluders and to determine t h a t each discrimination h a d been learned on tile basis of visual cues alone. After periods ranging from 0.5 to 17.5 months some of the cats were tested for retention of the previously learned horizontM-verticM and triangles discriminations. I n some cases, a cat received two or three separate retention tests on the same task after varying periods of time (In most cases, the cats also received training or testing on other visual discriminations during the time intervening between original learning and retention testing.) The tasks on which retention tests were administered and the a m o u n t of time intervening between learning the discrimination and retention testing are shown in Table 1. The procedure for retention testing was exactly the same as for original learning, and testing was continued until the cat reached the original learning criterion. These retention tests allowed an evaluation of the a m o u n t of forgetting which could be expected from visually deprived cats simply resulting from the passage of time or training on other discriminations. T h a t is, the possibility t h a t visual deprivation itself produces long-term retention deficits for learned visual discrimination behaviors could be assessed. Following training, the cats received one of the three types of visual cortex lesions. I n all b u t two cases the cats were a t criterion levels of performance within 2--3 weeks prior to the cortical removal (see Table 2). For the horizontal-vertical discrimination in two MD cats, a period of 17--19 months intervened between criterion performance on the task and surgery. Each type of visual cortex lesion (total, central, or peripheral) was administered to two MD cats. I n addition, two normal cats received central lesions and two received peripheral lesions (Table 2). Postoperative retention testing was begun after a 4 - - 5 week recovery period. The cats were retrained on the two discriminations using the same procedures as for original learning. Postoperative training was continued until criterion was attained or for 800--1000 trials if performance h a d not exceeded chance levels b y this time.

Results Histology Figure I shows dorsal and medial surface views of a normal cat brain, including demarcation of the positions of areas 17, 18, and 19 according to Otsuka and Hassler (1962). On the medial surface diagrams in Figure 1 and subsequent figures showing lesion reconstructions, the splenial sulcus has been represented as retracted with the dorsal b a n k of the sulcus exposed. Area 17 continues well into the depths of the splenial sulcns along this dorsal bank. However, maps showing the precise position of the medial border of area 17 along the length of the splenial sulcus are not available. Therefore, the medial border of area 17 shown in Fig. 1 was determined from our own material. Where possible, comparisons were made with material shown in the cytoarchitectonic studies of Otsuka and ttassler (1962) and Sanides and Hoffmann (1969), and the results were found to be in excellent agreement. They also were in excellent agreement with the data of Kalia and Whitteridge (1973) showing the medial border of area 17 at several positions along the splenial sulcus determined electrophysiologically. I t is i m p o r t a n t to note t h a t all of these sources agree t h a t the medial border of area 17 does not extend to the b o t t o m of the splenial sulcus. Anatomical studies indicate t h a t the monocular segment of the LGD projects to striate cortex along this same area of the dorsal b a n k of the splenial sulcus (Rosenquist et al., 1974) a n d electrophysiological studies verify t h a t the temporal peripheral visual field projection (monocular segment) onto striate cortex lies in this area (Talbot a n d Marshall, 1941; Bilge et al., 1967; Woolsey, 1971; Kalia and Whitteridge, 1973). The major landmarks of the visual field projection onto area 17 on the medial surface of the hemisphere are indicated in Fig. 1. Lesion reconstructions and coronal sections through the cortical lesions in three representative cats (one of each lesion type) are shown in Figs. 2 ~ 4 . The e x t e n t of cortical removal and undercutting, including t h a t on the dorsal b a n k of the splenial sulcus, is shown in each case. Also shown are projection drawings of four coronal sections through the right and left LGD of each cat, illustrating the p a t t e r n of retrograde cellular degeneration.

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+10 0

[]17

U18

Fig. 1. Visual cortex in a normal cat brain. The center drawing shows a dorsal view of the brain, including the locations of areas 17, 18, and 19 according to Otsuka and Hassler (1962). To either side are partial drawings of the medial surface of the left and right hemispheres. On the medial surface drawings, the splenial sulcus is shown as retracted so that the dorsal bank of the sulcus is completely exposed. The line marked A in each medial surface drawing represents the dorsal lip of the splenial sulcus where it joins the medial surface of the hemisphere. The line B represents the bottom of the splenial sulcus. The space between these two lines thus represents the dorsal bank of the splenial sulcus and has been drawn to scale from the atlas of ReinosoSuarez (1961). The extent of striate cortex along the dorsal bank of the splenial sulcus, as determined from our own material, is shown (see text for further details). The line marked H represents the projection of the horizontal meridian of the visual field onto area 17 on the medial surface of the brain, and 5 deg. and 20 deg. projection lines also are shown. These visual field projections have been drawn with reference to their stereotaxic positions given by Bilge et al. (1967) and conform to the visual field projections shown by Woolsey (1971). The zero (interaura]) and d-10 stereotaxic coordinate planes are indicated in the figure

Retrograde degeneration was interpreted according to the results of Garey and Powell (1967), Niimi and Sprague (1970}, and Burrows and Hayhow (1971}. According to these studies, damage to area 17 alone results in marked degeneration in the main laminae, although many of the large cells are unaffected and do not degenerate. This pattern of degeneration is represented by light stippling in the LGD drawings in Figs. 2 ~ 4 . Lesions which involve both areas 17 and 18 result in severe degeneration in the main laminae including all of the large ceils. Severe degeneration is represented by dark stippling in the LGD drawings. Combined damage of both areas 18 and 19 results in marked degeneration in the MIN and CIN and little or no degeneration in the main laminae. However, even with damage to both of these areas, many scattered healthy appearing cells may still be seen in the MIN (see Garey and Powell, 1967; and Burrows and Hayhow, 1971), possibly due to its remaining projection to the lateral syprasylvian gyrus visual area (Garey and Powell, 1967; Glickstein st al., 1967; Burrows and Hayhow, 1971; Rosenquist st al., 1974). This pattern of degeneration is also represented by light stippling in the LGD drawings. Undegenerated areas in the MIN are considered to indicate the presence of remaining cortical tissue in both areas 18 and 19. Histological analysis for the ten cats is presented below according to the three lesion types. Total. Two MD eats received lesions intended to include all of areas 17, 18 and 19. Figure 2 shows the extent of cortical removal in one of these, cat XR-11. Analysis of LGD retrograde degeneration showed severe degeneration throughout both LGD. However, a cluster of healthy large cells was present in the lateral monocular segment of the right LGD (ipsilateral to the deprived eye) in the middle of its anterior-posterior extent (see Fig. 2). This corresponds to the island of cortical tissue remaining at the medial border of area 17 in the right hemisphere.

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CATXR-11 (RIGHT DEP.)

Fig. 2. Total lesion for cat XR-11, right eye initially deprived. Upper le/t: Surface reconstruction showing a dorsal view and the medial surface of the left and right hemispheres. The retracted splenial sulcus on the medial surface allows representation of the extent of the lesion along the dorsal bank of the sulcus (see Fig. 1). Light stippling indicates cortex which was removed, and heavy stippling indicates cortex which was undercut. Right: Projection drawings of coronal sections through the lesion at positions indicated by the lines extending through the surface reconstruction. The number above each section indicates its stereotaxic coordinates in millimeters anterior ( 4 ) or posterior (--) from the interaural zero plane (0). SS on the second coronal section indicates the right suprasylvian gyrus for reference. Light stippling in the coronal sections indicates remaining cortical tissue, although in some cases it may be seen to be damaged or undercut. Lower left: Projection drawings of coronal sections through the left and right lateral geniculate nuclei at four different levels through the nuclei. Laminae of the dorsal lateral geniculate nucleus are labeled according to the terminology of Thuma (1928) and Guillery (1970): The main laminae A, A1, and C, and the central and medial intcrlaminar nuclei, CIN and MIN, respectively. The sublayers within lamina C are not indicated. MS, moncular segment of lamina A; DIS, cellulur discontinuity representing the optic disc projec~ tion in lamina A (see text); LGV, ventral lateral geniculate nucleus. Light stippling in the lateral gcniculate drawings represents marked retrograde degeneration with scattered healthy apperaring cells remaining. Heavy stippling represents severe retrograde degeneration including all of the large cells. Details of the retrograde degeneration criteria are described in the text

No such clusters of cells were seen on the left, the LGD contralateral to the deprived eye. The MIN of both sides showed marked degeneration, with only scattered large cells present predominantly in the ventral MIN. These were most prevalent on the right side. Based on the lesion reconstruction (compare Figs. 1 and 2) and LGD degeneration, it is concluded that the lesion in this cat was complete, with the exception of a small area of intact striate cortex deep in the splenial sulcus of the right side. This area of spared monocular segment is ipsilateral to the deprived eye, and thus received its sole input from the eontralateral normal eye which was sutured closed during training. The monocular segment of visual cortex contralateral to the deprived eye used in training was totally removed. The cortical lesion of cat MSL-13 was more extensive than that of XR-11. On the convexity of the hemisphere, the lesion extended to the bottom of the lateral snleus and slightly

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CAT XR-6 (RIGHT DEP.) Fig. 3. Central type lesion for eat X1%6, right eye initially deprived. All conventions as in Fig. 2. See text for detailed description

undercut the lateral bank of the sulcus on both sides. On the medial surface of the hemisphere, the lesion went to the b o t t o m of the splenial sulcus along all b u t its most anterior portion on the right (contralateral to the deprived eye) and nearly to the b o t t o m on the left. Retrograde degeneration was severe throughout the main laminae of b o t h LGD, and included the large cells. The MIN also were degenerated, with a few scattered cells present in the MIN of each side. Therefore, the lesion in this cat was considered complete as intended. Central. Two normal cats and two MD cats received lesions intended to include all of areas 19 and 18 and the central 5 - - 1 0 deg. of area 17. Figure 3 shows the extent of cortical removal in one of the MD cats, X1~-6. The lesion on the dorsal convexity of the hemisphere is very similar to t h a t of cat XR-11 with a total lesion (compare with Fig. 2). However, on the medial surface the lesion continued only several millimeters beyond the dorsal and posterior rim of the hemispheres, with no damage to the dorsal b a n k of the splenial sulcus on either side. Corresponding to the total removal of areas 18 and 19, retrograde degeneration was present throughout the MIN of both LGD, with only scattered ceils present (Fig. 3). The medial 25% of the main laminae of b o t h LGD showed severe retrograde degeneration resulting from the additional damage to the lateral aspects of area 17. According to retinotopic maps of the LGD (Kinston et al., 1969; Guillery and Kaas, 1971; Sanderson, 1971; Kaas et al., 1972), this degeneration includes the representation of approximately the central 5 deg. of the visual field projection (see also Fig. 1). The cellular discontinuity which is present in layer A (labeled DIS in Fig. 2) corresponds to the optic disc which is at 15.8 dog. retinal eccentricity from the zero vertical meridian (Guillery a n d Kaas, 1971; Sanderson, 1971, Kaas et al., 1972). The lateral 75% of the LGD of this cat, including the monocular segment, was free of retrograde degeneration. The laminar differences in cell size resulting from monocular deprivation were very clear in the lateral, undegenerated portion of the nucleus. These laminar differences were obscured by the retrograde degeneration in the medial 25% of the nucleus. The lesion in eat XI~-I included all of areas 18 and 19 except for a small p a t c h of areas 18 and 19 anterior on the lateral gyrus of the right side (ipsilateral to the deprived eye) which resulted in a p a t c h of undergenerated cells antero-ventrally in the MIN. I n area 17, the lesion was very similar to XR-6 (Fig. 3) except t h a t on the left side (contralateral to the deprived eye)

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there was a small region of undercutting (5 m m in length) extending down nearly to the dorsal lip of the splenial suleus anteriorly. This resulted in a more lateral extension of the degeneration in the main laminae of the LGD anteriorly. The monocular segment of area 17 remained intact bilaterally. The cortical lesion of eat N2 also included all of areas I8 and 19 except for a small region of tissue anteriorly on the left side (contralateral to the trained eye). The damage to area 17 extended somewhat more medially on the left t h a n in cat XR-6 (Fig. 3), resulting in degeneration in the main laminae of the LGD which reached the cellular discontinuity representing the optic disc. On the right, only the medial 25% of the main laminae were involved. The monocular segment of area 17 was intact bilaterally. I n eat N5, the lesion to areas 18 a n d 19 was complete except for a small a m o u n t of tissue remaining in the depths of the lateral sulcus on the right (ipsilateral to the trained eye). Correspondingly, there was a very sm~ll area of sparing in the ventral MIN in the middle of its antero-posterior extent on this side. There was slight undercutting of the medial quarter of the posterior middle suprasylvian gyrus on the left. The damage to area 17 on the right was similar to the other eats and the LGD degeneration was confined to the medial 25% of the nucleus throughout its anterior-posterior extent. On the left (eontralateral to the trained eye), however, this eat received more extensive damage to medial aspects of area 17. Undercutting was present a quarter to a half of the way down the splenial suleus in two places, and the anterior half of the left LGD was almost completely degenerated throughout its medio-lateral extent. However, in the posterior half of the LGD, the degeneration was confined to the medial 250/o. Thus, the monocular segment was intact only in the posterior portions of area 17 on the left, and was i n t a c t t h r o u g h o u t on the right. I n summary, the four cats receiving central lesions h a d most or all of areas i8 and 19 removed. The damage to area 17 included the central 5 deg. of visual field projection in every ease, and in two eases (one MD and one normal) the lesion extended somewhat further into the visual field projection. The temporal monocular segment of area 17 remained intact bilaterally in all eats, with the exception of one normal eat (N5) in which there was some damage to this area on the side eontrolateral to the trained eye. Peripheral. Two normal cats and two MD eats received lesions intended to include the peripheral visual field projection in area 17, leaving the central 5 - - 1 0 deg. projection and all of areas 18 and 19 intact. Figure 4 shows the extent of cortical removal in one of the MD cats, XL-IO. Dorsally a n d posteriorly, the lesion was larger t h a n intended and undercutting included much of the central visual field projection. I n this respect, this eat had the largest of any of the peripheral ablations. The LGD retrograde degeneration reflects the extensive damage of area 17 and sparing of areas 18 and 19 (Fig. 4). I n the anterior sections, the degeneration is confined to the lateral 25o/0 of the nucleus. Throughout much of the remaining LGD, the degeneration extends more medially, especially on the right. The most posterior sections on the left were free of degeneration laterally; however, this LGD is eontralaterM to the normal eye which was closed during training. Scattered large cells are present in the degenerated portions of the main laminae bilaterally, corresponding to the restriction of the lesion in area 17 (Garey and Powell, 1967; Niimi and Sprague, 1970); however, they are less evident in laminae receiving their inputs from the deprived eye. Many large cells also are evident in the ventral component of the CIN in some sections (see Fig. 4, left LGD) corresponding to the absence of damage to area 18 (Garey and Powell, 1967; Burrows a n d Hayhow, 1971). Finally, the MIN on b o t h sides appears normal. Thus, the lesion in cat XL-1O completely removed the temporal peripheral visual field projection in the striate cortex eontralateral to the deprived eye and nearly all of it eontralateral to the normal eye. Most, b u t not all, of the central visual field projection in area 17 also was damaged. No damage was caused to areas 18 or 19 (compare Figs. 1 a n d 4). Cat XR-5 received a somewhat smaller lesion which did not undercut as much of the central visual field projection on the dorsal convexity of the hemisphere, especially on the right. Correspondingly, the retrograde degeneration was confined to the lateral two-thirds of the right LGD throughout most of the nucleus. There was clear localized sparing in the lateral monocular segment of lamina A in the middle p a r t of the right LGD. However, this portion of the nucleus receives its sole i n p u t from the left (normal) eye which was sutured closed during training. On the left side, contralateral to the deprived eye, all of the monocular segment of

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CAT XL-IO (LEFT DEP.)

Fig. 4. Peripheral type lesion for eat XL-10, left eye initially deprived. All conventions as in Fig. 2. See t e x t for detailed description

area 17 was removed or damaged and retrograde degeneration was present throughout the lateral monocular segment of the LGD. Damage to the central visual field projection was somewhat greater on this side t h a n on the right. There was no damage to areas 18 or 19 on either side. Cat N3 received a very similar lesion, although there was even less undercutting of the central projection area of striate cortex. Consequently, the retrograde degeneration was limited to the lateral one-third to two-thirds of the main laminae of the LGD throughout nearly its entire antero-posterior extent bilaterally. Damage to the area 17 monocular segment was complete on the right side (eontralateral to the eye used during training) and the LGD monocular segment showed degeneration throughout. On the left side (contralateral to the eye occluded during training), part of the monocular segment was spared in the middle of the LGD, as in cat XR-5. Areas 18 and 19 were completely spared on b o t h sides, as intended. I n cat N4, the central projection area of striate cortex was extensively undercut on the right side and almost entirely spared on the left, and this was reflected in the LGD degeneration. The monocular segment was completely removed on the right (eontralateral to the trained eye). On the left side (receiving its sole input from the occluded eye), p a r t of the monocular segment was spared. Areas 18 and 19 were intact bilaterally. I n summary, the peripheral monocular segment of striate cortex was completely damaged contralateral to the deprived eye (in the case of MD cats) or the trained eye (in the case of normal eats) in all of the eats receiving peripheral type lesions. I n all of the eats, p a r t of the monocular segment eontralateral to the eye occluded during training remained intact. All of the eats h a d some damage to the central visual field projection in area 17, although in no case was all of area 17 removed. Areas I8 and 19 remained intact in all of the eats.

Behavior Tables 1 and 2 show the results for preoperative training, preoperative retention t e s t i n g , a n d p o s t o p e r a t i v e r e t e n t i o n t e s t i n g for e a c h e a t . T h e c o n t r o l s e s s i o n s d u r i n g w h i c h b o t h e y e s w e r e o c c l u d e d f o r 20 t r i a l s f o l l o w i n g c r i t e r i o n p e r f o r m a n c e

N

MD

MD

N N

MD

MD

N4

XR-5

XL-10

N2 N5

XR-1

XR-6

R

R

R R

L

R

L

L

L

R

920

240

0 80

120

470

40

110

640

970

Total Trials 1

530

520

280 160

880

700

260

200

(670)

(1500)

Total Trials

TRI

7

--

17 0.5

.

--

17.5

9

6

9.5

Months ~

.

B. P r e - o p Retention H-V

--

15 20

19

--

20

--

18

9

16

.

First 20 Trials 8

0

--

10 0

.

--

0

--

0

140

30

Total Trials

. 6.5 4 0.5 11

1.5

11 0.5 11

--

2

--

--

.

Months

TRI

20 12 16 20 11

.

10 16 14

18

--

--

First 20 Trials

200 0 0 580

0

200 20 240

0

--

--

Total Trials

1 Total Trials indicate n u m b e r of trials to criterion, n o t including the criterion block of 60 trials. P a r e n t h e s e s indicate t h a t p e r i o r m a n c e w a s still at chance levels a n d t r a i n i n g w a s d i s c o n t i n u e d after t h e indicated n u m b e r of trials. 2 M o n t h s indicate n u m b e r of m o n t h s b e t w e e n last c o n t a c t w i t h t h a t t a s k a n d r e t e n t i o n testing. 3 Scores indicate the n u m b e r of correct choices o u t of t h e first d a y of 20 r e t e n t i o n t e s t i n g trials.

MD

N

MSL-13

MD

XR-11

N3

Rearing Cond.

Cat

Dep./ Training Eye

A. P r e - o p Training tt-V

Table 1. P r e o p e r a t i v e t r a i n i n g a n d r e t e n t i o n scores for each eat

9

3

~'

Q

~"

5-

9

192

P.D. Spear and L. Ganz

on each task are not shown in the tables. The cats always performed at chance levels during these sessions. This verified that the data to be presented all were based on the use of visual cues, and that the contact lens occluders used for monocular training were effective in eliminating visual input to the occluded eye.

Preoperative Training All of the MD cats were able to reach criterion on the horizontal-vertical discrimination (Table IA). However, in every case the MD cats required more training trials (from 120 to 970 trials) than any of the normal cats (0 to i l0 trials). The difference between MD and normal cats on this task was statistically significant (Mann-Whitney test, U ~ 0, p --~ 0.01, two-tailed). Similarly, on the triangles discrimination, four of the MD cats were able to reach the learning criterion, again requiring a greater number of trials (520 to 880) than any of the normal cats (160 to 280). The remaining two MD cats remained at chance levels of performance for 670 to 1500 trials, and training was discontinued. The difference between MD cats and normal cats was statistically significant for the triangles discrimination (U --~ 0, p ~ 0.01). These results are consistent with previous reports of deficient visual discrimination learning ability by monocularly deprived cats using their previously deprived eye (Ganz and Fitch, 1968 ; Dews and Wiesel, 1970 ; Rizzolatti and Tradardi, 1971 ; Chow and Stewart, 1972 ; Ganz et al., 1972 ; Ganz and Haffner, 1974). More detailed results concerning the discrimination learning and tiansposition ability of the MD cats used in the present study are presented elsewhere (Ganz and Haffner, 1974). Comparison of performance on the two discriminations for each cat indicated that the triangles discrimination was more difficult than the horizontal-vertical discrimination for both normal and MD cats. I n every case but one (cat X]~-6), more trials were required to reach criterion on the triangles task than on the horizontal-vertical task (Binomial test, p = 0.022, two-tailed).

Preoperative Retention I n order to determine the extent to which monocular deprivation may produce long-term retention deficits in addition to the deficits in original learning of the discriminations, retention tests were administered after periods of time ranging from two weeks to 17.5 months. Two measures of retention were taken. The first was the number of correct choices in the first session of 20 retention testing trials. According to a binomial test, 15 or more correct choices out of 20 trials is significantly above chance (p ~ 0.021, one-tail, for 15 out of 20 correct) and 14 out of 20 is marginally significant (p ~- 0.058). The second retention measure was the total number of trials required to reach criterion performance. The criterion trials were not included in this measure. As may be seen in Table ]B, when retention was tested over a period of from 2 weeks to 4 months, the MD cats showed perfect or nearly perfect retention of both the horizontal-vertical and triangles discriminations. I n every case, performance during the first 20 trials was significantly above chance and criterion was reached immediately or within 20 trials. Over longer retention periods of from 6 to 17.5 months, the MD cats also generally showed high initial performance on the horizontal-vertical discrimination

Role of Visual Cortex in P~eeoveryfrom MD

193

and rapidly attained criterion. Three of the cats were significantly above chance in the initial 20 trials on this task and reached criterion in from 0 to 30 trials. A fourth cat (MSL-13) showed an initial drop to chance performance after a 6 months retention period; however, criterion was reached in 140 trials, substantially fewer than were required in original learning of this discrimination. On the more difficult triangles discrimination, there was a general tendency for the MD cats to show an initial drop to within chance levels of performance following retention intervals of 6 months or more. All four MD cats performed within chance levels in the first 20 trials. Nevertheless, in every case but one (cat XR-6), considerable savings were shown and criterion performance was reached in a much smaller number of trials than were required in original learning. Thus, once MD cats have learned a visual discrimination they generally show perfect or near perfect retention of the discrimination over periods of up to four months. With retention intervals of 6 months or longer, there is a tendency for the MD cats to show an initial drop in performance, particularly on the more difficult triangles discrimination. However, criterion performance is typically attained with considerable savings, indicating good retention even over these extended intervals. The two normal cats (N2 and N3) which were given preoperative retention testing showed perfect retention of both tasks over periods of form 1.5 to 9.5 months (Table 1B). These results provide a baseline against which to compare the effects of the various types of visual cortex lesions. The period of time between last contact with a task (i.e., original learning or a retention test) and postoperative retention testing was two months or less for both normal and MD cats. There weIe only two exceptions to this: on the horizontal-vertical discrimination, eat XL-10 had 20 months between preoperative training and postoperative testing, and cat XR-6 had 23.5 months (see Table 2).

Postoperative Retention a) Total Lesions. Previous studies with normal cats have demonstrated that combined lesions of visual cortical areas 17, 18 and 19 produces a complete loss of preoperatively learned form and pattern discriminations of various types (Spear and Braun, 1939 ; Dalby et al., 1970 ; Dory, 1971 ; Winans, 1971 ; Wood et al., 1974). Under certain conditions and with adequate training, cats with total visual cortex removal are able to relearn such tasks (Spear and Braun, 1969; Dalby et al., 1970; Winans, 1971; Wood et al., 1974); however, many more trials typically are required than in original learning. Similar results were obtained in the present study with two monocnlarly deprived cats which had undergone lesions of areas 17, 18 and 19 (Table 2). Both of these cats (Xl%ll and MSL-13) showed a complete postoperative loss of the horizontal-vertical discrimination, and neither eat performed at better than chance levels for from 800 to over 1000 training trials, at which time training was discontinued. I n both cases, this is greater than the number of trials required to reach criterion preoperatively. Therefore, it is concluded that one or more of visual cortical areas 17, 18, and 19 were involved in the recovered ability of the monoeularly deprived cats to perform the pattern discrimination. 14

E x p . B r a i n ttes. Vol. 23

N2 N5 XR-1 XP~-6

Central

N N MD MD

N N MD MD

MD MD

l~earing Cond.

20 13 17 10

19 16 20 4

12 13

tt-V First 20 Trials

0 40 40 350 a

0 l0 0 640 a

(1020) (800)

Total Trials

0% 33% 71% 45%

100% 60% 100% --68%

m

Percent Savingsb

17 10 12 17

19 14 16 15

TP~I First 20 Trials

20 300 110 (I000)

0 80 20 100

Total Trials

87% --30% 65% --

100% 53% 94% 80%

Percent Savings

a 20 months intervened between training on the t t - V task and postoperative retention testing for cat XL-10, and 23.5 months intervened between training and testing on this task for cat Xl~-6. I n all other eases, including the triangles discrimination for these two eats, the retention interval was 2 months or less. b Savings scores were computed as pre-op trials to criterion minus post-op trials to criterion, divided by the sum of these two quantities, times 100.

N3 N4 XR-5 XL-10

MSL-13

Xl~-ll

Cat

Peripheral . . . . . . . .

Total

Lesion Type

Table 2. Postoperative retention scores for each cat

9~

O~

Role of Visual Cortex in Recovery from MD

195

With the remaining cats, an attempt was made to determine if any particular subregion of the visual cortex was necessary and/or sufficient for the recovered pattern discrimination ability in the MD cats, and whether these subregions would be different from those in normal cats. Particular interest was focused on the peripheral monocular segment of striate cortex. b) Peripheral Lesions. The two normal cats (N3 and N4) with area 17 monocular segment damage showed excellent retention of both visual discriminations (Table 2). One cat (N4) showed a slight initial drop in performance on the triangles discrimination; however, criterion was attained with savings. On the remaining tasks, both cats performed significantly above chance during the first 20 retention trials and reached criterion with substantial savings. Similar results were obtained with the two MD eats (XR-5 and XL-10) with area 17 monocular segment damage. There was generally excellent retention of the discriminations following the lesion (Table 2). An exception to this is cat XL-10 which showed a loss of the horizontal-vertical discrimination. However, this cat had an unusually long (20 months) retention interval for this task. From the results with preoperative retention testing in MD cats, it is possible that this loss was due to simple forgetting over the long interval rather than to the lesion. On the remaining tasks, including the more difficult triangles discrimination for cat XL-10, both cats performed significantly above chance during the first 20 retention trials and reached criterion with nearly perfect savings (Table 2). e) Central Lesions. The results with the two normal cats (N2 and N5) having lesions of areas 18, 19, and the central 5--10 deg. of area 17 were somewhat more variable. Cat N2 appeared to have nearly perfect retention of both discriminations following the lesion (Table 2). However, the significance of this is uncertain for the horizontal-vertical discrimination: In original learning this cat had an initial preference for the correct vertical stimulus and required no training to reach criterion preoperatively (Table 1A). As 9 result, cat N2 had a savings score of 0% in spite of perfect postoperative performance. Cat N5 showed an initial postoperative drop in performance during the first 20 trials on both tasks, and relearned the horizontal-vertical discrimination with positive savings and the triangles discrimination with negative savings. Thus, it is difficult to draw firm conclusions regarding the effects of central type lesions on postoperative retention in the normal eats. However, their ability to relearn the discriminations relatively quickly in every ease is in clear contrast to the effects of total visual cortex lesions in normal cats (Spear and Braun, 1969 ; Dalby et al., 1970; Dory, 1971 ; Winans, 1971 ; Wood et al., 1974). Similar results were obtained with the two MD eats (XI~-I and XR-6) with central type lesions. Cat XR-1 showed excellent postoperative retention of the horizontal-vertical discrimination and also relearned the triangles task with positive savings (Table 2). However, on the latter task performance was within chance levels during the first 20 trials. The second cat (XR-6) dropped to chance performance during the first 20 trials on the horizontal-vertical discrinfination, but relearned with savings. The initial drop may have been due to the 23.5 month retention interval for this task (Table 2). On the triangles discrimination, cat XR-6 performed at significantly above chance levels during the first 20 trials. Subsequent performance was consistently around 70--80 o/o correct; however, it was unstable 14

Exp. :Brain l~es.

VoL 23

196

P.D. Spear and L. Ganz

and criterion was never attained in 1000 trials. This eat had shown the same unstable performance during preoperative retention testing on the triangles discrimination (Table 1B). These variations in the results again make it difficult to draw firm conclusions iegarding the effects of the central type lesions on postoperative retention in MD eats. Nevertheless, the subsequent performance of these eats and especially the rapid acquisition of criterion performance with positive savings scores on the horizontal-vertical discrimination by both eats, contrasts sharply with the prolonged deficits produced b y total visual cortex lesions in MD cats. Discussion Combined damage to visual cortical areas 17, 18, and 19 in recovered MD eats produced a complete loss of a preopeiatively learned pattern discrimination in the present experiment. Aarons et al. (1963) found similar results with dark-reared cats which had learned a brightness discrimination. I n their eats, removal of "visual areas I and I I " produced a postoperative loss of the discrimination. Taken together, these results indicate t h a t one or more of the affected visual cortical areas are involved in the recovery of visual discrimination capacities in both darkreared and monocularly deprived cats. Although MD cats use their visual cortex to learn visual pattern discriminations, the monocular segment of striate cortex does not appear to be specially involved in this ability. Total removal of this area in two recovered MD cats produced no loss of the discriminations beyond what is expected on the basis of normal forgetting. Furthermore, these results with MD cats were the same as those with normal cats after removal of the monocular segments of area 17, and in marked contrast to the loss produced b y total visual cortex damage in MD cats. Thus, it appears t h a t the part of striate cortex receiving its input from the monocular visual field of the deprived eye was not specially involved in or necessary for the recovered visual discrimination performance. The effects of damage to areas 18, 19, and the central 5--10 deg. of area 17 on retention of the form and pattern discriminations were somewhat more variable. Nevertheless, the reacquisition results are suggestive t h a t these areas were not crucial to the discrimination performance in the recovered MD cats. In three cases the MD cats relearned the discriminations with savings following the lesions and in every case their performance was clearly superior to the MD cats receiving total visual cortex lesions. These results are consistent with observations with normal cats in the present experiment. Further, previous studies have shown little or no loss of various preoperatively learned visual discriminations by undeprived cats with extensive damage to the central binocular projection area of striate cortex, but leaving cortex in the splenial sulcus (including the monocular segment) intact (Smith, 1937; Kennedy, 1939; Taravella and Clark, 1963; Fischman and Meikle, 1965; Chow, 1968; Berkley, 1971; Winans, 1971 ; Berlucchi et al., 1972). Thus, the central retinal projection area of striate cortex does not appear to be crucial for continued visual discrimination performance in either normal or recovered MD cats. Of course, the possibility remains t h a t the whole binocular segment of striate cortex is necessary for continued performance in normal cats and the recovered discrimination performance in MD cats. None of the animals in

Role of Visual Cortex in Recovery from MD

197

the present study, nor any of those previously reported, received complete deStruction of the binocular segment without additionaldamage to the monocular segment. Our results also suggest t h a t areas 18 and 19 alone are not crucial to continued performance of visual discriminations in either normal or MD eats, since the cases with central area 17 lesions also included removal of areas 18 and 19. Previous studies with normal cats also found little or no loss of preoperatively learned visual discriminations following extensive damage to areas 18 and 19 and incomplete removal of area 17 (Smith, 1937; Kennedy, 1939; Taravella and Clark, 1963; Fischman and Meikle, 1965; Chow, 1968; Winans, 1971). The present results thus show t h a t the area 17 monocular segment is not necessary for visual discrimination performance in recovered MD cats and suggest t h a t areas 18 and 19 (and therefore their monocular segments) also m a y not be crucial. However, it is possible t h a t the monocular segments of both areas 17 and 18 are being specially employed, and t h a t simultaneous damage to both monocular segments is necessary to produce a loss. The present study was based on anatomical and physiological findings t h a t the effects of monocular deprivation which are observed in the binocular laminated portion of the LGD are absent in the monocular segment of the nucleus (Guillery and Stelzner, 1970 ; Sherman et al., 1972 ; Guillery, 1972, 1973; Garey et al., 1973; Sherman et al., 1974). The LGD in turn sends afferents to both areas 17 and 18 (Glickstein et al., 1967 ; Wilson and Cragg, 1967; Garey and Powell, 1967, 1971; C31onnier and l~ossignol, 1969; Niimi and Sprague, 1970; Burrows and Hayhow, 1971; Health and Jones, 1971; Rossignol and Cololmier, 1971 ; Stone and Dreher, 1973 ; Rosenquist et aL, 1974). Therefore, it m a y be necessary to remove the monocular segments of both areas 17 and 18 simultaneously to produce a loss of the learned visual discriminations. At the present time, no data are available to decide on this possibility conclusively. However, recent findings suggest t h a t area 18 m a y include little or no representation of the monocular visual field along the horizontal meridian. For example, electrophysiological mapping studies of area 18 indicate t h a t as one moves laterally along the projection of the horizontal meridian, the centers of the receptive fields extend to no further t h a n 40--50 deg. into the peripheral visual field (Hubel and Wiesel, 1965; Bilge et al., 1967; Woolsey, 1971; Tusa, 1974). Further, a recent anatomical study (Rosenquist et al., 1974) found that this same mid-portion of lateral area 18 receives no projection from the monocular segment of the LGD. I t is, of course, possible t h a t area 18 contains a representation of the monocular visual field, but t h a t it has been displaced on the cortical surface. However, if one is present, it m a y not receive direct projections from the LGD since there is no evidence t h a t such a displaced geniculo-cortical projection exists from the monocular segment of the LGD to area 18 (Rosenquist st al., 1974). I n t h a t case, inputs to an area 18 monocular segment would come from striate cortex (tIubel and Wiesel, 1965; Garey et al., 1968; Wilson, 1968; Kawamura, 1973), and they would therefore be eliminated by removal of the striate cortex monocular segment as was done in the present experiment. Since removal of the monocular segment of area 17 in our MD cats produced no postoperative effect, the above considerations suggest t h a t it m a y not be necessary to remove additionally a monocular segment of area 18 if one is present. However, further research is needed before a firm conclusion can be drawn on this question.

198

P.D. Spear and L. Ganz

I f the MD cats do not rely on the monocular segment for their recovered visual discrimination performance, as is suggested by the foregoing discussion, then it becomes relevant to consider what other mechanisms within the visual cortex m a y subserve the recovered ability. The most likely possibility is t h a t the small percent of abnormally responsive cells which remain following monocular deprivation are being utilized when MD cats are forced to learn a discrimination through the deprived eye. This possibility is consistent with studies in cats (Dews and Wiesel, 1970 ; Ganz et al., 1972 ; Blakemore and Van Sluyters, 1974) and monkeys (Baker et al., 1974) demonstrating that the percent and severity of abnormally driven cells in visual cortex is correlated with the degree of perceptual deficits following various types of visual deprivation. Further, t h a t animals are capable of utilizing only a small percent of visual cells to subserve visual discrimination behavior has been shown previously in both rats (Lashley, 1939) and cats (Galambos et al., 1967 ; Norton et al., 1967; Chow, 1968). I t seems likely t h a t if this abnormal visual information is employed by the MD cats to solve the discrimination tasks, it is used in a way t h a t is different from the mechanisms used in normal form and pattern vision. For example, the scanning head movements observed by Rizzolatti and Tradardi (1971) might represent attempts to stimulate larger portions of the visual field (rather than any specific portion in particular) or to produce differential flicker cues by moving the retinae relative to the visual stimuli. Sherman (Sherman, 1972a, 1974; Sherman et al., 1974) has demonstrated t h a t MD eats perform normal visual orienting and approach responses to stimuli presented in the peripheral monocular visual field but do not respond to stimuli presented in the central binocular visual field. The present results and discussion suggest that the peripheral monocular visual field m a y not be used selectively for visual discrimination behaviors in MD cats. Therefore, it would seem t h a t the neural substrates for the orientation and approach response m a y be different from those involved in visual discrimination learning and performance. For example, the monocular segment of striate cortex m a y subserve the orienting and approach response to stimuli in the peripheral field, but not visual discrimination behaviors. Alternatively, ~ second structure (e.g., the superior collieulus) m a y subserve the orienting and approach response in MD cats, while the visual cortex subserves visual discrimination performance. Sherman (1972a, 1972b) has proposed t h a t this is the case for binocularly deprived cats, and the same m a y be true for monocularly deprived cats. We express our gratitude to Ann Harris and Benjamin Dawson for technical assistance. Supported by a grant from Kansas State University Bureau of General Research and USPHS grant 5 ROl EY01170 to P.D.S., and USPHS grant 1 R01 EY01241 to L.G. References Aarons, L., Halasz, H,K., Riesen, A. H. : Interocular transfer of visual intensity discrimination after ablation of striate cortex in dark-reared kittens. J. comp. physiol. Psychol. 56, 196-199 (1963) Baker, F.H., Grigg, P., yon Noorden, G.K. : Effects of visual deprivation and strabismus on the response of neurons in the visual cortex of the monkey, including studies on the striate and prestriate cortex in the normal animal. Brain Res. 66, 185--208 (1974) Berkley, M.A.: Line orientation discrimination deficits following partial ablation of the geniculo-cortical system in cats. Prec. Soc. Neurosci. 1, 125 (1971)

Role of Visual Cortex in Recovery from MD

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Berlucchi, G., Sprague, J.M., Levy, J., Di Berardino, A. C. : Pretectum and superior colliculus in visually guided behavior and in flux and form discrimination in the cat. J. comp. physiol. Psychol. 78, 123--172 (1972) Bilge, M., Bingle, A., Seneviratne, K.N., Whitteridge, D. : A map of the visual cortex in the cat. J. Physiol. (Lond.) 191, 116--118 (1967) Blakemore, C., Van Sluyters, R.C. : Reversal of the physiological effects of monocular deprivation in kittens: Further evidence for a sensitive period. J. Physiol. (Lond.) 237, ]95--216 (] 974) Burrows, G.R., Hayhow, W.K. : The organization of the thalamo-cortical visual pathways in the cat. An experimental degeneration study. Brain Bchav. Evol. 4, 220--270 (1971) Chow, K.L. : Visual discriminations after extensive ablation of optic tract and visual cortex in cats. Brain Res. 9, 363--366 (1968) Chow, K.L., Stewart, D.L. : Reversal of structural and functional effects of long-term visual deprivation in cats. Exp. Neurol. 34, 409--433 (1972) Colonnier, M., Rossignol, S. : On the heterogeneity of ttm cerebral cortex. In: H.H. Jasper, A.A. Ward, A. Pope (Eds.). Basic Mechanisms of the Epilepsies. pp. 29--40. Boston: Little, Brown & Co. 1969 Dalby, D.A., Meyer, D.R., Meyer, P.M. : Effects of occipital neocortical lesions upon visual discriminations in the eat. Physiol. Behav. 5, 727--734 (1970) Dews, P.B., Wicsel, T.N.: Consequences of monocular deprivation on visual behavior in kittens. J. Physiol. (Lond.) 206, 4 3 7 4 5 5 (1970) Dory, R.W. : Survival of pattern vision after removal of striate cortex in the adult cat. J. comp. Neurol. 143, 341--370 (1971) Fischman, M.W., Meikle, T.H., Jr. : Visual intensity discrimination in cats after serial tectal and cortical lesions. J. comp. physiol. Psychol. 59, 193--201 (1965) Galambos, R., Norton, T.T., Frommer, G. P. : Optic tract lesions sparing pattern vision in cats. Exp. Neurol. 18, 8--25 (1967) Ganz, L., Fitch, M. : The effect of visual deprivation in perceptual behavior. Exp. Neurol. 22, 638--660 (1968) Ganz, L., Fitch, M., Satterberg, J.A. : The selective effect of visual deprivation on receptive field shape determined ncurophysiologically. Exp. Neurol. 22, 614--637 (1968) Ganz, L., Haffner, M.E.: Permanent perceptual and neurophysiologicaI effects of visual deprivation in the cat. Exp. Brain Res. 20, 67--87 (1974) Ganz, L., Hirsch, H. V. B., Tieman, S. B. : The nature of perceptual deficits in visually deprived cats. Brain Res. 44, 547--568 (1972) Garey, L.J., Fiskin, R.A., Powell, T. P. S. : Effects of experimental deafferentation on cells in the lateral genieulate nucleus of the eat. Brain Res. 52, 363--369 (1973) Garey, L.J., Powell, T. P. S. : The projection of the lateral geniculate nucleus upon the cortex in the cat. Proe. roy. Soc. B 169, 107--126 (1967) Garey, L.J., Powell, T. P. S. : An experimental study of the termination of the lateral geniculocortical pathway in the cat and monkey. Proc. roy. Soc. B 179, 41--63 (1971) Garey, L.J., Jones, E.G., Powell, T. P. S. : Interrelationships of striate and extrastriate cortex with primary relay sites of the visual pathway. J. Neurol. Neurosurg. Psychiat. 31, 135-157 (1968) Gellerman, L.W. : Chance orders of alternating stimuli in visual discrimination experiments. J. genet. Psyehol. 42, 206--208 (1933) Glass, J . D . : Photically evoked potentials from cat neocortex before and after recovery from visual deprivation. Exp. Neurol. 39, 123--139 (1973) Glickstein, M., King, R., Miller, J., Berkley, M. : Cortical projections from the dorsal lateral geniculate nucleus of cats. J. comp. Neurol. l~lO, 55--76 (1967) Guillery, R.W. : The laminar distribution of retinal fibers in the dorsal lateral geniculate nucleus of the cat: A new interpretation. J. comp. Neurol. 138, 339--368 (1970) Guillery, R.W. : Binocular competition in the control of geniculate cell growth. J. comp. Neurol. 144, 117--130 (1972) Guillery, R.W. : The effect of lid suture upon the growth of cells in the dorsal lateral geniculate nucleus of kittens. J. comp. Neurol. 148, 4 1 7 ~ 2 2 (1973)

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Guillery, R.W., Kaas, J. H. : A study of normal and congenitally abnormal retino-geniculate projections in cats. J. comp. Neurol. 143, 73--100 (1971) Guillery, 1~. W., Stelzner, D.J. : The differential effects of unilateral lid closure upon the monocular and binocular segments of the dorsal lateral geniculate nucleus in the cat. J. comp. Neurol. 139, 413--422 (1970) Heath, C.J., Jones, E.G. : The anatomical organization of the suprasylvian gyrus of the cat. Ergebn. Anat. Entwickl.-Gesch. 45 (3), 1--64 (1971) Hoffmann, K.P., Sherman, S.M. : Effects of early monocular deprivation of visual input to cat superior colliculus. J. Neurophysiol. 37, 1276--1286 (1974) Hubel, D.H., Wiesel, T.H.: Receptive fields and functional architecture in two nonstriate visual areas (18 and 19) of the cat. J. Neurophysiol. 28, 229--289 (1965) ttubel, D. H., Wiesel, T. H. : The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J. Physiol. (Lend.) 206, 4 1 9 ~ 3 6 (1970) Kaas, J . H . , Guillery, I%W., Allman, J.M. : Some principles of organization in the dorsal lateral genieulate nucleus. Brain Behav. Evol. 6, 253--299 (1972) Kalia, M., Whitteridge, D. : The visual areas in the splenial sulcus of the cat. J. Physiol. (Lend.) 232, 275--284 (1973) Kawamura, K. : Cortico-cortical fiber connections of the cat cerebrum. III. The occipital region. Brain Res. 51, 41--60 (1973) Kennedy, J.L. : The effects of complete and partial occipital lobeetomy upon thresholds of visual real movement discrimination in the cat. J. genet. Psychol. 54, 119--150 (1939) Kinston, W. J., Vadas, M. A., Bishop, P. O. : Multiple projection of the visual field to the medial portion of the dorsal lateral geniculate nucleus and the adjacent nuclei of the thalamus of the cat. J. comp. Neurol. 136, 295--316 (1969) Lashley, K. S. : The mechanism of vision: XVI. The functioning of small remnants of the visual cortex. J. eomp. Neurol. 76, 45--67 (1939) Niimi, K., Sprague, J.M.: Thalamo-cortical organization of the visual system in the cat. J. comp. Neurol. 138, 219--250 (1970) Norton, T.T., Galambos, 1~., Frommer, G.P. : Optic tract lesions destroying pattern vision in eats. Exp. Ncurol. 18, 26--37 (1967) Otsuka, P~., Hassler, 1% : ~ b e r Aufbau und Gliederung der cortiealen Sehsphiire bei der Katze. Arch. Psychiat. Z. NeuroI. 203, 212--234 (1962) Reinoso-Suarez, F.: Topographischer Hirnatlas der Katze fiir experimental-physiologische Untersuchungen. Darmstadt: E. Merck A.G. 1961 Rizzolatti, G., Tradardi, V. : Pattern discrimination in monoeularly reared cats. Exp. Neurol. 33, 181--194 (1971) l~osenquist, A. C., Edwards, S.B., Palmer, L.A. : An autoradiographic study of the projections of the dorsal lateral geniculate nucleus and the posterior nucleus in the eat. Brain l~es. 80, 71--94 (1974) l~ossignol, S., Collonier, M. : A light microscopic study of degeneration patterns in cat cortex after lesions of the lateral geniculate nucleus. Vision P~es. Suppl. 3, 329--338 (1971) Sanderson, K . J . : The projection of the visual field to the lateral geniculate and medial interlaminar nuclei in the cat. J. comp. Neurol. 143, 101--118 (1971) Sanides, F., Hoffmann, J. : Cyto- and myeloarchitecture of the visual cortex of the cat and of the surrounding integration cortices. J. Hirnforsch. l l , 79--104 (1969) Sherman, S.M. : Visual field defects in monocularly and binocularly deprived cats. Brain Res. 48, 25--46 (1972a) Sherman, S.M.: Visual development in cats. Invest. OphthM. l l, 394--401 (1972b) Sherman, S.M.: Permanence of visual perimetry deficits in monocularly and binocularly deprived cats. Brain Res. 73, 491--502 (1974) Sherman, S.M., Guillery, R.W., Kaas, J . H . , Sanderson, K . J . : Behavioral, cleetrophysiologieal and morphological studies of binocular competition in the development of the geniculocortical pathways of cats. J. comp. Neurol. 158, 1--18 (1974) Sherman, S.M., Hoffmann, K.P., Stone, J.: Loss of a specific cell type from dorsal lateral geniculate nucleus in visually deprived cats. J. Neurophysiol. 35, 532--54] (1972) Smith, K . U . : Visual discrimination in the cat. V. The postoperative effects of removal of the striate cortex upon intensity discrimination. J. genet. Psychol. 51,329--370 (1937)

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Spear, P.D., Braun, J.J. : Pattern discrimination following removal of visual neocortex in the cat. Exp. Neurol. 25, 331--348 (1969) Sperry, R.W., Myers, R.E., Schrier, A.M.: Perceptual capacity of the isolated visual cortex in the cat. Quart. J. exp. Psychol. 12, 65--71 (1960) Stone, J., Dreher, B." Projection of X- and Y-ce|Is of the cats' lateral geniculate nucleus to areas 17 and 18 of visual cortex. J. Neurophysiol. 36, 551--567 (1973) Talbot, S. If., Marshall, W. I-I.: Physiological studies on neural mechanisms of visual localization and discrimination. Amer. J. Ophthal. 24, 1255--1264 (1941) Taravella, C.L., Clark, G.: Discrimination of intermittent photic stimulation in normal and brain-damaged cats. Exp. Neurol. 7, 282--293 (1963) Thuma, B.D.: Studies on the diencephalon of the eat. I. The cyto-arehitecture of the corpus geniculatum laterale. J. comp. Neurol. 46, 173--198 (1928) Tusa, R.: Retinotopic organization of area 18 in the eat. Anat. Rec. 178, 479 (1974) Wiesel, T.N., Hubel, D. H. : Single-cell responses in striate cortex of kittens deprived of vision in one eye. J. Neurophysiol. 26, I003--I017 (1963) Wiesel, T.N., I-Iubel, D. I-I.: Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. J. l~europhysiol. 28, I029--i040 (1965a) Wiesel, T.N., Hubel, D. H. : Extent of recovery from the effects of visual deprivation in kittens. J. Neurophysiol. 28, 1060--1072 (1965b) Wilson, M.E. : Cortico-cortical connexions of the cat visual areas. J. Anat. (Lond.) 102, 375-386 (1968) Wilson, IK.E., Cragg, B.G." Projections from the lateral geniculate nucleus in the cat and monkey. J. Anat. (Lond.) 101, 677--692 (1967) Winans, S.S. : Visual cues used by normal and visual-decorticate cats to discriminate figures of equal luminous flux. J. comp. physiol. Psychol. 74, 167--178 (1971) Wood, C.C., Spear, P.D., Braun, J.J. : Effects of sequential lesions of suprasylvian gyri and visual cortex on pattern discrimination in the eat. Brain Res. 66, 443~466 (1974) Woolsey, C.N. : Comparative studies on cortical representation of vision. Vision Res. Suppl. 3, 365--382 (1971) Dr. P.D. Spear Department of Psychology Anderson Hall Kansas State University Manhattan, Kansas 66506 USA