Exp. Brain Res. 23, 353--365 (1975) @ by Springer-Verlag1975

Effects of Serial Lesions of Somatosensory Cortex and Further Neodecortication on Tactile Retention in Rats* D. Simons, J. Puretz and S. Finger Department of Psychology, Washington University, St. Louis, Missouri (USA) Received April 22, 1975 Summary. Four groups of rats with bilaterallesions of somatosensory cortex and one of animals sustaining only sham operations were tested for retention of a difficult tactile discrimination. Two of the lesion groups had serial ablations, in one case with interoperative testing, and two had one-stage lesions. Bilateral ablations of somatosensory cortex severely retarded retention in all lesion groups relative to the control group and serial and one-stage groups did not differ from each other. The sham operated rats then experienced lesions of cortex anterior and posterior to the somatosensory areas. These lesions only marginally affected retention. Somatosensory cortex then was ablated a n d severe performance decrements were seen. Removal of additional neocortex in animals that previously had relearned the discrimination after somatosensory cortex lesions also resulted in very poor retention. These data demonstrate the importance of the somatosensory cortex in mediating tactile discriminations and suggest that non-somatosensory cortex m a y play a role in recovery after somatosensory cortical lesions. Key words: Somatosensory - - Tactile - - Cortex - - Serial lesions - - Ablation

Introduction The importance of the electrophysiologically defined somatosensory areas of the cortex in tactile performance in rats has been demonstrated in several experiments employing extirpation techniques (Finger st al., 1072 ; Finger and Frommer, 1968a, b ; Zubek, 1051 a, 1952a). These studies have shown that damage to somatic cortex areas 1 and 2, alone or together, generally results in marked deficits in postoperative performance on rough-smooth and some tactile form discriminations. Recent experiments, however, have revealed that rats with extensive damage to cortical somatosensory areas may perform as well as sham operated animals under certain conditions. Finger et al. (1971 b) observed little or no impairment in the acquisition of tactile discriminations in rats that had sustained bilateral somatic cortex damage in two sequential operations. Further, Weese et al. (1973) found that some postoperative performance deficits could be circumvented with preoperative overtraining. * This research was supported by NIMI-I Grant MH-25397, NINDS Grant NS-11002, NIGMS Grant GMO-1900 and by Biomedical Sciences Support Grant Fund 54993. Preliminary data were presented at the 1974Meetings of the Society for Neuroscience (St. Louis, Missouri)

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S ev eral e x p e r i m e n t e r s h a v e i n v e s t i g a t e d t h e relationship b e t w e e n seriM s u r g e r y a n d t r a i n i n g v a r i a b le s in r e t e n t i o n of b l a c k - w h i t e d i scr i m i n at i o n s in t h e rat. T h e results of th e s e studies h a v e b e e n f o u n d to v a r y w i t h p a r a m e t e r s such as lesion size a n d t h e n a t u r e a n d c o m p l e x i t y of t h e t a s k (Kircher et al., 1970 ; Mey er et al., 1958; P e t r i n o v i e h a n d Carew, 1969). A n al o g o u s r e t e n t i o n studies i n v o l v i n g serial lesions in t h e s o m a t o s e n s o r y s y s t e m h a v e n o t b e e n conducted. H e n c e , t h e first e x p e r i m e n t was u n d e r t a k e n to i n v e s t i g a t e t h e effects of serial lesions w i t h a n d w i t h o u t i n t e r o p e r a t i v e t r a i n i n g on r e t e n t i o n of a difficult r i d g e - s m o o t h d i s cr i m i n at i o n . I t was p r e d i c t e d t h a t serial a b l a t i o n of s o m a t o s e n s o r y c o r t e x w o u l d result in less severe p e r f o r m a n c e deficits t h a n c o m p a r a b l e lesions p r o d u c e d in a single o p e r a t i o n a n d t h a t i n t e r o p e r a t i v e t r a i n i n g w o u l d f u r t h e r e n h a n c e r e t e n t i o n .

Experiment 1 Methods Subjects Thirty-five naive male rats derived from the Sprague-Dawley strain (Bio-Labs, White Bear, Minnesota) were used in the study. The animals were approximately 90 days old at the beginning of the investigation and weighed approximately 250 gins. They were housed by threes in 30.5 • 35.6 • 17.7 cm plastic cages under constant illumination. Water was available ad libitum, although food (Purina Rat Chow mixed with water) was restricted to a 15 rain period at the end of each test session.

Apparatus The animals were tested for the ability to discriminate between two tactile surfaces in the T-maze that had been used in previous experiments conducted in this laboratory (e.g., Finger et al., 1971 a, b, 1972). The maze was constructed from plywood and the startbox measured 35.6 cm long, while each maze alley was 57.2 cm in length. The walls of the maze stood 21.6 cm high and were spaced 10.2 cm apart. A single sheet-metal guillotine door in the shape of an inverted "T" separated the start box from the two wings of the maze and the wings from each other. Two aluminum plates (one smooth and the other milled) covered the floors of the wings of the maze and served as the discriminanda. The plates extended 43.0 cm from the choice point in the maze to the food cups. Previous testing has shown that the use of aluminum plates circumvents an olfactory confounding which could be present when sandpaper stimuli are used (Finger et al., 1970a). Furthermore, earlier studies (e.g., Finger and Frommer, 1968b) which frequently involved inserting a probe into the ear and damaging the eardrum and associated structures as an auditory control have not provided data different from those in later studies (e. g., Finger et al., 1971 b) in which this procedure was abandoned. Thus, differential auditory cues either are not available or can not be used by the animals in the maze. The surfaces, taken from the set first described by Finger and Frommer (1968b), are shown in cross section in

Fig. 1. Preliminary Surgery and Testing The animals were anesthetized with ether and blinded by enucleation 2 weeks prior to the start of testing. This was done to eliminate the possible use of visual cues in the maze. Ten days later the rats were introduced to the 15 min feeding schedule and were handled for 5 rain/ day until testing began. The blinded rats were assigned at random to two squads to facilitate testing and three experimenters alternated testing these squads. Each rat was given 5 trials per day (7 days/ week), and individual animals within each squad were run in random order on each of the 5 successive trials. The ridged plated was designated as the positive stimulus for half of the animals while the smooth plate served as the correct stimulus for the remaining animals. The position of the positive stimulus in either the right or left wing of the maze was determined by a random

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procedure with the restriction t h a t it would not appear in the same wing more t h a n three consecutive times for a n y animal on a given day. Olfactory cues were balanced b y placing Purina R a t Chow mixed with water in a food cup a t the end of each discriminandum. A sheetmetal barrier blocked the food cup in the wing containing the incorrect stimulus. A noncorrective method of training was used; t h a t is, the guillotine door was lowered to prevent retracing as soon as the animal extended its body past the choice point and placed all four paws on one of the surfaces. Animals were left in the maze for 20 sec regardless of whether a choice was correct or incorrect. The discriminanda were scrubbed with a Lysol solution after the group completed each trial to minimize odor trials. Following the procedure used b y Weese et al. (1973), an a priori criterion of no errors on two consecutive days was chosen to define learning. Subjects were removed from testing after meeting this criterion. Operations were performed no less t h a n three and no more t h a n 5 days later.

Surgery Animals were assigned to one of five experimental groups as they met criterion. An a t t e m p t was made to have fast a n d slow learners distributed evenly among these groups. The groups underwent the following surgical procedures: a) two control (sham) operations (C-C); b) a sham operation followed b y one-stage bilateral lesions of somatesensory cortex areas 1 and 2 with retraining te criterion interposed between operations (Ct-SS) ; c) one-stage lesions of the same areas followed b y a sham operation (SS-C); d) successive unilateral lesions of the somatosensory areas (1/2SS-1/2SS); and e) successive unilateral lesions of the somatesensory areas with retraining to criterion interposed between operations (1/2SSt-1/2SS). A 30 day interoperative period was used for groups C-C, SS-C, a n d 1/2SS-1/2SS. This was determined b y adding the mean n u m b e r of days for retraining rats in groups C*-SS and 1/2SSt-1/~SS to criterion during the interoperative interval (11.13 days) to b o t h the preceding recovery period of 14 days and to the mean home cage duration of slightly more t h a n 4 days just preceding the second surgery. All surgery was conducted under pentobarbital sodium anesthesia (Diabutal, 60 mg/kg, IP). Cortical extirpations were accomplished b y aspiration and lesion placement was based on previously constructed electrophysiological maps of the r a t cortex (Welker, 1971; Zubek, 1951 b). A mid-line incision exposing the dorsal surface of the skull constituted the sham condition. Wounds were sutured with silk thread and rats were treated with 100 000 U benzathine penicillin G (Bicillin, Wyeth) before being placed in cages for recovery. Ten days of ad libitum feeding constituted the first p a r t of the recovery period for b o t h interoperative a n d postoperative testing. After this the animals were placed on a 15 rain feeding schedule for 4 days to enhance motivated running.

Postoperative Testing All rats were tested for retention of the same ridge-smooth discrimination t h a t was used in the original training sessions. The choice of the plate (ridged or smooth) was not changed

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and mastery was determined according to the same criterion used for preoperative training. The first and thereafter every third animal that mastered the problem in groups Ct-SS, 1/eSSt-i/2SS and i/2SS-i/eSS was saerified for histological study. Sixty days was considered a suitable cut-off point for postoperative testing in the absence of learning as this was 3 standard deviations from the preoperative mean. Each animal that failed to master the problem within 60 days (300 trials) received its cumulative error score plus a conservative maximum day score of 63 days to criterion and also was sacrificed. All remaining animals were advanced to the next experiment (see Experiment 2 below). This included all rats without lesions (C-C) and all SS-C subjects that reached criterion. No animals that learned the problem in the latter condition were sacrificed because only two rats in this group met criterion within the allotted time.

Histological Procedure Animals to be sacrificed were deeply anesthetized with pentobarbital sodium and were pcrfused with 0.90/0 saline followed by 10% Formalin solution injected through the aorta. The dorsal and two lateral surfaces of the brains were photographed. Coronal sections were cut at 50 micra on a freezing microtome after preparation in Formalin solution, and every third section was saved and stained with cresyl-violet acetate. The extirpations were studied with a low power microscope to confirm the location and extent of neural damage and drawings of the surface lesions were made with aid of the photographs.

Results N o n - p a r a m e t r i c s t a t i s t i c a l t e s t s were a p p l i e d t o all of t h e d a t a since t h e a s s u m p t i o n s u n d e r l y i n g p a r a m e t r i c t e s t s (e. g., h o m o g e n e i t y of variance) were n o t m e t on m a n y of t h e c o m p a r i s o n s (Siegel, 1956). F u r t h e r , for all s t a t i s t i c a l tests, a n i m a l s r e w a r d e d on t h e s m o o t h surface were p o o l e d w i t h r a t s r e w a r d e d on t h e m i l l e d surface since t h i s f a c t o r d i d n o t a p p e a r to affect t h e b e h a v i o r of t h e a n i m a l s in a n y of t h e groups. S t a t i s t i c a l a n a l y s e s first were c o n d u c t e d on t h e p r e o p e r a t i v e scores t o confirm g r o u p equivalence p r i o r to surgery. These error scores are seen in Fig. 2. Significant differences b e t w e e n t h e five e x p e r i m e n t a l groups were n o t f o u n d on errors to criterion or on d a y s t o c r i t e r i o n p r i o r t o s u r g e r y i n d i c a t i n g t h a t f a s t a n d slow learners were d i s t r i b u t e d e q u a l l y a m o n g t h e v a r i o u s conditions ( K r u s k a l - W a l l i s o n e - w a y A N O V A : H -~ 1.40, p ~ 0.05). F i g u r e 3 shows t h e results of t e s t i n g d u r i n g t h e i n t e r o p e r a t i v e p e r i o d for a n i m a l s in groups Ct-SS a n d i/2SSt-1/2SS. R a t s w i t h u n i l a t e r a l s o m a t i c c o r t e x lesions d i d n o t differ f r o m t h e s h a m - o p e r a t e d animMs in errors or d a y s t o criterion, or on error a n d d a y difference scores ( M a n n - W h i t n e y U tests, one-tail, all p 0.05). T h e i n t e r o p e r a t i v e p e r f o r m a n c e of i/2SSt-i/~SS a n i m a l s was c o m p a r e d to t h e p o s t o p e r a t i v e p e r f o r m a n c e of SS-C a n i m a l s since b o t h groups h a d a n e q u i v a l e n t a m o u n t of t r a i n i n g p r i o r t o this comparison. O n e - t a i l e d M a n n - W h i t n e y t e s t s on t h e v a r i o u s p e r f o r m a n c e scores showed t h a t b i l a t e r a l insult r e s u l t e d in significantly worse r e t e n t i o n t h a n d i d u n i l a t e r a l d a m a g e (all i0 ~ 0.05). H e n c e , a l t h o u g h t h e d a t a r e v e a l e d no significant i m p a i r m e n t s a f t e r u n i l a t e r a l ablations, t h e b i l a t e r a l lesions p r e c i p i t a t e d p r o n o u n c e d deficits. F i g u r e 4 shows t h e results of all t e s t i n g a f t e r t h e second surgery. A o n e - w a y a n a l y s i s of v a r i a n c e b y r a n k s r e v e a l e d a significant difference a m o n g t h e groups ( K r u s k a l - W a l l i s , H ~ 12.67, p ~ 0.02). O n e - t a i l e d M a n n - W h i t n e y U t e s t s showed t h a t t h e t w o groups of serial a n i m a l s d i d n o t differ f r o m each o t h e r ; t h a t t h e t w o groups of one-stage a n i m a l s d i d n o t differ f r o m each o t h e r ; a n d t h a t t h e p o o l e d

Serial Lesions and Tactile Retention

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Fig. 3. Performance of rats in groups Ct-SS and 1/2S8~-1/~$8after the first of two operations. Each column shows the interoperative error score of one subject. Group means are presented in brackets above columns serial a n i m a l s did n o t differ from the pooled one-stage a n i m a l s (p > 0.05 for each comparison). B o t h the combined serial group a n d the pooled one-stage group differed from the control group a t the 0.001 level. F u r t h e r , a significantly smaller p r o p o r t i o n of a n i m a l s s u s t a i n i n g bilateral somatic cortex lesions remastered the p r o b l e m w i t h i n the alloted time i n comparison to a n i m a l s with two sham operations (X2 = 4.72, d / = 1, p < 0.05).

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Fig. 4. Postoperative performance scores of rats following successive or simultaneous lesions of somatosensory cortex or two sham operation. Subjects in two of the lesion groups received training to criterion during the interoperativc period (Fig. 2). Each column shows the error score of one subject and a dot indicates that the problem was not mastered within the 60 day time limit for learning. Group means are presented in brackets above the columns Examination of preoperative and postoperative performance scores revealed that no C-C animals had negative day or error difference scores whereas the percentages of negative scores were 80, 29, 60 and 43% for groups Ct-SS, SS-C, 1/2SS-1/2SS and 1/2SSt-1/2SS , respectively. When two Kruskal-Wallis one-way analyses of variance were performed on these scores, significant differences between the groups were found (p < 0.05). Again, these differences reflected the fact that the sham-operated rats relearned the discrimination faster than did the animals with somatic cortex lesions (Mann-Whitney U tests, all p < 0.05). Examination of individual performance scores obtained by the 11 rats that failed to reach criterion following bilateral destruction of somatosensory cortex revealed that nine of the animals performed above chance on the 300 trials (Binomial tests, p ~ 0.05). However, none of these rats performed above chance when only the last five days of testing were examined (Binomial tests, p, ~ 0.05). These data suggest that discriminative performance was impaired but not entirely abolished in most animals that failed to reach criterion. No consistent differences in ~erms of lesions size and placement were found between the brains of animals that failed to remaster the problem and those that reached criterion and subsequently were sacrificed for comparison purposes. The brains of the 16 animals in the four lesion groups closely resembled those described in earlier publications (Finger et al., 1970b, 1971 a, b) and are presented in Fig. 5. While some sparing of tissue occurred in the second somatic area, most lesions were large and encompassed both paw and facial areas in the two somatosensory areas of the cortex (see Welker, 1971 ; Zubek, 1951b, for cortical maps). Although the lesions frequently extended to and involved the corpus callosum, no animals showed septal or hippocampal damage or direct insult to the thalamic nuclei. Motor cortex damage also appeared to be minimal. Retrograde degeneration was seen scattered throughout the ventrobasal thalamus and typically appeared heaviest in the dorsolateral parts of the complex.

Serial Lesions and Tactile Retention

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Fig. 5. Drawings showing the surface areas of the lesions of those rats in groups Ct-SS (Column 1), SS-C (Column 2), 1/2SS-1/2SS (Column 3) and 1/2SS~-1/2SS (Column 4) that were sacrificed in Experiment 1 (see text). The number under each brain signifies errors to criterion after the second operation. A line under this number indicates that the animal was unable to master the problem within the allotted time (see text)

Experiment 2 I n E x p e r i m e n t 1 it was f o u n d t h a t b i l a t e r a l d a m a g e to t h e s o m a t o s e n s o r y c o r t e x r e s u l t e d in severe deficits in t a c t i l e r e t e n t i o n even when t h e a b l a t i o n s were a c c o m p l i s h e d in t w o o p e r a t i o n s a n d when t r a i n i n g was p e r m i t t e d b e t w e e n surgeries. Some of these animals, however, d i d relearn t h e d i s c r i m i n a t i o n a n d t h i s is consistent w i t h m o s t r e p o r t s on t h e effects of these a b l a t i o n s on t h e r e t e n t i o n of t a c t i l e d i s c r i m i n a t i o n s b y r a t s (Finger et al., 1971 a; Weese et al., 1973; Zubek, 1951 a). U n i t s t h a t r e s p o n d t o t a c t i l e s t i m u l a t i o n o f t h e b o d y are k n o w n t o exist in neocortical areas o u t s i d e t h e s o m a t o s e n s o r y p r o j e c t i o n zones (e. g., B u s e r a n d I m b e r t , 1961), suggesting t h a t n o n - s o m a t o s e n s o r y c o r t e x m a y p l a y a role in learning or recovery. E x p e r i m e n t 2 was designed to i n v e s t i g a t e t h e effects of placing lesions in cortical areas a n t e r i o r a n d p o s t e r i o r t o t h e s o m a t o s e n s o r y p r o j e c t i o n zones in a n i m a l s t h a t d e m o n s t r a t e d learning in E x p e r i m e n t 1. I t was h y p o t h e s i z e d t h a t t h e s e lesions w o u l d h a v e l i t t l e effect on a n i m a l s w i t h s o m a t o s e n s o r y c o r t e x i n t a c t , b u t t h a t t h e y w o u l d m a r k e d l y affect those r a t s t h a t p r e v i o u s l y h a d e x p e r i e n c e d cortical e x t i r p a t i o n s .

Methods Subjects Nineteen of the 24 animals that had performed to criterion in Experiment 1 served as subjects in the second experiment. They included 8 animals from group C-C and 11 animals that had sustained successive or simultaneous bilateral removal of somatic cortex areas 1 and 2. Specifically, groups C~-SS, SS-C, 1/~SS-1/2SS and 1/2SS~-1/2SS contributed 3, 2, 4 and 2 animals, respectively.

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General Procedures Surgery was conducted 3--5 days after an animal had successfully completed postoperative testing in Experiment 1. Subjects that previously had experienced bilateral removal of somatic cortex areas 1 and 2 received bilateral cortical lesions both anterior and posterior to the somatosensory projection zones in a single operation. Animals in the sham operated condition (C-C) underwent the same neocortical surgery designed to leave only somatic cortex areas 1 and 2 intact. The rats then were tested for retention of the same ridge-smooth discrimination that was learned in the first experiment. This testing began two weeks after surgery. Animals in groups C-SS, SSt-C, 1/2SS-1/2SSand 1/2SS~-1/2SSwere sacrificed after relearning the problem or, alternatively, after 60 days of testing. Six animals in group C-C were subjected to bilateral removal of somatic cortex areas 1 and 2 after relearning the problem and 15 days later were retested to criterion or to the 60 day limit on the same discrimination. Thus, all five groups of animals had extensive portions of somatosensory, frontal and occipital cortex ablated by the end of this experiment. The surgical, beha,vioral and histological procedures used in Experiment 2 were identical to those employed in Experiment 1. An attempt was made to leave a ridge of bone above the sagital sinus and a ridge just anterior and posterior to the somatic cortex in each preparation. Only one animal (C-C) died while undergoing these surgeries. Two other rats, however, were discarded from this part of the experiment upon showing signs of infection (C-C, Ct.SS). The remaining animals, while showing some signs of spasticity, appeared strong and eagerly ran and ate in the maze.

Results T h e results of t h e second e x p e r i m e n t are s u m m a r i z e d in Fig. 6. A n i m a l s in groups Ct-SS, SS-C, 1/2SS-1/2SS a n d 1/2SSt-1/2SS t h a t p r e v i o u s l y h a d l e a r n e d t h e d i s c r i m i n a t i o n in t h e absence of s o m a t i c c o r t e x areas 1 a n d 2 were s e v e r e l y i m p a i r e d following a b l a t i o n of f r o n t a l a n d occipital c o r t e x a n d o n l y 4 0 % of t h e r a t s were a b l e t o r e l e a r n t h e h a b i t . E x a m i n a t i o n of i n d i v i d u a l scores r e v e a l e d t h a t t h e four r a t s t h a t were able to r e m a s t e r t h e d i s c r i m i n a t i o n were from t h e t w o serial lesion groups. N o n e of t h e r a t s from t h e original one-stage lesion groups r e a c h e d criterion. This difference b e t w e e n one-stage a n d t w o - s t a g e a n i m a l s was f o u n d t o be m a r g i n a l b u t n o t s t a t i s t i c a l l y significant (Fisher E x a c t P r o b a b i l i t y Test, p ~ 0.07] ; M a n n - W h i t n e y U Test, p ~ 0.057), in p a r t reflecting t h e small n u m b e r of s u b j e c t s involved. All 6 r a t s t h a t failed t o r e a c h criterion p e r f o r m e d a b o v e chance levels on t h e 300 t r i a l s (Binomial tests, p ~ 0.05) b u t n o t on t h e l a s t 25 trials of t e s t i n g (Binom i a l tests, p ~ 0.05). T h e p e r f o r m a n c e of t h e 10 a n i m a l s as a group was signific a n t l y worse t h a n t h a t of a n i m a l s in g r o u p C-C who now h a d e x p e r i e n c e d r e m o v a l of f r o n t a l a n d occipital c o r t e x ( M a n n - W h i t n e y test, p ~ 0.01). F i g u r e 6 also p r e s e n t s t h e e r r o r scores o b t a i n e d b y g r o u p C-C a n i m a l s as t h e y progressed t h r o u g h t h r e e e x p e r i m e n t a l conditions. All of these r a t s r e a d i l y rem a s t e r e d t h e p r o b l e m w i t h t h e c o r t e x i n t a c t ( E x p e r i m e n t 1). l%emoval of f r o n t a l a n d occipital c o r t e x h a d a negligible effect on p e r f o r m a n c e as d e t e r m i n e d b y a Sign t e s t (p ~ 0.05). F o l l o w i n g a b l a t i o n of s o m a t i c c o r t e x areas 1 a n d 2, 3 of t h e 5 r e m a i n i n g a n i m a l s were u n a b l e t o r e l e a r n t h e h a b i t w i t h i n t h e a l l o t t e d time. Sign t e s t s on t h e r e p e a t e d m e a s u r e s showed p o o r e r p e r f o r m a n c e here t h a n in t h e t w o p r e c e d i n g conditions (both p < 0.05). M a n n - W h i t n e y U t e s t s on errors a n d d a y s to criterion showed t h a t r a t s t h a t h a d s o m a t i c c o r t e x e x t i r p a t e d a f t e r a b l a t i o n of f r o n t a l a n d occipital c o r t e x p e r f o r m e d as p o o r l y as d i d r a t s in groups Ct-SS, SS-C, 1/~SS-1/2SS, a n d 1/~SSt1/2SS t h a t h a d occipital a n d f r o n t a l c o r t e x r e m o v e d a f t e r s o m a t i c c o r t e x lesions

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SHAM OPERATION

I

FRONTAL-OCCIPITAL SOMATOSENSORY CORTEX ~ CORTEX I GROUP C-C

FRONTAL-OCCIPI'TAL CORTEX AFTER , SOMATOSENSORYCORTEX OTHER GROUPS COMBINED

SURGICAL PROCEDURES Fig. 6. The diagrams on the left show the error scores of rats in group C-C following each of three surgical procedures. Upon reaching criterion after two sham operations these animals experienced destruction of cortex anterior and posterior to the somatosensory zones. They then were retrained to criterion. Next they were subjected to lesions of the somatosensory cortex and tested one more time. The diagram to the right shows the performance scores of 10 rats that relearned the tactile discrimination after large lesions of the somatosensory cortex in Experiment i and subsequently were tested after experiencing lesions anterior and posterior to the original destruction. A dot indicates that the problem was not mastered within the 60 day time limit for learning. Group means are presented in brackets above the columns

(p > 0.05). proportion a n i m a l s in frontal and performed.

F u r t h e r , these t w o divisions were a p p r o x i m a t e l y equal in t e r m s of t h e of a n i m a l t h a t failed to relearn t h e d i s c r i m i n a t i o n problem. Hence, all groups were i m p a i r e d after r e m o v a l of large p o r t i o n s of somatic, occipital cortex, regardless of t h e sequence in which t h e a b l a t i o n s were

D r a w i n g s of t h e surface lesions of animals t h a t experienced a n t e r i o r a n d p o s t e r i o r n e o c o r t e x a b l a t i o n s in a d d i t i o n t o , s o m a t i c cortex lesions are p r e s e n t e d in Fig. 7. All r a t s s u s t a i n e d extensive d a m a g e to n e o c o r t e x a b o v e t h e rhinal fissure. H o w e v e r , in m o s t animals islands of tissue were n o t e d i m m e d i a t e l y a n t e r i o r a n d p o s t e r i o r to t h e somatic cortex as well as j u s t a n t e r i o r to t h e cerebellum. I n a d d i t i o n , m o s t lesions of n o n - s o m a t o s e n s o r y c o r t e x failed to e x t e n d t o t h e r h i n a l fissure. The serial sections showed t h a t t h e r e was no d i r e c t d a m a g e to t h e h i p p o c a m p u s , s e p t u m or t h a l a m u s in a n y brain. H o w e v e r , as in E x p e r i m e n t 1, m a n y of t h e lesions d i d e x t e n d to a n d involve p o r t i o n s of t h e corpus callosum. There were no a p p a r e n t differences in t e r m s of lesion size or locus a m o n g those animals t h a t p e r f o r m e d s a t i s f a c t o r i l y a n d those t h a t d i d n o t . I n fact, t h e two r a t s (both SS-C) w i t h t h e smallest lesions were a m o n g those who failed to l e a r n t h e discrimination.

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Fig. 7. Diagrams showing the surface topography of the ablations of 15 rats that had lesions of frontal, occipital and somatic cortex. Animals in group C-C (Column 1) had frontal and occipital cortex damage prior to ablation of somatosensory cortex, while animals in groups Ct-SS, SS-C, 1/2SS-1/2SS and 1/2SSt-1/2SS (Columns 2, 3, 4 and 5, respectively) experienced frontal and occipital cortex lesions after ablations of somatosensory cortex. The reconstruction in the upper left-hand corner shows the brain of one C-C rat that was sacrificed for comparison purposes after only sustaining frontal and occipital cortex lesions

Discussion The poor performance of animals sustaining bilateral damage involving the somatosensory cortex demonstrates the importance of these cortical areas in ridge-smooth discrimination in the rat. Tactile retention deficits also have been observed in cats (Zubck, 1952b), dogs (Allen, 1947; Norrsell, 1967, 1971) and monkeys (Orback and Chow, 1959) following insult to the somatosensory cortex, although considerable recovery has been witnessed under some conditions (e.g., Schwartzman, 1972 ; Weese et al., 1973). Further, the observation t h a t extensive lesions sparing the somatosensory cortex did not result in deficits (unless somatosensory cortex was removed previously) parallels Zubek's (1952a) finding t h a t the somatosensory areas are sufficient b y themselves to maintain previously learned tactile discriminations (see also Sperry, 1959). The observation t h a t the serial animals were as impaired as their one-stage counterparts (Experiment 1) stands in marked contrast to the results of an earlier experiment conducted in this laboratory in which rats with two-stage cortical lesions acquired a series of five tactile discriminations as rapidly as did sham operated animals (Finger et al., 1971b). Differences in lesion size and locus cannot explain these divergent results since most ablations in the present study resembled those described previously. I n addition, the change in the paradigm (retention vs. acquisition) would not explain the differences inasmuch as better performance typically follows preoperative training (see Weese et al., 1973). I n contrast, the divergent results could be attributed to the different learning histories of the animals. I n the present investigation the rats were tested only on the

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fourth problem of the battery of five problems used in the earlier study. Serially operated and even normal control animals are known to have difficulty learning this problem if not first exposed to easier tactile discriminations (Walbran, 1974). Thus, if capacity differences among the lesion groups did exist in the present experiment, they may have been obscured by the testing procedure in association with the physical stimuli; i.e., limited previous training may have made this particular discrimination too difficult for the brain damaged animals. This conclusion would appear to be supported by the results of one part of a follow-up retention experiment involving an easier tactile discrimination (rough vs. smooth) than that used here (Simons, Finger and Baldinger, 1975). Animals with one-stage lesions performed worse than rats with two-stage lesions in the more recent study, although rats in both groups were able to relearn the discrimination within a reasonable period of time. Failure to find serial sparing under conditions in which specific formal training was imposed during the interlesion interval conflicts with some reports involving two-choice visual discriminations in rats with lesions of the posterior neocortex (Petrinovich and Carew, 1969 ; Thompson, 1960). The results of the present experiment suggest that such interpolated practice may not always enhance retention with successive unilateral lesions in the somatosensory system. The data, however, do parallel those of Glendenning (1972) who reported, among other things, that limited overtraining administered prior to simultaneous removal of cortical tissue may not protect a previously learned visual habit. The excellent retention by rats in group C-C following extensive damage restricted to non-somatosensory cortex argues strongly that the tactile retention deficits observed after somatic cortex lesions cannot be attributed to general cortical damage (vide, Semmes, 1973). In addition, the lesion effects do not appear to be applicable to all somesthetic submodalities since ablations similar to those described here do not impair acquisition or retention of temperature discriminations in rats (Downer and Zubek, 1954; Finger et al., 1970b). Nevertheless, since these stimuli demanded complex exploratory movements, the impairments could have been multiple in nature and it cannot be assumed that the scores demonstrated by the animals in the different experimental groups reflect the same underlying deficits (see Finger, 1974). Specifically, while it can be claimed that the animals were not able to use visual, auditory or olfactory cues in the maze, the possibility that animals in the different experimental groups were using different strategies (simultaneous vs. successive sampling of the discriminanda) and/or different mechanoreceptors (vibrissae vs. paws) in the experiment cannot be excluded. However, in this context it should be emphasized that most of the animals in each of the groups appeared to be relying heavily on their paws for making the discrimination and that consistent differences did not appear among the groups with regard to the lesions which almost always encompassed both paw and facial afferents in the two somatosensory areas. The poor performance of animMs in groups SS-C, Ct-SS, 1/2SS-1/2SS and i/2SSt-i/2SS after anterior and posterior neocortical damage implies that nonsomatosensory cortex may be involved in relearning the tactile habit following damage to the somatosensory areas. Spared fragments of functional tissue in the presence of otherwise complete somatic cortex lesions also may play a role in the

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r e l e a r n i n g process ( D i a m o n d et al., 1962; G a l a m b o s et al., 1967; Lashley, 1939). The suggestion ( E x p e r i m e n t 2) t h a t serial a n i m a l s m a y be b e t t e r able to l e a r n t h a n one-stage a n i m a l s following a d d i t i o n a l neocortical i n s u l t should be explored further. I f confirmed, t h e b e h a v i o r a l d a t a would raise the i n t e r e s t i n g theoretical possibility t h a t the s u b s t r a t e s u n d e r l y i n g recovery are n o t necessarily t h e same after one-stage a n d two-stage lesions.

References Allen, W. F. : Effects of partial and complete destruction of tactile cerebral cortex on correct conditioned differential foreleg responses from cutaneous stimulation. Amer. J. Physiol. 151, 325--337 (1947) Buser, P., Imbert, M. : Sensory projections to the motor cortex in cats: A microeleetrode study. In: Sensory Communication. (Ed. W.A. Rosenblith) pp. 607--626. Cambridge, Mass.: M.I.T. Press 1961 Diamond, I.T., Goldbcrg, J.M., Neff, W.D. : Tonal discrimination after ablation of auditory cortex. J. Neurophysiol. 25,223---235 (1962) Downer, J. de C., Zubek, J.P. : Role of the cerebral cortex in temperature discrimination in the rat. J. comp. physiol. Psychol. 47, 199--203 (1954) Finger, S.: Recovery after somatosensory forebrain damage. In: Plasticity and recovery of function in the central nervous system. (E d. D.G. Stein et al.), pp. 237--264. New York: Academic Press 1974 Finger, S., Cohen, M., Alongi, R.: Roles of somatosensory cortical areas 1 and 2 in tactile discrimination in the rat. Int. J. Psychobiol. 2, 93--102 (1972) Finger, S., Frommer, G.P. : Effects of somatosensory thalamic and cortical lesions on roughness discrimination in the albino rat. Physiol. Behav. 3, 83--89 (1968a) Finger, S., Frommer, G.P. : Effects of cortical lesions on tactile discriminations graded in difficulty. Life Sci. 7, 897--904 (1968b) Finger, S., Frommer, G.P., Carmon, A., Inbal, R. : Roughness discrimination with sandpaper surfaces: An olfactory confounding. Psyehon. Sci. 18, 165--166 (1970a) Finger, S., Lennard, P.R., Hammer, R., Ehrman, R.: Retention of tactile discriminations following somatosensory cortical lesions in the rat. Exp. Brain Res. 12, 354--360 (1971a) Finger, S., Marshak, R.A., Cohen, M., Seheff, S., Trace, R., Niemand, D. : Effects of successive and simultaneous lesions of somatosensory cortex on tactile discrimination in the rat. J. comp. physiol. Psyehol. 77, 221--227 (1971b) Finger, S., Scheff, S., Warshaw, I., Cohen, M.: Retention and acquisition of fine temperature discriminations following somatosensory cortical lesions in rat. Exp. Brain Res. 10, 340-346 (1970b) Galambos, R., Norton, T.T., Frommer, G.P.: Optic tract lesions sparing pattern vision in cats. Exp. Neurol. 18, 8--25 (1967) Glendenning, R.L. : Effects of training between two unilateral lesions of visual cortex upon ultimate retention of black-white discrimination habits by rats. J. comp. physiol. Psychol. 80, 216--229 (1972) Kircher, K.A., Braun, J.g., Meyer, D.R., Meyer, P.M.: Equivalence of simultaneous and successive neocorticM ablations in production of impairments of retention of black-white habits in rats. J. comp. physiol. Psychol. 71, 420--425 (1970) Lashley, K.S. : The mechanism of vision. XVI. The functioning of small remnants of the visual cortex. J. comp. Neurol. 70, 45--67 (1939) Meyer, D.R., Isaac, W., Maher, B. : The role of stimulation in spontaneous reorganization of visual habits. J. comp. physiol. Psychol. 51, 546--548 (1958) Norrsell, U. : A conditioned reflex study of sensory deficits caused by cortical somatosensory ablations. Physiol. Behav. 2, 73--81 (1967) Norrsell, U. : A comparison of function of the first and second somatesensory areas of the dog. Experientia (Basel) 27, 1284 (1971) Orbach, J., Chow, K.L. : Differential effects of resections of somatic areas I and I I in monkeys. J. Neurophysiol. 22, 195--203 (1959)

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Petrinovich, L., Carew, T . J . : Interaction of neoeortical lesion size and interoperative experience in retention of a learned brightness discrimination. J. comp. physiol. Psychol. 68, 451--454 (1969) Schwartzman, R . J . : Somesthetic recovery following primary somatosensory cortex ablations. Arch. Neurol. (Chic.) 27, 340--349 (1972) Semmes, J. : Somesthetic effects of damage to the central nervous system. In: Handbook of sensory physiology, Part I I : Somatosensory system. (Ed. A, Iggo), pp. 714--742. BerlinHeidelberg-New York: Springer 1973 Siegel, S. : Nonparametric statistics for the behavioral sciences. New York: McGraw-Hill 1956 Simons, D., Finger, S., Baldinger, A.: Enhanced retention of rough-smooth discrimination following overtraining or serial lesions of SS cortex in rats. Paper read at Annual Meetings of Society for l~euroscience, New York City, November 1975 Sperry, R.W. : Preservation of high-order function in isolated somatic cortex in callosumsectioned eat. J. Neurophysiol. 22, 78--87 (1959) Thompson, R. : Retention of a brightness discrimination following neocortical damage in the rat. J. comp. physiol. Psychol. 53, 212---215 (1960) Walbran, B. : Effects of simultaneous and successive ablations of somatosensory cortex on tactile discriminations in 30-, 270-, and 570-day old rats. Paper read at Annual Meetings of Midwestern Psychological Association, Chicago, May 1974 Weese, G.D., Neimand, D., Finger, S.: Cortical lesions and somesthesis in rats: Effects of training and overtraining prior to surgery. Exp. Brain Res. 16, 542--550 (1973) Welker, C. : Microelectrode delineation of fine grain somatotopic organization of Sml cerebral neocortex in albino rat. Brain Res. 2~, 259 275 (1971) Zubek, J . P . : Studies in somesthesis. I. Role of somatic cortex in roughness discrimination in the rat. J. comp. physiol. Psychol. 44, 339--353 (1951a) Zubek, J . P . : Recent electrophysiological studies of the cerebral cortex: Implications for localization of sensory function. Canad. J. Psychol. 5, 110--121 (1951b) Zubek, J . P . : Studies in somesthesis. III. Role of somatic areas 1 and 2 in roughness discrimination in the rat. Canad. J. Psychol. 6, 183--193 (1952a) Zubek, J . P . : Studies in somesthesis. IV. Role of somatic areas 1 and 2 in roughness discrimination in cat. J. Neurophysiol. 15, 401--408 (1952b) D. Simons Psychology Department Washington University St. Louis, Missouri 63130 USA

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