Brain Research, 88 (1975) 353-356
353
© Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
Recovery of pattern vision following serial lesions of striate cortex in rats
DENISE DRU, JUDITH BOAS WALKER AND JAMES PAUL WALKER Huntington Institute of Applied Medical Research, Pasadena, Calif. and Andrus Gerontology Center, University of Southern California, Los Angeles, Calif. (U.S.A.)
(Accepted January 27th, 1975)
When a structure represented bilaterally in the brain is lesioned in two separate operations, with a certain number of days intervening between surgeries, other areas of the brain seem to take over lost function 8,5,1~,15,~6,19. If the same structure is bilaterally lesioned in a single operation, the resulting deficits in behavior are more severe and sometimes permanent 4,s,13. For example, single-stage bilateral ablation of the visual cortex in mammals produces a severe deficit in preoperatively learned discriminations of light intensity 9,1°. This habit can be relearned postoperatively with prolonged retraining and practice. When identical ablations are performed in two separate operations with 14 days intervening between surgeries, the discrimination habit is spared 9,11. Recovery of visual function is presumed to depend on the takeover of function by remaining portions of the visual system. However, mediation of the light intensity discrimination is known to be related to several visual areas other than striate cortex ~7. In fact, the task can be acquired with or without an intact visual cortex 2,6,14. The present experiment is an attempt to determine whether the serial-lesion effect occurs for behavioral functions known to be dependent upon very specific regions of the visual system. The capacity to differentiate visual patterns has been reliably associated with function of the visual 'cortex. Ablation of this cortical region results in the abolition of pattern discriminationS,V, 17. Thus, the occurrence of recovery of pattern vision following sequential removal of visual cortex would suggest functional and perhaps physical reorganization of areas not primarily responsible for this visual capacity. Four groups of adult male Long-Evans rats were tested for ability to discriminate horizontal-vertical patterns, were given two-stage lesions of the striate cortex, and were retested for ability to discriminate visual patterns. During the 11 days between each two-stage surgery, the subjects remained in their home cages on a 12 h alternating dark-light cycle. Rats were tested in a modified ThompsonBryant box is. Before surgery, 5 days of pretraining were given whereby the rats were trained to run to a goal box to escape or avoid shock. On days 3, 4 and 5 two white translucent doors were gradually lowered over the goal box openings, and the rats were trained to push through the doors to enter the goal box.
354 The animals were then taught to discriminate between a vertical black-white striped door which led to the goal box and a horizontal black-white striped door which was always locked. The position of the correct door was varied randomly. U p o n the lifting of the start gate, the animal was required to run through the vertically striped door into the goal box within 10 sec to avoid or escape a constant current 1 mA shock of 2 msec duration, 3 times/sec. An incorrect response to the negative stimulus involved the animal entering the wrong alley by 2 or more inches. Preoperatively, animals were discarded if they failed to reach the criterion of 9 out of 10 correct discriminations within 10 days. Postoperatively, animals were run to an upper limit of 20 days to the same criterion. Recordings were made of the number of discrimination trials to criterion and the number of discrimination errors committed before learning the task. Surgery was performed under Nembutal anesthesia. Bone was removed from a region bounded by an area 2 m m in from the sagittal suture and the bregmoid suture and 1 m m in from the lambdoid suture. The temporal crest was left intact. Area 17 was aspirated with special care to leave subcortical tissue untouched. Lesions in group I were performed bilaterally in one operation; lesions in group II were performed in two stages with half the animals receiving left first-stage lesions and half receiving right first-stage lesions. Groups III and IV received one- and two-stage sham operations in which the scalp was incised and bone was removed overlying area 17. Eleven interoperative days intervened between the two-stage operations. At the end of the experiment all animals were sacrificed and upon histological examination, those animals with lesions involving greater than 15 ~ of the total neocortex, or involving extensive destruction beyond area 17, were discarded. O f the original 60 animals, 3 were discarded because of damage to subcortical structures and 8 were discarded because of respiratory infections. Mean cortical destruction in group I was 11.7 ~ ( ~ 2.8 ~ ) and in group II, 11.9 ~ ( ~ 2.5 ~). Minimal and maximal extent of damage are shown in Fig. I. One week following the one-stage bilateral or second-stage unilateral ablation, animals were tested for sparing of the pattern discrimination habit. Postoperative discrimination ability was compared t o preoperative ability by means of savings scores for both the number of trials and the number of discrimination errors committed in reaching criterion.
Fig. 1. Minimal and maximal extent of cortical damage in groups I and II.
355 TABLE 1 MEDIAN PREOPERATIVE LEARNING AND POSTOPERATIVE SAVINGS SCORES
Group
I. One-stage striate II. Two-stage striate IlL One-stage sham IV. Two-stage sham * Percent savings :
N
13 12 12 12
Preoperative learning
Postoperative savings (%) *
Trials to criterion
Errors to criterion
Trials
Errors
65 65 60 70
27 31 28 33
--207.7 - - 84.6 q- 41.7 q- 42.7
--179.3 - - 92.6 q- 75 q- 84
median preoperative performance - - median postoperative performance median preoperative performance
x
100.
Data for pre- and postoperative performance of all groups are summarized in Table I. A Kruskal-Wallis analysis of variance revealed no differences among groups in preoperative learning in terms of trials (H = 0.87, P > 0.05) or errors to criterion (H = 0.73, P > 0.05). A comparison of postoperative retention scores indicates that groups I I I and IV of sham operates were equivalent in retention and demonstrated sparing of the habit (Mann-Whitney U = 64, P > 0.05), i.e., postoperative performance was superior to preoperative performance. In contrast, both experimental groups (I and II) showed deficits in pattern vision postoperatively compared to shams. The experimental groups of subjects differed significantly from one another in postoperative performance on both trials (U = 5, P < 0.001) and errors (U -----3, P < 0.001) to criterion. Single-stage operates of group I demonstrated severe postoperative impairments in the capacity to differentiate visual patterns. All but 3 animals failed to relearn the task within the 20 day postoperative period. In contrast, all two-stage operates of group II relearned the task postoperatively while 5 animals demonstrated sparing. Thus, animals that received two-stage serial lesions of the visual cortex demonstrated recovery of pattern vision postoperatively. In addition, interoperative practice on the task was not necessary to recovery, although sparing of the task was not typical. These results extend the findings of earlier studies 9-1z of visual serial lesion effects to behavioral functions mediated more specifically within the visual cortex. Recovery of pattern vision following sequential removal of visual cortex is a consequence of functional and possibly physical reorganization of areas not primarily responsible for this visual capacity.
1 BAUER,J. H., AND HUGHES,K. R., Visual and nonvisual behaviors of the rat after neonatal and adult posterior neocortical lesions, Physiol. Behav., 5 (1970) 427-441. 2 BLAND, B. H., AND COOPER, R. M., Experience and vision of the posterior neodecorticate rat, Physiol. Behav,, 5 (1970) 211-214. 3 BUTTERS,N., PANDYA,D., STEIN,O., AND ROSEN,J., A search for the spatial engram within the frontal lobes of monkeys, Acta Neurobiol. exp. (Warszawa), 32 (1972) 305-330. 4 FINGER,S., MARSHAK,R. A., COHEN, M., SCHEFF,S., TRACE, R., AND NIEMAND,D., Effects of
356 successive and simultaneous lesions of somatosensory cortex on tactile discrimination in the rat,
J. comp. physiol. Psychol., 77 (197t) 221-227. 5 FLEMING,A., AND ROSENBLATT,J. S., Olfactory regulation of maternal behavior in rats. 11. Effects of peripherally-induced anosmia and lesions of the lateral olfactory tract in pup-induced virgins, J. comp. physiol. Psyehol., 86 (1974) 233-239. 6 HOREL, J. A., Effects of subcortical lesions on brightness discrimination acquired by rats without visual cortex, J. comp. physiol. Psychol., 65 (1968) 103-109. 7 HOREL, J. A., BETTINGER, L. A., ROYCE, J. G., AND MEYER, D. R., Role of neocortex in the learning and relearning of two visual habits by the rat, J. comp. physiol. Psyehol., 61 (1966) 66-78. 8 MCINTYRE, M., AND STEIN, D. G., Differential effects of one- vs. two-stage amygdaloid lesions on activity, exploratory, and avoidance behavior in the Albino rat, Behav. Biol., 9 (1973) 451~,65. 9 MEYER, D. R., ISAAC, W., AND MAHER, B., The role of stimulation in spontaneous reorganization of visual habits, J. comp. physiol. Psychol., 51 (1958) 546-548. 10 PETRINOVICH, L., AND BLISS, O., Retention of a brightness discrimination following ablations of the occipital cortex in the rat, J. comp. physiol. Psyehol., 61 (1966) 136-138. 11 PETRINOVICH, L., AND CAREW, T. J., Interaction of neocortical lesion size and interoperative experience in retention of a learned brightness discrimination, J. comp. physiol. Psychol, 68 (1969) 451454. 12 ROSEN, J., STEIN, D., AND BUTTERS, N., Recovery of function after serial ablation of prefrontal cortex in the Rhesus monkey, Science, 173 (1971) 353-356. 13 ROWE, F. A., AND SMITH, W. E., Simultaneous and successive olfactory bulb removal: influences on the mating behavior of male mice, Physiol. Behav., l0 (1973) 445-449. 14 SPEAR, P. D., AND BRAUN, J. J., Nonequivalence of normal and posteriorly neodecorticated rats on two brightness discrimination problems, J. comp. physiol. Psyehol., 67 (1969) 235-239. 15 STEIN, D., ROSEN, J., GRAZIADEI, J., MISHKIN, D., AND BRINK, J. J., Central nervous system: recovery of function, Science, 166 (1969) 528-530. 16 TANAKA, D., Sparing of an escape response following serial prefrontal decortication in the monkey, Brain Research, 65 (1974) 195-201. 17 THOMPSON, R., Localization of the 'visual memory system' in the white rat, Physiol. psychol. Monogr., 69 (1969) 1-29. 18 THOMPSON, R., AND BRYANT, J. H., Memory as affected by activity of a relevant receptor, Psychol. Rep., 1 (t955) 393-400. 19 TIEMAN, S. B., AND HAMILTON, C. R., Interocular transfer in split brain monkeys following serial disconnection, Brain Research, 63 (1973) 368-373.
353
© Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
Recovery of pattern vision following serial lesions of striate cortex in rats
DENISE DRU, JUDITH BOAS WALKER AND JAMES PAUL WALKER Huntington Institute of Applied Medical Research, Pasadena, Calif. and Andrus Gerontology Center, University of Southern California, Los Angeles, Calif. (U.S.A.)
(Accepted January 27th, 1975)
When a structure represented bilaterally in the brain is lesioned in two separate operations, with a certain number of days intervening between surgeries, other areas of the brain seem to take over lost function 8,5,1~,15,~6,19. If the same structure is bilaterally lesioned in a single operation, the resulting deficits in behavior are more severe and sometimes permanent 4,s,13. For example, single-stage bilateral ablation of the visual cortex in mammals produces a severe deficit in preoperatively learned discriminations of light intensity 9,1°. This habit can be relearned postoperatively with prolonged retraining and practice. When identical ablations are performed in two separate operations with 14 days intervening between surgeries, the discrimination habit is spared 9,11. Recovery of visual function is presumed to depend on the takeover of function by remaining portions of the visual system. However, mediation of the light intensity discrimination is known to be related to several visual areas other than striate cortex ~7. In fact, the task can be acquired with or without an intact visual cortex 2,6,14. The present experiment is an attempt to determine whether the serial-lesion effect occurs for behavioral functions known to be dependent upon very specific regions of the visual system. The capacity to differentiate visual patterns has been reliably associated with function of the visual 'cortex. Ablation of this cortical region results in the abolition of pattern discriminationS,V, 17. Thus, the occurrence of recovery of pattern vision following sequential removal of visual cortex would suggest functional and perhaps physical reorganization of areas not primarily responsible for this visual capacity. Four groups of adult male Long-Evans rats were tested for ability to discriminate horizontal-vertical patterns, were given two-stage lesions of the striate cortex, and were retested for ability to discriminate visual patterns. During the 11 days between each two-stage surgery, the subjects remained in their home cages on a 12 h alternating dark-light cycle. Rats were tested in a modified ThompsonBryant box is. Before surgery, 5 days of pretraining were given whereby the rats were trained to run to a goal box to escape or avoid shock. On days 3, 4 and 5 two white translucent doors were gradually lowered over the goal box openings, and the rats were trained to push through the doors to enter the goal box.
354 The animals were then taught to discriminate between a vertical black-white striped door which led to the goal box and a horizontal black-white striped door which was always locked. The position of the correct door was varied randomly. U p o n the lifting of the start gate, the animal was required to run through the vertically striped door into the goal box within 10 sec to avoid or escape a constant current 1 mA shock of 2 msec duration, 3 times/sec. An incorrect response to the negative stimulus involved the animal entering the wrong alley by 2 or more inches. Preoperatively, animals were discarded if they failed to reach the criterion of 9 out of 10 correct discriminations within 10 days. Postoperatively, animals were run to an upper limit of 20 days to the same criterion. Recordings were made of the number of discrimination trials to criterion and the number of discrimination errors committed before learning the task. Surgery was performed under Nembutal anesthesia. Bone was removed from a region bounded by an area 2 m m in from the sagittal suture and the bregmoid suture and 1 m m in from the lambdoid suture. The temporal crest was left intact. Area 17 was aspirated with special care to leave subcortical tissue untouched. Lesions in group I were performed bilaterally in one operation; lesions in group II were performed in two stages with half the animals receiving left first-stage lesions and half receiving right first-stage lesions. Groups III and IV received one- and two-stage sham operations in which the scalp was incised and bone was removed overlying area 17. Eleven interoperative days intervened between the two-stage operations. At the end of the experiment all animals were sacrificed and upon histological examination, those animals with lesions involving greater than 15 ~ of the total neocortex, or involving extensive destruction beyond area 17, were discarded. O f the original 60 animals, 3 were discarded because of damage to subcortical structures and 8 were discarded because of respiratory infections. Mean cortical destruction in group I was 11.7 ~ ( ~ 2.8 ~ ) and in group II, 11.9 ~ ( ~ 2.5 ~). Minimal and maximal extent of damage are shown in Fig. I. One week following the one-stage bilateral or second-stage unilateral ablation, animals were tested for sparing of the pattern discrimination habit. Postoperative discrimination ability was compared t o preoperative ability by means of savings scores for both the number of trials and the number of discrimination errors committed in reaching criterion.
Fig. 1. Minimal and maximal extent of cortical damage in groups I and II.
355 TABLE 1 MEDIAN PREOPERATIVE LEARNING AND POSTOPERATIVE SAVINGS SCORES
Group
I. One-stage striate II. Two-stage striate IlL One-stage sham IV. Two-stage sham * Percent savings :
N
13 12 12 12
Preoperative learning
Postoperative savings (%) *
Trials to criterion
Errors to criterion
Trials
Errors
65 65 60 70
27 31 28 33
--207.7 - - 84.6 q- 41.7 q- 42.7
--179.3 - - 92.6 q- 75 q- 84
median preoperative performance - - median postoperative performance median preoperative performance
x
100.
Data for pre- and postoperative performance of all groups are summarized in Table I. A Kruskal-Wallis analysis of variance revealed no differences among groups in preoperative learning in terms of trials (H = 0.87, P > 0.05) or errors to criterion (H = 0.73, P > 0.05). A comparison of postoperative retention scores indicates that groups I I I and IV of sham operates were equivalent in retention and demonstrated sparing of the habit (Mann-Whitney U = 64, P > 0.05), i.e., postoperative performance was superior to preoperative performance. In contrast, both experimental groups (I and II) showed deficits in pattern vision postoperatively compared to shams. The experimental groups of subjects differed significantly from one another in postoperative performance on both trials (U = 5, P < 0.001) and errors (U -----3, P < 0.001) to criterion. Single-stage operates of group I demonstrated severe postoperative impairments in the capacity to differentiate visual patterns. All but 3 animals failed to relearn the task within the 20 day postoperative period. In contrast, all two-stage operates of group II relearned the task postoperatively while 5 animals demonstrated sparing. Thus, animals that received two-stage serial lesions of the visual cortex demonstrated recovery of pattern vision postoperatively. In addition, interoperative practice on the task was not necessary to recovery, although sparing of the task was not typical. These results extend the findings of earlier studies 9-1z of visual serial lesion effects to behavioral functions mediated more specifically within the visual cortex. Recovery of pattern vision following sequential removal of visual cortex is a consequence of functional and possibly physical reorganization of areas not primarily responsible for this visual capacity.
1 BAUER,J. H., AND HUGHES,K. R., Visual and nonvisual behaviors of the rat after neonatal and adult posterior neocortical lesions, Physiol. Behav., 5 (1970) 427-441. 2 BLAND, B. H., AND COOPER, R. M., Experience and vision of the posterior neodecorticate rat, Physiol. Behav,, 5 (1970) 211-214. 3 BUTTERS,N., PANDYA,D., STEIN,O., AND ROSEN,J., A search for the spatial engram within the frontal lobes of monkeys, Acta Neurobiol. exp. (Warszawa), 32 (1972) 305-330. 4 FINGER,S., MARSHAK,R. A., COHEN, M., SCHEFF,S., TRACE, R., AND NIEMAND,D., Effects of
356 successive and simultaneous lesions of somatosensory cortex on tactile discrimination in the rat,
J. comp. physiol. Psychol., 77 (197t) 221-227. 5 FLEMING,A., AND ROSENBLATT,J. S., Olfactory regulation of maternal behavior in rats. 11. Effects of peripherally-induced anosmia and lesions of the lateral olfactory tract in pup-induced virgins, J. comp. physiol. Psyehol., 86 (1974) 233-239. 6 HOREL, J. A., Effects of subcortical lesions on brightness discrimination acquired by rats without visual cortex, J. comp. physiol. Psychol., 65 (1968) 103-109. 7 HOREL, J. A., BETTINGER, L. A., ROYCE, J. G., AND MEYER, D. R., Role of neocortex in the learning and relearning of two visual habits by the rat, J. comp. physiol. Psyehol., 61 (1966) 66-78. 8 MCINTYRE, M., AND STEIN, D. G., Differential effects of one- vs. two-stage amygdaloid lesions on activity, exploratory, and avoidance behavior in the Albino rat, Behav. Biol., 9 (1973) 451~,65. 9 MEYER, D. R., ISAAC, W., AND MAHER, B., The role of stimulation in spontaneous reorganization of visual habits, J. comp. physiol. Psychol., 51 (1958) 546-548. 10 PETRINOVICH, L., AND BLISS, O., Retention of a brightness discrimination following ablations of the occipital cortex in the rat, J. comp. physiol. Psyehol., 61 (1966) 136-138. 11 PETRINOVICH, L., AND CAREW, T. J., Interaction of neocortical lesion size and interoperative experience in retention of a learned brightness discrimination, J. comp. physiol. Psychol, 68 (1969) 451454. 12 ROSEN, J., STEIN, D., AND BUTTERS, N., Recovery of function after serial ablation of prefrontal cortex in the Rhesus monkey, Science, 173 (1971) 353-356. 13 ROWE, F. A., AND SMITH, W. E., Simultaneous and successive olfactory bulb removal: influences on the mating behavior of male mice, Physiol. Behav., l0 (1973) 445-449. 14 SPEAR, P. D., AND BRAUN, J. J., Nonequivalence of normal and posteriorly neodecorticated rats on two brightness discrimination problems, J. comp. physiol. Psyehol., 67 (1969) 235-239. 15 STEIN, D., ROSEN, J., GRAZIADEI, J., MISHKIN, D., AND BRINK, J. J., Central nervous system: recovery of function, Science, 166 (1969) 528-530. 16 TANAKA, D., Sparing of an escape response following serial prefrontal decortication in the monkey, Brain Research, 65 (1974) 195-201. 17 THOMPSON, R., Localization of the 'visual memory system' in the white rat, Physiol. psychol. Monogr., 69 (1969) 1-29. 18 THOMPSON, R., AND BRYANT, J. H., Memory as affected by activity of a relevant receptor, Psychol. Rep., 1 (t955) 393-400. 19 TIEMAN, S. B., AND HAMILTON, C. R., Interocular transfer in split brain monkeys following serial disconnection, Brain Research, 63 (1973) 368-373.
