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Enhancement of discrimination learning following unilateral lesions of posterior neocortex in guinea pigs
Physiology & Behavior, Vol. 19, pp. 513-517. Pergamon Press and Brain Research Publ., 1977. Printed in the U.S.A.
Enhancement of Discrimination Learning Following Unilateral Lesions of Posterior Neocortex in Guinea Pigs I D A N I E L M. LEVINSON, 2 DONALD W. R I F F L E , DENNIS L. REEVES AND CHARLES L. SHERIDAN
Department o f Psychology, University o f Missouri - Kansas Oty, Kansas City, MO 64110 (Received 11 April 1977)
LEVINSON, D. M., D. W. RIFFLE, D. L. REEVES AND C. L. SHERIDAN. Enhancement of discrimination learning following unilateral lesions of posterior neocortex in guinea pigs. PHYSIOL. BEHAV. 19(4) 513-517, 1977. - Monocular acquisition and interocular transfer of a horizontal-vertical discrimination were measured in 16 male albino guinea pigs which were restricted to ufing either the contralateral or ipsilateral primary visual fibers; restriction was accomplished by introduction of a unilateral striate lesion coupled with monocular occlusion. Eight sham-operated animals served as controls. The animals restricted to use of the eontralateral fibers showed reliably enhanced rates of acquisition as compared to the controls, while the animals restricted to the ipsilateral fibers were unable to master the discrimination. The control animals learned readily, but demonstrated fairly low levels of interocular transfer. The data suggest that there is some form of interbemispheric interference which is eliminated by the introduction of unilateral ablations of the posterior neocortex. Enhancement
Discrimination learning
Unilateral striate lesions
Guinea pigs
light-dark task, enhancement was not observed. Thus the generality of the phenomenon appeared to be somewhat limited. We felt that further assessment of the generality of the enhancement phenomenon should include not only different types of problems, but also other species. Since the original studies were performed with albino rats, we sought a species that like the rat, possesses a meager number of nondecussated visual fibers. Although it was reported [9] that 25% of the visual fibers do not cross in the guinea pig, a value closer to 1% was also reported [18]. Recent research clearly supports the estimate of 1%. In an electrophysiological study of the visually evoked response (VER) of intact guinea pigs [3], impoverished ipsilateral VERs were found, indicating a functionally weak ipsilateral system of fibers. Subsequently, both electrophysiological and anatomical studies of ocularly pigmented and albino guinea pigs were performed [4]. They indicated that the pigmented animal possesses only a small percentage ( 1 - 2 % ) of ipsilateral fibers and that the albino's ipsilateral component is even smaller and lacking in organization. In the wake of these findings we performed a study to assess further the generality of the enhancement phenomenon
DATA from several studies [2, 5, 6, 14] have indicated that unilateral lesions of the striate cortex in albino rats result in enhanced rates of acquisition of a pattern discrimination. To assess the function of crossed and uncrossed primary visual fibers of albino rats, the animals were restricted to the use of one or the other of these fiber systems by introducing a unilateral striate lesion and then covering one eye with a contact occluder [5]. The ipsilateral fiber system was found to be capable of mediating some retention, but not original acquisition, of a pattern task. Surprisingly, however, the animals that were restricted to using the contralateral fibers learned faster than did the sham-operated controls, and almost reliably so (p<0.07). Several studies [2,14] were performed subsequently to assess both the reliability and generality of the enhancement. In the first [2], which replicated and extended the earlier study, the enhancement phenomenon was confirmed and was reliable (p<0.05). In another experiment [14], reliably enhanced rates of acquisition by rats of a pattern discrimination, but not of a light-dark discrimination, were observed. Further, the enhancement only occurred when the pattern task was learned originally. If training on the pattern discrimination occurred after training on the
1Much gratitude is expressed to Don R. Justesen, Kansas City Veterans Administration Hospital, for his counsel and criticism in preparing the manuscript. 2 Requests for reprints should be sent to Daniel M. Levinson, Department of Psychology, CB Annex, University of Missouri - Kansas City, Kansas City, MO 64110. 513
514
LEVINSON, R I F E L t , REEVES ANI) S H [ R I i ) ' \ N
using guinea pigs; secondarily, our aim was to measure the functional competence of the uncrossed fiber system in the albino animal.
V
METHOD
Animals
( )
Twenty-four male albino guinea pigs of the Hartley strain were used. Obtained from Camm Research Institute, in Wayne, NJ, they were 6 0 - 9 0 days old at the onset of the study.
Apparatus The animals were trained in an apparatus modified from an earlier one [23] ; the dimensions are virtually the same as those described more recently [ 12]. The apparatus consisted of a startbox, runway, choice-point (that faced two cue-doors), and a goalbox. The discriminanda were horizontal or vertical stripes that were painted on either of the cue doors. Performance was motivated by electrical shock to the feet (250 mW, power stabilized 60 Hz current). Reversible monocular occlusion was achieved by one of several black acrylic contact occluders [ 1 5 ] ; an occluder was placed upon an animal's eye only after being thoroughly moistened with Barnes and Hind wetting solution.
B'-.J
A
I I
! I
Procedure Unilateral lesions of the striate cortex were made in 16 animals while 8 served as sham-operated controls. Each animal was anesthetized with chloral hydrate (250 mg/Kg). Striate ablations were accomplished by subpial aspiration after removal of a bone flap; sham operations were identical except for an aspiration of cortex. Laterality of ablation was determined randomly, with the constraint that half the operations be performed on the right side and half on the left. The animals had a period of postsurgical recovery of 1 2 - 1 4 days. At commencement of training, ten animals with lesions were restricted to use of contralateral visual fibers; and the other six, to the ipsilateral fibers. Restriction was accomplished by covering one eye with a contact occluder. The unequal ns reflected our emphasis on testing the generality of the enhancement phenomenon. The various experimental conditions are schematically illustrated in Fig. 1. Condition A represents animals restricted to contralateral fibers (contras), while condition B represents animals restricted to the ipsilateral system (ipsis). Condition C represents the sham-operated animals. During training, a guinea pig was placed in the start area of the apparatus, and the guillotine door was elevated. If an animal did not leave the start area within 10 sec or the runway within 20 sec, the shock grid in the respective area was electrified. The incorrect cue door was locked and the grid in front of it was electrified; any contact by an animal with that grid was scored as an error. Detection of contact was facilitated by neon lamps connected to the entryway grids, which changed in illumination when shock current was made available to the grids, and when contact was made with them. The left-right position of the correct cue door was varied across trials in a quasi-random sequence [7]. The animals were trained 25 trials per day until they had either reached a criterion of 18 correct responses in 20 consecutive trials or reached a cutoff point of 250 trials. At this point, the occluder was shifted to the opposite eye, and
C FIG. 1. Schematic illustration of the experimental conditions~ A: an animal restricted to the contralateral fibers (CONTRA); B: an animal restricted to the ipsilateral fibers (IPSI); C: a sham-operated animal (CONTROL). reacquisition of the task was attempted by 6 controls, 6 contras, and all 6 ipsis. Not all of the animals were restrained, since the effects measured in this portion of the study were so pronounced as to require the testing of fewer animals. The animals were again trained either to criterion or to the 250-trial cutoff. At conclusion of the study, several animals were observed during 20 test trials with both eyes covered as a test for effectiveness of the occluders. Finally, histological analyses were performed to determine the extent of the lesions. RESULTS
Mean and median trials to criterion are presented in Table 1 ; mean trials are presented histographicaUy in Fig. 2. The lesioned animals restricted to using the crossed fiber system (the contras) quickly mastered the task (~ = 70.90) and required fewer trials than did the sham-operated controls (~ = 101.00); the enhancement is highly reliable, t(16) = 3.37, p<0.01. No animals with visual input restricted to the uncrossed fibers (the ipsis) demonstrated original learning, but when shifted to the crossed fibers
ENHANCEMENT IN GUINEA PIGS
515
TABLE 1 MEAN AND MEDIAN TRIALS TO CRITERION FOR ACQUISITION AND REACQUISITION Sham-Operates £ Mdn n
"
0 "7.
101.00 97 8
55.67 50 6
Contra-Ipsi 70.90 65 lO
237.17 250 6
Ipsi-Contra 250 250 6
88.67 77.5 6
250200-
o
150100 50'
learning was demonstrated (£ = 88.67), although not reliably faster than that of the sham-operated controls, t(12) = 0.99. The 6 contras that were retrained following shift of the occluder showed little or no retention when shifted to use of the ipsilateral system; only 2 of them reacquired the task within 250 trials (£ = 237.17). The two animals that relearned the discrimination required 206 and 217 trials, and their lesions were somewhat smaller than average. The 6 controls after the shift of occlusion showed intermediate levels (42.17%) of interocular transfer. In the test for effectiveness of binocular occlusion, the performance of the animals fell to chance (~ 50%) levels. Histological analyses revealed that there was some variability in size of lesion. Figure 3 consists of photographs of whole brains showing maximal and minimal extent of lesions. Animal No. 7 has a left striate lesion, while animal No. 17 has a right lesion; animal No. 14 is a sham-operate. Generally, however, lesion sizes were fairly uniform. The brains were embedded in combined celloidin and paraffin, and sections from 1 0 - 2 0 ~ in thickness were made, with several sections taken from the lateral geniculate nuclei. All sections were stained with cresyl violet. Figures 4 and 5 represent photomicrographs of cells in the lateral geniculate nuclei from a control and lesioned hemisphere, respectively. A comparison of these two figures reveals that damage to the striate area resulted in some degeneration of cells in the LGN. DISCUSSION
CONTROLS
C ONTRA
(S HAMS)
~
I PSI
I P S I ,,-4. C ONTRA
FIG. 2. Mean trials to criterion. Black bars represent original acquisition; white bars represent retraining on the opposite eye.
The data obtained with rats [2, 5, 6, 13] have repeatedly indicated that unilateral striate removals can enhance the learning of pattern discriminations when mediated by the eye that remains truly functional, namely the eye contralateral to the intact hemisphere. Our study demonstrates that the phenomenon is at least somewhat
FIG. 3. Dorsal views of brains showing range of lesion sizes: No. 7 - left striate lesion; No. 17 - fight striate lesion; No. 14 - sham-operate.
I t
516
LEVINSON, RIFFL[-,. REEVES AND SIIERII)AN
FIG. 4. Photomicrograph of lateral geniculate nucleus from a control hemisphere.
FIG. 5. Photomicrograph showing degeneration in the lateral geniculate nucleus from a lesioned hemisphere.
general across mammalian species. Related phenomena have been reported in other species, and for at least one modality other than the visual; e.g., unilateral tectal lesions augmented the learning of visual discriminations in pigeons [ 1 ], and a reciprocally interfering relationship was reported to hold between the two superior colliculi in cats under some circumstances [22]. In addition, unilateral lesions of the visual and somesthetic cortex of rats were found to result in a significant increase in cholinesterase activity in the contralateral cortex [10]. Though we cannot say whether these superficially similar phenomena have similar functional bases, the accumulated evidence indicates that there is some highly general form of across-the-midline interference. The level of interocular transfer that was observed in the sham-operated animals was much lower than that reported for intact ocularly pigmented guinea pigs, and even somewhat lower than that obtained in split-brain pigmented animals [12]. A partial explanation of the low level of transfer appears to stem from the very small, poorly organized component of ipsilateral visual fibers in the albino animal. Our data on the guinea pig compare favorably with those of intact albino and pigmented (hooded) rats [20]. Nonetheless, even though the present data are consistent with those obtained using rats, the level of transfer is remarkably low, especially in light of the size of the corpus caUosum in guinea pigs as well as the high levels of transfer observed in shock-motivated split-brain
cats [19]. Our data also agree with anatomical and electrophysiological data [4] and further confirm that the ipsilateral fiber system in the albino guinea pig is functionally incapable of mediating acquisition or retention of a horizontal-vertical discrimination. The enhanced rate of acquisition by the unilaterally visually decorticated guinea pig was more pronounced than that reported in any of the earlier studies of rats. An explanation for the differences between the two species may stem from split-brain studies, wherein the effects of section of the corpus callosum on interocular transfer were measured. In one of these [201, it was found that split-brain albino rats showed an 18% loss in transfer of a pattern discrimination as compared to control animals; in another [ 13], it was reported that split-brain hooded rats showed a 16% loss as compared to controls. However, still another study [12] revealed that section of the corpus callosum of the guinea pig results in a 38% loss in transfer of a pattern habit, twice as great as that observed in rats. It appears that in the guinea pig more information transfers from one hemisphere to the other. If it is assumed that some of the interhemispherically transferring information is of an interfering nature, then one could conclude that there is more interhemispheric interference in the guinea pig than in the rat. Therefore, removal of interference by introduction of a unilateral striate lesion would result in more pronounced enhancement in the guinea pig. Support for this hypothesis stems from the above-mentioned study on
E N H A N C E M E N T IN G U I N E A PIGS
517
g u i n e a pigs [ 1 2 ] , in w h i c h split-brain a n i m a l s s h o w e d enhanced rates of acquisition of both pattern and shape tasks as c o m p a r e d t o s h a m - o p e r a t e d c o n t r o l s . A l t h o u g h n o t statistically reliable, these d a t a suggest t h a t s e c t i o n o f t h e c o r p u s c a l l o s u m results in a loss o f i n t e r - h e m i s p h e r i c
i n t e r f e r e n c e t h a t is similar to t h a t w h i c h results f r o m a u n i l a t e r a l striate lesion. T h e e n h a n c e m e n t p h e n o m e n o n was n o t o b s e r v e d in e i t h e r a l b i n o or h o o d e d split-brain rats [13,20].
REFERENCES 1. Bingelli, R. L., R. D. Tschirgi and B. M. Wenzel. Effects of unilateral hemispheric and optic tectal ablations on visual discrimination learning in pigeons. Physiologist 6 : 1 4 0 (Abstract), 1963. 2. Boles, T. J. and C. L. Sheridan. Enhanced pattern discrimination learning following unilateral damage to posterior cortex in rats. Psychon. Sci. 16: 2 7 3 - 2 7 4 , 1969. 3. Creel, D. J., R. E. Dustman and E. C. Beck. Visually evoked response in guinea pigs: Strains compared. J. comp. physiol. Psychol. 73: 4 9 0 - 4 9 3 , 1970. 4. Creel, D. J. and R. A. Giolli. Retino-geniculostriate projections in guinea pigs: Albino and pigmented strains compared. Expl Neurol. 36: 4 1 1 - 4 2 5 , 1972. 5. Creel, D. J. and C. L. Sheridan. Monocular acquisition and interocular transfer in albino rats with unilateral striate ablations. Psychon. Sci. 6: 8 9 - 9 0 , 1966. 6. Dunsmore, N., D. J. Creel and C. L. Sheridan. Enhanced discrimination learning in hemidecorticated rats. Paper read at the annual meeting of the Midwestern Psychological Association, 1965. 7. Fellows, B. J. Chance discrimination sequences for discrimination tasks. Psychol. Bull. 67: 8 7 - 9 2 , 1967. 8. Geschwind, N. Disconnexion syndromes in animals and man: I. Brain 88: 2 3 7 - 2 9 4 , 1965. 9. Hess, A. Optic centers and pathways after eye removal in fetal guinea pigs. J. comp. Neurol. 109: 9 1 - 1 1 5 , 1958. 10. Krech, D., M. R. Rosenzweig and E. L. Bennett. Interhemispheric effects of cortical lesions on brain biochemistry. Science 132: 352-353, 1960. 11. Krech, D. M., R. Rosenzweig, E. L. Bennet and B. Krueckel. Enzyme concentrations in the brain and adjustive behavior patterns. Science 120: 9 9 4 - 9 9 6 , 1954.
12. Levinson, D. M. Interocular transfer in guinea pigs following section of the corpus callosum. J. comp. physiol. Psychol. 78: 2 6 - 3 1 , 1972. 13. Levinson, D. M. and C. L. Sheridan. Monocular acquisition and interocular transfer of two types of pattern discriminations in hooded rats. J. comp. physiol. Psychol. 67: 4 6 8 - 4 7 2 , 1969. 14. Levinson, D. M., T. J. Hottman and C. L. Sheridan. Assessment of the generality of enhanced learning following lesions of posterior neocortex in rats. Psychon. Sci. 22: 1 - 3 , 1971. 15. Levinson, D. M., C. L. Sheridan, T. J. Hottman, D. R. Justesen, D. J. Creel and R. E. Sanders. A Monograph on the assessment of the contact eye-cover as an effective method of restricting visual input. Behav. Res. Meth_ Inst., in press, 1977. 16. Miller, G. The magical number seven, plus or minus two. PsychoL Rev. 63: 8 1 - 9 7 , 1956. 17. Nauta, W. J. H. and V. M. Bucher. Efferent connection of the striate cortex in the albino rat. J. comp. Neurol. 100: 2 5 7 - 2 5 8 , 1954. 18. Polyak, S. The Vertebrate Visual System. Chicago: University of Chicago Press, 1957. 19. Sechzer, J. A. Successful interocular transfer of pattern discrimination in "split-brain" cats with shock avoidance motivation. J. comp. physiol. Psychol. 58: 7 6 - 8 3 , 1964. 20. Sheridan, C. L. Interocular transfer of brightness and pattern discriminations in normal and corpus caUosum-sectioned rats. J. comp. physiol. Psychol. 59: 292-294, 1965. 21. Sheridan, C. L. Interocular interaction of conflicting discrimination habits in the albino rat: A preliminary report. Psychon. Sci. 3: 303-304, 1965. 22. Sprague, J. W. Interaction of cortex and superior colliculus in mediation of visually guided behavior in the cat. Science 153: 1544-1547, 1966. 23. Thompson, R. and H. Bryant. Memory as affected by activity of the relevant receptor. Psychol. Rep. 1: 393-400, 1955.
Enhancement of Discrimination Learning Following Unilateral Lesions of Posterior Neocortex in Guinea Pigs I D A N I E L M. LEVINSON, 2 DONALD W. R I F F L E , DENNIS L. REEVES AND CHARLES L. SHERIDAN
Department o f Psychology, University o f Missouri - Kansas Oty, Kansas City, MO 64110 (Received 11 April 1977)
LEVINSON, D. M., D. W. RIFFLE, D. L. REEVES AND C. L. SHERIDAN. Enhancement of discrimination learning following unilateral lesions of posterior neocortex in guinea pigs. PHYSIOL. BEHAV. 19(4) 513-517, 1977. - Monocular acquisition and interocular transfer of a horizontal-vertical discrimination were measured in 16 male albino guinea pigs which were restricted to ufing either the contralateral or ipsilateral primary visual fibers; restriction was accomplished by introduction of a unilateral striate lesion coupled with monocular occlusion. Eight sham-operated animals served as controls. The animals restricted to use of the eontralateral fibers showed reliably enhanced rates of acquisition as compared to the controls, while the animals restricted to the ipsilateral fibers were unable to master the discrimination. The control animals learned readily, but demonstrated fairly low levels of interocular transfer. The data suggest that there is some form of interbemispheric interference which is eliminated by the introduction of unilateral ablations of the posterior neocortex. Enhancement
Discrimination learning
Unilateral striate lesions
Guinea pigs
light-dark task, enhancement was not observed. Thus the generality of the phenomenon appeared to be somewhat limited. We felt that further assessment of the generality of the enhancement phenomenon should include not only different types of problems, but also other species. Since the original studies were performed with albino rats, we sought a species that like the rat, possesses a meager number of nondecussated visual fibers. Although it was reported [9] that 25% of the visual fibers do not cross in the guinea pig, a value closer to 1% was also reported [18]. Recent research clearly supports the estimate of 1%. In an electrophysiological study of the visually evoked response (VER) of intact guinea pigs [3], impoverished ipsilateral VERs were found, indicating a functionally weak ipsilateral system of fibers. Subsequently, both electrophysiological and anatomical studies of ocularly pigmented and albino guinea pigs were performed [4]. They indicated that the pigmented animal possesses only a small percentage ( 1 - 2 % ) of ipsilateral fibers and that the albino's ipsilateral component is even smaller and lacking in organization. In the wake of these findings we performed a study to assess further the generality of the enhancement phenomenon
DATA from several studies [2, 5, 6, 14] have indicated that unilateral lesions of the striate cortex in albino rats result in enhanced rates of acquisition of a pattern discrimination. To assess the function of crossed and uncrossed primary visual fibers of albino rats, the animals were restricted to the use of one or the other of these fiber systems by introducing a unilateral striate lesion and then covering one eye with a contact occluder [5]. The ipsilateral fiber system was found to be capable of mediating some retention, but not original acquisition, of a pattern task. Surprisingly, however, the animals that were restricted to using the contralateral fibers learned faster than did the sham-operated controls, and almost reliably so (p<0.07). Several studies [2,14] were performed subsequently to assess both the reliability and generality of the enhancement. In the first [2], which replicated and extended the earlier study, the enhancement phenomenon was confirmed and was reliable (p<0.05). In another experiment [14], reliably enhanced rates of acquisition by rats of a pattern discrimination, but not of a light-dark discrimination, were observed. Further, the enhancement only occurred when the pattern task was learned originally. If training on the pattern discrimination occurred after training on the
1Much gratitude is expressed to Don R. Justesen, Kansas City Veterans Administration Hospital, for his counsel and criticism in preparing the manuscript. 2 Requests for reprints should be sent to Daniel M. Levinson, Department of Psychology, CB Annex, University of Missouri - Kansas City, Kansas City, MO 64110. 513
514
LEVINSON, R I F E L t , REEVES ANI) S H [ R I i ) ' \ N
using guinea pigs; secondarily, our aim was to measure the functional competence of the uncrossed fiber system in the albino animal.
V
METHOD
Animals
( )
Twenty-four male albino guinea pigs of the Hartley strain were used. Obtained from Camm Research Institute, in Wayne, NJ, they were 6 0 - 9 0 days old at the onset of the study.
Apparatus The animals were trained in an apparatus modified from an earlier one [23] ; the dimensions are virtually the same as those described more recently [ 12]. The apparatus consisted of a startbox, runway, choice-point (that faced two cue-doors), and a goalbox. The discriminanda were horizontal or vertical stripes that were painted on either of the cue doors. Performance was motivated by electrical shock to the feet (250 mW, power stabilized 60 Hz current). Reversible monocular occlusion was achieved by one of several black acrylic contact occluders [ 1 5 ] ; an occluder was placed upon an animal's eye only after being thoroughly moistened with Barnes and Hind wetting solution.
B'-.J
A
I I
! I
Procedure Unilateral lesions of the striate cortex were made in 16 animals while 8 served as sham-operated controls. Each animal was anesthetized with chloral hydrate (250 mg/Kg). Striate ablations were accomplished by subpial aspiration after removal of a bone flap; sham operations were identical except for an aspiration of cortex. Laterality of ablation was determined randomly, with the constraint that half the operations be performed on the right side and half on the left. The animals had a period of postsurgical recovery of 1 2 - 1 4 days. At commencement of training, ten animals with lesions were restricted to use of contralateral visual fibers; and the other six, to the ipsilateral fibers. Restriction was accomplished by covering one eye with a contact occluder. The unequal ns reflected our emphasis on testing the generality of the enhancement phenomenon. The various experimental conditions are schematically illustrated in Fig. 1. Condition A represents animals restricted to contralateral fibers (contras), while condition B represents animals restricted to the ipsilateral system (ipsis). Condition C represents the sham-operated animals. During training, a guinea pig was placed in the start area of the apparatus, and the guillotine door was elevated. If an animal did not leave the start area within 10 sec or the runway within 20 sec, the shock grid in the respective area was electrified. The incorrect cue door was locked and the grid in front of it was electrified; any contact by an animal with that grid was scored as an error. Detection of contact was facilitated by neon lamps connected to the entryway grids, which changed in illumination when shock current was made available to the grids, and when contact was made with them. The left-right position of the correct cue door was varied across trials in a quasi-random sequence [7]. The animals were trained 25 trials per day until they had either reached a criterion of 18 correct responses in 20 consecutive trials or reached a cutoff point of 250 trials. At this point, the occluder was shifted to the opposite eye, and
C FIG. 1. Schematic illustration of the experimental conditions~ A: an animal restricted to the contralateral fibers (CONTRA); B: an animal restricted to the ipsilateral fibers (IPSI); C: a sham-operated animal (CONTROL). reacquisition of the task was attempted by 6 controls, 6 contras, and all 6 ipsis. Not all of the animals were restrained, since the effects measured in this portion of the study were so pronounced as to require the testing of fewer animals. The animals were again trained either to criterion or to the 250-trial cutoff. At conclusion of the study, several animals were observed during 20 test trials with both eyes covered as a test for effectiveness of the occluders. Finally, histological analyses were performed to determine the extent of the lesions. RESULTS
Mean and median trials to criterion are presented in Table 1 ; mean trials are presented histographicaUy in Fig. 2. The lesioned animals restricted to using the crossed fiber system (the contras) quickly mastered the task (~ = 70.90) and required fewer trials than did the sham-operated controls (~ = 101.00); the enhancement is highly reliable, t(16) = 3.37, p<0.01. No animals with visual input restricted to the uncrossed fibers (the ipsis) demonstrated original learning, but when shifted to the crossed fibers
ENHANCEMENT IN GUINEA PIGS
515
TABLE 1 MEAN AND MEDIAN TRIALS TO CRITERION FOR ACQUISITION AND REACQUISITION Sham-Operates £ Mdn n
"
0 "7.
101.00 97 8
55.67 50 6
Contra-Ipsi 70.90 65 lO
237.17 250 6
Ipsi-Contra 250 250 6
88.67 77.5 6
250200-
o
150100 50'
learning was demonstrated (£ = 88.67), although not reliably faster than that of the sham-operated controls, t(12) = 0.99. The 6 contras that were retrained following shift of the occluder showed little or no retention when shifted to use of the ipsilateral system; only 2 of them reacquired the task within 250 trials (£ = 237.17). The two animals that relearned the discrimination required 206 and 217 trials, and their lesions were somewhat smaller than average. The 6 controls after the shift of occlusion showed intermediate levels (42.17%) of interocular transfer. In the test for effectiveness of binocular occlusion, the performance of the animals fell to chance (~ 50%) levels. Histological analyses revealed that there was some variability in size of lesion. Figure 3 consists of photographs of whole brains showing maximal and minimal extent of lesions. Animal No. 7 has a left striate lesion, while animal No. 17 has a right lesion; animal No. 14 is a sham-operate. Generally, however, lesion sizes were fairly uniform. The brains were embedded in combined celloidin and paraffin, and sections from 1 0 - 2 0 ~ in thickness were made, with several sections taken from the lateral geniculate nuclei. All sections were stained with cresyl violet. Figures 4 and 5 represent photomicrographs of cells in the lateral geniculate nuclei from a control and lesioned hemisphere, respectively. A comparison of these two figures reveals that damage to the striate area resulted in some degeneration of cells in the LGN. DISCUSSION
CONTROLS
C ONTRA
(S HAMS)
~
I PSI
I P S I ,,-4. C ONTRA
FIG. 2. Mean trials to criterion. Black bars represent original acquisition; white bars represent retraining on the opposite eye.
The data obtained with rats [2, 5, 6, 13] have repeatedly indicated that unilateral striate removals can enhance the learning of pattern discriminations when mediated by the eye that remains truly functional, namely the eye contralateral to the intact hemisphere. Our study demonstrates that the phenomenon is at least somewhat
FIG. 3. Dorsal views of brains showing range of lesion sizes: No. 7 - left striate lesion; No. 17 - fight striate lesion; No. 14 - sham-operate.
I t
516
LEVINSON, RIFFL[-,. REEVES AND SIIERII)AN
FIG. 4. Photomicrograph of lateral geniculate nucleus from a control hemisphere.
FIG. 5. Photomicrograph showing degeneration in the lateral geniculate nucleus from a lesioned hemisphere.
general across mammalian species. Related phenomena have been reported in other species, and for at least one modality other than the visual; e.g., unilateral tectal lesions augmented the learning of visual discriminations in pigeons [ 1 ], and a reciprocally interfering relationship was reported to hold between the two superior colliculi in cats under some circumstances [22]. In addition, unilateral lesions of the visual and somesthetic cortex of rats were found to result in a significant increase in cholinesterase activity in the contralateral cortex [10]. Though we cannot say whether these superficially similar phenomena have similar functional bases, the accumulated evidence indicates that there is some highly general form of across-the-midline interference. The level of interocular transfer that was observed in the sham-operated animals was much lower than that reported for intact ocularly pigmented guinea pigs, and even somewhat lower than that obtained in split-brain pigmented animals [12]. A partial explanation of the low level of transfer appears to stem from the very small, poorly organized component of ipsilateral visual fibers in the albino animal. Our data on the guinea pig compare favorably with those of intact albino and pigmented (hooded) rats [20]. Nonetheless, even though the present data are consistent with those obtained using rats, the level of transfer is remarkably low, especially in light of the size of the corpus caUosum in guinea pigs as well as the high levels of transfer observed in shock-motivated split-brain
cats [19]. Our data also agree with anatomical and electrophysiological data [4] and further confirm that the ipsilateral fiber system in the albino guinea pig is functionally incapable of mediating acquisition or retention of a horizontal-vertical discrimination. The enhanced rate of acquisition by the unilaterally visually decorticated guinea pig was more pronounced than that reported in any of the earlier studies of rats. An explanation for the differences between the two species may stem from split-brain studies, wherein the effects of section of the corpus callosum on interocular transfer were measured. In one of these [201, it was found that split-brain albino rats showed an 18% loss in transfer of a pattern discrimination as compared to control animals; in another [ 13], it was reported that split-brain hooded rats showed a 16% loss as compared to controls. However, still another study [12] revealed that section of the corpus callosum of the guinea pig results in a 38% loss in transfer of a pattern habit, twice as great as that observed in rats. It appears that in the guinea pig more information transfers from one hemisphere to the other. If it is assumed that some of the interhemispherically transferring information is of an interfering nature, then one could conclude that there is more interhemispheric interference in the guinea pig than in the rat. Therefore, removal of interference by introduction of a unilateral striate lesion would result in more pronounced enhancement in the guinea pig. Support for this hypothesis stems from the above-mentioned study on
E N H A N C E M E N T IN G U I N E A PIGS
517
g u i n e a pigs [ 1 2 ] , in w h i c h split-brain a n i m a l s s h o w e d enhanced rates of acquisition of both pattern and shape tasks as c o m p a r e d t o s h a m - o p e r a t e d c o n t r o l s . A l t h o u g h n o t statistically reliable, these d a t a suggest t h a t s e c t i o n o f t h e c o r p u s c a l l o s u m results in a loss o f i n t e r - h e m i s p h e r i c
i n t e r f e r e n c e t h a t is similar to t h a t w h i c h results f r o m a u n i l a t e r a l striate lesion. T h e e n h a n c e m e n t p h e n o m e n o n was n o t o b s e r v e d in e i t h e r a l b i n o or h o o d e d split-brain rats [13,20].
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