Auditory cortical lesions and visual pattern discrimination in cat

Auditory cortical lesions and visual pattern discrimination in cat

437 BRAIN RESEARCH AUDITORY CORTICAL LESIONS AND VISUAL PATTERN DISCRIMINATION IN CAT FRANCIS B. COLAVITA* Department of Psychology, University of ...

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437

BRAIN RESEARCH

AUDITORY CORTICAL LESIONS AND VISUAL PATTERN DISCRIMINATION IN CAT

FRANCIS B. COLAVITA* Department of Psychology, University of Pittsburgh, Pittsburgh, Pa. 15213 (U.S.A.)

(Accepted October 29th, 1971)

INTRODUCTION

Based upon numerous anatomical and electrophysiological investigations, certain cortical areas of the cat brain are known to have auditory function. The role played by these cortical areas in various auditory discrimination tasks has been the subject of a series of ablation experiments extending over the last 20 years. Briefly, these studies have indicated that in the cat, auditory cortex is apparently unnecessary for the discrimination of sound onset 7, and for discriminating changes in the intensity8,9 or frequency of tones1,5, 7. These basic capacities of the auditory system seem to be mediated subcortically, in as much as they are largely or completely preserved following bilateral ablation of auditory areas At, A n , Ep, and the insulartemporal region. A deficit in auditory discrimination can be produced by cortical lesions, however, when the cat is required to discriminate a change in the temporal pattern of two recurring tones. Loss of tonal pattern discrimination has been reported in cats with bilateral lesions of areas AI, AII, and Ep, although such animals can still respond to sound onset and make frequency and intensity discriminations4, 5. For the present purpose it is especially noteworthy that bilateral lesions restricted to the insular-temporal area alone are also capable of disrupting auditory pattern discrimination, even though insular-temporal lesions produce only moderate degeneration restricted to the caudal pole of the medial geniculate body4,L The present experiment was conducted to test the idea that the insular-temporal region in the cat permits the animal to detect changes in temporal patterns in general, irrespective of the modality of the stimuli. Bilateral lesions of areas AI, A n , and Ep, which also disrupt auditory temporal pattern discriminations, are not expected to interfere with the discrimination of changes in temporal patterns of non-auditory stimuli. The procedure used to test the above notion was to replicate some of the earlier work on auditory pattern discrimination, except that temporal sequences of visual stimuli were substituted for the auditory stimuli. *

Present address: Department of Psychology,Universityof Pittsburgh, Pittsburgh, pa. 15213, U.S.A. Brain Research, 39 (1972) 437-447

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MATERIALS A N D METHOD

The subjects for this experiment were 10 adult cats, obtained from a local supplier. The animals, 7 males and 3 females, were between 1 and 5 years of age and ranged in weight from 1.8 to 3.5 kg. The cats were housed in individual cages and were given ad lib. access to Purina cat chow and water. All 10 animals were trained in a double-grill box to avoid foot shock by crossing from one compartment to the other following a change in the temporal sequence of two blinking lights. The double-grill box, of dimensions 40 in. × 20 in. × 16 in., was located in a sound-shielded room. The patterns of visual stimuli to be discriminated were produced by two blinking lights shining through a piece of milk glass of dimensions 10 in. × 20 in., located on top of the double-grill box. The lights were positioned such that the interior of the box was uniformly illuminated. The direction in which the cat was facing was of little consequence as long as its eyes were open. One light (a 7 5 W , 120V incandescent bulb) had a brightness of 151 luxes, while the other (a 6 W, 120 V incandescent bulb) had a brightness of 0.44 luxes. The ambient light intensity in the experimental chamber was 0.22 luxes. The animals were observed through a one-way window in the sound-shielded room by the experimenter, who was partially dark adapted. For 5 of the cats the neutral signal was a recurring sequence of blinking lights in the order 'bright-dim-bright'. The avoidance signal was a change in this ongoing sequence to the order 'dim-bright-dim'. The neutral and avoidance signals were reversed for the remaining 5 animals. The interstimulus interval was 0.1 sec within a triplet of flashes, while there was a 2 sec empty interval between successive triplets. Each flash lasted for 0.9 sec. On each trial the neutral signal was presented for an interval of time ranging from 45 to 120 sec. The avoidance signal was then presented for 15 sec. If the cat failed to make a crossing response during the 15 sec presentation of the avoidance signal, foot shock was delivered through the bars of the double-grill box until an escape response was made. The foot shock was produced by an adjustable shock-scrambler circuit with an upper limit of 1800 V AC. Shock voltage was determined individually for each animal and consisted of the lowest intensity that would quickly and reliably drive the cat from one compartment to the other. The sequence of events comprising a single trial is depicted in Fig. 1. The interstimulus intervals were the same for all animals. All cats received 20 trials per day, and were trained to a criterion of 2 successive days at 90 ~ shock avoidance or better. Crossing responses made in the absence of the avoidance signal were also punished with foot shock, so that by the time the animals had attained the learning criterion they were no longer making any spontaneous crossings. Following preoperative training on the visual pattern discrimination task, different parts of auditory cortex were bilaterally ablated in 8 of the cats. The remaining 2 animals received bilateral lesions of visual cortex. Surgery was performed under Nembutal anesthesia, with routine sterile precautions being observed. Cortical tissue was removed by subpial aspiration. Brain Research, 39 (1972) 437-447

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SHocK Fig. 1. Sequence of stimuli used to study visual temporal pattern discrimination. Each light flash lasted 0.9 sec, with a 0.1 sec interflash interval. There was a 2 sec empty interval between successive triplets of flashes. The animals were divided into groups of two as follows: Two animals received bilateral ablation of cortical areas At, A n , Ep, and the insular-temporal region; two cats had bilateral lesions of areas AI, A n , Ep, and the dorsal portion of insulartemporal cortex, with sparing of ventral insular-temporal. Two animals had lesions limited to areas Az, A n , and Ep, with total sparing of the insular-temporal region. Two additional cats had bilateral lesions restricted to insular-temporal cortex, and the final two animals received bilateral lesions of visual areas Vz and Vn. A postoperative recovery period of two weeks was allowed before retraining on the visual pattern discrimination was initiated. Retraining was continued until either the 90 ~ correct avoidance criterion was again achieved, or until the animal showed no signs of relearning despite having at least as many trials as preoperatively. Those cats which failed to reacquire the pattern discrimination were also tested with a brightness discrimination involving the same two light intensities that had been used in the visual pattern task. In such a case the cat would be trained to discriminate a change from the light sequence 'dim-dim-dim' to the sequence 'bright-bright-bright'. Animals were given 20 trials a day on the brightness task, with all intertrial and interstimulus intervals the same as in the pattern discrimination situation. At the conclusion of postoperative testing, each animal was deeply anesthetized and perfused with saline and 10~o formalin. The brains were removed and stored in 1 0 ~ formalin for various lengths of time prior to being sectioned on a freezing microtome at 50/~m. Serial sections through the medial and lateral geniculate nuclei of the thalamus were stained with thionin and studied for retrograde degeneration. RESULTS

The behavioral data are presented in the following figures for the 5 pair of animals having similar lesions. Also included are diagrams showing the extent of the ablation. These diagrams were based upon inspection of 50/~m sections through the ablated regions in each animal. Drawings of frontal sections through the thalamus for one cat from each group receiving auditory cortical lesions are shown in Fig. 2. As the lesions were essentially symmetrical, only the left hemisphere is depicted. Cats C-2 and C-7 received large bilateral lesions of all auditory cortex following Brain Research, 39 (1972) 437-447

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Fig. 2. Thalamic degeneration in cats with auditory cortical lesions. Degeneration indicated by stippling. Abbreviations used: GL, corpus geniculatum laterale, pars dorsalis; GMp, corpus geniculatum mediale, pars principalis; LP, nucleus lateralis posterior; mc, corpus geniculatum mediale, pars rnagnocellularis; Po, posterior group; Pul, pulvinar; VPL, nucleus ventralis posterolateralis. acquisition of the visual pattern discrimination (Fig. 3). The lesions in C-2 were found to extend into the suprasylvian gyrus, and caused considerable damage to the optic radiations. A less extensive lesion was produced in C-7, and no damage was done to the optic radiations in this subject. In each case the ablation was seen to extend ventrally to the rhinal sulcus. The auditory cortical lesions in both animals were complete, as was evidenced by total retrograde degeneration of the medial geniculate body. There was no evidence of postoperative relearning of the temporal pattern discrimination task in either of these animals, although both were readily able to acquire the postoperative brightness discrimination (see inset in Fig. 3). Throughout postoperative testing, no spontaneous crossings were noted in these cats. They crouched passively on each trial, making a crossing response only to escape the shock. Two other animals, C-4 and C-8, received large bilateral lesions of auditory areas Az, AI~, Ep, and the dorsal aspect of insular-temporal cortex. There was some sparing of ventral insular-temporal, as is shown in Fig. 4. Postoperatively, neither animal was able to achieve the preoperative learning criterion of 9 0 ~ conditioned avoidance responses or better, even after as many as 1400 postoperative trials. Some degree of relearning did occur in these animals, apparently reaching a terminal level somewhere between 45 and 55 ~ correct. In contrast to the previous two animals, alerting responses were occasionally noted in cats C-4 and C-8 in the presence of the Brain Research, 39 (1972) 437-447

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avoidance signal. Most of the time that an alerting response was made, the cat would successfully avoid the shock. On around 4 0 ~ of the trials, however, there was a complete failure to show any response to the avoidance signal. As in the previous two animals, the postoperative brightness discrimination was successfully acquired in less than 200 trials. Severe retrograde degeneration occurred throughout the anterior two-thirds of the medial geniculate body, although some normal appearing cells were noted in the caudal portion of this nucleus. Fig. 5 presents the data obtained from two cats (C-10 and C-1 l) in which the ablations were bilaterally restricted to the insular-temporal region. Postoperative retraining revealed an inability to relearn the visual pattern discrimination even after 1200 trials. These cats had no difficulty in acquiring the visual brightness discrimination, as is indicated by the inset in Fig. 5. Retrograde degeneration was confined to Brain Research, 39 (1972) 437-447

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the posterior tip of the medial geniculate body, where a large region of atrophied cells was observed. The last two animals with auditory cortical lesions were cats C-12 and C-18. In these animals the ablations were restricted to areas AI, AH, and Ep, with complete sparing of insular and temporal cortex. In contrast to the impaired performance that previous studies have reported for such animals on an auditory pattern discrimination task, both C-12 and C-18 showed rapid postoperative relearning of the visual pattern discrimination, reaching the criterion of 90~ correct or better by the end of the first block of 100 trials (Fig. 6). Thalamic degeneration in these two animals was extensive throughout the anterior two-thirds of the principal division of the medial geniculate body, while the cells in the posterior portion appeared to be unaffected. The final two cats studied, C-26 and C-28, received bilateral lesions in visual areas Vz and VII after reaching the preoperative learning criterion (Fig. 7). In both Brain Research, 39 (1972) 437-447

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animals there was very rapid postoperative recovery of the visual discrimination; in fact, C-28 showed near perfect retention of the problem, failing to make a conditioned avoidance response only on the first 5 postoperative trials. The lesions in these animals included both the lateral and posterolateral gyri of both hemispheres. Degeneration in all laminae of the dorsal lateral geniculate nucleus was seen to be extensive. DISCUSSION

The data of the present experiment indicate that insular-temporal cortex in the cat, usually considered to be solely an auditory area, is essential to the cat's ability to discriminate changes in the temporal sequence of two blinking lights of different intensities. The procedures carried out in this study would seem to rule out alternative Brain Research, 39 (1972) 437-447

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Fig. 6. Preoperative and postoperative performance on visual pattern discrimination for two cats with bilateral lesions restricted to areas At, A~, and Ep. explanations such as the 'mass action effect', or inadvertent damage to the classical visual pathways. The insular-temporal lesions that prevented relearning were actually smaller than the lesions of areas AI, AII, and Ev, which did not prevent relearning. Furthermore, the two animals with partial sparing of insular-temporal cortex showed partial relearning of the visual pattern task. Also of interest was the fact that cats with extensive damage to visual cortex required relatively few postoperative trials to relearn the discrimination, suggesting that insular-temporal cortex is more critical in this situation than striate cortex, even though the visual modality is involved in the problem. We have interpreted our data as supporting the hypothesis that insular-temporal cortex plays a role in temporal pattern discrimination. However, a comparison of the acquisition rates for the preoperative pattern sequence task and the postoperative brightness discrimination indicates that the brightness discrimination was a much easier task for the animals. An alternative interpretation of our data might be that Brain Research, 39 (1972) 437-447

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insular-temporal lesions affect difficult tasks, but not easy ones. The present data do not permit us to unequivocally choose between these alternative interpretations. Yet even if the latter interpretation were correct, it would still be the case that insulartemporal lesions interfere with discriminations other than auditory ones. It is unlikely that the animals failing to relearn the pattern discrimination would have eventually done so with further training. All cats received at least as many postoperative trials as preoperative trials, and in some cases they received several hundred more postoperative trials than preoperative ones. Indirect evidence can be found in previous research that insular-temporal cortex is in some way 'different' from other auditory cortical areas of the cat brain. Compared with areas AI, AII, and Ep, the insular-temporal region is known to receive only sparse projections from the medial geniculate body a. It has also been proposed on the basis of degeneration studies that insular-temporal cortex receives a more indirect anatomical projection of auditory fibers than do a r e a s A I a n d AI110. Brain Research, 39 (1972) 437-447

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There is also some evidence that insular-temporal cortex in the cat is responsive to stimuli other than auditory ones. Visual evoked activity has been reported in this region 2, and more recently single units have been found in the insular cortex of the cat that respond to both auditory and visual stimuli 6. Short latency responses to somatic sensory stimulation have been noted in the insular region as welPL It has already been shown that disruption of the cat's ability to discriminate changes in temporal sequences of auditory stimuli can be accomplished either by bilateral ablation of auditory areas AI, AH, and Ev, or by bilateral ablation of the insular-temporal region alone4, 5. The present data indicate that this functional equivalence of dorsal and ventral auditory cortex breaks down when a visual pattern discrimination is substituted for the auditory one. Bilateral lesions of areas AI, AH, and Ev bring about no lasting change in the cat's ability to discriminate changes in the temporal sequence of two blinking lights, while insular-temporal lesions produce an apparently irreversible loss of the discrimination. Based upon the present study, as well as upon the results of previous degeneration and electrophysiological research, it appears reasonable to propose that insulartemporal cortex in the cat is in some way involved in tasks requiring the discrimination of changes in the temporal patterning of various classes of sensory stimuli. Such has now been shown to be the case with auditory and visual temporal pattern tasks, suggesting that it would be worthwhile to investigate the consequences of insulartemporal lesions as related to the discrimination of changes in temporal patterns of stimuli other than auditory or visual ones, for example tactile stimulus patterns. SUMMARY

Ten cats were trained in a double-grill box to avoid foot shock by crossing from one compartment to the other whenever a change occurred in an ongoing sequence of blinking lights. All animals eventually learned to cross when the light sequence 'dim-bright-dim' changed to the sequence 'bright-dim-bright'. Following acquisition of the avoidance response, all animals were prepared with bilateral cortical lesions. Ablations in different cats involved significant portions of either auditory or visual cortex. Postoperative testing indicated that only those animals having damage to the insular-temporal region were impaired on the visual pattern discrimination. Postoperative learning was seen in animals with ablations of areas AI, AII, and Ep, or o f visual areas VI and VH. It was proposed that insular-temporal cortex in the cat, bilateral ablation of which is also known to disrupt auditory pattern discrimination, may serve the general function of mediating the cat's perception of changes in the temporal patterning of various classes of sensory stimuli. ACKNOWLEDGEMENT

This research was supported by U.S. Public Health Service Grant NS09027-02 from the National Institute of Neurological Diseases and Stroke. Brain Research, 39 (1972) 437-447

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REFERENCES 1 BUTLER, R. A., DIAMOND, I. T., AND NEFF, W. D., Role of auditory cortex in discrimination of changes in frequency, J. Neurophysiol., 20 (1957) 108-120. 2 D~S~DT, J. E., ET MECHELSE,K., Mise en 6vidence d'une quatri/~me aire de projection acoustique dans 1'6corce cAr6brale du chat, J. Physiol. Path. gdn., 51 (1959) 448-449. 3 DIAMOND,I. T., CHOW, K. L., AND NEFF, W. D., Degeneration of caudal medial geniculate body following lesions ventral to auditory area II in cat, J. comp. Neurol., 109 (1958) 349-362. 4 DtAMOND, I. T., AND NEFF, W. D., Ablation of temporal cortex and discrimination of auditory patterns, J. Neurophysiol., 20 (1957) 300-315. 5 GOLDBERG,J. M., AND NEFF, W. D., Frequency discrimination after bilateral ablation of cortical auditory areas, J. Neurophysiol., 24 (1961) 119-128. 6 LOE, P. R., AND BENEVENTO,L. A., Auditory-visual interaction in single units in the orbito-insular cortex of the cat, Electroenceph. clin. Neurophysiol., 26 (1969) 395-398. 7 MEYER, D. R., AND WOOLSEY, C. N., Effects of localized cortical destruction upon auditory discriminative conditioning in the cat, J. Neurophysiol., 19 (1956) 500-512. 8 RAAB, O. W., AND ADES, H. W., Cortical and midbrain mediation of a conditioned discrimination of acoustic intensities, Amer. J. Psyehol., 59 (1946) 59-83. 9 ROSENZWEIG, M., Discrimination of auditory intensities in the cat, Amer. J. Psychol., 59 (1946) 127-136. 10 SINDBERG,R. M., AND THOMPSON,R. F., Auditory response fields in ventral temporal and insular cortex of cat, J. Neurophysiol., 25 (1962) 21-28. 11 THOMPSON,R. F., JOHNSON,R. H., AND HOOPES, J. J., Organization of auditory, somatic sensory, and visual projection to association fields of cerebral cortex in the cat, J. Neurophysiol., 26 (1963) 343-364.

Brain Research, 39 (1972) 437-447