Polysensory cortical lesions and auditory temporal pattern discriminations in the cat

80 (1974) 317-327 © ElsevierScientificPublishingCompany,Amsterdam- Printed in The Netherlands

Brain Research,

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POLYSENSORY CORTICAL LESIONS AND AUDITORY TEMPORAL PATTERN DISCRIMINATIONS IN THE CAT

J A C K B. KELLY

Department of Psychology, Carleton University, Ottawa, Ont. KIS 5B6 (Canada) (Accepted June 30th, 1974)

SUMMARY

Thirteen cats were tested in two types of auditory pattern discrimination before and after lesions of the suprasylvian gyrus, anterior lateral gyrus and pericruciate cortex. In 5 cats the lesions included all of these areas in both hemispheres; in 4 cats the lesions were in suprasylvian and anterior lateral gyri and in the remaining 4 cats the lesions were restricted to pericruciate cortex. The pattern discriminations used were rising v e r s u s falling frequency modulated tones and low-high v e r s u s high-low pure tone patterns. Although both of these discriminations are affected by auditory cortical lesions, neither discrimination was impaired by lesions of suprasylvian, anterior lateral or pericruciate cortex.

I NTRODUCTION

The ability of cats to discriminate auditory temporal patterns is highly dependent on auditory cortex. Bilateral lesions of AI, All and Ep result in an inability to discriminate between triads of pure tones such as low-high-low v e r s u s high-low-high3. Lesions of insular-temporal cortex, which is also included in traditional definitions of auditory cortex 14, result in severe impairments in discriminations of either triads or dyads of pure tonesT,10 as well as other auditory pattern discriminations1,2. In auditory pattern discriminations with frequency modulated tones, lesions of either dorsal (AI, All, Ep) or ventral (I-T) auditory areas alone fail to produce marked deficits, but larger lesions which include all of these areas do result in impaired performance11. Thus, auditory cortex can be considered an important structure for auditory pattern discrimination. The projections from auditory cortex include, in addition to intrinsic connections, callosal connections with auditory cortex in the opposite hemisphere, descending connections to subcortical structures, and extrinsic connections with other cortical

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areas 4-6. Three primary target areas which receive transcortical connections are located in the suprasylvian gyrus, anterior lateral gyrus, and pericruciate cortex. These areas have been described as 'association' cortex in the cat although they have extensive connections with the thalamus as well as transcortical connections ~,9. They also include areas described as polysensory according to electrophysiological responses19, z3 although the anatomical substrate for these regions is not yet clearly defined 9. The following paper is concerned with the effects of lesions in these areas on auditory pattern discrimination. METHODS

Subjects Thirteen adult cats were tested for their ability to discriminate auditory patterns after cortical lesions. Four of the animals had lesions in the pericruciate region; 4 had lesions in the suprasylvian gyrus and anterior lateral gyrus and the remaining 5 had large lesions involving all of these areas.

Procedure The procedure was the same as that reported previously 1°. Two pattern discriminations were used" one involving frequency modulated sounds (FM), the other

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involving pure tone dyads (TONE). The details of these stimuli are given in Fig. 1. The FM stimulus was composed of a continuous frequency change from 3.78 kHz to 4.22 kHz over a 350 msec period. Rise and fall times were 15 msec. Single gliding tones were presented at a rate of 1/sec and the animals were trained to discriminate a change from tones of rising frequency to tones of falling frequency. The T O N E stimulus was composed of pure tone pairs with frequencies of 3.78 kHz and 4.22 kHz. Each tone within a pair was 135 msec in duration and the two tones were separated by an 80 msec interval for a total period of 350 msec. Rise and fall times were 15 msec. As in the case of F M patterns, the animals were trained to discriminate the direction of frequency change, i.e., from a series of low-high dyads to a series of high-low ones. The animals were trained in these discriminations both before and after cortical lesions. Training was begun in both preoperative and postoperative sessions with a series of preliminary trials designed to establish a reliable avoidance response to sounds before training with patterned stimuli was started. During these trials each animal was trained to cross from one side of a double grill box to the other in response to the onset of a sound. After the animal had acquired a reliable response to the onset of a sound, training with frequency modulated sounds was begun. A series of F M sounds of rising frequency was presented throughout intertrial intervals. These intervals constituted a safe period during which animals were free to remain on one side or move about in the grill box without punishment. During a trial period the series of rising tones was replaced by a series of falling tones which served as a warning signal. Ten seconds of the warning signal were allowed for an animal to make an avoidance response. If a response occurred the warning signal was replaced by a safe signal. If a response did not occur the animal received a shock to the feet until the barrier was crossed. Five warning trials were given in each daily session with intertrial intervals ranging from 60 to 300 sec. Sessions with frequency modulated sounds were followed immediately by sessions with pure tone patterns. Training methods were the same as described above but the safe signal was a series of low-high tone pairs and the warning signal was a series of high-low tones. Occasionally spontaneous responses occurred during training sessions even though no change in stimulus conditions had been introduced. In order to more precisely evaluate the level of correct responses it was necessary to estimate the level of spontaneous crossing responses. This was done by considering the safe periods between 60 and 3130 sec as a series of 10 sec mock trials during which a signal might have occurred but did not. Responses occurring during these mock trials were counted as false positives and the percentage of spontaneous crosses was determined by the number of trials during which a response occurred divided by the total number of trials during the safe period.

Surgical and histological procedure During surgery the animals were deeply anesthetized with pentobarbital sodium. The skull overlying areas of interest was removed and lesions were made by sub-pial

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CAT 70

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Fig. 2. Illustrations of the extent of cortical damage in 5 cases with combined lesions of suprasylvian gyrus, anterior lateral gyrus, and pericruciate region. The standard diagram was derived from individual reconstructions.

aspiration. The wound was packed with Gelfoam and sutured closed. Two weeks were allowed for recovery after surgery. Following postoperative testing, the animals were perfused with 10 % formalin and the brains were prepared for histology. Sections were cut in the frontal plane at a thickness of 5 0 / ~ m and every fourth section was stained with cresyl violet. Reconstructions were made through projection of individual sections and the extent of damage was then translated to standard diagrams. RESULTS

Cases with extensive lesions Five cats were tested before and after large lesions which included the pericruciate, suprasylvian gyrus and anterior lateral gyrus. The extent of the lesions varied somewhat as can be seen in Fig. 2. The 3 most extensive lesions in cats 70, 71 and 74 destroyed the suprasylvian gyrus and anterior lateral gyrus in both hemispheres. The dorsal aspect of the pericruciate cortex was also destroyed and the lesions extended to tissue located deep within the cruciate sulcus. Some small areas of cortical tissue were found in the depth of this sulcus in the right hemisphere in each case. These large lesions were accompanied by severe thalamic degeneration in the lateroposterior nucleus including parts of the pulvinar and the laterodorsal nucleus. The rostral areas of the lateral geniculate were severely degenerated. The ventroposterior nucleus was

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Fig. 3. Thalamic degeneration for cat 71. Severe degeneration is shown as black. Areas of partial degeneration are more lightly shaded. Abbreviations: A.M. = anteromedial nucleus; A.V. = anteroventral nucleus; G.L. = lateral geniculate body; G.M. = medial geniculate body; L.D. = laterodorsal nucleus; L.P. = lateroposterior nucleus; M.D. = mediodorsal nucleus; Pul. = Pulvinar; V.A. = ventroanterior nucleus; V.L. = ventrolateral nucleus; V.M. = ventromedial nucleus; V.P. = ventroposterior nucleus. affected by the lesions b u t large areas with n o r m a l cells r e m a i n e d in each case. T h e v e n t r o l a t e r a l a n d v e n t r o a n t e r i o r nuclei were also affected b u t the severity o f degenera t i o n was n o t the same f o r all 3 cases. T h e m o s t extensive d e g e n e r a t i o n in these areas was seen in cat 71 b u t d e g e n e r a t i o n was also present in cats 70 a n d 74. D e g e n e r a t i o n o f the a n t e r o v e n t r a l nucleus was seen in cat 71 and, to a lesser extent, in cat 74 b u t was n o t seen in cat 70. T h a l a m i c d e g e n e r a t i o n f o r eat 71 is s h o w n in Fig. 3.

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Fig. 4. Thalamic degeneration for cat 62. Abbreviations as in Fig. 3.

In the remaining cats, 62 and 65, lesions included all intended areas, but areas of intact tissue were found in the anterior lateral gyrus and damage to tissue within the depth of the cruciate sulcus was less extensive than for the other 3 cases. Severe thalamic degeneration was seen in the lateroposterior nucleus in both cases. The degeneration in the ventrolateral and ventroanterior nuclei was less extensive than in cats 70, 71 and 74 and no degeneration was found in the anterior nuclei. Thalamic degeneration for cat 62 is shown in Fig. 4. Following surgery these cats had obvious difficulty in locomotor behavior which improved rapidly over the first several days and showed a more gradual improvement over the 2 week recovery period. In some of the cats, for example 74, an early re-

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Fig. 5. Behavioral data for cats 70, 71, 74, 65 and 62 before and after cortical lesions. Filled circles represent percentage of correct responses in each daily session. Open circles represent the percentage of false positive or spontaneous responses. Vertical dashed lines indicate a series of preliminary sessions with sound onset. These sessions are followed first by F M and then by pure tone pattern discriminations.

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sponsiveness to sounds was noticed during the recovery period. Accurate orientation to sounds was observed to stimuli such as jangling keys, etc., in spite of motor impairments or possible visual deficits. Results of discrimination tests for each of the five cases are shown in Fig. 5. Comparison of behavior before and after cortical lesions revealed little evidence for impairment in pattern discrimination. Moreover, the number of sessions required to reach criterion performance postoperatively was generally less than preoperatively, indicating some retention of learned responses following surgery. In some cases a reacquisition of the response was necessary but this does not necessarily reflect an impairment in retention. For example, postoperative motor or visual impairments m a y have had an influence on performance levels. In any case the ability to perform the task was very little affected by the lesions. Even cats 70, 71 and 74 could discriminate auditory patterns without difficulty. Cases with restricted lesions The remaining 8 cases had bilateral lesions restricted to either the suprasylvian and anterior lateral cortex or the pericruciate cortex. The results confirm the expectation from cases with combined lesions of these areas. Each of the 4 cases with lesions of suprasylvian and anterior lateral areas rapidly reached criterion on both types of pattern discrimination. The mean number of sessions required postoperatively was 2 for FM patterns and 4 for two tone patterns. A similar result was obtained for the 4 animals with lesions of pericruciate cortex. The mean number of post-

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operative sessions to criterion was 3 for FM patterns and 8 for pure tone patterns. The lesions for these 8 cases are shown in Fig. 6. Thalamic degeneration for cases with lesions of suprasylvian and anterior lateral areas was seen in rostral parts of the lateroposterior nucleus and in parts of the lateral geniculate. The severity of degeneration varied among individual cases but the general pattern was consistent. The degeneration found in cases with pericruciate lesions was minimal with no consistent pattern across cases. DISCUSSION

The anatomical results for cats with large lesions indicate extensive damage to the suprasylvian gyri, the anterior lateral gyri and pericruciate cortex, areas which have been described as polysensory or 'association' areas by electrophysiological studies 17. In all our cases with lesions of the suprasylvian and anterior lateral cortex, degeneration was found in the lateral thalamic group. This pattern of degeneration is consistent with more detailed studies of thalamic projections to association cortexS, 9. Corresponding degeneration in the lateral geniculate is probably due to disruption of projections to areas 17 and 18 (see ref. 9). Degeneration of the ventral nuclei is expected following pericruciate lesions 21, and was confirmed in our cases with extensive lesions. The anteroventral nucleus, which underwent noticeable degeneration in two cases, 71 and 74, has established connections with cingulate cortex located along the medial surface of the hemisphere 15. The lack of impairment in pattern discrimination following these large lesions stands in marked contrast to the effects of lesions in auditory cortical areas. Lesions of AI, A l l and Ep produce severe impairments in discriminations of pure tone patterns 6. Even relatively small lesions of insular-temporal cortex result in an inability to discriminate pure tone patterns7, TM. Pattern discriminations with rising and falling frequency modulated sounds, although still possible, are nevertheless disrupted following large bilateral lesions of AI, All, Ep, I and T (see ref. 11). In cases with large polysensory lesions the total amount of damage is commensurate with the area destroyed by total auditory cortical lesions (AI, All, Ep, I and T) and far exceeds the area of insular-temporal cortex which is essential for pattern discrimination. Thus, it is clear that the extent of cortical damage is not the sole factor in producing impaired pattern discrimination. Impairments in auditory pattern discrimination are closely related to specific lesions of the classical auditory cortex. The pericruciate region, the anterior lateral gyrus and the suprasylvian gyrus receive major transcortical projections from the auditory cortexL According to Heath and Jones 9 these projections are from AI, All and Ep to the suprasylvian fringe area and from the suprasylvian fringe to area 6 in pericruciate cortex and area 7 in the middle suprasylvian and anterior lateral gyri. Bilateral destruction of these projection areas does not impair the ability to discriminate auditory patterns. Therefore, these transcortical efferents do not constitute an essential link in pattern discrimination. The effects of association lesions on other auditory tasks are also different from the effects of lesions in auditory cortex itself. For example, although impairments have

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been o b s e r v e d in p e r f o r m a n c e on certain types o f frequency discriminationl~, '~0 and in sensory p r e c o n d i t i o n i n g tasks 18, the effects do not resemble the i m p a i r m e n t s p r o d u c e d by a u d i t o r y cortical lesions. These o b s e r v a t i o n s are consistent with L a s h l e y ' s d e - e m p h a s i s o f transcortical connections in cortical function 12. In the absence o f a s s o c i a t i o n cortical areas o t h e r p r o j e c t i o n s f r o m a u d i t o r y cortex m u s t be sufficient to m a i n t a i n a u d i t o r y p a t t e r n discrimination. These projections include two areas in the p o s t e r i o r suprasylvian gyrus a n d in t e m p o r a l cortex which are c o n t i n u o u s with a u d i t o r y cortex itselfL The r e m a i n i n g t r a n s c o r t i c a l connections to areas n o t d e s t r o y e d by lesions o f m i d d l e suprasylvian, a n t e r i o r lateral and pericruciate cortex are p r o b a b l y m i n i m a l . O n the other hand, substantial subcortical p r o j e c t i o n s have been described f r o m a u d i t o r y cortex to the c o r p u s striatum, the m e d i a l geniculate, the p o s t e r i o r t h a l a m i c nucleus, p o n t i n e nuclei, inferior colliculi and o t h e r areas6,1a, 22. Therefore, e m p h a s i s is placed on the possible role o f these remaining descending o r subcortical c o n n e c t i o n s in p a t t e r n discrimination. The question remains, however, whether o r not the descending a u d i t o r y system is essential for a u d i t o r y cortical function, or whether one c o m p o n e n t is m o r e i m p o r t a n t than another. ACKNOWLEDGEMENTS

T h e a u t h o r w o u l d like to t h a n k the N a t i o n a l R e s e a r c h Council o f C a n a d a for financial s u p p o r t . R o b e r t G r a y a n d Cheryl S t a r k p r o v i d e d expert technical assistance.

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13 RASMUSSEN,G. L., Anatomical relationships of the ascending and descending auditory systems. In W. S. FIELDS AND B. R. ALFORD (Eds.), Neurological Aspects of Auditory and Vestibular Disorders, Thomas, Springfield, Ill., 1964, pp. 1-15. 14 ROSE, J. E., AND WOOLSEY, C. N., Cortical connections and functional organization of the thalamic auditory system of the cat. In H. F. HARLOWAND C. N. WOOLSEY(Eds), Biological and Biochemical Bases of Behavior, Univ. of Wisconsin Press, Madison, Wisc., 1958, pp. 127-150. 15 ROSE, J. E., AND WOOLSEY,C. N., Structure and relations of limbic cortex and anterior thalamic nuclei in rabbit and cat, J. comp. Neurol., 89 (1948) 279-347. 16 THOMPSON, R. F., Role of cortical association fields in auditory frequency discrimination, J. comp. physiol. Psychol., 57 (1964) 335-339. 17 THOMPSON,R. F., JOHNSON,R. H., AND HOOPES, J. J., Organization of auditory, somatic sensory, and visual projections to association fields of cerebral cortex in the cat, J. Neurophysiol., 26 (1963) 343-364. 18 THOMPSON, R. F., AND KRAMER, R. F., Role of association cortex in sensory preconditioning, J. comp. physiol. Psychol., 60 (1965) 186-191. 19 THOMPSON,R. F., AND SINDBERG,R. M., Auditory response fields in association and motor cortex of cat, J. Neurophysiol., 23 (1960) 87-105. 20 THOMPSON,R. F., AND SMITH, M. E., Effects of association area lesions on auditory frequency discrimination in cat, Psychon. Sci., 8 (1967) 123-124. 21 WALLER,W. H., Thalamic connections of the frontal cortex of the cat, J. comp. Neurol., 73 (1940) 117-138. 22 WEBSTER,K. E., The cortico-striatal projection in the cat, J. Anat. (Lond.), 99 (1965) 329-337. 23 WOOLSEY,C. N., Organization of cortical auditory system: a review and a synthesis. In G. L. RASMUSSENAND W. F. WINDLE(Eds.), Neural Mechanisms of the Auditory and Vestibular Systems, Thomas, Springfield, Ill., 1961, pp. 165-180.