The effects of insular and temporal lesions in cats on two types of auditory pattern discrimination

Brain Research, 62 (1973) 71-87

71

© Elsevier ScientificPublishing Company, Amsterdam - Printed in The Netherlands

T H E EFFECTS OF I N S U L A R A N D T E M P O R A L LESIONS IN CATS ON TWO TYPES OF A U D I T O R Y P A T T E R N D I S C R I M I N A T I O N

JACK B. KELLY

Department of Psychology, Carleton University, Ottawa, Ont. KIS 5B6 (Canada) (Accepted April 9th, 1973)

SUMMARY

Seven cats were tested before and after bilateral lesions of insular-temporal cortex on two types of auditory pattern discrimination. The first discrimination was between two frequency modulated tones, i.e., rising vs. falling frequencies. The second discrimination was between two pairs of pure tones, i.e., low-high vs. high-low frequencies. The animals were trained in a double grill box to avoid a shock when they detected a change in the temporal pattern. Normal cats readily learned to discriminate FM patterns and two-tone patterns. Cats with large bilateral lesions of insular-temporal cortex (4 cases), however, failed to relearn the two-tone pattern discrimination even though in 3 cases discrimination of frequency modulated patterns was relearned. For each of these animals discriminations of sound onset and frequency change were also possible. Thus the effects of large insular-temporal lesions are more severe for pure tone pattern discriminations than for FM patterns. In 3 additional cases with smaller lesions of the insular-temporal area both F M and pure tone patterns were easily relearned and no differences were seen for the two types of pattern discrimination.

INTRODUCTION

Insular and temporal cortex in the cat is considered to be an essential area for discriminations o f temporally patterned stimuliZ-4,6, 9. Bilateral lesions of this area result in an apparently permanent inability to discriminate between patterns of pure tone triads even in cats with auditory cortex (A I, A I1) intact. For example, it has not been possible to retrain cats with insular-temporal lesions to discriminate lowhigh-low from high-low-high frequency patterns 9. On the other hand, certain types o f auditory patterns can still be discriminated by cats with lesions of insular-temporal cortex and other auditory cortical areas combined10, is. For example, discrimination

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of temporal patterns composed of rising and falling frequency modulated (FM) tones are still possible following bilateral cortical lesions which include A I, A II, Ep and insular-temporal areas 10. It has been suggested that the basic difference between pure tone patterns and frequency modulated patterns lies in the continuity or discontinuity of frequency change. But there are several other differences which might account for the effects of cortical lesions. For example, the range of frequencies, the duration of the stimuli, or the direction of frequency change may be important. The following study compares directly the effects of insular-temporal lesions on FM patterns and pure tone patterns in order to determine more precisely the type of temporal pattern discrimination which requires insular-temporal cortex. METHODS

Subjects Seven adult cats were tested before and after cortical lesions in discriminations of two types of auditory temporal pattern. The patterns were composed of frequency modulated (FM) sounds in one task and pure tone pairs (TONE) in the other. All animals were tested in sequence first on the FM discrimination and then on the twotone one. The same sequence of testing was used pre-operatively and post-operatively in a standard shock avoidance training paradigm. Patterned stimuli: FM and TONE Details of the two types of patterned stimuli are shown in Fig. 1. The frequency modulated (FM) stimuli were produced by a Hewlett-Packard type 3310 A oscillator. The output of the oscillator was controlled by the linear voltage ramp of a saw toothed signal and generated continuous gliding frequency changes from 3.78 to 4.22 kHz. Single gliding tones were triggered at a rate of 1/sec. The duration of each tone was set at 350 msec, and the rise and fall times of each presentation were 15 msec. The requirement of the FM discrimination task was to detect a change from tones of rising frequency to tones of falling frequency. This change could be introduced without disrupting the rate of stimulus presentation. Thus a series of rising tones could be replaced by a series of falling tones as shown in Fig. 1. Also notice that both rising and falling stimuli covered the same range of frequencies and were the same duration. The only difference between the two stimuli was the direction of frequency change. The paired tonal stimuli (TONE) were quite similar to frequency modulated stimuli in several respects. The method of generating these tones was essentially the same as described above except frequency changes were controlled by a square-wave signal and each presentation was a pair of separate frequencies. As can be seen in Fig. 1 a single patterned presentation consisted of two 135 msec tones separated by an interval of 80 msec. Thus the total duration for a single dyad was 350 msec. The rise and fall times were 15 msec. The frequencies of the two tones were 3.78 and 4.22 kHz. Stimulus pairs were presented at a rate of 1/sec. Thus the major difference between an FM pattern and a tonal pattern was the mode of frequency change rather

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than duration, range of frequencies, or repetition rate. As in the case of the FM task, the requirement of the tonal pattern task was to discriminate the direction of frequency change, Lel, to detect a change in the configuration from low-high to highlow frequencies. Switching from a series of low-high pairs to a series of high-low pairs was carried out without altering the rate of presentation. The only change was the temporal order of high and low frequencies within each pair. Both FM and tonal stimuli were presented to the animals through a 10 in. speaker located approximately 6 ft. from the testing apparatus. The intensity of each stimulus was held constant during testing at a level between 72 and 82 dB SPL depending on the exact location in the testing chamber. The sound pressure level for high and low frequencies was found to differ somewhat (max., 8 dB) for specific locations in the testing apparatus, but the direction of the difference was not the same for other locations. Considering that the animals changed their position in the apparatus from trial to trial, it is unlikely that intensity patterns rather than frequency patterns were used.

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Training procedure 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 buzzer or a series of 4 kHz tones. The animals were given 10 sec to make a crossing response. If a response did not occur during this period an intermittent shock was delivered through the grid floor of the box until a response was completed. After the animal acquired a reliable response to the onset of a sound, training with F M 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 the 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 the safe signal. If a response did not occur the animal received 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. Training was continued until the animals showed a high level of performance, which in 5 cases was 9 correct responses in two daily sessions. In two cases, 28 and 29, the less stringent criterion of 5 correct responses in a single session was employed. Training beyond this level of performance was introduced in some cases during postoperative sessions. Sessions with F M 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. Discriminations of tone onset and sound frequency were also introduced during postoperative sessions for cases with deficits in pattern discrimination. The tone onset task involved a silent safe period and 10 sec warning periods filled with tone pairs (high-high). Frequency discriminations consisted of safe periods filled with 3.78 kHz tone pairs (low-low) and warning periods filled with 4.22 k H z tone pairs (high-high). The intensity and frequency of the tones were the same as described for tonal patterns. 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, therefore, it was necessary to estimate the level of spontaneous crossing responses. This was done by considering the safe periods between 60 and 300 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

CORTEX AND AUDITORY PATTERNS

75

total number of trials during the safe period. The percentage of spontaneous crosses for each daily session was compared to the percentage of correct responses.

Surgical and histologicalprocedure During surgery the animals were deeply anesthetized with pentobarbital sodium and bilateral cortical lesions were made by subpial aspiration. Two weeks were allowed for postoperative recovery before training was begun. When all training sessions had been completed the animals were again anesthetized with pentobarbital sodium, the temporal muscles were retracted, and the ectosylvian gyrus was exposed. Evoked potentials were recorded using a silver ball electrode placed on the cortical surface at various locations along the primary auditory cortex, A I. A reference electrode was inserted into subcutaneous tissue. The potentials evoked by a loud click were amplified and displayed on an oscilloscope. Recordings were made successively from right and left hemispheres with the location of the stimulus contralateral to the exposed hemisphere. The recordings allowed identification of the presence or absence of short latency, surface positive cortical potentials which are typical of normal animals under these conditions. Following electrophysiological sessions the animals were perfused through the carotid artery with isotonic saline and 1 0 ~ formalin. The brains were removed and embedded in nitrocellulose. Frontal sections were cut at a thickness of 50 #m. Every fourth section was stained with cresyl violet. Additional sections were stained through the region of the posterior thalamus. The extent of cortical damage was reconstructed by lateral projection of frontal sections for each brain. The extent of damage to right and left hemispheres was then translated to standard diagrams for the purpose

Fig. 2. Illustration of the extent of cortical lesions in 7 cats. The standard view of each hemisphere was derived from individual reconstructions. Left hemisphere is shown on left of figure for each animal.

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KELLY

CAT 4 7 R

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Fig. 3. The extent of thalamic degeneration in cat 47 for right and left sides of the brain. Shaded area represents areas of total or partial degeneration. Small numbers correspond to individual sections. Distance between sections is 200/zm. Abbreviations: G.M., medial geniculate; G.L., lateral geniculate; L.P., lateral posterior nucleus; Po., posterior thalamic nucleus. of illustration. The condition of the posterior thalamic nuclei was examined and the extent of retrograde degeneration was noted for each case. External and middle ears were dissected and examined for abnormalities. RESULTS

Anatomical results The extent of insular-temporal lesions in each of the 7 cases is shown in Fig. 2. In 4 animals, 47, 41, 56, and 46, the lesions included both insular and temporal cortex in right and left hemispheres and were generally larger than lesions in the remaining 3 cases. The underlying claustrum was partially damaged in cats 47, 41, 56, and 46 and to a lesser extent in cat 57. No substantial damage was seen in other subcortical areas. In examining the extent of damage to neocortical tissue the possibility was considered that areas of auditory cortex other than the insular and temporal regions were damaged indirectly, and that lateral projections of directly damaged tissue grossly underestimated the functional extent of the lesion. Two lines of evidence indicated that the extent of indirect damage of this sort was not great. First, for each of the animals including the 4 with large lesions it was possible to record surface

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Fig. 4. The extent of thalamic degeneration in cat 41. Symbols as in Fig. 3. positive evoked potentials along the anterior-posterior extent of A I. The only exception noticed was the lack of surface positive responses for some locations in anterior A I in cat 46. Positive responses were seen in posterior A I in this case, however, indicating that thalamocortical connections were still present. A second source of evidence reflecting the lack of damage to dorsal auditory areas comes from examination of thalamic degeneration. The extent of retrograde degeneration in each of the 4 cases with large lesions is shown in Figs. 3-6. Without exception the anterior portion of the medial geniculate which is known to degenerate following lesions of A I and A I I was normal in appearance. Degenerative changes were present in each of these cases only in the posterior part of the medial geniculate which is consistent with the idea that cortical damage was largely restricted to the ventral auditory areas 5. Study of thalamic nuclei for the remaining 3 cases with smaller lesions revealed no degenerative changes in the medial geniculate. Behavioral results Behavioral records for the 4 animals with large insular-temporal lesions are shown in Figs. 7-10. The sequence of tests represented in these figures includes preoperative acquisition of frequency modulated and two-tone patterns, postoperative

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tests with FM and two-tone patterns, and finally discriminations of stimulus onset and frequency change. Tests of normal cats indicated that the two types of pattern discrimination were easily acquired provided the FM pattern was learned before the two-tone one. With this sequence of testing the two tasks were acquired at approximately the same rate for each of the animals. Postoperative tests of FM patterns revealed in 3 of the 4 animals (Figs. 7-9) a clear-cut ability to discriminate rising from falling FM tones. Each of the animals relearned the discrimination without signs of any prolonged impairment in discriminative ability. To insure that the animals' performance was reliable additional sessions were added after the animals reached 9 0 ~ correct responses in 2 successive days. Each animal was capable of maintaining his performance well above a chance level during these sessions. A fourth animal, cat 46, with lesions very similar to the other 3 cats, was found to have a prolonged postoperative difficulty with FM patterns (see Fig. 10). This animal failed to reach criterion performance with 45 sessions but did show some improvement during the last 10 sessions. The interpretation of the behavioral record in this case is complicated by the presence of accumulated wax in the external ear canals which may have produced some peripheral hearing loss. Following tests with FM patterns, each of the 4 animals was immediately transferred to two-tone patterns. As can be seen in Figs. 7-10 there was a severe postoperative impairment in this discrimination which was still present after 50 consecutive testing sessions. None of the animals reached a criterion of 9 out of l0 correct responses during these sessions and with the possible exception of several sessions in the record of cat 41 (see Fig. 8) performance levels remained at chance during the entire test period. Also close observation of the behavior of the cats during discrimination trials failed to reveal any other behavioral signs of detection such as orienting or alerting responses. In spite of this general lack of responsiveness to tonal patterns the animals were still capable of detecting and responding to the onset of a tone and discriminating between two tones of different frequency. Postoperative performance on these tasks was very good for cats 41, 47 and 56. The performance for cat 46 was somewhat worse, although it was readily demonstrated that the animal could respond to tones and discriminate between frequencies in spite of the possible peripheral hearing loss mentioned above. Figs. 11-13 show behavioral records for 3 additional cases with lesions in the temporal area alone (cats 28 and 29) or in the anterior insular area (cat 57). It is quite clear from the ease with which these animals could discriminate either FM patterns or two-tone patterns postoperatively that destruction of neither of these areas had effects comparable to the larger insular-temporal lesions. In fact examination of the general lack of impairment following these smaller lesions provides an important comparison in assessing the severity of deficits in cats 41, 47, 56 and 46. DISCUSSION

The effects of insular-temporal cortical lesions have been tested using two different types of auditory pattern discrimination and discrimination of tone onset

CORTEX AND AUDITORY PATTERNS

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and frequency changes. Although animals with insular-temporal lesions can easily discriminate between two sound frequencies, low and high, they show impairments in discriminating temporal patterns of sounds. This is consistent with observations of Goldberg e t aL 9 who used auditory patterns composed of pure tone triads with frequencies of 800 and 1000 Hz. It is also consistent with reports of deficits in similar discriminations of temporally organized visual patterns of high and low intensity 2

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and auditory pattern discriminations using different training methods a. The fact that severe deficits occur in our discriminations of tone dyads indicates that neither the simplicity of the pattern nor the specific sound frequencies involved are particularly crucial factors in characterizing the effects of insular-temporal lesions. On the other hand, we find that the severity of deficit in auditory pattern discriminations is dependent upon the type of temporal configuration employed. FM patterns of rising and falling tones are less severely affected than are simple two-tone patterns of low-high v s . high-low frequencies even though the stimuli are selected to match each other closely with respect to such particulars as frequency range, duration, and direction of frequency change. A similar difference in results is seen following bilateral lesions of auditory cortical areas, A I, A II, Ep6,10. Thus there would seem to be a basic difference between these two types of auditory discrimination. One possible factor in the differences in postoperative performance is the relative ease of learning the two discriminations preoperatively. As was pointed out by Kelly and Whitfield1°, discriminations of FM patterns are rapidly learned by normal animals, whereas discriminations of pure tone triads seem to be more slowly acquired. In the present study it was found that if a normal animal first learned to discriminate between FM patterns, the animal would subsequently learn to discriminate between two-tone patterns in approximately the same number of sessions. In this sense it can

CORTEX A N D AUDITORY PATTERNS

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be said that the two discriminations are of equal difficulty. It should be pointed out, however, that different rates of acquisition might be expected for FM and pure tone pattern discriminations if the sequence of testing is altered. Indeed, our observations of cats trained initially to discriminate between tone pairs suggest that this task requires more sessions to learn than FM patterns (unpublished results). Under these conditions of testing the slight differences between the stimulus configurations in the two tasks can impose differences in acquisition rate. The most obvious difference between the FM tones and the two tone patterns used in the present study is the continuity of the frequency changes involved. In the case of FM patterns there is a continuous change in frequency which is perceived by human observers as a single event. Corresponding to this frequency change one would expect a continuous change in the pattern of activity along the basilar membrane in such a way that interaction might occur at a relatively low level of the auditory pathway. Indeed there is evidence that neural interaction does occur between neurons stimulated by FM tones resulting in a directional sensitivity of single neurons located in various auditory nuclei v,s,11,12,1a. In contrast, pure tone patterns involve a discontinuous frequency change. The two tones are perceived as separate events grouped together to form a pair. Although little is known at present about neural interactions associated with two-tone patterns 1, it is reasonable to believe that the neural events initiated by the two tones are more likely to remain independent and have less chance for interaction than with FM stimuli at least at peripheral levels of the auditory system. The degree of subcortical interaction associated with continuous and discontinuous patterns may be related to the severity of behavioral effects produced by insular-temporal lesions. In any case the effects of insular-temporal lesions are quite severe for pure tone patterns and are less pronounced for discriminations of directional FM patterns. ACKNOWLEDGEMENTS

This study was supported by the National Research Council of Canada. The author would like to thank Robert Gray and Cheryl Stark for technical assistance.

REFERENCES

1 ABELES, M., AND GOLDSTEIN, M . H . , Responses of single units in the primary auditory cortex of the cat to tones and to tone pairs, Brain Research, 42 (1972) 337-352. 2 COLAVITA,F. B., Auditory cortical lesions and visual pattern discrimination in cat, Brain Research, 39 (1972) 437-447. 3 CORNWALL,P., Loss of auditory pattern discrimination following insular-temporal lesions in cats, J. comp. physiol. Psychol., 63 (1967) 165-168. 4 DEWSON, J. H., Speech sound discrimination by cats, Science, 144 (1964) 555-556. 5 DIAMOND,I. T., CHOW, K. L., AND NEFF, W. n., Degeneration of caudal medial geniculate body following lesions ventral to auditory area II in cat, J. comp. Neurol., 109 (1958) 349-362. 6 DIAMOND, I. T., AND NEFF, W. n., Ablation of temporal cortex and discrimination of auditory patterns, J. Neurophysiol., 20 (1957) 300-315.

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