Auditory cortex lesions and auditory-visual associative learning in cats.
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Biomedical subjects
Publications and source records attributed to J L Cranford.
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In recent years, a number of investigators have provided evidence that the auditory cortex has a critical role in both the detection and discrimination of brief sounds. Dogs and humans with lesions of the neocortical auditory centers have been reported to exhibit significantly elevated detection thresholds for signals shorter than 16 ms in duration. In tests of frequency discrimination, the same subjects also exhibited severe deficits whenever tonal signals were less than 20--40 mn in lengths. In the present report, we present evidence brief tones. Operated cats, while exhibiting normal difference limens for 1-kHz tones of 100-ms duration, have significantly elevated limens for discriminating tones of 8- and 2-ms duration. With further testing, the same operated cats can be shown to have normal absolute thresholds for detecting brief tones.
1. A currently unresolved question concerning the effects of auditory decortication on sound localization is whether or not operated animals have a normal capacity for discriminating the small interaural differences in phase angle or intensity that result from the spatial separation of sound sources relative to the head. The present experiment was designed to provide data relevant to this question. 2. Four normal and three operated cats (bilateral ablations of AI, AII Ep, SII, I-T), wearing stereo headsets, were tested with an active avoidance procedure to detect reversals in the interaural phase-angle or intensity relations of binaural 1-kHz tones. For both groups of cats, the detection thresholds for interaural intensity and phase angle were found to be close to 1 dB and 5 degrees, respectively. 3. In addition, we found that both unoperated and operated cats exhibited positive transfer from the original lateralization task involving the detection of interaural reversals of phase angle or intensity to a new test, which required the cats to identify, in an absolute sense, which ear received the leading or louder signals. 4. Thus, the present investigation provides additional evidence that the neocortex has no primary sensory role in sound localization.
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Anterograde degeneration resulting from small lesions placed in either the insular or temporal cortex were traced with the Fink-Heimer reduced silver procedure. In neocortical regions ipsilateral to the lesion axonal degeneration was present in auditory subdivisions AI, AII, Ep, I, T, in the second somatosensory area (SII), in the anterior and middle suprasylvian gyrus, in the posteromedial suprasylvian and posterior lateral gyri, in the posterior splenial gyrus, in the anterior two-thirds of the cingulate gyrus and in the orbitofrontal regions. With respect to interhemispheric connections, evidence was obtained for a dual pattern of projection. In addition to significant amounts of axonal and terminal degeneration in the corresponding insular or temporal fields, axonal degeneration was also present in posterior AII. In the thalamus degeneration was found in the medial dorsal, suprageniculate, and lateral posterior-pulvinar nuclei. In the posterior nuclear group (Po) and the principal division of the medial geniculate (GMp) evidence was obtained for a topographic pattern of projection; significantly more degeneration occurred in caudal Po following insular lesions whereas with temporal lesions more degeneration occurred in caudal GMp. Degeneration was also found in the dorsal cortex of the ipsilateral inferior colliculus, bilaterally in the deep layers of the superior colliculus and the periventricular central gray region, ipsilaterally in the ventromedial aspects of the head and body of the caudate nucleus, and in the lateral and central nuclei of the amygdala. These findings are discussed in terms of their significance for a possible role for the insular and temporal neocortex (I-T) in both multimodal sensory discrimination and sensory-visceral integrative functions.
Six experimental and 3 unoperated cats were trained with a go, no-go shock avoidance procedure to discriminate increases from decreases in the rate of presentation of all auditory cortex between the suprasylvian sulcus and rhinal fissure while 3 cats had bilateral auditory cortex lesions plus ablation of the cortex of the anterior lateral and anterior and middle suprasylvian gyri. A sixth 'naive' experimental cat received the present tests only after recovery from a bilateral auditory cortex ablation. After bilateral lesions, 5 of the experimental cats unexpectedly made no errors on no-go trials during retraining. This contrasts with their preoperative performance, as well as the performance of the 3 unoperated and the 'naive' operated cat, in which training was required for the successful discrimination of the two types of trials. This suggests that the neocortex may be more critical for mediating active 'go' responses to auditory stimuli than in preserving a memory for the difference between go and no-go stimuli. Further testing revealed that the thresholds of the operated cats did not differ from normal cats. All cats discriminated rates of 4/sec versus 6/sec clicks both with and without a neutral 5/sec background at levels significantly above chance.
The 'precedence effect' in sound localization refers to the situation in which two speakers, separated in space, emit identical sounds but one speaker leads by a few milliseconds. Normal observers perceive all the sound as originating from the leading speaker. In the present experiment cats were tested before and after unilateral ablation of auditory cortex on how well they could transfer a learned sound loclization response from situations involving unpaired sound sources to those with paired sources. Cats were tested with tone pairs separated by 5 msec and with clicks separated by delays of 3, 5, 7, 9, 12 and 16 msec. Preoperatively, the cats averaged 98% correct at a delay of 3 msec and 58% correct at 16 msec. Before surgery the probability of an error was independent of which speaker was leading; after surgery cats made significantly more errors when the leading speaker was located opposite the side of the lesion. Considerable individual variability was found with the 3 and 5 msec delay tests; some cats showed no evidence of a cortical deficit while others exhibited initial severe deficits which disappeared with training. At delays of 7-16 msec all cats showed severe directional deficits which were still present after 9 months of retraining. Results are interpreted as supporting the hypothesis that unilateral lesions disrupt binaural loudness rather than temporal relations.
Cats with earphones were trained with a shock avoidance procedure to detect the occurrence of 1 kHz tone pulses at one ear while continuous noise pulses were simultaneously presented to the opposite ear. For normal cats the presence of the noise produced a mean increase of 5.4 dB in the thresholds for detection of tones at the opposite ears. After large unilateral auditory cortex ablations the same cats exhibited an asymmetry between the ears in the size of the contralateral masking effect. There was a mean increase of 10.9 dB in the detection thresholds for tones at the ear contralateral to the damaged hemisphere when noise was presented to the ear opposite the intact hemisphere. Noise of the same physical intensity when presented to the ear contralateral to the damaged cortex produced no significant changes from the preoperative masking levels. Subsequent ablation of the auditory cortex of the opposite hemisphere resulted in a cancellation of the unilateral lesion effect; the cats exhibited interaurally symmetrical masking levels of the same magnitude as those observed prior to the first operation. Additional control tests indicate that the unilateral lesion effect is a central nervous system phenomenon and is specific to lesions of auditory cortex.
Four cats were trained to avoid shock by responding to the intermittent occurrence of 1-kHz tone pulses at one ear, while a continual train of noise pulses was simultaneously presented either to the signal ear alone or to both ears. Using the masked threshold levels determined with monaural noise as a reference, the amount of unmasking produced by the addition of noise to the nonsignal ear was measured. Significantly lower tonal detection thresholds were observed when noise equal in intensity to that at the signal ear was added to the nonsignal ear. Additional unmasking occurred when the intensity of the noise at the latter ear was raised to a level 10 db. higher than that at the signal ear.
This report describes the results in cats of a visual-auditory dual modal experiment after translateral olivo-cochlear bundle ablation at the floor of fourth ventricle. Subjects were behaviorally conditioned (avoidance) to respond in a shuttle box to show that they detected changes in ambient light intensity during the existence of intense background noise. With the given experimental paradigm, no noticeable difference was found between the response of the experimental animals and those of animals that underwent sham operation.
The present report describes the frequency discrimination capability of the cat based on behavioral auditory measurements in conjunction with transection of the crossed olivo-cochlear bundle at the floor of the fourth ventricle. Using the repetitive method, cats were trained to respond to frequency differences from 8000 Hz. For the measurement of the frequency discrimination threshold, instead of using the descending method, the cats were trained to detect the absolute change in the frequency. With the given experimental paradigm, the average pre- and post-operative frequency discrimination thresholds were 114.3 Hz and 133.6 Hz in experimentals, and 128.3 Hz and 140.0 Hz in shams. Differences between the two groups were minimal and may simply represent functional biological variance.
This report describes the cat's ability to discriminate pure-tone intensity differences after transection of the crossed olivo-cochlear bundle at the floor of the fourth ventricle. Cats were trained by behavioral (avoidance) conditioning to detect intensity difference above 75 dB re 0.0002 dyne/cm2 of 10 000 Hz tones, using the repetitive method. Postoperative comparison of data from 5 experimental animals and 5 sham-operated control animals showed minimal differences which reflects merely functional biological variance. Neurohistological examination confirmed the accuracy of the lesion placement.