William D. Neff

Behavioral Studies of Auditory Discrimination: Central Nervous System

For convenience of review, the history of research that has used behavioral tests before and after ablation of auditory centers or transection of neural pathways in order to understand the neural basis of auditory discrimination*1 may be divided into four periods; each period represents a time during which new methods were being developed that led to new information: (A) 1860–1900; (B) 1900–1930; (C) 1930–1940; (D) 1940–1975. Throughout all of these periods, advance in knowledge depended upon progress along a number of lines, principally the following: (1) refinement of methods used to trace neural pathways and identify neural centers, (2) development of adequate methods by which to measure auditory discriminations, (3) improvement of surgical techniques.

Sound localization: the role of the commissural pathways of the auditory system of the cat

Abstract Three main commissural pathways transmit auditory information from one side of the brain to the other. They are the trapezoid body, the commissure of the inferior colliculus and the corpus callosum. The present experiment was an attempt to determine whether one or more of these commissures are part of a neural mechanism that encodes the binaural auditory cues which enable an animal to localize sound in space. The accuracy with which cats can localize sound was determined by behavioral methods. Then in separate operations the trapezoid body, the commissure of the inferior colliculus and the corpus callosum were transected; the order of these operations varied from animal to animal. After each operation, the animals accuracy at localizing sound was again determined. The only operations that had any effect on localization ability were those in which transection of the trapezoid body was attempted. Transection of the commissure of the inferior colliculus or of the corpus callosum, or of both, had no observable effect on localization ability. We concluded that: (1) the auditory pathways in the medulla appear to transmit information important for localization of sound, and (2) neither the corpus callosum nor the commissure of the inferior colliculus appears to carry this information.

Efferent projections of the insular and temporal neocortex of the cat

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.

Inner ear damage and hearing loss after exposure to tones of high intensity.

Experimental animals (cats) were exposed to tones of 125, 1000, 2000, and 4000 Hz at sound pressure levels in the range 120 to 157.5 dB, and for durations of one hour (1000, 2000, 4000 Hz) or four hours (125 Hz). Pure tone audiograms were obtained for each animal before and after exposure. Post-exposure tests were continued until complete recovery of hearing had occurred or until a stable permanent threshold shift had been measured. Cochleas of animals were examined by phase-contrast microscopy; condition of all hair cells was recorded. Extent of inner-ear damage and range of frequencies for which hearing loss occurred increased as exposure tone was decreased in frequency. For example, exposure to 4000 Hz produced damage in a restricted region of the cochlea and hearing loss for a relatively narrow range of frequencies; exposure to 125 Hz produced wide-spread inner ear damage and hearing loss throughout the frequency range 125 to 6000 Hz.

Auditory Information from Subcortical Electrical Stimulation in Cats

Animals trained to respond to sound stimuli were found to perform the learned response when they were electrically stimulated through electrodes chronically implanted in subcortical structures of the auditory pathway. Other animals trained to respond to electrical stimulation of subcortical auditory structures showed differential transfer effects depending on the positions of the stimulating electrodes.

Neural structures mediating differential sound intensity discrimination in the cat

Abstract Nine cats were trained to discriminate changes in intensity of a 1000 c/sec tone. Differential intensity limens were measured. Limens were redetermined following (1) unilateral and bilateral 2-stage ablation of auditory cortex, (2) bilateral section of the brachium of the inferior colliculus, (3) bilateral ablation of the inferior colliculus, and (4) bilateral cortical ablation in combination with one or the other subcortical lesion. Four cats needed retraining after bilateral cortical ablation, but had little or no change in limen. No significant loss was seen after removal of the inferior colliculus. In 3 animals with both cortical and inferior colliculus lesions, the differential intensity limen was elevated by 5.0–6.8 dB. Bilateral section of the brachium of the inferior colliculus caused elevation of the differential limen by about 10 dB. One animal subsequently given a cortical showed no further impairment. Another cat given a bilateral grachium lesion following prior cortical ablations had a 20 dB threshold elevation. This cat sustained extensive damage in the midbrain tegmentum in addition to destruction of the acoustic brachium. Findings that lesions of the brachium of the inferior colliculus caused greater losses than either cortical or inferior colliculus lesions are attributed to interruption of extralemniscal fiber systems which bypass the inferior colliculus as well as the medial geniculate body and its cortical projection field.

Sequential auditory and visual discriminations after temporal lobe ablation in monkeys

Studies in the monkey have shown that cortex outside of the primary projection areas in the superior temporal gyrus and in the inferotemporal region in important for the execution of some auditory and visual descriminations. In this study, six monkeys were trained to perform four auditory and two visual discriminations. Retention tests were given prior to bilateral removal of the anterior part of the lateral surface of the superior temporal gyrus, the inferotemporal region, or both areas together. Superior temporal ablations elicited severe deficits on some auditory discriminations. Inferotemporal ablations caused little or no impairment on visual discriminations. This negative finding is attributed to the sequential rather than spatial mode of presentation of visual stimuli, and to overtraining. A single monkey trained on a spatial visual pattern problem without overtraining was impaired. Another monkey tranied to perform an auditory reverse intensity discrimination exhibited a deficit in ability to perform the problem after removal of auditory cortex within the lateral fissure.

The Brain and Hearing: Auditory Discriminations Affected by Brain Lesions

After bilateral ablation of the auditory areas of the cerebral cortex, experimental animals have a severe deficit in ability to discriminate between temporal patterns of tonal stimuli and to localize sound in space. These two kinds of discrimination are basic for communication and for attack or avoidance of prey and predator. Recognition of which ear is stimulated may also depend upon excitation of auditory cortex contralateral to the given ear. Binaural discriminations are dependent upon interaction of nerve impulses from the two ears at a low level in the auditory nervous system. Similar hearing losses have been reported for human patients.

The Medial Geniculate Body and Associated Thalamic Cell Groups: Behavioral Studies

Deficits in auditory discrimination aredescribed after cortical ablations that produce thalamic degeneration that differs in amount and in locus. The posterior region of the medial geniculate body app