Perceptual Consequences of Disrupted Auditory Nerve Activity
Fan-Gang Zeng, Ying-Yee Kong, Henry J. Michalewski, Arnold Starr
Journal of Neurophysiology
Perceptual consequences of disrupted auditory nerve activity were systematically studied in 21 subjects who had been clinically diagnosed with auditory neuropathy (AN), a recently defined disorder characterized by normal outer hair cell function but disrupted auditory nerve function. Neurological and electrophysical evidence suggests that disrupted auditory nerve activity is due to desynchronized or reduced neural activity or both. Psychophysical measures showed that the disrupted neural
... y has minimal effects on intensity-related perception, such as loudness discrimination, pitch discrimination at high frequencies, and sound localization using interaural level differences. In contrast, the disrupted neural activity significantly impairs timing related perception, such as pitch discrimination at low frequencies, temporal integration, gap detection, temporal modulation detection, backward and forward masking, signal detection in noise, binaural beats, and sound localization using interaural time differences. These perceptual consequences are the opposite of what is typically observed in cochlear-impaired subjects who have impaired intensity perception but relatively normal temporal processing after taking their impaired intensity perception into account. These differences in perceptual consequences between auditory neuropathy and cochlear damage suggest the use of different neural codes in auditory perception: a suboptimal spike count code for intensity processing, a synchronized spike code for temporal processing, and a duplex code for frequency processing. We also proposed two underlying physiological models based on desynchronized and reduced discharge in the auditory nerve to successfully account for the observed neurological and behavioral data. These methods and measures cannot differentiate between these two AN models, but future studies using electric stimulation of the auditory nerve via a cochlear implant might. These results not only show the unique contribution of neural synchrony to sensory perception but also provide guidance for translational research in terms of better diagnosis and management of human communication disorders. Gordon-Salant S, and Fitzgibbons PJ. Profile of auditory temporal processing in older listeners. J Speech Lang Hear Res 42: 300 -311, 1999. Hall JW, Tyler RS, and Fernandes MA. Factors influencing the masking level difference in cochlear hearing-impaired and normal-hearing listeners. J Speech Hear Res 27: 145-154, 1984. Hallpike CS, Harriman DG, and Wells CE. A case of afferent neuropathy and deafness. J Laryngol Otol 94: 945-964, 1980. Harrison RV. An animal model of auditory neuropathy. Ear Hear 19: 355-361, 1998. Hausler R, Colburn S, and Marr E. Sound localization in subjects with impaired hearing. Spatial-discrimination and interaural-discrimination tests. Acta Otolaryngol Suppl 400: 1-62, 1983. Hawkins DB and Wightman FL. Interaural time discrimination ability of listeners with sensorineural hearing loss. Audiology 19: 495-507, 1980. Heinz MG, Colburn HS, and Carney LH. Evaluating auditory performance limits: I. One-parameter discrimination using a computational model for the auditory nerve. Neural Comput 13: 2273-2316, 2001a. Heinz MG, Colburn HS, and Carney LH. Evaluating auditory performance limits: II. One-parameter discrimination with random-level variation. Neural Comput 13: 2317-2338, 2001b. Joris PX. Envelope coding in the lateral superior olive. II. Characteristic delays and comparison with responses in the medial superior olive. J Neurophysiol 76: 2137-2156, 1996. Joris PX, Smith PH, and Yin TC. Coincidence detection in the auditory system: 50 years after Jeffress.