Abstract
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 activity 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.
Highlights
Perception is a delicate chain of events including conversion of a sensory stimulus into electrical signals at the receptor level, transmission of the electrical signals via the peripheral nerve, and processing and interpretation of the electrical signal in the CNS
In the inner ear and the auditory nerve leads to threshold elevation, abnormal loudness, pitch, and temporal processing (Buss et al 1998; Formby 1986; Moore 1996; Moore and Oxenham 1998; Nienhuys and Clark 1978; Oxenham and Bacon 2003; Prosen et al 1981; Ryan and Dallos 1975); central disorders and degeneration produce complex processing deficits in speech and sound object recognition (Cacace and McFarland 1998; Gordon-Salant and Fitzgibbons 1999; Levine et al 1993; Wright et al 1997); and electric stimulation of the auditory nerve via a cochlear implant in deaf persons results in fundamental changes in the brain affecting behaviors ranging from basic psychophysics to language development (Giraud et al 2001; Simmons et al 1965; Svirsky et al 2000; Zeng and Shannon 1994)
The auditory neuropathy (AN) subjects showed slightly larger difference limens at low levels than the normal controls, no significant main effect was observed between groups [F(1,69) ϭ 3.17; P Ͼ 0.05]
Summary
Perception is a delicate chain of events including conversion of a sensory stimulus into electrical signals at the receptor level, transmission of the electrical signals via the peripheral nerve, and processing and interpretation of the electrical signal in the CNS. Examination of the above-mentioned studies shows that detailed documentation of behavioral changes coupled with a clearly defined pathology can make significant contributions in two important ways These studies often lead to better diagnosis and management of a particular disease. We focus on perceptual consequences of a recently defined hearing disorder that preserves the outer hair cell function but apparently disrupts auditory nerve activity. This hearing disorder was first described in one single subject and considered to involve a dysfunction of the auditory nerve (Starr et al 1991). The group difference between the AN and normal-hearing control subjects is emphasized here, interesting individual cases will be presented to highlight the perceptual consequences of disrupted auditory nerve activity
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