Physiological Correlates of Perceptual Deficits Following Sensorineural Hearing Loss

Introduction Several translational issues related to sensorineural hearing loss (SNHL) have recently re-invigorated an active debate in the field of psychological and physiological acoustics regarding the perceptual role of the temporal structure of sound. Much of this recent interest over the last decade has centered on the mathematical fact that any sound can be separated into slowly-varying temporal envelope (ENV) and rapidly varying temporal fine-structure (TFS) components (Fig. 1). This dichotomy has been motivated in part from cochlear implants, which are neural prostheses that can restore the sense of hearing for patients with profound deafness through electrical stimulation of remaining cochlear neurons. Although often quite successful in understanding speech in quiet conditions, cochlear-implant patients often struggle to understand speech in noisy conditions or to appreciate music. These limitations have motivated numerous perceptual studies to understand the relative importance of ENV and TFS cues because cochlear implants currently only provide slowly varying ENV cues and are unable to provide rapidly varying TFS cues. Envelope cues have been shown to be sufficient for understanding speech, even in a minimal number of frequency bands (Shannon et al., 1995; Smith et al., 2002). Fine structure has been argued to be useful for music perception, sound localization, lexical-tone perception, and source segregation (Smith et al., 2002; Xu and Pfingst, 2003; Qin and Oxenham, 2005). Such findings have been given as motivation for efforts to develop cochlear-implant strategies to provide fine-structure in addition to envelope cues (e.g., Rubinstein et al., 1999; Nie et al., 2005). It is also believed that the use of temporal fine structure relates to the remarkable ability of normal-hearing listeners to “listen in the dips” of background sounds, e.g., in the presence of concurrent talkers (Moore and Glasberg, 1987; Schooneveldt and Moore, 1987). In contrast, listeners with SNHL often face great difficulty in understanding speech in the presence of temporally varying backgrounds (Peters et al., 1998), and this difficulty is only partially resolved with advanced amplification algorithms (Moore et al., 1999). A number of recent perceptual studies suggest that listeners with SNHL have a reduced ability to use TFS cues, and that this deficit may be correlated with their inability to listen in the dips (Lorenzi et al., 2006; Moore et al., 2006; Hopkins and Moore, 2007). These results have fueled an active debate about the role of temporal coding in normal and impaired hearing, and have important implications for improving the ability of hearing aids and cochlear implants to restore speech perception in noise. However, the translational implications of perceptual deficits in temporal processing with SNHL depend critically on their physiological basis, which unfortunately remains unknown. The most straightforward hypothesis is that auditory-nerve fibers, which provide all of the information at the output of the cochlea (Fig. 2), are no longer able to encode the rapidly varying TFS information following SNHL. Prior to our recent studies, the physiological evidence regarding auditory nerve (AN) fiber phase locking with SNHL was conflicting (Harrison and Evans, 1979; Woolf et al., 1981; Miller et al., 1997). Thus, a number of important questions exist: (1) are TFS coding deficits peripheral or central, and (2) is it the quantity and/or quality of TFS coding that is diminished following SNHL? This article describes recent work in our lab exploring the physiological bases for these perceptual results through a combination of neurophysiological, perceptual, and computational modeling approaches. Specifically, we have been exploring three hypotheses for the physiological bases of perceptual TFS deficits: (1) the temporal coding within individual AN fibers is degraded in quantity and/or quality following SNHL, (2) even if there is not diminished phase locking in individual fibers, the relative temporal coding across AN fibers may be degraded in ways that diminish spatio-temporal cues that have been proposed to be perceptually relevant, and (3) the perceptual TFS deficits may not actually reflect diminished TFS coding in the periphery due to “artifacts” that complicate the separation of TFS and ENV cues within the cochlea. Overall, our results suggest that the fundamental ability of fibers to phase lock to temporal fine structure is not degraded by SNHL; however, a number of other effects of SNHL have been observed that may contribute to perceptual deficits in temporal processing of complex stimuli. These results have important translational implications for auditory prostheses because they suggest that perceptual “fine-structure deficits” do not simply reflect degraded phase locking, but likely involve more complicated coding mechanisms. “The translational