Subcortical Neural Synchrony and Absolute Thresholds Predict Frequency Discrimination Independently

F. Marmel,R. P. Carlyon,C. J. Plack,D. Linley,K. Hopkins,H. E. Gockel

doi:10.1007/s10162-013-0402-3

Abstract

The neural mechanisms of pitch coding have been debated for more than a century. The two main mechanisms are coding based on the profiles of neural firing rates across auditory nerve fibers with different characteristic frequencies (place-rate coding), and coding based on the phase-locked temporal pattern of neural firing (temporal coding). Phase locking precision can be partly assessed by recording the frequency-following response (FFR), a scalp-recorded electrophysiological response that reflects synchronous activity in subcortical neurons. Although features of the FFR have been widely used as indices of pitch coding acuity, only a handful of studies have directly investigated the relation between the FFR and behavioral pitch judgments. Furthermore, the contribution of degraded neural synchrony (as indexed by the FFR) to the pitch perception impairments of older listeners and those with hearing loss is not well known. Here, the relation between the FFR and pure-tone frequency discrimination was investigated in listeners with a wide range of ages and absolute thresholds, to assess the respective contributions of subcortical neural synchrony and other age-related and hearing loss-related mechanisms to frequency discrimination performance. FFR measures of neural synchrony and absolute thresholds independently contributed to frequency discrimination performance. Age alone, i.e., once the effect of subcortical neural synchrony measures or absolute thresholds had been partialed out, did not contribute to frequency discrimination. Overall, the results suggest that frequency discrimination of pure tones may depend both on phase locking precision and on separate mechanisms affected in hearing loss.

Highlights

The neural mechanisms of pitch, the sensation whose variation is associated with melodies (Plack 2005), have been debated for more than a century
The aforementioned frequency-following response (FFR) studies relating neural phase locking to frequency discrimination focused on normal-hearing listeners: The current study investigated the relation between FFR neural phase locking and frequency difference limens (FDLs) in listeners with normal as well as with elevated hearing thresholds
The association between absolute thresholds and frequency discrimination could not be attributed to confounding effects of FFR synchronization strength or age: absolute thresholds were significantly correlated with FDLs even when both FFR synchronization strength and age were partialed out (r23 =0.50, P=0.011)

Summary

Introduction

The neural mechanisms of pitch, the sensation whose variation is associated with melodies (Plack 2005), have been debated for more than a century (de Cheveigné2005). Possible mechanisms rely on the profiles of neural firing rates across auditory nerve fibers with different characteristic frequencies (place-rate coding), and on the temporal firing patterns of auditory neurons that phase lock to sound periodicities (temporal coding). For low-frequency pure tones (up to 4–5 kHz), temporal mechanisms based on phase locking are thought to be dominant For listeners with a cochlear hearing loss (CHL), the generally observed degradation in frequency discrimination is not well explained in terms of frequency selectivity (Tyler et al 1983; Moore and Peters 1992). Impaired frequency difference limens (FDLs) in CHL listeners may be better accounted for in terms of reduced phase locking precision than in terms of rateplace code degradation. In animals, Harrison and Evans (1979) did not observe phase locking deterioration following drug-induced loss of outer hair cells in guinea pigs, but Woolf et al

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