Neural Processing of Acoustic and Electric Interaural Time Differences in Normal-Hearing Gerbils

Bilateral cochlear implants (CIs) provide benefits for speech perception in noise and directional hearing, but users typically show poor sensitivity to interaural time differences (ITDs). Possible explanations for this deficit are deafness-induced degradations in neural ITD sensitivity, between-ear mismatches in electrode positions or activation sites, or differences in binaural brain circuits activated by electric versus acoustic stimulation. To identify potential limitations of electric ITD coding in the normal-hearing system, responses of single neurons in the dorsal nucleus of the lateral lemniscus and in the inferior colliculus to ITDs of electric (biphasic pulses) and acoustic (noise, clicks, chirps, and tones) stimuli were recorded in normal-hearing gerbils of either sex. To maintain acoustic sensitivity, electric stimuli were delivered to the round window. ITD tuning metrics (e.g., best ITD) and ITD discrimination thresholds for electric versus transient acoustic stimuli (clicks, chirps) obtained from the same neurons were not significantly correlated. Across populations of neurons with similar characteristic frequencies, however, ITD tuning metrics and ITD discrimination thresholds were similar for electric and acoustic stimuli and largely independent of the spectrotemporal properties of the acoustic stimuli when measured in the central range of ITDs. The similarity of acoustic and electric ITD coding on the population level in animals with normal hearing experience suggests that poorer ITD sensitivity in bilateral CI users compared with normal-hearing listeners is likely due to deprivation-induced changes in neural ITD coding rather than to differences in the binaural brain circuits involved in the processing of electric and acoustic ITDs.

SIGNIFICANCE STATEMENT Small differences in the arrival time of sound at the two ears (interaural time differences, ITDs) provide important cues for speech understanding in noise and directional hearing. Deaf subjects with bilateral cochlear implants obtain only little benefit from ITDs. It is unclear whether these limitations are due to between-ear mismatches in activation sites, differences in binaural brain circuits activated by electric versus acoustic stimulation, or deafness-induced degradations in neural ITD processing. This study is the first to directly compare electric and acoustic ITD coding in neurons of known characteristic frequencies. In animals with normal hearing, populations of auditory brainstem and midbrain neurons demonstrate general similarities in electric and acoustic ITD coding, suggesting similar underlying central auditory processing mechanisms.