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

Abstract

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 the inferior colliculus to ITDs of electric (biphasic pulses) and acoustic stimuli (noise, clicks, chirps, and tones) 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 to normal-hearing listeners is likely due to deprivation-induced changes in neural ITD coding rather than due to differences in the binaural brain circuits involved in the processing of electric and acoustic ITDs.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.

Microsecond Interaural Time Difference Discrimination Restored by Cochlear Implants After Neonatal Deafness

“…1b). As might be expected in light of previous studies investigating ITD sensitivity in the IC [22,24,28,29], we observed that the large majority of multi-units exhibited at least some, and at times substantial degrees of tuning to stimulus ITD.…”

“…1b). As might be expected in light of previous studies investigating ITD sensitivity in the IC [22,24,28,29], we observed that the large majority of multi-units exhibited at least some, and at times substantial degrees of tuning to stimulus ITD.The manner in which changes in ITD changed neural discharge patterns was also highly variable from one recording site to the next. While many multi-units showed typical shortlatency onset responses to the stimulus which varied in response amplitude ( Fig.…”

“…In the IC of our ND rats we found significant ITD sensitivity in 85% of recordings sites, compared to only 48% previously reported for congenitally deaf cats [22]. The proportion of ITD sensitive sites in our ND rats is thus more similar to reported proportions in adult deafened cats (84%-86%; [22,28]), rabbits (73%; [38]) or gerbils (at least 74%; [29]). Our Figure 2a also shows a relatively greater proportion of units showing ITD SNRs above 0.6 for our ND rats than for ND cats of [22].…”

Evaluating the Impact of Age, Acoustic Exposure, and Electrical Stimulation on Binaural Sensitivity in Adult Bilateral Cochlear Implant Patients

“…Studies with single-neuron recordings in non-human species provide insight into the role of acoustic exposure on binaural sensitivity. In acutely deafened animals, the encoding of neurally evoked ITDs presented through electrical stimulation of a CI can provide just as accurate encoding of ITDs as those presented with acoustic stimulation [ 26 ]. This finding suggests that the length of acoustic impairment might be a key factor contributing to poor vs. good sensitivity to ITDs and not the mode of stimulation.…”

Optimal Multichannel Artifact Prediction and Removal for Neural Stimulation and Brain Machine Interfaces

“…Advances in neural implant and electrical stimulation technologies, such as cochlear implants (CIs) and vagal nerve stimulators, increasingly rely on concurrent neural stimulation and recordings to either assess functional transformations between connected brain regions ( Lim and Anderson, 2007 ; Kral et al, 2009 ; Atencio et al, 2014 ; Hancock et al, 2017 ; Vollmer, 2018 ; Li et al, 2019 ) or to optimize electrical stimulation via closed-loop feedback control ( Wilson et al, 1991 ; Schachter and Saper, 1998 ; Dhillon and Horch, 2005 ; Lebedev and Nicolelis, 2006 ; O’Doherty et al, 2011 ; Mc Laughlin et al, 2012 ; Hartmann et al, 2014 ). In such applications, capacitive and inductive coupling between the stimulating and recording electrodes leads to stimulus-evoked artifacts in the extracellular recordings that are often several orders of magnitude larger (i.e., milli-volts) than the extracellular neural signals (typically micro-volts).…”