Dissociated Representation of Binaural Cues in Single-Sided Deafness: Implications for Cochlear Implantation

Abstract

Congenital single-sided deafness (SSD) leads to an aural preference syndrome that is characterized by overrepresentation of the hearing ear in the auditory system. Cochlear implantation (CI) of the deaf ear is an effective treatment for SSD. However, the newly introduced auditory input in congenital SSD often does not reach expectations in late-implanted CI recipients with respect to binaural hearing and speech perception. In a previous study, a reduction of interaural time difference (ITD) sensitivity has been shown in unilaterally congenitally deaf cats (uCDC). In the present study, we focused on the interaural level difference (ILD) processing in the primary auditory cortex. The uCDC group was compared with hearing cats (HC) and bilaterally congenitally deaf cats (CDC). The ILD representation was reorganized, replacing the preference for the contralateral ear with a preference for the hearing ear, regardless of the cortical hemisphere. In accordance with the previous study, uCDCs were less sensitive to interaural time differences than HCs, resulting in unmodulated ITD responses, thus lacking directional information. Such incongruent ITDs and ILDs cannot be integrated for binaural sound source localization. In normal hearing the predominant effect of each ear is excitation of auditory cortex in the contralateral cortical hemisphere and inhibition in the ipsilateral hemisphere. In SSD, however, auditory pathways reorganized such that the hearing ear produced greater excitation in both cortical hemispheres and the deaf ear produced weaker excitation and preserved inhibition in both cortical hemispheres.Significance statementCongenital single-sided deafness is a clinically relevant form of hearing loss. We studied this phenomenon in a unique animal model with congenital deafness of one ear and normal hearing of the other ear with electrical stimulation on both ears. Differential effects of single-sided deafness on interaural time and level difference sensitivity were observed, consistent with the aural preference syndrome. The influence of the previously hearing ear became dominant and the deaf ear mildly suppressive in the majority of units in both hemispheres, resulting in an inconsistent representation of binaural cues. These changes in neuronal representation of the two ears explain why late restoration with cochlear implants in single-sided deafness often results in insufficient benefit of the previously deaf ear.