Activities of the Right Temporo-Parieto-Occipital Junction Reflect Spatial Hearing Ability in Cochlear Implant Users

Eusebia Schäfer,Hans-Otto Karnath,Philipp Gamerdinger,Christoph Braun,Marlies Knipper,Ana-Elena Vedoveli,Anke Tropitzsch,Giulia Righetti,Yiwen Li Hegner

doi:10.3389/fnins.2021.613101

Abstract

Spatial hearing is critical for us not only to orient ourselves in space, but also to follow a conversation with multiple speakers involved in a complex sound environment. The hearing ability of people who suffered from severe sensorineural hearing loss can be restored by cochlear implants (CIs), however, with a large outcome variability. Yet, the causes of the CI performance variability remain incompletely understood. Despite the CI-based restoration of the peripheral auditory input, central auditory processing might still not function fully. Here we developed a multi-modal repetition suppression (MMRS) paradigm that is capable of capturing stimulus property-specific processing, in order to identify the neural correlates of spatial hearing and potential central neural indexes useful for the rehabilitation of sound localization in CI users. To this end, 17 normal hearing and 13 CI participants underwent the MMRS task while their brain activity was recorded with a 256-channel electroencephalography (EEG). The participants were required to discriminate between the probe sound location coming from a horizontal array of loudspeakers. The EEG MMRS response following the probe sound was elicited at various brain regions and at different stages of processing. Interestingly, the more similar this differential MMRS response in the right temporo-parieto-occipital (TPO) junction in CI users was to the normal hearing group, the better was the spatial hearing performance in individual CI users. Based on this finding, we suggest that the differential MMRS response at the right TPO junction could serve as a central neural index for intact or impaired sound localization abilities.

Highlights

When acting in a multisensory environment, it is predominantly the auditory cues which direct our attention to relevant targets and help us orient in space when the events happen outside the field of view
We introduce a multi-modal repetition suppression (MMRS) paradigm that is suitable for both testing and eventually training spatial hearing, and that allows to identify brain regions that are involved in the discrimination of sound locations using high-density electroencephalography (EEG)
We investigated the neural correlates of horizontal sound localization in 17 normal hearing participants and found that the differential EEG signals (DIFFSAME, i.e., MMRS responses) upon sound location changes were evident in various cortical regions across time

Summary

Introduction

When acting in a multisensory environment, it is predominantly the auditory cues which direct our attention to relevant targets and help us orient in space when the events happen outside the field of view. This skill is of crucial importance for us to become aware of potential pertinent incidents, such as threats. Cochlear implants (CIs) are until now the most successful treatment for patients with severe to profound sensorineural hearing loss as they restore hearing to such an extent that speech recognition is reestablished or considerably improved, enabling verbal communication in numerous deaf and hearing impaired patients (Krueger et al, 2008). The rehabilitation of sound spatial localization after cochlear implantation has been comparatively less invested into (Faulkner and Pisoni, 2013), still restricting rare success to gain modifications through automatic gain control of CI devices (Potts et al, 2019)

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