Direct cochlear recordings in humans show a theta rhythmic modulation of the auditory nerve by selective attention

Abstract

The architecture of the efferent auditory system enables prioritization of strongly overlapping spatiotemporal cochlear activation patterns elicited by relevant and irrelevant inputs. So far, attempts at finding such attentional modulations of cochlear activity delivered indirect insights in humans or required direct recordings in animals. The extent to which spiral ganglion cells forming the human hearing nerve are sensitive to selective attention remains largely unknown. We investigated this question by testing the effects of attending to either the auditory or visual modality on human hearing nerve activity that was directly recorded with standard commercial MED-EL cochlear implants (CI) during a stimulus-free (anticipatory) cue-target interval. When attending the upcoming auditory input, ongoing hearing nerve activity within the theta range (5-8 Hz) was enhanced. Crucially, using the broadband signal (4-25 Hz), a classifier was even able to decode the attended modality from single-trial data. Follow-up analysis showed that the effect was not driven by a narrow frequency in particular. Using direct cochlear recordings from deaf individuals, our findings suggest that cochlear spiral ganglion cells are sensitive to top-down attentional modulations. Given the putatively broad hair-cell degeneration of these individuals, the effects are likely mediated by alternative efferent pathways as compared to previous studies using otoacoustic emissions. Successful classification of single-trial data could additionally have a significant impact on future closed-loop CI developments that incorporate real-time optimization of CI parameters based on the current mental state of the user.

Neural speech tracking shifts from the syllabic to the modulation rate of speech as intelligibility decreases

“…Recent studies using non-invasive electrophysiology have shown that auditory activity at putative subcortical processing stages can be measured for complex natural sounds (such as speech; [19][20][21][22]. Furthermore, this subcortical activity can even be modulated by attention (19,20,23). Interestingly, top-down attentional modulations of auditory activity can already be detected at the hair cells in the inner ear measured as otoacoustic activity (faint sounds emitted by the outer hair cells; see 24).…”