Cochlear activity in silent cue-target intervals shows a theta-rhythmic pattern and is correlated to attentional alpha and theta modulations

Abstract

Background A long-standing debate concerns where in the processing hierarchy of the central nervous system (CNS) selective attention takes effect. In the auditory system, cochlear processes can be influenced via direct and mediated (by the inferior colliculus) projections from the auditory cortex to the superior olivary complex (SOC). Studies illustrating attentional modulations of cochlear responses have so far been limited to sound-evoked responses. The aim of the present study is to investigate intermodal (audiovisual) selective attention in humans simultaneously at the cortical and cochlear level during a stimulus-free cue-target interval. Results We found that cochlear activity in the silent cue-target intervals was modulated by a theta-rhythmic pattern (~ 6 Hz). While this pattern was present independently of attentional focus, cochlear theta activity was clearly enhanced when attending to the upcoming auditory input. On a cortical level, classical posterior alpha and beta power enhancements were found during auditory selective attention. Interestingly, participants with a stronger release of inhibition in auditory brain regions show a stronger attentional modulation of cochlear theta activity. Conclusions These results hint at a putative theta-rhythmic sampling of auditory input at the cochlear level. Furthermore, our results point to an interindividual variable engagement of efferent pathways in an attentional context that are linked to processes within and beyond processes in auditory cortical regions.

Direct Cochlear Recordings in Humans Show a Theta Rhythmic Modulation of Auditory Nerve Activity by Selective Attention

“…This, however, may also be the result of low signal-to-noise ratios (SNRs), as commercial CIs are so far not optimized to do these kinds of continuous electrophysiological recordings. Indeed, a grand average of the condition differences points to maximal effects in a frequency range overlapping with the one reported by Köhler et al (2021), resulting in enhanced theta power while attending to the auditory modality (Figure 2B). This result corroborates our previous finding using a similar paradigm, where ongoing OAEs in the theta band (~6 Hz) were enhanced while attending an upcoming auditory stimulus (Köhler et al, 2021).…”

“…Indeed, a grand average of the condition differences points to maximal effects in a frequency range overlapping with the one reported by Köhler et al (2021), resulting in enhanced theta power while attending to the auditory modality (Figure 2B). This result corroborates our previous finding using a similar paradigm, where ongoing OAEs in the theta band (~6 Hz) were enhanced while attending an upcoming auditory stimulus (Köhler et al, 2021). We found no selective attention effect in the alpha nor in the beta band in concordance with aforementioned studies of otoacoustic activity.…”

“…The resulting power spectra (see Figure 2A) by themselves showed no clear peaks, however the grand average condition contrast spectrum indicates differences that are mainly centered in distinct frequency ranges. Based on previous OAE and M/EEG work (Mazaheri et al, 2014;Köhler et al, 2021), we statistically compared the two conditions in the theta (averaged between 5-8 Hz) and alpha frequency band (averaged between 9-13 Hz; Figure 2B). A cluster-based permutation test in the theta frequency band showed that prestimulus power is higher when attending the auditory domain (p = 10.00e -05 , d = 0.49).…”

“…Spiral ganglion cells making up the auditory-nerve fibers are mainly innervated by connections of the lateral olivocochlear complex (LOC), respectively ( Warr and Guinan, 1979 ; Elgueda and Delano, 2020 ). Attentional modulations of OAEs can thus be seen as a proxy for subcortical attentional modulations via MOC synapses and have been connected with low-frequency (<10 Hz) oscillatory mechanisms at the cochlear level during alternating selective attention ( Dragicevic et al, 2019 ), with increases in the theta band (∼6 Hz) when attending to upcoming auditory input during a silent cue-target interval ( Köhler et al, 2021 ).…”

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

“…Spiral ganglion cells making up the auditory-nerve fibers are mainly innervated by connections of the lateral olivocochlear complex (LOC) respectively (Warr and Guinan, 1979;Elgueda and Delano, 2020). Attentional modulations of OAEs can thus be seen as a proxy for subcortical attentional modulations via MOC synapses and have been connected with low-frequency (<10 Hz) oscillatory mechanisms at the cochlear level during alternating selective attention (Dragicevic et al, 2019), with increases in the theta band (~6 Hz) when attending to upcoming auditory input during an silent cue-target interval (Köhler et al, 2021).…”