Neural and Perceptual Correlates of Eye-Movement Related Eardrum Oscillations – a New Window into Brain Function?

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  • Cochlear and middle ear efferents modulate sensory information in the hearing system, shaping auditory waveforms and refining sound perception. These efferent pathways innervate the middle ear muscles and cochlear outer hair cells; eardrum oscillation patterns reflect an aggregate signal of these muscles pulling on the ossicles and cochlear cells moving the basilar membrane. These two sets of actuators are mechanically coupled and transmit soundwaves to the eardrum. Their combined activity is thus recordable with microphones in the ear canal. How might one then isolate neural activity through microphone recording? In primates, saccades cause frequent shifts between the visual and auditory scenes. Robust cross-referencing is critical to audiovisual processing. Eye movements generate a phenomenon in the auditory periphery called Eye-Movement Related Eardrum Oscillations (EMREOs). The EMREO encodes precise, parametric information about saccade direction and amplitude. What rapport does the signal have with central nervous system activity and what insight does it provide into human perception? The Inferior Colliculus (IC) is a midbrain auditory processing center with efferent control of putative actuators of EMREOs. We used Local Field Potential (LFP) recordings from the IC of rhesus macaques to identify a neural signature of the animals’ free saccades. We discovered 1) stereotypic oscillations before saccade onset, 2) an evoked response with greater amplitude for ipsilateral saccades, and 3) as with the EMREO, greatest encoding of saccade horizontal displacement in the LFP. We also compared EMREOs to performance on audiovisual localization tasks. In normal-hearing human subjects 1) sound localization ability varied widely, with some subjects’ azimuth discrimination >30°, 2) larger EMREOs correlated with greater inaccuracy and imprecision localizing sounds, 3) initial fixation influenced visual task performance more in those with more variable EMREOs. These findings highlight EMREO as an audio annotation, demarcating visual orientation in relation to sounds at the eardrum. Future clinical work should aim to quantify how changes in EMREOs reflect depreciation of auditory efferent signaling in the context of central nervous system pathologies.
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  • 0000-0002-0803-1499
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