Characterizing Correlates of Eye-Movement Related Eardrum Oscillations in Human Sound Perception and the Macaque Inferior Colliculus

Abstract

How does the brain translate coordinates between the auditory system's head-centered and the visual system's eye-centered reference frames? 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. How does it shape auditory processing and 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.