Parametric information about eye movements is sent to the ears

Abstract

Eye movements alter the relationship between the visual and auditory spatial scenes. Signals related to eye movements affect neural pathways from the ear through auditory cortex and beyond, but how these signals contribute to computing the locations of sounds with respect to the visual scene is poorly understood. Here, we evaluated the information contained in eye movement-related eardrum oscillations (EMREOs), pressure changes recorded in the ear canal that occur in conjunction with simultaneous eye movements. We show that EMREOs contain parametric information about horizontal and vertical eye displacement as well as initial/final eye position with respect to the head. The parametric information in the horizontal and vertical directions combines linearly, allowing accurate prediction of the EMREOs associated with oblique eye movements from their respective horizontal and vertical components. Target location can also be inferred from the EMREO signals recorded during eye movements to those targets. We hypothesize that the thus-far unknown mechanism underlying EMREOs could impose a two-dimensional eye-movement related transfer function on any incoming sound, permitting subsequent processing stages to compute the positions of sounds in relation to the visual scene.

Detection of spatially-localized sounds is robust to saccades and concurrent eye movement-related eardrum oscillations (EMREOs)

“…The latencies of the first two peaks of the EMREOs occurred after 14.9 ± 3.4 ms and 21.0 ± 7.9 ms (mean ± SD). The vertical saccades (performed only in experiment 1) reveal a similar albeit less clear relationship between EMREO phase and saccade direction, as expected based on previous reports (Gruters et al, 2018;Murphy et al, 2020;Lovich et al, 2022). The scaling of the EMREO with saccade direction and amplitude could pertain to the instructed saccade vector that was indicated on the screen, or could directly pertain to the actually executed movement.…”

“…The eye-movement related eardrum oscillations (EMREOs) may be a signature of such an active hearing process. However, the precise neurobiological substrate generating the EMREO and the functional implications of these for hearing remain unclear (Gruters et al, 2018;Murphy et al, 2020;Lovich et al, 2022;King et al, 2023). Our data corroborate that the eardrum moves consistently and specifically in relation to saccadic eye movements.…”

“…These EMREOs exhibit functional specificity as they are systematically related to the direction and amplitude of saccades. More so, these EMREOs have been shown to reliably contain information about initial fixation points and saccade direction in two-dimensional space (Murphy et al, 2020;Lovich et al, 2022). Incoming sounds are transduced by setting the eardrum in vibration, therefore one may expect that these EMREOs shape the transduction of sounds and thereby how they are perceived.…”

Eye movements track prioritized auditory features in selective attention to natural speech

“…In complex, naturalistic environments, eye movements could aid the auditory system in unraveling the vastly overlapping spectrotemporal information that reaches the ears. Recent evidence in humans suggests that eye movements contribute to the computation of sound locations in relation to the visual scene at the very first stages of sound processing (Lovich et al, 2022; Murphy et al, 2022). Similar studies with monkeys and cats suggest a midbrain hub of inferior and superior colliculus (IC, SC) that affects auditory processing based on eye positions (e.g.…”

“…Bulkin & Groh, 2012; Lee & Groh, 2012; Porter et al, 2007). This circuit has recently been extended to the auditory periphery in humans (Lovich et al, 2022; Murphy et al, 2022). Accordingly, several studies in humans point towards interactions between eye movements and auditory cognition in sound localization (Getzmann, 2002), spatial discrimination (Maddox et al, 2014), and spatial attention (Pomper & Chait, 2017) with lateralized engagement of the posterior parietal cortex in unison with lateralized gaze direction (Popov et al, 2022).…”