Individual similarities and differences in eye-movement-related eardrum oscillations (EMREOs)

Eye movements are critical to linking vision and spatial hearing. Sounds create spatial cues across the head and ears while visual stimuli are detected based on patterns of light impinging on the eye (e.g. e.g. e.g. e.g. Groh and Sparks, 1992; Blauert, 1997; Groh, 2014). Every eye movement shifts the relative relationship between the visual and auditory reference frames. Thus, information about angle of the eye with respect to head/ears is crucial for integrating the locations of auditory and visual stimuli. However, exactly how this computation occurs is not yet known.

We previously identified a unique type of otoacoustic emission that may play a role in this process (Gruters et al., 2018; Murphy et al., 2020; Lovich et al., 2023a; Lovich et al., 2023b) and this finding has been confirmed by other labs (Abbasi et al., 2023; Bröhl and Kayser, in press). Unlike traditional otoacoustic emissions that can occur spontaneously or in response to auditory stimuli (for review see (Probst et al., 1991; Lonsbury-Martin and Martin, 2003; Shera, 2004), eye movement-related eardrum oscillations (EMREOs) are time-locked to saccade onset and phase-reset at saccade offset (i.e. EMREOs continue after saccades stop with phases that align at saccade offset). Both initial eye position and change in eye position parametrically impact EMREO magnitude and phase (Gruters et al., 2018; Murphy et al., 2020; Lovich et al., 2023a; Lovich et al., 2023b), demonstrating the presence of eye-movement-related information at the auditory periphery. This provides the auditory system early access to signals necessary for communication with visual maps of space.

The mechanism(s) underlying such signals may alter auditory transduction in an eye-movement dependent fashion and contribute to previous neurophysiological observations of eye-movement-related modulation of both subcortical (Groh et al., 2001; Zwiers et al., 2004; Porter et al., 2006; Bulkin and Groh, 2012a, b) and cortical (Werner-Reiss et al., 2003; Fu et al., 2004; Maier and Groh, 2010; Willett et al., 2019; O'Connell et al., 2020) stages of the auditory pathway. Indeed, recent work in humans indicates that eye-movement related modulation is widespread throughout auditory-selective regions of cortex (Leszczynski et al., 2023). A full understanding of the eye-movement related signals present at the periphery will ultimately prove vital for understanding these aspects of central processing.

Our initial study suggested that there are individual differences in the precise nature of this signal (Gruters et al., 2018) and such variation has also been reported in other studies (Bröhl and Kayser, in press). Given that all individuals with normal or corrected-to-normal vision, hearing, and eye movements are confronted with the same computational challenge of achieving spatial perceptual stability between vision and hearing across eye movements, the similarities and differences in the EMREOs observed across normal participants can provide clues as to what particular aspects of these signals are relevant to that underlying computational process. Furthermore, like conventional OAEs, EMREOs could eventually have clinical relevance for diagnosing the nature of hearing deficits or auditory-visual integrative dysfunction. Accordingly, in this work, we seek to ascertain which aspects of the EMREO signal are most consistent across normal hearing individuals and which exhibit the most variability. An overarching goal is to establish norms for EMREO data collection and analysis and set the stage for future clinical research in this area.

We report here that certain basic properties of EMREOs were present in all participants: specifically, varying phase and amplitude based on the direction and amplitude of the associated eye movement. Generally, EMREOs are larger when saccades are made to the hemi-field contralateral to the recorded ear than to the ipsilateral field. Individuals varied in the maximum amplitude of their EMREO signals. There was also a slight jitter in the latency of the peaks of the EMREO across individuals, but the pattern of latency changes in the EMREO relating to saccade length/duration is maintained within individual subjects’ responses. Finally, there is greater response variability across subjects for ipsilateral compared to contralateral saccades. Within subjects, EMREOs were highly repeatable across different blocks of trials and recording days.

Identifying and quantifying aspects of EMREO signals that are similar across normal hearing subjects, as we have done here, will ultimately allow comparisons to responses in individuals with different types of auditory system dysfunction. These comparisons should provide insight into the mechanisms that generate and/or modulate the EMREO response as well as provide a means for assessing the feasibility of the EMREO as a future clinical measure of auditory-visual integration.

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