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

Abstract

A unique type of low-frequency otoacoustic emission (OAE) time-locked to the onset (and offset) of saccadic eye movements was recently discovered in our laboratory (Gruters et al., 2018). The specific underlying mechanisms that generate these eye-movement-related eardrum oscillations (termed EMREOs) and their possible role in auditory perception are unknown. Clues to both the drivers of EMREOs and their purpose can be gleaned by examining responses in normal hearing human subjects. Do EMREOs occur in all individuals with normal hearing? If so, what components of the response occur most consistently? Understanding which attributes of EMREOs are similar across participants and which show more variability will provide the groundwork for future comparisons with individuals with hearing abnormalities affecting the ear's various motor components. Here we report that in subjects with normal hearing thresholds and normal middle ear function, all ears show (a) measurable EMREOs, (b) a phase reversal for contra- versus ipsilaterally-directed saccades, (c) a large peak in the signal occurring soon after saccade onset, (d) an additional large peak time-locked to saccade offset and (e) evidence that saccade duration is encoded in the signal. We interpret the attributes of EMREOs that are most consistent across subjects as the ones that are most likely to play an essential role in their function. The individual differences likely reflect normal variation in individuals' auditory system anatomy and physiology, much like traditional measures of auditory function such as auditory-evoked OAEs, tympanometry and auditory-evoked potentials. Future work will compare subjects with different types of auditory dysfunction to population data from normal hearing subjects.

Conserved features of eye movement related eardrum oscillations (EMREOs) across humans and monkeys

“…Auditory signals in both the SC and the IC are sensitive to changes in eye position (SC: [3][4][5][6][7][8]49]; IC: [18][19][20][21][22][23]), and the IC conveys descending projections to both the superior olivary complex [55]-the source of descending input to the outer hair cells [56,57]-and the cochlear nucleus [58,59] which in turn projects to the facial and trigeminal nerves that innervate the stapedius and tensor tympani, respectively [60]. Preliminary findings from our group are consistent with a role for all three of these types of motor actuators in the generation of EMREOs [30]. Future studies regarding these motor components and how they control mechanical processes in the ear will benefit from an animal model with a significant and consistent EMREO and with comparable ear anatomy to humans.…”

“…[3][4][5][6]9,[11][12][13][14][15][16][17][18][19][20][21][22][23]49,50]; see also [7,8]). The discovery of EMREOs in both humans and monkeys [27][28][29][30][31][32] afforded an opportunity to study an early aspect of this process in the same way in two different species. Given that how EMREOs actually contribute to auditory coordinate transformations has not yet been established, a comparison between human and monkey EMREOs provides an opportunity to identify clues as to which aspects of the EMREO signal are conserved across species.…”

“…[24][25][26]), the impact of such signals might produce movements of the eardrum that could be detected by microphones in the ear canal. This led to the discovery of eye movement-related eardrum oscillations (EMREOs) [27][28][29][30] and inquiries into their relationship to visual and auditory perception [31,32].…”

Conserved features of eye movement related eardrum oscillations (EMREOs) across humans and monkeys

“…Auditory signals in both the SC and the IC are sensitive to changes in eye position (SC: Sparks, 1984, 1987b, a;Hartline et al, 1995;Zella et al, 2001;Populin et al, 2004;Lee and Groh, 2012) ; IC: Zwiers et al, 2004;Porter et al, 2006;Bulkin and Groh, 2012b, a;Willett et al, 2019), and the IC conveys descending projections to both the superior olivary complex (Faye-Lund, 1986), the source of descending input to the outer hair cells (Guinan, 2006;Ciuman, 2010) and the cochlear nucleus (Milinkeviciute et al, 2017;Balmer and Trussell, 2022) which in turn projects to the facial and trigeminal nerves that innervate the stapedius and tensor tympani respectively (Mukerji et al, 2010). Preliminary findings from our group are consistent with a role for all three of these types of motor actuators in the generation of EMREOs (King et al, 2023). Further study regarding these motor components and how they control mechanical processes in the ear will benefit from an animal model with a significant and consistent EMREO and with comparable ear anatomy to humans.…”

Parametric information about eye movements is sent to the ears

“…1,2,3). Most previous work about how eye movement information is incorporated into auditory processing has focused on cortical and subcortical brain structures , but the recent discovery of eyemovement related eardrum oscillations (EMREOs) (25)(26)(27)(28) suggests that the process might manifest much earlier in the auditory periphery. EMREOs can be thought of as a biomarker of underlying efferent information impacting the internal structures of the ear in association with eye movements.…”