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

Abstract

Auditory and visual information involve different coordinate systems, with auditory spatial cues anchored to the head and visual spatial cues anchored to the eyes. Information about eye movements is therefore critical for reconciling visual and auditory spatial signals. The recent discovery of eye movement-related eardrum oscillations (EMREOs) suggests that this process could begin as early as the auditory periphery. How this reconciliation might happen remains poorly understood. Because humans and monkeys both have mobile eyes and therefore both must perform this shift of reference frames, comparison of the EMREO across species can provide insights to shared and therefore important parameters of the signal. Here we show that rhesus monkeys, like humans, have a consistent, significant EMREO signal that carries parametric information about eye displacement as well as onset times of eye movements. The dependence of the EMREO on the horizontal displacement of the eye is its most consistent feature, and is shared across behavioural tasks, subjects and species. Differences chiefly involve the waveform frequency (higher in monkeys than in humans) and patterns of individual variation (more prominent in monkeys than in humans), and the waveform of the EMREO when factors due to horizontal and vertical eye displacements were controlled for. This article is part of the theme issue ‘Decision and control processes in multisensory perception’.

Absence of eye position effects in the early auditory cortex of monkeys

“…Eye position effects in AC may become even stronger if subjects are also required to associate the information gained from eye position with auditory information. In these conditions, neuronal activity in AC may be affected by eye position signals through feedforward projections from the ear or inferior colliculus or feedback projections from frontal and parietal cortical regions [2–8,21–25].…”

“…Studies in primates have demonstrated that the position of the eyes can affect the responses to sounds and the ongoing activity in the ear [1–3] and the inferior colliculus [4–8]. These findings indicate that in these stages of the auditory pathway, auditory information can be combined with information about the eye position and thus with the visual space in which eye position can be used as a reference.…”

How the brain controls decision making in a multisensory world

“…Here, Lovich et al. [ 18 ] extend this fascinating story, elucidating quantitative relationships between eardrum oscillations and saccade metrics in both humans and monkeys. They suggest that similarities and differences in these relationships across species will help guide generation of hypotheses about the functional role of this surprising phenomenon.…”