Sound elicits stereotyped facial movements that provide a sensitive index of hearing abilities

Abstract

SUMMARYSound elicits rapid movements of muscles in the face, ears, and eyes that protect the body from injury and trigger brain-wide internal state changes. Here, we performed quantitative facial videography from mice resting atop a piezoelectric force plate and observed that broadband sounds elicit rapid, small, and highly stereotyped movements of a facial region near the vibrissae array. Facial motion energy (FME) analysis revealed sensitivity to far lower sound levels than the acoustic startle reflex and greater reliability across trials and mice than sound-evoked pupil dilations or movement of other facial and body regions. FME tracked the low-frequency envelope of sounds and could even decode speech phonemes in varying levels of background noise with high accuracy. FME growth slopes were disproportionately steep in mice with autism risk gene mutations and noise-induced sensorineural hearing loss, providing an objective behavioral measure of sensory hyper-responsivity. Increased FME after noise-induced cochlear injury was closely associated with the emergence of excess gain in later waves of the auditory brainstem response, suggesting a midbrain contribution. Deep layer auditory cortex units were entrained to spontaneous facial movements but optogenetic suppression of cortical activity facilitated – not suppressed – sound-evoked FME, suggesting the auditory cortex is a modulator rather than a mediator of sound-evoked facial movements. These findings highlight a simple involuntary behavior that is more sensitive and integrative than other auditory reflex pathways and captures higher-order changes in sound processing from mice with inherited and acquired hearing disorders.

Facial expressions in mice reveal latent cognitive variables and their neural correlates

“…Similarly, pupil diameter is linked not only to changes in luminance, directly relevant for seeing, but also to more abstract cognitive variables related to arousal and uncertainty, even when they have no direct relationship to perception (10)(11)(12). In line with this, in mice, even neutral sounds of different spectral or temporal content evoke stimulus-specific facial movements (13,14).…”

“…A key step in this direction has been to link facial expressions to controllable and quantifiable variables. Recent examples of this are facial expressions being linked to auditory-evoked responses (13,14) and to arousal state (16,21). Clayton et al 2024 (14), in particular, showed that facial movement is not only more sensitive to the intensity of auditory stimuli, but also that it reports the spectral and temporal structure of sound.…”

“…In our study, we explored whether the cognitive significance of incidental facial expressions extends beyond (i) fast, reflex-like encoding of the current sensory environment (13,14) and (ii) the immediate demands that tasks requiring temporally-extended computations place on the motor system. To do so, we took advantage of the recent finding that mice compute several different decision variables simultaneously when performing a foraging task (22).…”