Physiological oculo-auricular-facial-mandibular synkinesis elicited in humans by gaze deviations

Integrated motor behaviors involving ocular motion-associated movements of the head, neck, pinna, and parts of the face are commonly seen in animals orienting to a visual target. A number of coordinated movements have also been observed in humans making rapid gaze shifts to horizontal extremes, which may be vestiges of these. Since such integrated mechanisms point to a nonpathological coactivation of several anatomically separate cranial circuits in humans, it is important to see how the different pairs of integrative motor behaviors with a common trigger (i.e., ocular motion) manifest in relation to one another. Here, we systematically examined the pattern of eye movement-induced recruitment of multiple cranial muscles in humans. Simultaneous video-oculography and bilateral surface electromyograms of transverse auricular, temporalis, frontalis, and masseter muscles were recorded in 15 healthy subjects (8 females; 29.3 ± 5.2 yr) while they made head-fixed, horizontal saccadic, pursuit, and optokinetic eye movements. Potential chin laterotrusion linked to contractions of masticator muscles was captured with a jaw-fixed accelerometer. Our findings objectively show an orchestrated aural-facial-masticatory muscle response to a range of horizontal eye movements (prevalence of 21%-93%). These responses were most prominent during eccentric saccades. We further reveal distinctions between the various observed activation patterns in terms of their profile (transient or sustained), laterality (with respect to direction of gaze), and timing (with respect to saccade onset). Possible underlying neural substrates, their atavistic behavioral significance, and potential clinical applications for monitoring sensory attention and designing attention-directed hearing aids in the future are discussed.NEW & NOTEWORTHY Healthy humans exhibit different combinations of nonpathological, synkinetic gaze-associated movements with aural, facial, and/or masticatory muscles during different types of voluntary and reflexive horizontal eye movements. The manifestations of these collective phenomena are strongest during large-scale horizontal saccades and accompanied by a detectable horizontal chin movement. Auricular muscle activations occur equally on both sides, whereas the activation of facial and masticatory muscles is predominantly ipsilateral (in regard to gaze direction).