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Extracellular single neuron recording and labelling studies of primary vestibular afferents in Scarpa's ganglion have shown that guinea-pig otolithic afferents with irregular resting discharge are preferentially activated by 500 Hz bone-conducted vibration (BCV) and many also by 500 Hz air-conducted sound (ACS) at low threshold and high sensitivity. Very few afferent neurons from any semicircular canal are activated by these stimuli and then only at high intensity. Tracing the origin of the activated neurons shows that these sensitive otolithic afferents originate mainly from a specialized region, the striola, of both the utricular and saccular maculae. This same 500 Hz BCV elicits vestibular-dependent eye movements in alert guinea-pigs and in healthy humans. These stimuli evoke myogenic potentials, vestibular-evoked myogenic potentials (VEMPs), which are used to test the function of the utricular and saccular maculae in human patients. Although utricular and saccular afferents can both be activated by BCV and ACS, the differential projection of utricular and saccular afferents to different muscle groups allows for differentiation of the function of these two sensory regions. The basic neural data support the conclusion that in human patients in response to brief 500 Hz BCV delivered to Fz (the midline of the forehead at the hairline), the cervical VEMP indicates predominantly saccular function and the ocular VEMP indicates predominantly utricular function. The neural, anatomical and behavioural evidence underpins clinical tests of otolith function in humans using sound and vibration.

Recent studies have described a phenomenon wherein the onset of a peripheral visual stimulus elicits short-latency (<100 ms) stimulus-locked recruitment (SLR) of neck muscles in nonhuman primates (NHPs), well before any saccadic gaze shift. The SLR is thought to arise from visual responses within the intermediate layers of the superior colliculus (SCi), hence neck muscle recordings may reflect presaccadic activity within the SCi, even in humans. We obtained bilateral intramuscular recordings from splenius capitis (SPL, an ipsilateral head-turning muscle) from 28 human subjects performing leftward or rightward visually guided eye-head gaze shifts. Evidence of an SLR was obtained in 16/55 (29%) of samples; we also observed examples where the SLR was present only unilaterally. We compared these human results with those recorded from a sample of eight NHPs from which recordings of both SPL and deeper suboccipital muscles were available. Using the same criteria, evidence of an SLR was obtained in 8/14 (57%) of SPL recordings, but in 26/29 (90%) of recordings from suboccipital muscles. Thus, both species-specific and muscle-specific factors contribute to the low SLR prevalence in human SPL. Regardless of the presence of the SLR, neck muscle activity in both human SPL and in NHPs became predictive of the reaction time of the ensuing saccade gaze shift ∼70 ms after target appearance; such pregaze recruitment likely reflects developing SCi activity, even if the tectoreticulospinal pathway does not reliably relay visually related activity to SPL in humans.

Goonetilleke SC, Doherty TJ, Corneil BD. A within trial measure of the stop signal reaction time in a head-unrestrained oculomotor countermanding task. J Neurophysiol 104: 3677-3690, 2010. First published October 20, 2010 doi:10.1152/jn.00495.2010. The countermanding (or stop-signal) task, which requires the cancellation of an impending response on the infrequent presentation of a stop signal, enables study of the contextual control of movement generation and suppression. Here we present a novel and empirical measure of the time needed to cancel an impending gaze shift by recording neck muscle activity during a head-unrestrained oculomotor countermanding paradigm. On a subset of STOP signal trials, subjects generated small head movements toward a target even though gaze remained stable due to a compensatory vestibular-ocular reflex. On such trials, we observed a burst of antagonist neck muscle activity during the small head-only error. Such antagonist neck muscle activity served as an active braking pulse as its magnitude scaled with the kinematics of the head-only error. This activity was selective for trials in which the head was arrested in mid-flight and did not appear on trials without a stop signal, on noncancelled STOP signal trials when the gaze shift was completed, or on STOP signal trials without head motion. Importantly, the timing of this antagonist activity related best to the onset of the stop signal (lagging it by ϳ180 ms), and strongly correlated with behavioral estimates of the time needed to cancel a movement (the stop signal reaction time). These results are consistent with the notion that such selective antagonist neck muscle activity arises as a peripheral expression of the oculomotor STOP process that successfully cancelled the gaze shift. Studying movement cancellation within nested systems like the head-unrestrained gaze shifting system offers a unique opportunity for investigating underlying neural mechanisms as the overall goal (i.e., to cancel a gaze shift) can be achieved despite motion of other components; on such individual trials, the oculomotor STOP process is expressed as an active braking pulse.