Samanthi C. Goonetilleke

A Within Trial Measure of the Stop Signal Reaction Time in a Head-Unrestrained Oculomotor Countermanding Task

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 ∼180 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.

Neck muscle responses evoked by transcranial magnetic stimulation of the human frontal eye fields

Transcranial magnetic stimulation (TMS) provides a non‐invasive means of investigating brain function. Whereas TMS of the human frontal eye fields (FEFs) does not induce saccades, electrical stimulation of the monkey FEF evokes eye–head gaze shifts, with neck muscle responses evoked at stimulation levels insufficient to evoke a saccade. These animal results motivated us to examine whether TMS of the FEF (TMS‐FEF) in humans evokes a neck muscle response. Subjects performed memory‐guided saccades to the left or right while TMS (two pulses at 20 Hz) was delivered on 30% of trials to the left FEF coincident with saccade instruction. As reported previously, TMS‐FEF decreased contralateral saccade reaction times. We simultaneously recorded the activity of splenius capitis (SPL) (an ipsilateral head turner). TMS‐FEF evoked a lateralized increase in the activity of the right SPL but not the left SPL, consistent with the recruitment of a contralateral head‐turning synergy. In some subjects, the evoked neck muscle response was time‐locked to stimulation, whereas in others the evoked response occurred around the time of the saccade. Importantly, evoked responses were greater when TMS was applied to the FEF engaged in contralateral saccade preparation, with even greater evoked responses preceding shorter latency saccades. These results provide new insights into both the nature of TMS and the human oculomotor system, demonstrating that TMS‐FEF engages brainstem oculomotor circuits in a manner consistent with a general role in eye–head gaze orienting. Our results also suggest that pairing neck muscle recordings with TMS‐FEF provides a novel way of assaying the covert preparation of oculomotor plans.

Greater benefits of multisensory integration during complex sensorimotor transformations

Multisensory integration enables rapid and accurate behavior. To orient in space, sensory information registered initially in different reference frames has to be integrated with the current postural information to produce an appropriate motor response. In some postures, multisensory integration requires convergence of sensory evidence across hemispheres, which would presumably lessen or hinder integration. Here, we examined orienting gaze shifts in humans to visual, tactile, or visuotactile stimuli when the hands were either in a default uncrossed posture or a crossed posture requiring convergence across hemispheres. Surprisingly, we observed the greatest benefits of multisensory integration in the crossed posture, as indexed by reaction time (RT) decreases. Moreover, such shortening of RTs to multisensory stimuli did not come at the cost of increased error propensity. To explain these results, we propose that two accepted principles of multisensory integration, the spatial principle and inverse effectiveness, dynamically interact to aid the rapid and accurate resolution of complex sensorimotor transformations. First, early mutual inhibition of initial visual and tactile responses registered in different hemispheres reduces error propensity. Second, inverse effectiveness in the integration of the weakened visual response with the remapped tactile representation expedites the generation of the correct motor response. Our results imply that the concept of inverse effectiveness, which is usually associated with external stimulus properties, might extend to internal spatial representations that are more complex given certain body postures.

Cross-species comparison of anticipatory and stimulus-driven neck muscle activity well before saccadic gaze shifts in humans and nonhuman primates

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.

Dynamic and Opposing Adjustment of Movement Cancellation and Generation in an Oculomotor Countermanding Task

Adaptive adjustments of strategies help optimize behavior in a dynamic and uncertain world. Previous studies in the countermanding (or stop-signal) paradigm have detailed how reaction times (RTs) change with trial sequence, demonstrating adaptive control of movement generation. Comparatively little is known about the adaptive control of movement cancellation in the countermanding task, mainly because movement cancellation implies the absence of an outcome and estimates of movement cancellation require hundreds of trials. Here, we exploit a within-trial proxy of movement cancellation based on recordings of neck muscle activity while human subjects attempted to cancel large eye–head gaze shifts. On a subset of successfully cancelled trials where gaze remains stable, small head-only movements to the target are actively braked by a pulse of antagonist neck muscle activity. The timing of such antagonist muscle recruitment relative to the stop signal, termed the “antagonist latency,” tended to decrease or increase after trials with or without a stop-signal, respectively. Over multiple time scales, fluctuations in the antagonist latency tended to be the mirror opposite of those occurring contemporaneously with RTs. These results provide new insights into the adaptive control of movement cancellation at an unprecedented resolution, suggesting it can be as prone to dynamic adjustment as movement generation. Adaptive control in the countermanding task appears to be governed by a dynamic balance between movement cancellation and generation: shifting the balance in favor of movement cancellation slows movement generation, whereas shifting the balance in favor of movement generation slows movement cancellation.

Validation of a within-trial measure of the oculomotor stop process

The countermanding (or stop signal) task requires subjects try to withhold a planned movement upon the infrequent presentation of a stop signal. We have previously proposed a within-trial measure of movement cancellation based on neck muscle recruitment during the cancellation of eye-head gaze shifts. Here, we examined such activity after either a bright or dim stop signal, a manipulation known to prolong the stop signal reaction time (SSRT). Regardless of stop signal intensity, subjects generated an appreciable number of head-only errors during successfully cancelled gaze shifts (compensatory eye-in-head motion ensured gaze stability), wherein subtle head motion toward a peripheral target was ultimately stopped by a braking pulse of antagonist neck muscle activity. Both the SSRT and timing of antagonist muscle recruitment relative to the stop signal increased for dim stop signals and decreased for longer stop signal delays. Moreover, we observed substantial variation in the distribution of antagonist muscle recruitment latencies across our sample. The magnitude and variance of the SSRTs and antagonist muscle recruitment latencies correlated positively across subjects, as did the within-subject changes across bright and dim stop signals. Finally, we fitted our behavioral data with a race model architecture that incorporated a lower threshold for initiating head movements. This model allowed us to estimate the efferent delay between the completion of a central stop process and the recruitment of antagonist neck muscles; the estimated efferent delay remained consistent within subjects across stop signal intensity. Overall, these results are consistent with the hypothesis that neck muscle recruitment during a specific subset of cancelled trials provides a peripheral expression of oculomotor cancellation on a single trial. In the discussion, we briefly speculate on the potential value of this measure for research in basic or clinical domains and consider current issues that limit more widespread use.

Ultrasound-guided insertion of intramuscular electrodes into suboccipital muscles in the non-human primate

The head-neck system is highly complex from a biomechanical and musculoskeletal perspective. Currently, the options for recording the recruitment of deep neck muscles in experimental animals are limited to chronic approaches requiring permanent implantation of electromyographic electrodes. Here, we describe a method for targeting deep muscles of the dorsal neck in non-human primates with intramuscular electrodes that are inserted acutely. Electrode insertion is guided by ultrasonography, which is necessary to ensure placement of the electrode in the target muscle. To confirm electrode placement, we delivered threshold electrical stimulation through the intramuscular electrode and visualized the muscle twitch. In one animal, we also compared recordings obtained from acutely- and chronically-implanted electrodes. This method increases the options for accessing deep neck muscles, and hence could be used in experiments for which the invasive surgery inherent to a chronic implant is not appropriate. This method could also be extended to the injection of pharmacological agents or anatomical tracers into specific neck muscles.