Short-duration stimulation of the supplementary eye fields perturbs anti-saccade performance while potentiating contralateral head orienting.

Many forms of brain stimulation utilize the notion of state dependency, whereby greater influences are observed when a given area is more engaged at the time of stimulation. Here, by delivering intracortical microstimulation (ICMS) to the supplementary eye fields (SEF) of monkeys performing interleaved pro- and anti-saccades, we show a surprising diversity of state-dependent effects of ICMS-SEF. Short-duration ICMS-SEF passed around cue presentation selectively disrupted anti-saccades by increasing reaction times and error rates bilaterally, and also recruited neck muscles, favoring contralateral head turning to a greater degree on anti-saccade trials. These results are consistent with the functional relevance of the SEF for anti-saccades. The multiplicity of stimulation-evoked effects, with ICMS-SEF simultaneously disrupting anti-saccade performance and facilitating contralateral head orienting, probably reflects both the diversity of cortical and subcortical targets of SEF projections, and the response of this oculomotor network to stimulation. We speculate that the bilateral disruption of anti-saccades arises via feedback loops that may include the thalamus, whereas neck muscle recruitment arises via feedforward polysynaptic pathways to the motor periphery. Consideration of both sets of results reveals a more complete picture of the highly complex and multiphasic response to ICMS-SEF that can play out differently in different effector systems.

Recruitment of a contralateral head turning synergy by stimulation of monkey supplementary eye fields.

The supplementary eye fields (SEF) are thought to enable higher-level aspects of oculomotor control. The goal of the present experiment was to learn more about the SEF's role in orienting, specifically by examining neck muscle recruitment evoked by stimulation of the SEF. Neck muscle activity was recorded from multiple muscles in two monkeys during SEF stimulation (100 µA, 150-300 ms, 300 Hz, with the head restrained or unrestrained) delivered 200 ms into a gap period, before a visually guided saccade initiated from a central position (doing so avoids confounds between initial position and prestimulation neck muscle activity). SEF stimulation occasionally evoked overt gaze shifts and/or head movements but almost always evoked a response that invariably consisted of a contralateral head turning synergy by increasing activity on contralateral turning muscles and decreasing activity on ipsilateral turning muscles (when background activity was present). Neck muscle responses began well in advance of evoked gaze shifts (~30 ms after stimulation onset, leading gaze shifts by ~40-70 ms on average), started earlier and attained a larger magnitude when accompanied by progressively larger gaze shifts, and persisted on trials without overt gaze shifts. The patterns of evoked neck muscle responses resembled those evoked by frontal eye field (FEF) stimulation, except that response latencies from the SEF were ~10 ms longer. This basic description of the cephalomotor command evoked by SEF stimulation suggests that this structure, while further removed from the motor periphery than the FEF, accesses premotor orienting circuits in the brain stem and spinal cord in a similar manner.

Neuromuscular consequences of reflexive covert orienting.

Visual stimulus presentation activates the oculomotor network without requiring a gaze shift. Here, we demonstrate that primate neck muscles are recruited during such reflexive covert orienting in a manner that parallels activity recorded from the superior colliculus (SC). Our results indicate the presence of a brainstem circuit whereby reflexive covert orienting is prevented from shifting gaze, but recruits neck muscles, predicting that similarities between SC and neck muscle activity should extend to other cognitive processes that are known to influence SC activity.

Neuromuscular recruitment related to stimulus presentation and task instruction during the anti-saccade task.

The contextual control of movement requires the transformation of sensory information into appropriate actions, guided by task-appropriate rules. Previous conceptualizations of the sensorimotor transformations underlying anti-saccades (look away from a stimulus) have suggested that stimulus location is first registered and subsequently transformed into its mirror location before being relayed to the motor periphery. Here, by recording neck muscle activity in monkeys performing anti-saccades, we demonstrate that stimulus presentation induces a transient recruitment of the neck muscle synergy used to turn the head in the wrong direction, even though subjects subsequently looked away from the stimulus correctly. Such stimulus-driven aspects of recruitment developed essentially at reflexive latencies (∼60-70 ms after stimulus presentation), and persisted at modest eccentricities regardless of head-restraint. Prior to stimulus presentation, neck muscle activity also reflected whether the animals were preparing for an anti-saccade or a pro-saccade (look toward a stimulus). Neck muscle activity prior to erroneous anti-saccades also resembled that observed prior to pro-saccades. These results emphasize a parallel nature to the sensorimotor transformations underlying the anti-saccade task, suggesting that the top-down and bottom-up processes engaged in this task influence the motor periphery. The bottom-up aspects of neck muscle recruitment also fit within the context of recent results from the limb-movement literature, showing that stimulus-driven activation of muscle synergies may be a generalizing strategy in inertial-laden systems.

Properties of human eye-head gaze shifts in an anti-gaze shift task.

We investigated the metrics and kinematics of human eye-head gaze shifts using the anti-gaze shift task. Surprisingly, no systematic difference was found between peak gaze velocities of large pro- and anti-gaze shifts. In a follow-up experiment that equated perceived stimulus luminance across multiple eccentricities, pro-gaze shifts were consistently faster than anti-gaze shifts. In both experiments, we did not observe any head-only errors where initial head motion dissociates from gaze direction, even though many subjects generated such movements in other paradigms. These experiments confirm the influence of stimulus luminance on comparative movement velocity, and demonstrate that the behavioural set assumed in this task discourages head-only errors.