Widespread Presaccadic Recruitment of Neck Muscles by Stimulation of the Primate Frontal Eye Fields

Abstract

We studied the role of the primate frontal eye fields (FEFs) in eye-head gaze shifts by recording EMG activity from multiple dorsal neck muscles after electrical stimulation of a broad distribution of sites throughout FEF. We assess our results in light of four mechanisms forwarded to account for why eye and head movements follow FEF stimulation. Two mechanisms propose that movements are generated indirectly by FEF stimulation in response to either a percept or an eccentric orbital position. Two other mechanisms propose that movements are evoked directly through the issuance of either a gaze command or separate eye and head commands. FEF stimulation evoked short-latency ( approximately 20 ms) neck EMG responses from the vast majority (>95%) of stimulation sites. Evoked responses usually preceded the gaze shift by approximately 20 ms, even for small gaze shifts (<10 degrees ) not typically associated with head motion. Evoked responses began earlier and attained a larger magnitude when accompanied by larger gaze shifts and took a form consistent with the recruitment of the appropriately directed head movements to accompany the evoked gaze shift. We also observed robust neck EMG even when stimulation failed to evoke a gaze shift and occasionally observed head-only movements when the head was unrestrained. These results resemble neck EMG evoked from the superior colliculus (SC). Neck EMG response latencies approached the minimal conduction time to the motor periphery and hence are not consistent with either of the indirect mechanisms. The widespread nature of the cephalomotor drive from the FEF, the scaling of neck EMG responses with gaze magnitude, and the consistently earlier generation of the EMG versus gaze response are difficult to reconcile with suggestions that separate FEF channels encode eye and head motion independently. The most parsimonious interpretation is that a gaze command issued by the FEF is decomposed into eye and head commands downstream of the SC. The relative timing of the neck EMG and gaze shift responses, and the presence of neck EMG responses on trials without gaze shifts, implies that head premotor elements are not subjected to the same brain stem control mechanisms governing gaze shifts.

Recruitment of a Head-Turning Synergy by Low-Frequency Activity in the Primate Superior Colliculus

“…Stimulation studies have demonstrated that low-current or short-duration dSC stimulation can engage cephalomotor circuits independent of gaze shifts (Corneil et al 2002a(Corneil et al ,b, 2007Pélisson et al 2001), consistent with the concept of selective OPN gating of gaze shifts. Such selective gating is also consistent with observations of transient visual bursts of neck muscle recruitment following visual target presentation (Corneil et al 2004) and with our more recent observation that such visual bursts of neck muscle recruitment are modulated by reflexive allocation of covert attention (Corneil et al 2008).…”

“…Details of these surgeries were previously provided (Elsley et al 2007). Herein, we focus on the EMG activity recorded from the obliquus capitis inferior (OCI) and rectus capitis posterior major (RCP maj) muscles (Fig.…”

“…Herein, we focus on the EMG activity recorded from the obliquus capitis inferior (OCI) and rectus capitis posterior major (RCP maj) muscles (Fig. 1A) because these muscles are known to constitute the core of the horizontal head-turning synergy (Corneil et al 2001(Corneil et al , 2002aElsley et al 2007). We focused on muscles involved in horizontal head movements because the head contributes more to horizontal versus vertical gaze shifts (Freedman 2005;Freedman and Sparks 1997a) and to ease comparison with our previous microstimulation results (Corneil et al 2002a, where stimulation was applied unilaterally.…”

“…To answer this question, we recorded both dSC activity and electromyographic (EMG) activity from neck muscles known to turn the head while monkeys performed a head-restrained saccade task. Neck EMG recordings provide a resolved measure of the neural drive to the head in a variety of behavioral and stimulation protocols, even when the head is restrained (Corneil et al , 2008Elsley et al 2007). The selected oculomotor task (Fig.…”

Stimulation of the Frontal Eye Field Reveals Persistent Effective Connectivity after Controlled Behavior

“…In addition, we confirmed that there was no significant main effect of previous task on EOGs during 20 -40 ms after TMS (horizontal EOG electrodes, F (1,18) ϭ 0.34, p ϭ 0.57, vertical EOG electrodes, F (1,18) ϭ 2.29, p ϭ 0.15). Furthermore, the TMS did not induce head rotation, either, which would have produced asymmetric electromyographic responses of the neck muscles in occipital electrodes (Elsley et al, 2007). It is unlikely that repetition or alternation in the laterality of saccade target and saccade direction affected the TMS-EPs, because TMS-EPs were recorded before the presentation of a saccade target.…”