Motor output evoked by subsaccadic stimulation of primate frontal eye fields.

In addition to its role in shifting the line of sight, the oculomotor system is also involved in the covert orienting of visuospatial attention. Causal evidence supporting this premotor theory of attention, or oculomotor readiness hypothesis, comes from the effect of subsaccadic threshold stimulation of the oculomotor system on behavior and neural activity in the absence of evoked saccades, which parallels the effects of covert attention. Here, by recording neck-muscle activity from monkeys and systematically titrating the level of stimulation current delivered to the frontal eye fields (FEF), we show that such subsaccadic stimulation is not divorced from immediate motor output but instead evokes neck-muscle responses at latencies that approach the minimal conduction time to the motor periphery. On average, neck-muscle thresholds were approximately 25% lower than saccade thresholds, and this difference is larger for FEF sites associated with progressively larger saccades. Importantly, we commonly observed lower neck-muscle thresholds even at sites evoking saccades

Representation of Horizontal head-on-body position in the primate superior colliculus.

Movement-related activity within the superior colliculus (SC) represents the desired displacement of an impending gaze shift. This representation must ultimately be transformed into position-based reference frames appropriate for coordinated eye-head gaze shifts. Parietal areas that project to the SC are modulated by the initial position of both the eye-re-head and head-re-body and SC activity is modulated by eye-re-head position. These considerations led us to investigate whether SC activity is modulated by the head-re-body position. We recorded activity from movement-related SC neurons while head-restrained monkeys performed a delayed-saccade task. Across blocks of trials, the horizontal position of the body was rotated under a space-fixed head to three to five different positions spanning +/-25 degrees . We observed a significant influence of body-under-head position on SC activity in 50/60 neurons. This influence was expressed predominantly as a linear gain field, scaling task-related SC activity without changing the location of the response field (linear gain fields explained >/=20% of the variance in neural activity in approximately 50% of our sample). Smaller nonlinear modulations were also observed in roughly 30% of our sample. SC activity was equally likely to increase or decrease as the body was rotated to the side of neuronal recording and we found no systematic relationship between the directionality or magnitude of the linear gain field with recording location in the SC. We conclude that a signal conveying head-re-body position is present in the SC. Although the functional significance remains open, our findings are consistent with the SC contributing to a displacement-to-position transformation for oculomotor control.

Widespread presaccadic recruitment of neck muscles by stimulation of the primate frontal eye fields.

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.