Neck muscle activity reflects neural patterns of sequential saccade planning in head-restrained primates.

Goal-directed behavior involves the transformation of neural movement plans into appropriate muscle activity patterns. Studies involving single saccades have shown that a rapid pathway links saccade planning in frontal eye fields (FEFs) to neck muscle activity. However, it is unknown if the rapid connection between FEF and neck muscle is also maintained during sequential saccade planning. Using neural recordings from FEF, and electromyographic (EMG) recordings from the dorsal neck muscles of head-restrained monkeys, we show that neural sequence planning signals are largely preserved in the neck EMG response. Like FEF movement neurons, we found that neck motor unit activity displayed an accumulation-to-threshold response before saccade onset. Responses of both neck motor units and FEF neurons displayed similar trends during saccade sequencing; multiple saccadic eye movements could be programmed in parallel, while processing bottlenecks, indexed by reduced accumulation rates, limited the extent of parallel programming. These results suggest that even without the need for overt head movements, neck muscle activity shows signatures of central gaze planning. We propose that multiple upcoming gaze plans are rapidly passed down from the FEF to the neck muscles to initiate recruitment for anticipated gaze movements. Similarities in neural and neck motor activity may enable synchronous yet controlled eye-head responses to sequential gaze shifts. Gaze shifts, brought about by coordinated eye-head movements through the eye and neck muscle system, are a part of everyday behavior, yet the neuromuscular underpinnings of gaze sequences are unclear. Using a combination of behavioral analyses, neural recordings, and electromyographic recordings, we show that sequential saccade plans developing in neural oculomotor centers can be extracted from the neck muscle activity of head-restrained macaques. Neck motor units, thus provide a readout of central sequence planning signals.