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Antimo Buonocore, Ziad M. Hafed; A sensory race between oculomotor control areas for coordinating motor timing. Journal of Vision 2021;21(9):2420. doi: https://doi.org/10.1167/jov.21.9.2420.
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For successful adaptive behavior, exogenous environmental events must be sensed and reacted to as efficiently as possible. However, exogenous onsets necessarily come asynchronously to internal brain state, leading to a so-called “race condition” within visual and visual-motor areas: while there is an ongoing process trying to plan and execute a given movement, a new competing process is triggered by the exogenous event. We hypothesized that to handle such a race condition, late motor control areas in the brainstem should exhibit hallmarks of early sensory areas, in addition to their classically accepted motor functions. We recorded (in 1 monkey) from omnipause neurons (OPN’s) in the nucleus raphe interpositus (rip), constituting the very final gateway for allowing or preventing saccades. We presented stimuli of different image features (spatial frequency, contrast, orientation, and motion). OPN’s, normally tonically active and only pausing to allow saccade execution, showed robust early (<50 ms) phasic visual responses, which were also feature-tuned. Consistent with another motor structure, superior colliculus (SC), OPN’s preferred low spatial frequencies. When we directly compared OPN and SC responses, we found that OPN “visual” activity was as early as, if not earlier, than in the SC. What is the functional role of such early visual flows to such two late motor control areas? In this case, it is to control motor timing, as we confirmed with electrical microstimulation. We injected short microstimulation pulse trains to “simulate” brief phasic visual responses in either OPN’s (1 monkey), SC (2 monkeys), or V1 (1 monkey) individually. In OPN’s, visual “bursts” inhibit saccades. Contrarily, SC visual “bursts” increase saccade likelihood, and V1 visual “bursts” are consistent with sensing phosphenes. Therefore, we uncovered a sensory race between sensory and motor areas, providing a highly mechanistic description of why even simple visually-guided saccades can exhibit surprisingly large timing variability.
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