Vision dominates sound in mediating classic cue-induced microsaccadic eye movement modulations in rhesus macaque monkeys

Abstract

Visual onsets in the environment cause a short-latency reduction in saccade generation likelihood. Concomitant with that, the metrics of the saccades that do happen near the time of saccadic inhibition reflect the landscape of stimulus-driven neural responses in topographically organized brain maps. While certain aspects of saccadic inhibition have already been explored from a neurophysiological perspective, several questions remain, including which sensory-motor pathways propagate visual input information to the final oculomotor control circuitry with such short latencies. Here, motivated by evidence of a dissociation between temporal and spatial aspects of saccadic inhibition, we devised behavioral paradigms experimentally manipulating either aspect. Rhesus macaque monkeys maintained gaze fixation, and we characterized visually-driven microsaccadic inhibition with and without paired auditory pulses. In one condition, the sound pulses were spatially-nonlateralized, thus only affecting the temporal processes associated with microsaccadic inhibition; in another, the pulses were spatially-lateralized, affecting both the temporal and spatial components. We found that sound pulses alone barely affected microsaccade rates. However, when paired with visual stimuli, they accelerated the timing of visually-driven microsaccadic inhibition by [~]14-18 ms. In terms of microsaccade directions, spatially-nonlateralized sounds interfered with, but did not eliminate, visually-driven direction modulations. Surprisingly, lateralized sounds had a much weaker effect on microsaccade direction modulations, even when the sound source was in the opposite hemifield as the appearing visual stimulus. We conclude that vision dominates sound in mediating classic microsaccadic inhibition, and we argue that our paradigms are ideal for neurophysiological investigations of the parallel sensory-motor pathways contributing to such inhibition. SignificanceCoordination of internal oculomotor eye movement plans with exogenous sensory events entails rapid inhibition of the saccadic eye movement system, but the pathways mediating the inhibition are unknown. We devised novel behavioral paradigms in primates, involving multisensory stimulation, which allow neurophysiological experiments to isolate the contributions of individual sensory, motor, and sensory-motor brain areas to saccadic inhibition. Such paradigms underscore that inhibition involves distinct temporal and spatial processes that are dominated by the visual modality.