Ocular following responses of the marmoset monkey are dependent on post-saccadic delay, spatiotemporal frequency and saccade direction

Abstract

Ocular following is a short-latency, reflexive eye movement that tracks wide-field visual motion. It has been studied extensively in humans and macaques and is an appealing behaviour for studying sensory-motor transformations in the brain due to its rapidity and rigidity. We explored ocular following in the marmoset, an emerging model in neuroscience because their lissencephalic brain allows direct access to most cortical areas for imaging and electrophysiological recordings. In three experiments, we tested ocular following responses in three adult marmosets. First, we varied the gap between saccade end and stimulus motion onset (post-saccadic delay), from 10 to 300 ms. As in other species, tracking had shorter onset latencies and higher eye speeds with shorter post-saccadic delays. Second, using sine-wave grating stimuli we explored the dependence of eye speed on spatiotemporal frequency. The highest eye speed was evoked at [~]16 Hz and [~]0.16 cycles per degree (cpd), however, the highest gain was elicited at [~]1.6 Hz and [~]1.2 cpd. The highest eye speed for each spatial frequency was observed at a different temporal frequency, but this interdependence was not consistent with complete speed tuning of the ocular following response. Finally, we found the highest eye speeds when saccade and stimulus motion directions were congruent, although latencies were unaffected by direction congruence. Our results showed comparable ocular following in marmosets, humans and macaques, despite over an order of magnitude variation in body and eye size across species. This characterization will help future studies examining the neural basis of sensory-motor transformations. New & NoteworthyPrevious ocular following studies focused on humans and macaques. We examined the properties of ocular following responses in marmosets in three experiments, in which post-saccadic delay, spatial-temporal frequency of stimuli and congruency of saccade and motion directions were manipulated. We have demonstrated short-latency ocular following in marmosets, and discuss the similarities across three species that vary markedly in eye and head size. Our findings will help future studies examining the neural mechanism of sensory-motor transformations.