Neuronal Response Gain Enhancement prior to Microsaccades

Abstract

Neuronal response gain enhancement is a classic signature of the allocation of covert visual attention without eye movements. However, microsaccades continuously occur during gaze fixation. Because these tiny eye movements are preceded by motor preparatory signals well before they are triggered, it may be the case that a corollary of such signals may cause enhancement, even without attentional cueing. In six different macaque monkeys and two different brain areas previously implicated in covert visual attention (superior colliculus and frontal eye fields), we show neuronal response gain enhancement for peripheral stimuli appearing immediately before microsaccades. This enhancement occurs both during simple fixation with behaviorally irrelevant peripheral stimuli and when the stimuli are relevant for the subsequent allocation of covert visual attention. Moreover, this enhancement occurs in both purely visual neurons and visual-motor neurons, and it is replaced by suppression for stimuli appearing immediately after microsaccades. Our results suggest that there may be an obligatory link between microsaccade occurrence and peripheral selective processing, even though microsaccades can be orders of magnitude smaller than the eccentricities of peripheral stimuli. Because microsaccades occur in a repetitive manner during fixation, and because these eye movements reset neurophysiological rhythms every time they occur, our results highlight a possible mechanism through which oculomotor events may aid periodic sampling of the visual environment for the benefit of perception, even when gaze is prevented from overtly shifting. One functional consequence of such periodic sampling could be the magnification of rhythmic fluctuations of peripheral covert visual attention.