The effect of microsaccades in the primary visual cortex: increased synchronization in the fovea during a two-phase response modulation.

Abstract

Our eyes are never still. Even when we attempt to fixate, the visual gaze is never motionless, as we continuously perform miniature oculomotor movements termed as fixational eye movements. The fastest eye movements during the fixation epochs are termed microsaccades (MSs), that are leading to continual motion of the visual input, affecting mainly neurons in the fovea. Yet our vision appears to be stable. To explain this gap, previous studies suggested the existence of an extra-retinal input (ERI) into the visual cortex that can account for the motion and produce visual stability. Here, we investigated the existence of an ERI to V1 fovea in macaque monkeys (male) while they performed spontaneous MSs, during fixation. We used voltage-sensitive dye imaging (VSDI) to measure and characterize at high spatio-temporal resolution the influence of MSs on neural population activity, in the foveal region of the primary visual cortex (V1). Microsaccades performed over a blank screen, induced a two-phase response modulation: an early suppression followed by an enhancement. A correlation analysis revealed a widespread foveal increase in neural synchronization, peaking around ∼100 ms after MS onset. Next, we investigated the MS effects in the presence of a small visual stimulus, and found that this modulation was different from the blank condition yet both modulations co-existed in the fovea. Finally, the VSD response to an external motion of the fixation point could not explain the MS modulation. These results support an ERI that may be involved in visual stabilization already at the level of V1.Significance statement Microsaccades are tiny fixational saccades, leading to the continual motion of the visual input on the fovea, during visual fixation. Yet our vision appears to be stable. To explain this gap, we investigated the existence of an extra-retinal input into the fovea of the primary visual cortex (V1) in behaving monkeys while they performed microsaccades over a blank screen with a tiny fixation point. The population response aligned on microsacades showed a widespread, transient increased neural synchronization along with a two-phase response modulation. Microsaccades in the presence of a visual stimulus induced distinct spatio-temporal response from that in the blank condition. Our results support the existence of an extra-retinal input that may be involved in visual stabilization at V1 area.