Visual feature tuning of superior colliculus neural reafferent responses after fixational microsaccades

Abstract

The primate superior colliculus (SC) is causally involved in microsaccade generation. Moreover, visually-responsive SC neurons across this structures topographic map, even at peripheral eccentricities much larger than the tiny microsaccade amplitudes, exhibit significant modulations of evoked response sensitivity when stimuli appear peri-microsaccadically. However, during natural viewing, visual stimuli are normally stably present in the environment and are only shifted on the retina by eye movements. Here we investigated this scenario for the case of microsaccades, asking whether and how SC neurons respond to microsaccade-induced image jitter. We recorded neural activity from two male rhesus macaque monkeys. Within the response field (RF) of a neuron, there was a stable stimulus consisting of a grating of one of three possible spatial frequencies. The grating was stable on the display, but microsaccades periodically jittered the retinotopic RF location over it. We observed clear short-latency visual reafferent responses after microsaccades. These responses were weaker, but earlier (relative to new fixation onset after microsaccade end), than responses to sudden stimulus onsets without microsaccades. The reafferent responses clearly depended on microsaccade amplitude, as well as microsaccade direction relative to grating orientation. Our results indicate that one way for microsaccades to influence vision is through modulating how the spatio-temporal landscape of SC visual neural activity represents stable stimuli in the environment. Such representation strongly depends on the specific pattern of temporal luminance modulations expected from the relative relationship between eye movement vector (size and direction), on the one hand, and spatial visual pattern layout, on the other. Significance statementDespite being diminutive, microsaccades still jitter retinal images. We investigated how such jitter affects superior colliculus (SC) activity. We found that SC neurons exhibit short-latency visual reafferent bursts after microsaccades. These bursts reflect not only the spatial luminance profiles of visual patterns, but also how such profiles are shifted by eye movement size and direction. These results indicate that the SC continuously represents visual patterns, even as they are jittered by the smallest possible saccades.