Cortical spatiotemporal reformatting tuned to saccadic amplitude

Abstract

Humans use rapid eye movements (saccades) to inspect objects of interest with the fovea, the region of the retina with highest acuity. In relocating gaze, saccades abruptly shift the image across the retina, strongly modulating the input signals experienced by photoreceptors. These transients have been traditionally regarded as problematic for visual encoding, and much research has focused on how the visual system discards them. This common view has been recently challenged, and a number of studies have now suggested that the luminance modulations caused by saccades may actually facilitate the establishment of spatial representations. Below a velocity-dependent spatial frequency cutoff, saccade-induced luminance modulations counterbalance (whiten) the spectral density of natural scenes, equalizing input signals across spatial frequencies and thereby discarding redundant information present in natural visual environments. Critically, the bandwidth of this effect is inversely proportional to saccade amplitude. Here, we examined the consequences of this spatiotemporal input reformatting on electroencephalographic responses in the occipital cortex of humans. We simultaneously recorded eye movements and EEG signals while participants (N=16) executed saccades of various amplitudes (1, 3, and 6 deg) over narrow-band white noise fields centered at low (0.03 c/deg), medium (0.16 c/deg), and high (2 c/deg) spatial frequencies. As established in the literature, a prominent event-related potential (the lambda-wave) peaked over the central-occipital electrode ~90 ms following saccade offset. We report that the amplitude of this lambda-wave closely follows the predictions of saccade-induced spatiotemporal reformatting, with an amplitude that depends on the spatial frequency of the noise field for small but not large saccades (F(4,60)=4.75; p<0.01). These findings show that the space-time reformatting of the visual input resulting from saccades strongly drives neural responses and propagates to the cortex, where it shapes neural activity immediately following saccades.