The unsteady eye: an information-processing stage, not a bug

Abstract

How is space represented in the visual system? At first glance, the answer to this fundamental question appears straightforward: spatial information is directly encoded in the locations of neurons within maps. This concept has long dominated visual neuroscience, leading to mainstream theories of how neurons encode information. However, an accumulation of evidence indicates that this purely spatial view is incomplete, and that even for static images, the representation is fundamentally spatiotemporal. The evidence for this new understanding centers on recent experimental findings concerning the functional role of fixational eye movements, the tiny movements humans and other species continually perform, even when attending to a single point. Here, we review some of these findings and discuss their functional implications.

Oculomotor inhibition covaries with conscious detection

“…Even when an observer fixates on a single point, spontaneous microsaccades correct gaze position, prevent and counteract visual fading, and explore tiny image details McCamy et al 2014;Otero-Millan et al 2013;Rolfs 2009;Rucci and Victor 2015). The onset of an irrelevant stimulus inhibits these movements within 100 ms, followed by a rebound in the microsaccade rate (Engbert and Kliegl 2003;Hafed and Ignashchenkova 2013).…”

The multifunctional lateral geniculate nucleus

“…Perhaps a bigger story regarding eye movements and visual computation is the emerging role of microsaccades (movements < 1°) in generating spikes at the level of the LGN (Martinez-Conde et al, 2002) and the related idea that microsaccades serve to enrich information from the visual environment (Martinez-Conde et al, 2004Rucci et al, 2007;McCamy et al, 2014;Rucci and Victor, 2015). Whereas we make large saccades to foveate interesting pieces of our environment, the eye is never still during 'fixations' (i.e.…”

“…periods between saccades). Far from being an artifact, 'perimicrosaccadic' periods are a major source of spike generation during fixation (Martinez-Conde et al, 2002), and these 'tremors' actually enrich available information by correlating spike activity to enrich and sharpen borders (Rucci and Victor, 2015). This is an emerging area because our past enquiry into the mechanisms of early vision have been heavily invested in the paralyzed eye (to control stimulus variability), and even in awake animals, these microsaccades were often either not observed due to technical limitations or simply viewed as noise (Martinez-Conde et al, 2004.…”

Receptive field center-surround interactions mediate context-dependent spatial contrast encoding in the retina

“…First, nonlinear processing in the retina can contribute more to decorrelating retinal ganglion cell (RGC) responses to natural scenes than the RF surround [10] (see also [11,12]). Second, human fixational eye movements can remove spatial correlations in natural inputs before any neural processing takes place [13,14,15,16]. These findings suggest a need to re-examine the role of the surround, especially as it relates to the encoding of natural visual stimuli.…”