Brain circuits underlying visual stability across eye movements—converging evidence for a neuro-computational model of area LIP

Abstract

The understanding of the subjective experience of a visually stable world despite the occurrence of an observer's eye movements has been the focus of extensive research for over 20 years. These studies have revealed fundamental mechanisms such as anticipatory receptive field (RF) shifts and the saccadic suppression of stimulus displacements, yet there currently exists no single explanatory framework for these observations. We show that a previously presented neuro-computational model of peri-saccadic mislocalization accounts for the phenomenon of predictive remapping and for the observation of saccadic suppression of displacement (SSD). This converging evidence allows us to identify the potential ingredients of perceptual stability that generalize beyond different data sets in a formal physiology-based model. In particular we propose that predictive remapping stabilizes the visual world across saccades by introducing a feedback loop and, as an emergent result, small displacements of stimuli are not noticed by the visual system. The model provides a link from neural dynamics, to neural mechanism and finally to behavior, and thus offers a testable comprehensive framework of visual stability.

A predictive coding model of gaze shifts and the underlying neurophysiology

“…17d, and these results are also similar to those obtained from the single-cell recordings in monkey cortex (Kusunoki and Goldberg, 2003). There has been much debate about whether remapping is a consequence of calculations performed within a retinotopic coordinate system (Dominey and Arbib, 1992;Droulez and Berthoz, 1991;Krommenhoek et al, 1993;Mender, 2014;Mender and Stringer, 2015;Quaia et al, 1998;Smith and Crawford, 2001;Wurtz, 2008;Xing and Andersen, 2000a), or if it is performed using neurons with responses that are partially invariant (gain-modulated cells) or fully invariant (real-position cells) to eye movement (Krommenhoek et al, 1993;Schneegans, S.and Schöner, 2012;Smith and Crawford, 2005;Ziesche and Hamker, 2014). The PC/BC-DIM model falls in the latter category.…”

The Dorsal Visual System Predicts Future and Remembers Past Eye Position

“…Duhamel et al, 1992 ; Bremmer et al, 2009 ; Ibbotson and Krekelberg, 2011 ) may provide sufficient information about impending eye movements to predict future/past eye positions. Similar ideas have been proposed in modeling studies to account for predictive remapping of visual activity during saccades in area LIP (Schneegans and Schöner, 2012 ; Ziesche and Hamker, 2014 ).…”

“…Several well-known peri-saccadic phenomena would benefit from easy access to past, current, and future eye positions. For instance, before executing a saccade, the visual system could use information on the future eye position to remap visual information from neurons currently receiving input from a specific spatial location to those receiving input from that location after the saccade (Duhamel et al, 1992 ; Morris et al, 2007 ; Schneegans and Schöner, 2012 ; Ziesche and Hamker, 2014 ). Similarly, the comparison of visual input before and after a saccade that may contribute to perceptual stability across saccades could benefit from knowledge of the eye position before and after that saccade (Prime et al, 2011 ; Crapse and Sommer, 2012 ).…”

Spatial updating of attention across eye movements: A neuro-computational approach

“…The model accounts for predictive remapping using two eye position related signals, a discrete eye position signal and a corollary discharge signal, to compute the perceived position of stimuli across saccades. Ziesche and colleagues demonstrated the model is in addition able to explain the perisaccadic mislocalization of briefly flashed stimuli in complete darkness (Ziesche & Hamker, 2011) and the observation of saccadic suppression of displacement (SSD) (Ziesche & Hamker, 2014;Ziesche, Bergelt, Deubel, & Hamker, 2017).…”