The Dorsal Visual System Predicts Future and Remembers Past Eye Position.

Adam P Morris,Frank Bremmer,Bart Krekelberg

doi:10.3389/fnsys.2016.00009

Abstract

Eye movements are essential to primate vision but introduce potentially disruptive displacements of the retinal image. To maintain stable vision, the brain is thought to rely on neurons that carry both visual signals and information about the current direction of gaze in their firing rates. We have shown previously that these neurons provide an accurate representation of eye position during fixation, but whether they are updated fast enough during saccadic eye movements to support real-time vision remains controversial. Here we show that not only do these neurons carry a fast and accurate eye-position signal, but also that they support in parallel a range of time-lagged variants, including predictive and post dictive signals. We recorded extracellular activity in four areas of the macaque dorsal visual cortex during a saccade task, including the lateral and ventral intraparietal areas (LIP, VIP), and the middle temporal (MT) and medial superior temporal (MST) areas. As reported previously, neurons showed tonic eye-position-related activity during fixation. In addition, they showed a variety of transient changes in activity around the time of saccades, including relative suppression, enhancement, and pre-saccadic bursts for one saccade direction over another. We show that a hypothetical neuron that pools this rich population activity through a weighted sum can produce an output that mimics the true spatiotemporal dynamics of the eye. Further, with different pooling weights, this downstream eye position signal (EPS) could be updated long before (<100 ms) or after (<200 ms) an eye movement. The results suggest a flexible coding scheme in which downstream computations have access to past, current, and future eye positions simultaneously, providing a basis for visual stability and delay-free visually-guided behavior.

Highlights

The primate visual system makes use of the exquisite sensitivity of the fovea by continually directing the eye toward new areas of interest
We have argued that suitable eye position signals (EPS) are available in the middle temporal (MT), medial superior temporal (MST), ventral intraparietal (VIP), and lateral intraparietal (LIP) areas of the posterior parietal cortex (PPC) (Bremmer et al, 1997a,b, 1999; Duhamel et al, 1997; Boussaoud and Bremmer, 1999; Schlack et al, 2005; Morris et al, 2012, 2013)
Almost all neurons, including those without significant eye position effects, showed modulations of neural activity around the time of the saccades. The dynamics of these changes varied greatly across neurons and in many cases depended on the direction of the saccadic eye movement, as we show

Summary

Introduction

The primate visual system makes use of the exquisite sensitivity of the fovea by continually directing the eye toward new areas of interest. As a consequence of this active strategy, visual information must be combined with up-to-the-moment information about eye (and head) position to make sense of the environment (Soechting and Flanders, 1992). This additional information allows the brain to take into account self-induced changes in the retinal image and to construct stable representations of visual space—a prerequisite for goal-directed behavior. 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). We asked whether such flexible eye-position signals are available in LIP, VIP, and MT/MST

Methods

Results

Conclusion