Role of visual and non-visual cues in constructing a rotation-invariant representation of heading in parietal cortex.

Adhira Sunkara,Gregory C DeAngelis,Dora E Angelaki

doi:10.7554/elife.04693

Adhira Sunkara, Gregory C DeAngelis + Show 1 more

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https://doi.org/10.7554/elife.04693

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Abstract

As we navigate through the world, eye and head movements add rotational velocity patterns to the retinal image. When such rotations accompany observer translation, the rotational velocity patterns must be discounted to accurately perceive heading. The conventional view holds that this computation requires efference copies of self-generated eye/head movements. Here we demonstrate that the brain implements an alternative solution in which retinal velocity patterns are themselves used to dissociate translations from rotations. These results reveal a novel role for visual cues in achieving a rotation-invariant representation of heading in the macaque ventral intraparietal area. Specifically, we show that the visual system utilizes both local motion parallax cues and global perspective distortions to estimate heading in the presence of rotations. These findings further suggest that the brain is capable of performing complex computations to infer eye movements and discount their sensory consequences based solely on visual cues.

Highlights

Retinal images of the environment are altered by self-generated rotations such as eye or head movements
In order to provide a rich visual environment, the first experiment simulated self-motion through a 3D cloud of dots, a stimulus that contains both local motion parallax cues resulting from translation (Helmholtz and Southall, 1924; Gibson, 1950; Longuet-Higgins and Prazdny, 1980; Koenderink and van Doorn, 1987) and global perspective cues to rotation (Koenderink and van Doorn, 1976; Grigo and Lappe, 1999)
Neuroscience explore the underpinnings of a retinal solution in achieving rotation-invariance, a second experiment used a fronto-parallel plane (FP) of dots, which eliminates the local motion parallax cues but retains global perspective cues to rotation

Summary

Introduction

Retinal images of the environment are altered by self-generated rotations such as eye or head movements. In order to perceive the world accurately, the component of retinal patterns resulting from such rotations needs to be discounted by the visual system. While walking down a sidewalk and simultaneously looking at a passing car using eye or head rotations, the brain must discount the visual consequences of the self-generated rotations to estimate and maintain one’s direction of translation (i.e., heading). The resulting retinal pattern is generally an expansionary or contractionary radial flow field from which the point of zero velocity (Focus of Expansion, FOE) can be used to estimate heading (Tanaka et al, 1986; Warren et al, 1988; Duffy and Wurtz, 1995; Britten, 2008).

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