Contrast sensitivity reveals an oculomotor strategy for temporally encoding space

Antonino Casile,Jonathan D Victor,Michele Rucci

doi:10.7554/elife.40924

Abstract

The contrast sensitivity function (CSF), how sensitivity varies with the frequency of the stimulus, is a fundamental assessment of visual performance. The CSF is generally assumed to be determined by low-level sensory processes. However, the spatial sensitivities of neurons in the early visual pathways, as measured in experiments with immobilized eyes, diverge from psychophysical CSF measurements in primates. Under natural viewing conditions, as in typical psychophysical measurements, humans continually move their eyes even when looking at a fixed point. Here, we show that the resulting transformation of the spatial scene into temporal modulations on the retina constitutes a processing stage that reconciles human CSF and the response characteristics of retinal ganglion cells under a broad range of conditions. Our findings suggest a fundamental integration between perception and action: eye movements work synergistically with the spatio-temporal sensitivities of retinal neurons to encode spatial information.

Highlights

Contrast sensitivity, the ability to distinguish a patterned input from a uniform background, is one of the most important measures of visual function (Robson, 1966; Campbell and Robson, 1968; De Valois et al, 1974; Owsley and sensitivity, 2003)
We show that a temporal scheme of spatial encoding, a scheme in which spatial vision is driven by temporal changes, predicts such dependencies when the temporal modulations introduced by incessant eye movements are taken into account
When these consequences of fixational drift are ignored, the known response characteristics of retinal ganglion cells fail to account for human contrast sensitivity function (CSF)

Summary

Introduction

The ability to distinguish a patterned input from a uniform background, is one of the most important measures of visual function (Robson, 1966; Campbell and Robson, 1968; De Valois et al, 1974; Owsley and sensitivity, 2003). It has long been established that sensitivity varies in a specific manner with the spatial frequency of the stimulus, yielding the so-called contrast sensitivity function ( CSF). A decline in sensitivity is expected for several reasons, including the filtering of the eyes’ optics (Campbell and Green, 1965) and the spatial limits in sampling imposed by the cone mosaic on the retina (Hirsch and Miller, 1987; Rossi and Roorda, 2010). The reasons for a reduced sensitivity have remained less clear

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