Abstract

Psychophysical inferences about the neural mechanisms supporting spatial vision can be undermined by uncertainties introduced by optical aberrations and fixational eye movements, particularly in fovea where the neuronal grain of the visual system is fine. We examined the effect of these preneural factors on photopic spatial summation in the human fovea using a custom adaptive optics scanning light ophthalmoscope that provided control over optical aberrations and retinal stimulus motion. Consistent with previous results, Ricco's area of complete summation encompassed multiple photoreceptors when measured with ordinary amounts of ocular aberrations and retinal stimulus motion. When both factors were minimized experimentally, summation areas were essentially unchanged, suggesting that foveal spatial summation is limited by postreceptoral neural pooling. We compared our behavioral data to predictions generated with a physiologically-inspired front-end model of the visual system, and were able to capture the shape of the summation curves obtained with and without pre-retinal factors using a single postreceptoral summing filter of fixed spatial extent. Given our data and modeling, neurons in the magnocellular visual pathway, such as parasol ganglion cells, provide a candidate neural correlate of Ricco's area in the central fovea.

Highlights

  • Vision science seeks to understand how the retinal image is encoded and processed by the visual system

  • A field-programmable gate array (FPGA)-based image acquisition and stimulus control module was incorporated into the existing system architecture, facilitating the high-speed retinal tracking and light source modulation required for cone-targeted stimulus delivery (Arathorn et al, 2007; Yang et al, 2010)

  • Imaging the retina with an adaptive optics-equipped ophthalmoscope enables the visualization of individual photoreceptor cells in living eyes (Liang, Williams, & Miller, 1997; Morgan, 2016)

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Summary

Introduction

Vision science seeks to understand how the retinal image is encoded and processed by the visual system. Ricco’s area of complete summation depends on a number of factors, including background intensity (Barlow, 1958; Glezer, 1965; Lelkens & Zuidema, 1983; Redmond, Zlatkova, Vassilev, Garway-Heath, & Anderson, 2013), the chromaticity and polarity of the stimulus and background (Brindley, 1954; Vassilev, Ivanov, Zlatkova, & Anderson, 2005; Vassilev, Mihaylova, Racheva, Zlatkova, & Anderson, 2003; Volbrecht, Shrago, Schefrin, & Werner, 2000), and distance from the fovea (Hallett, 1963; Inui, Mimura, & Kani, 1981; Khuu & Kalloniatis, 2015; Scholtes & Bouman, 1977; Wilson, 1970) Together, these results suggest that the summation area is shaped by the functional architecture of the postreceptoral visual pathways mediating stimulus detection at threshold. The summation areas we measured encompassed multiple foveal cones, more closely resembling the anatomical dimensions of parasol ganglion cell dendritic fields in the human fovea, suggesting that the magnocellular pathway mediates the detection of circularly-shaped increments at visual threshold (Swanson, Sun, Lee, & Cao, 2011; Volbrecht et al, 2000)

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