Peaked Encoding of Relative Luminance in Macaque Areas

It is widely presumed that throughout the primate visual pathway neurons encode the relative luminance of objects (at a given light adaptation level) using two classes of monotonic function, one positively and the other negatively sloped. Based on computational considerations, we hypothesized that early visual cortex also contains neurons preferring intermediate relative luminance values. We tested this hypothesis by recording from single neurons in areas V1 and V2 of alert, fixating macaque monkeys during presentation of a large, spatially uniform patch oscillating slowly in luminance and surrounded by a static texture background. A substantial subset of neurons responsive to low spatial frequency luminance stimuli in both areas exhibited prominent and statistically reliable response peaks to intermediate rather than minimal or maximal luminance values. When presented with static patches of different luminance but of the same spatial configuration, most neurons tested retained a preference for intermediate relative luminance. Control experiments using luminance modulation at multiple low temporal frequencies or reduced amplitude indicate that in the slow luminanceoscillating paradigm, responses were more strongly modulated by the luminance level than the rate of luminance change. These results strongly support our hypothesis and reveal a striking cortical transformation of luminance-related information that may contribute to the perception of surface brightness and lightness. In addition, we tested many luminance-sensitive neurons with large chromatic patches oscillating slowly in luminance. Many cells, including the gray-preferring neurons, exhibited strong color preferences, suggesting a role of luminance-sensitive cells in encoding information in 3D color space. Introduction: Luminance, the density of light energy absorbed by retinal photoreceptors, is an essential dimension of visual information. It is obviously important for neurophysiologists to understand how each stage of the visual system encodes various aspects of luminance-related information. This includes absolute luminance, spatial contrast in luminance (relative to a background or surround) and temporal contrast in luminance (relative to the recent average luminance). Luminance provides a basic cue to brightness and lightness, two important and related surface attributes that can be influenced by many global as well as local visual cues (Knill & Kersten, 1991; Adelson, 1993; Williams et al., 1998; Purves et al., 1999; Lotto et al., 1999). Given that in natural vision, luminance often varies slowly in space and in time (except during eye movements or object motion), it is particularly important to understand how low spatial and temporal frequency luminance information is encoded and transformed at successive stages of the visual hierarchy. However, our knowledge about the neuronal representation of luminance at low spatial and temporal frequencies (herein referred as luminance) is far from complete, especially for visual cortex. At subcortical levels, primate retinal ganglion cells and LGN neurons have an unbalanced centersurround antagonistic receptive field structure (Croner and Kaplan, 1995; Irvin et al., 1993), allowing them to convey low spatial frequency luminance as well as high spatial frequency contrast information. When these cells are presented with step increases in luminance of a large spatially Articles in PresS. J Neurophysiol (November 3, 2004). doi:10.1152/jn.00793.2004 Copyright © 2004 by the American Physiological Society. Final Accepted Version# JN-00793-2004.R1 uniform patch covering both the center and surround (i.e. of low spatial frequency), the responses either increase progressively (on-center cells) or decrease progressively (off-center cells) as a function of luminance level (Sakmann and Creutzfeldt, 1969; Virsu and Lee, 1983; Creutzfeldt et al., 1986). These results, along with the hyperbolic contrast tuning curves of early cortical neurons probed with sinusoidal gratings (Albrecht and Hamilton, 1982; Levitt et al., 1994) have contributed to the widespread assumption that throughout the primate visual pathway low spatial frequency luminance information is encoded by a purely monotonic encoding strategy, in which progressively brighter or darker stimuli evoke progressively stronger responses (Fig. 1A). In the monotonic encoding strategy, intermediate luminance values (gray) elicit at most moderate firing from individual neurons and a low aggregate firing rate from the population. This constitutes a qualitatively different representation, with lower signal to noise ratio, than for low and high luminance values (dark and bright). Natural images, on the other hand, are typically dominated by intermediate luminance values (Laughlin, 1981), which may warrant an alternate processing strategy in order to effectively represent many subtle shades of gray. Accordingly, we hypothesize that visual cortex includes luminance-sensitive neurons with peaked luminance encoding functions that explicitly represent intermediate values of relative luminance (bold curves in Figure 1B). Figure 1. Encoding strategies and stimulus configuration. A, A pure Monotonic Encoding strategy. B, Peaked luminance tuning included (Bold curves). C, Spatial configuration of the stimuli. D, Oscillating Final Accepted Version# JN-00793-2004.R1 paradigm. In each trial, fixation onset was at time 0, uniform texture background onset was at 0.3 sec; the luminance patch onset was at 1.0 sec; and the oscillation lasted 5 sec (solid curve: phase 0; dashed curve: phase π). E, Static paradigm. In each trial, luminance changed every 1.4 sec. F, Chromatic paradigm. In each trial, the intensity of one or two phosphors (one color) oscillated successively for three cycles, each lasting 1.7 sec. At the cortical level, studies using large spatially uniform stimuli suggest that only a subset of neurons encode low spatial frequency luminance information (Bartlett and Doty, 1974; Maguire and Baizer, 1982; Komatsu et al., 1996; Rossi et al., 1996; Kinoshita and Komatsu, 2001). Although it has been asserted that luminance encoding by V1 neurons is purely monotonic, the available evidence is not compelling (see Discussion). The present study used a combination of approaches to systematically examine luminance encoding at low spatial and temporal frequencies by V1 and V2 neurons. In one paradigm, we used a slowly and continuously varying (oscillating) luminance patch, in which the sampling of luminance values was much finer-grained than in previous studies. A second and more conventional paradigm used step changes in luminance to better characterize the temporal characteristics of luminance-sensitive neurons. Our results strongly support the hypothesis that some early cortical neurons are maximally responsive to intermediate rather than low or high luminance values. In addition, we analyzed responses to chromatic patches oscillating in luminance to explore the role of luminance-sensitive neurons in encoding color information. Materials and Methods Physiological preparation Two male Macaca mulatta were trained to fixate on a small dot within a fixation window of radius 0.4-0.6 o for 6 seconds. Eye position was monitored by standard scleral search eyecoil implanted before training. Before recording, a craniotomy of 5 mm in diameter was made through an acrylic patch mounted on the skull, and a stainless chamber with a screw-on cap was cemented to the acrylic. All surgical procedures were conducted in accordance with NIH guideline, reviewed and approved in advance by Washington University Animal Studies Committee.