Parallel colour-opponent pathways to primary visual cortex

Chatterjee, Soumya; Callaway, Edward M.

doi:10.1038/nature02167

Cited by 218 publications

(199 citation statements)

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“…In addition to projection to the supragranular layers of primary visual cortex (V1, area 17), targets of the koniocellular layers of the LGN include the middle temporal area (MT, V5) and other prestriate cortical areas (35)(36)(37). Our results suggest that a blue-off pathway, like the blue-on pathway (6, 7), thus could contribute directly to S-cone-mediated motion processing (38,39) as well as to cortical pathways for color vision.…”

Section: Discussionmentioning

confidence: 89%

Geniculocortical relay of blue-off signals in the primate visual system

Szmajda

Buzás

FitzGibbon

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

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A fundamental dichotomy in the subcortical visual system exists between on-and off-type neurons, which respectively signal increases and decreases of light intensity in the visual environment. In primates, signals for red-green color vision are carried by both on-and off-type neurons in the parvocellular division of the subcortical pathway. It is thought that on-type signals for blueyellow color vision are carried by cells in a distinct, diffusely projecting (koniocellular) pathway, but the pathway taken by blue-off signals is not known. Here, we measured blue-off responses in the subcortical visual pathway of marmoset monkeys. We found that the cells exhibiting blue-off responses are largely segregated to the koniocellular pathway. The blue-off cells show relatively large receptive fields, sluggish responses to maintained contrast, little sign of an inhibitory receptive-field surround mechanism, and negligible functional input from an intrinsic (melanopsin-based) phototransductive mechanism. These properties are consistent with input from koniocellular or ''W-like'' ganglion cells in the retina and suggest that blue-off cells, as previously shown for blue-on cells, could contribute to cortical mechanisms for visual perception via the koniocellular pathway.color vision ͉ short-wavelength-sensitive cones ͉ blue cones ͉ koniocellular pathway ͉ lateral geniculate nucleus T his study addresses the properties of sensory afferent pathways for primate color vision. Chromatic information is transmitted from the retina to the cortex via the lateral geniculate nucleus (LGN). Many neurons in the LGN show ''cone opponent'' responses: they are activated by a restricted range of wavelengths in the visible spectrum and inhibited by others. In trichromatic primates, the dorsal (parvocellular) layers of the LGN are dominated by neurons that show red-green cone opponent responses, as a result of antagonistic inputs arising in medium-wavelength-sensitive (M or ''green'') and longwavelength-sensitive (L or ''red'') cones. A smaller proportion of neurons in the retina and LGN shows blue-on responses, as a result of excitatory input arising in short-wavelength-sensitive (S) cones (1-5). Blue-on ganglion cells in the retina show a distinct bistratified morphology (5), and blue-on signals reach the visual cortex via the koniocellular/intercalated layers of the LGN (6, 7). Unlike cells in the parvocellular (PC) and ventral (magnocellular) layers, the constituent cells of koniocellular pathways show diverse functional properties and widespread cortical terminations and are considered to have arisen early in the evolutionary history of the visual system (7-9). The blue-on koniocellular cells thus have been considered as part of a primordial pathway for color vision (10). By contrast, the divergence of M and L cones to yield red-green signals in PC pathway cells occurred relatively recently (Ϸ15 million years ago) in the evolution of the primate visual system (11,12).Receptive fields receiving off-type signals from S cones (''blue-off'') r...

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Section: Discussionmentioning

confidence: 89%

Geniculocortical relay of blue-off signals in the primate visual system

Szmajda

Buzás

FitzGibbon

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

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“…The results here show that those V1 neurons specifically specialized for color (by virtue of cone opponency) do. This suggests that the cortex maintains a distinction between subcortical red-green and blue-yellow channels (Dacey and Lee, 1994;Martin et al, 1997;Hendry and Reid, 2000;Chatterjee and Callaway, 2003). The cortex must do some mixing of subcortical channels, however, to account for the S-cone input to red-green cells;…”

Section: Red-green and Blue-yellow Cellsmentioning

confidence: 99%

Spatial and Temporal Properties of Cone Signals in Alert Macaque Primary Visual Cortex

Conway¹,

Livingstone²

2006

J. Neurosci.

139

185

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7°) than spatial-opponent cell centers (ϳ1°). We found that red-green cells received S-cone input, which aligned with M input, and, unlike blue-yellow cells, red-green cells gave push-pull responses: receptivefield centers of red-ON cells were excited by both L increments (bright red) and M decrements (dark red) and were suppressed by both L decrements (dark green) and M increments (bright green). Excitatory responses to decrements were slightly larger than to increments, which may account for the lower detection and discrimination thresholds of decrements shown psychophysically. By virtue of their specialized receptive fields, the neurons described here spatially transform the cone signals and represent the first stage in the visual system at which spatially opponent color calculations are made.

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“…For instance, the magnocellular pathway could provide an LMdominated signal (via spiny stellate cells in layer 4C␣) that modulates the gain of blue-yellow signals carried by the koniocellular (and possibly parvocellular) afferents to layers 4A and 2/3 of V1, as schematized in Fig. 10 (Allison et al 2000;Chatterjee and Callaway 2003;Lachica et al 1993;Nealey and Maunsell 1994;Schiller and Malpeli 1978;Yabuta et al 2001). In this scenario, we would expect that ablation of magnocellular neurons would eliminate nonlinear RFs but spare linear RFs.…”

Section: Neural Substrate Of Color Interactionmentioning

confidence: 99%

Blue-Yellow Signals Are Enhanced by Spatiotemporal Luminance Contrast in Macaque V1

Horwitz

Chichilnisky

Albright

2005

Journal of Neurophysiology

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Blue-yellow signals are enhanced by spatiotemporal luminance contrast in macaque V1. J Neurophysiol 93: 2263-2278, 2005; doi:10.1152/jn.00743.2004. We measured the color tuning of a population of S-cone-driven V1 neurons in awake, fixating monkeys. Analysis of randomly chosen color stimuli that were effective in evoking action potentials showed that these neurons received opposite sign input from the S cones and a combination of L and M cones. Surprisingly, these cells also responded to LM cone contrast irrespective of polarity, a nonlinear sensitivity that was masked by conventional linear analysis methods. Taken together, these observations can be summarized in a nonlinear model that combines nonopponent and opponent signals such that luminance contrast enhances color processing. These findings indicate that important aspects of the cortical representation of color cannot be described by classical linear analysis, and reveal a possible neural correlate of perceptual color-luminance interactions. I N T R O D U C T I O NColor perception results from a complex neuronal computation. The early steps of this computation are well understood: the sensitivity of the cone photoreceptors to lights of various wavelength has been characterized thoroughly (Baylor et al. 1987;Wandell 1995) as has the subsequent synergistic and antagonistic combination of cone signals in the retina and lateral geniculate nucleus (Derrington et al. 1984;DeValois 1965; Gouras 1968). How color information is processed in cortex, however, is less clear. The goal of the current experiments was to extend our understanding of how neurons in the primary visual cortex (V1) combine signals that originate in the cones.One possibility is that V1 neurons combine cone signals linearly. This assumption has been made, either implicitly or explicitly, in studies that employ cone-isolating stimuli to estimate the weights with which cone inputs are integrated (Conway 2001;Johnson et al. 2001;Landisman and Ts'o 2002). While the linearity assumption is justified for many V1 neurons, it is clearly inappropriate for others (Conway 2001;Hanazawa et al. 2000;Hubel and Wiesel 1968;Lennie et al. 1990;Vautin and Dow 1985). For example, a V1 neuron that responds to S cone stimulation, but only when L-and M-cone excitations are appropriately balanced, does not integrate cone inputs linearly and thus cannot be characterized with coneisolating stimuli (Hanazawa et al. 2000).Recently developed data-analysis tools have provided new ways to characterize neurons that combine inputs nonlinearly (de Ruyter van Steveninck and Bialek 1988;Paninski 2003;Rust et al. 2004; Schwartz et al. 2001;Sharpee et al. 2004;Simoncelli et al. 2004;Touryan et al. 2002). Here we use one of these techniques to reveal a surprising nonlinear computation performed by blue-yellow neurons in V1.We excited V1 neurons in awake monkeys with a dynamic, randomly colored stimulus and analyzed the stimulus sequences that preceded spikes. Analysis proceeded in two steps. First, we computed the average stimulus ...

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Parallel colour-opponent pathways to primary visual cortex

Cited by 218 publications

References 28 publications

Geniculocortical relay of blue-off signals in the primate visual system

Geniculocortical relay of blue-off signals in the primate visual system

Spatial and Temporal Properties of Cone Signals in Alert Macaque Primary Visual Cortex

Blue-Yellow Signals Are Enhanced by Spatiotemporal Luminance Contrast in Macaque V1

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