Bevil R. Conway

Specialized Color Modules in Macaque Extrastriate Cortex

Imaging studies are consistent with the existence of brain regions specialized for color, but electrophysiological studies have produced conflicting results. Here we address the neural basis for color, using targeted single-unit recording in alert macaque monkeys, guided by functional magnetic resonance imaging (fMRI) of the same subjects. Distributed within posterior inferior temporal cortex, a large region encompassing V4, PITd, and posterior TEO that some have proposed functions as a single visual complex, we found color-biased fMRI hotspots that we call globs, each several millimeters wide. Almost all cells located in globs showed strong luminance-invariant color tuning and some shape selectivity. Cells in different globs represented distinct visual field locations, consistent with the coarse retinotopy of this brain region. Cells in interglob regions were not color tuned, but were more strongly shape selective. Neither population was direction selective. These results suggest that color perception is mediated by specialized neurons that are clustered within the extrastriate brain.

Toward a Unified Theory of Visual Area V4

Visual area V4 is a midtier cortical area in the ventral visual pathway. It is crucial for visual object recognition and has been a focus of many studies on visual attention. However, there is no unifying view of V4s role in visual processing. Neither is there an understanding of how its role in feature processing interfaces with its role in visual attention. This review captures our current knowledge of V4, largely derived from electrophysiological and imaging studies in the macaque monkey. Based on recent discovery of functionally specific domains in V4, we propose that the unifying function of V4 circuitry is to enable selective extraction of specific functional domain-based networks, whether it be by bottom-up specification of object features or by top-down attentionally driven selection.

Neural basis for unique hues

Summary All colors can be described in terms of four non-reducible ‘unique hues: red, green, yellow, and blue [1]. These four hues are also the most common ‘focal colors — the best examples of color terms in language [2]. The significance of the unique hues has been recognized since at least the 14 th century [3] and is universal [4,5], although there is some individual variation [6,7]. Psychophysical linking hypotheses predict an explicit neural representation of unique hues at some stage of the visual system, but no such representation has been described [8]. The special status of the unique hues remains one of the central mysteries of color science [9]. Here we report that a population of recently identified cells in posterior inferior temporal cortex of macaque monkey contains an explicit representation of unique hues.

Color signals through dorsal and ventral visual pathways

Explanations for color phenomena are often sought in the retina, lateral geniculate nucleus, and V1, yet it is becoming increasingly clear that a complete account will take us further along the visual-processing pathway. Working out which areas are involved is not trivial. Responses to S-cone activation are often assumed to indicate that an area or neuron is involved in color perception. However, work tracing S-cone signals into extrastriate cortex has challenged this assumption: S-cone responses have been found in brain regions, such as the middle temporal (MT) motion area, not thought to play a major role in color perception. Here, we review the processing of S-cone signals across cortex and present original data on S-cone responses measured with fMRI in alert macaque, focusing on one area in which S-cone signals seem likely to contribute to color (V4/posterior inferior temporal cortex) and on one area in which S signals are unlikely to play a role in color (MT). We advance a hypothesis that the S-cone signals in color-computing areas are required to achieve a balanced neural representation of perceptual color space, whereas those in noncolor-areas provide a cue to illumination (not luminance) and confer sensitivity to the chromatic contrast generated by natural daylight (shadows, illuminated by ambient sky, surrounded by direct sunlight). This sensitivity would facilitate the extraction of shape-from-shadow signals to benefit global scene analysis and motion perception.

Color-Biased Regions of the Ventral Visual Pathway Lie between Face- and Place-Selective Regions in Humans, as in Macaques

The existence of color-processing regions in the human ventral visual pathway (VVP) has long been known from patient and imaging studies, but their location in the cortex relative to other regions, their selectivity for color compared with other properties (shape and object category), and their relationship to color-processing regions found in nonhuman primates remain unclear. We addressed these questions by scanning 13 subjects with fMRI while they viewed two versions of movie clips (colored, achromatic) of five different object classes (faces, scenes, bodies, objects, scrambled objects). We identified regions in each subject that were selective for color, faces, places, and object shape, and measured responses within these regions to the 10 conditions in independently acquired data. We report two key findings. First, the three previously reported color-biased regions (located within a band running posterior–anterior along the VVP, present in most of our subjects) were sandwiched between face-selective cortex and place-selective cortex, forming parallel bands of face, color, and place selectivity that tracked the fusiform gyrus/collateral sulcus. Second, the posterior color-biased regions showed little or no selectivity for object shape or for particular stimulus categories and showed no interaction of color preference with stimulus category, suggesting that they code color independently of shape or stimulus category; moreover, the shape-biased lateral occipital region showed no significant color bias. These observations mirror results in macaque inferior temporal cortex (Lafer-Sousa and Conway, 2013), and taken together, these results suggest a homology in which the entire tripartite face/color/place system of primates migrated onto the ventral surface in humans over the course of evolution. SIGNIFICANCE STATEMENT Here we report that color-biased cortex is sandwiched between face-selective and place-selective cortex on the bottom surface of the brain in humans. This face/color/place organization mirrors that seen on the lateral surface of the temporal lobe in macaques, suggesting that the entire tripartite system is homologous between species. This result validates the use of macaques as a model for human vision, making possible more powerful investigations into the connectivity, precise neural codes, and development of this part of the brain. In addition, we find substantial segregation of color from shape selectivity in posterior regions, as observed in macaques, indicating a considerable dissociation of the processing of shape and color in both species.

Perspectives on science and art

Artists try to understand how we see, sometimes explicitly exploring rules of perspective or color, visual illusions, or iconography, and conversely, scientists who study vision sometimes address the perceptual questions and discoveries raised by the works of art, as we do here.

Color tuning in alert macaque V1 assessed with fMRI and single-unit recording shows a bias toward daylight colors

Colors defined by the two intermediate directions in color space, orange-cyan and lime-magenta, elicit the same spatiotemporal average response from the two cardinal chromatic channels in the lateral geniculate nucleus (LGN). While we found LGN functional magnetic resonance imaging (fMRI) responses to these pairs of colors were statistically indistinguishable, primary visual cortex (V1) fMRI responses were stronger to orange-cyan. Moreover, linear combinations of single-cell responses to cone-isolating stimuli of V1 cone-opponent cells also yielded stronger predicted responses to orange-cyan over lime-magenta, suggesting these neurons underlie the fMRI result. These observations are consistent with the hypothesis that V1 recombines LGN signals into higher-order mechanisms tuned to noncardinal color directions. In light of work showing that natural images and daylight samples are biased toward orange-cyan, our findings further suggest that V1 is adapted to daylight. V1, especially double-opponent cells, may function to extract spatial information from color boundaries correlated with scene-structure cues, such as shadows lit by ambient blue sky juxtaposed with surfaces reflecting sunshine.

Evolution of Neural Computations: Mantis Shrimp and Human Color Decoding

Mantis shrimp and primates both possess good color vision, but the neural implementation in the two species is very different, a reflection of the largely unrelated evolutionary lineages of these creatures. Mantis shrimp have scanning compound eyes with 12 classes of photoreceptors, and have evolved a system to decode color information at the front-end of the sensory stream. Primates have image-focusing eyes with three classes of cones, and decode color further along the visual-processing hierarchy. Despite these differences, we report a fascinating parallel between the computational strategies at the color-decoding stage in the brains of stomatopods and primates. Both species appear to use narrowly tuned cells that support interval decoding color identification.

Response: Towards a neural representation for unique hues

Summary We recently reported that a population of color-tuned neurons in posterior inferior temporal cortex of macaque monkey represents all colors and that this population shows a bias towards certain colors: we found that many cells were tuned to red, followed by peaks to green, blue, and an indistinct peak corresponding to yellow [1]. This appears to be the closest explicit neural representation of unique hues found in the primate. John Mollon suggests that the distribution is what one would expect of neurons found earlier in the visual pathway, in lateral geniculate nucleus (LGN), if tested with the colors we used to measure tuning. Previous work has shown that LGN cells respond linearly to changes in cone contrast and do not represent unique hues. While we acknowledge that our stimuli would constrain the populations color-tuning distribution if the neurons were linear, the recorded cells have narrow nonlinear color tuning, quite unlike LGN cells. Thus, the population tuning is consistent with our initial interpretation.

Color naming across languages reflects color use

Significance The number of color terms varies drastically across languages. Yet despite these differences, certain terms (e.g., red) are prevalent, which has been attributed to perceptual salience. This work provides evidence for an alternative hypothesis: The use of color terms depends on communicative needs. Across languages, from the hunter-gatherer Tsimane people of the Amazon to students in Boston, warm colors are communicated more efficiently than cool colors. This cross-linguistic pattern reflects the color statistics of the world: Objects (what we talk about) are typically warm-colored, and backgrounds are cool-colored. Communicative needs also explain why the number of color terms varies across languages: Cultures vary in how useful color is. Industrialization, which creates objects distinguishable solely based on color, increases color usefulness. What determines how languages categorize colors? We analyzed results of the World Color Survey (WCS) of 110 languages to show that despite gross differences across languages, communication of chromatic chips is always better for warm colors (yellows/reds) than cool colors (blues/greens). We present an analysis of color statistics in a large databank of natural images curated by human observers for salient objects and show that objects tend to have warm rather than cool colors. These results suggest that the cross-linguistic similarity in color-naming efficiency reflects colors of universal usefulness and provide an account of a principle (color use) that governs how color categories come about. We show that potential methodological issues with the WCS do not corrupt information-theoretic analyses, by collecting original data using two extreme versions of the color-naming task, in three groups: the Tsimane, a remote Amazonian hunter-gatherer isolate; Bolivian-Spanish speakers; and English speakers. These data also enabled us to test another prediction of the color-usefulness hypothesis: that differences in color categorization between languages are caused by differences in overall usefulness of color to a culture. In support, we found that color naming among Tsimane had relatively low communicative efficiency, and the Tsimane were less likely to use color terms when describing familiar objects. Color-naming among Tsimane was boosted when naming artificially colored objects compared with natural objects, suggesting that industrialization promotes color usefulness.