Elizabeth N. Johnson

The spatial transformation of color in the primary visual cortex of the macaque monkey

Perceptually, color is used to discriminate objects by hue and to identify color boundaries. The primate retina and the lateral geniculate nucleus (LGN) have cell populations sensitive to color modulation, but the role of the primary visual cortex (V1) in color signal processing is uncertain. We re-evaluated color processing in V1 by studying single-neuron responses to luminance and to equiluminant color patterns equated for cone contrast. Many neurons respond robustly to both equiluminant color and luminance modulation (color-luminance cells). Also, there are neurons that prefer luminance (luminance cells), and a few neurons that prefer color (color cells). Surprisingly, most color-luminance cells are spatial-frequency tuned, with approximately equal selectivity for chromatic and achromatic patterns. Therefore, V1 retains the color sensitivity provided by the LGN, and adds spatial selectivity for color boundaries.Perceptually, color is used to discriminate objects by hue and to identify color boundaries. The primate retina and the lateral geniculate nucleus (LGN) have cell populations sensitive to color modulation, but the role of the primary visual cortex (V1) in color signal processing is uncertain. We re-evaluated color processing in V1 by studying single-neuron responses to luminance and to equiluminant color patterns equated for cone contrast. Many neurons respond robustly to both equiluminant color and luminance modulation (color-luminance cells). Also, there are neurons that prefer luminance (luminance cells), and a few neurons that prefer color (color cells). Surprisingly, most color-luminance cells are spatial-frequency tuned, with approximately equal selectivity for chromatic and achromatic patterns. Therefore, V1 retains the color sensitivity provided by the LGN, and adds spatial selectivity for color boundaries.

Advances in Color Science: From Retina to Behavior

Color has become a premier model system for understanding how information is processed by neural circuits, and for investigating the relationships among genes, neural circuits, and perception. Both the physical stimulus for color and the perceptual output experienced as color are quite well characterized, but the neural mechanisms that underlie the transformation from stimulus to perception are incompletely understood. The past several years have seen important scientific and technical advances that are changing our understanding of these mechanisms. Here, and in the accompanying minisymposium, we review the latest findings and hypotheses regarding color computations in the retina, primary visual cortex, and higher-order visual areas, focusing on non-human primates, a model of human color vision.

The Representation of S-Cone Signals in Primary Visual Cortex

Recent studies of middle-wavelength-sensitive and long-wavelength-sensitive cone responses in primate primary visual cortex (V1) have challenged the view that color and form are represented by distinct neuronal populations. Individual V1 neurons exhibit hallmarks of both color and form processing (cone opponency and orientation selectivity), and many display cone interactions that do not fit classic chromatic/achromatic classifications. Comparable analysis of short-wavelength-sensitive (S) cone responses has yet to be achieved and is of considerable interest because S-cones are the basis for the primordial mammalian chromatic pathway. Using intrinsic and two-photon imaging techniques in the tree shrew, we assessed the properties of V1 layer 2/3 neurons responsive to S-cone stimulation. These responses were orientation selective, exhibited distinct spatiotemporal properties, and reflected integration of S-cone inputs via opponent, summing, and intermediate configurations. Our observations support a common framework for the representation of cone signals in V1, one that endows orientation-selective neurons with a range of chromatic, achromatic, and mixed response properties.

Color in the Cortex

We begin with a discussion of the role of human color vision, asking what value the possession of color vision adds to the perception of the natural scene, both in terms of our ability to see color differences (contrast) and in color identification. We then consider the psychophysical properties of cortical color vision and what they reveal about its use in determining shape and form. We pit against each other different models accounting for how achromatic (luminance) contrast and color contrast may be linked in the determination of shape, comparing a coloring book model, in which color plays only a subordinate or minor role, an intrinsic images model in which color contrast makes an independent contribution, and an integration model in which color and luminance contrast both provide cue-invariant form information to color–luminance shape detectors. These models are also interpreted in the light of what we know about the physiological basis of color vision through primate single cell recordings, particularly in area V1. Finally, we discuss what has been revealed about human color vision in V1 and extra striate cortex from fMRI studies.

Contrast Gain, Area Summation and Temporal Tuning in Primate Visual Cortex

Neurones at all levels of the visual pathway have receptive fields that can be described by measuring the neurone’s response to stimuli that vary in space and time. The result of this mapping is referred to as the spatiotemporal receptive field. In the retina and the lateral geniculate nucleus (LGN), the spatial receptive field has a center surround organization that is approximately circularly symmetric. For some retinal and LGN cells, the temporal component of the response is sustained: they are low-pass temporal-frequency tuning. Other retinal and LGN cells show transient temporal characteristics; they are bandpass in their temporal-frequency tuning. In the primary visual cortex, there is refinement of some characteristics of the spatio-temporal receptive field and the emergence of new properties (Hubel and Wiesel, 1962, 1968). The sharper tuning for spatial frequency is an example of refinement, whereas the appearance of orientation selectivity is an example of an emergent property. In addition, the temporal characteristics of many neurones are modified compared to their LGN inputs.

Distribution and diversity of intrinsically photosensitive retinal ganglion cells in tree shrew

Intrinsically photosensitive retinal ganglion cells (ipRGCs) mediate the pupillary light reflex, circadian entrainment, and may contribute to luminance and color perception. The diversity of ipRGCs varies from rodents to primates, suggesting differences in their contributions to retinal output. To further understand the variability in their organization and diversity across species, we used immunohistochemical methods to examine ipRGCs in tree shrew (Tupaia belangeri). Tree shrews share membership in the same clade, or evolutionary branch, as rodents and primates. They are highly visual, diurnal animals with a cone‐dominated retina and a geniculo‐cortical organization resembling that of primates. We identified cells with morphological similarities to M1 and M2 cells described previously in rodents and primates. M1‐like cells typically had somas in the ganglion cell layer, with 23% displaced to the inner nuclear layer (INL). However, unlike M1 cells, they had bistratified dendritic fields ramifying in S1 and S5 that collectively tiled space. M2‐like cells had dendritic fields restricted to S5 that were smaller and more densely branching. A novel third type of melanopsin immunopositive cell was identified. These cells had somata exclusively in the INL and monostratified dendritic fields restricted to S1 that tiled space. Surprisingly, these cells immunolabeled for tyrosine hydroxylase, a key component in dopamine synthesis. These cells immunolabeled for an RGC marker, not amacrine cell markers, suggesting that they are dopaminergic ipRGCs. We found no evidence for M4 or M5 ipRGCs, described previously in rodents. These results identify some organizational features of the ipRGC system that are canonical versus species‐specific.