Color in the cortex: single- and double-opponent cells

Abstract

This is a review of the research during the past 25years on cortical processing of color signals. At the beginning of the period the modular view of cortical processing predominated. However, at present an alternative view, that color and form are linked inextricably in visual cortical processing, is more persuasive than it seemed in 1985. Also, the role of the primary visual cortex, V1, in color processing now seems much larger than it did in 1985. The re-evaluation of the important role of V1 in color vision was caused in part by investigations of human V1 responses to color, measured with functional magnetic resonance imaging, fMRI, and in part by the results of numerous studies of single-unit neurophysiology in non-human primates. The neurophysiological results have highlighted the importance of double-opponent cells in V1. Another new concept is population coding of hue, saturation, and brightness in cortical neuronal population activity.

Figure 1

Color contrast, brightness contrast and color appearance. All four central squares have identical wavelength spectra. Yet the color appearance of each central square can be strongly influenced by the surrounding region. A: the red disk surrounded by an equiluminant green or B: an equiluminant grey results in a saturated red disk. C: when the surround is red but reduced in luminance compared to the central patch then the central red square appears a desaturated pink and almost white. D: The red square on a black background results in the perception of reduced saturation and increased apparent brightness, a bright pink square.

Figure 2

A: Lateral view of the Old-World monkey brain. The striate (V1) and extrastriate regions are shown on a surface where the sulci have been “opened” to allow viewing of the borders between regions that are otherwise embedded in a sulcus. The regions in the upper parietal region of extrastriate cortex form the dorsal stream whereas those in the lower temporal region form the ventral stream. B: A schematic view of the processing in V1. The darker brown regions indicate the cytochrome oxidase (CO) rich regions of V1 that correspond to layers receiving the stronger input from the lateral geniculate nucleus (LGN), the light brown shows an intermediate level of CO staining. The input streams from the different divisions of the LGN magnocellular (magno or M), parvocellular (parvo or P) and koniocellular (konio or K) are shown at the lower left of the figure. The main axonal projections within the cortex (intracortical projections) are shown as the 1^st and 2^nd intracortical projections in the center and right of the figure. The cytochrome rich regions of V1 in layer 3 and lower 2 are referred to as “CO blobs”. The regions between blobs are the interblobs. C: The axonal projections to the first extrastriate visual area V2 from neurons in the CO-rich blobs (dark brown barrels in V1) project preferentially to the thin CO-rich stripes. The axonal projections from the interblob regions in V1 (turquoise) preferentially project to the CO poor (pale) and thick CO-rich stripes in V2. The further projections from the V2 regions are shown to visual area V4 and MT (V5). These two extrastriate areas are those that were identified by Zeki as the ‘Color’ area (V4) and the ‘Motion’ area (MT or V5).

Figure 3

Human fMRI responses in cone contrast space from Engel et al, 1997. The amount of contrast required to reach a criterion response is plotted for 18 different stimulus color directions – shown by the small dots in the panel labeled 1Hz in a. Each of the panels shows the responses modulated at three different temporal frequencies: 1, 4 and 10 Hz for two subjects. The data for BW is shown in the row marked a, for SE in the row marked b. The shape of the threshold contour is reciprocal to the relative strength of the response in different color directions. When the contour is close to the origin it means that the amount of contrast required to evoke a criterion response was low. If the points on the negative diagonal are closer to the origin than the points on the positive diagonal it means that the opponent L-M mechanism is more sensitive than the luminance L+M mechanism. The L-M opponent mechanism is more sensitive than the luminance mechanism for 1 and 4 Hz. Similar results were obtained in psychophysical experiments.

Figure 4

Color and orientation selectivity in V1 and V2 from Friedman et al (2003). Selectivity for stimulus orientation (x-axis) and for color (y-axis) is shown for neurons recorded in V1 and V2 of the awake monkey (from Friedman et al 2003). The orientation modulation was measured with bars of the optimal color oscillating across the receptive field at 1 Hz. The Orientation Modulation index was calculated as [Rmax − Rmin]/[Rmax + Rmin]. An Orientation Modulation index of 1 indicates that there was no response at the orientation 90 degrees to the optimal orientation, and an index close to zero means that the neuron was untuned for orientation. The Color Selectivity index was calculated as the relative response to 15 flashed bars of different colors. A Color Selectivity index of 0.93 indicates a response to only one of the colored bars, whereas an index close to zero indicates an equal response across all colors. There are many orientation-selective neurons that are also color-selective in both V1 and V2 shown by points in the upper right quadrant of both the panels.

Figure 5

The average spatial frequency tuning for three populations of V1 neurons. The tuning functions were estimated by Schluppeck and Engel (2002) from 230 neurons recorded by Johnson, Hawken, and Shapley. The dotted line represents the responses of the color-preferring neurons. It shows the characteristic low-pass spatial frequency tuning reported in most studies (Thorell et al, 1984; Lennie et al, 1990; Johnson et al, 2001, 2004; 2008; Solomon et al, 2004; 2005). The dashed line shows the responses of color-luminance neurons: cells classified as having robust responses to equiluminant color and to black/white luminance when the stimuli are matched for cone-contrast. Most of the chromatically opponent color-luminance simple cells are double opponent in that they have spatially separated chromatically opponent responses to L- and M-cones (Johnson et al, 2008; Figure 6). The solid line is the average spatial frequency tuning of the luminance-preferring neurons. The maximum responses of luminance cells to luminance patterns are more than twice the amplitude of the best response to equiluminance. The tuning of the color-luminance and luminance cells are bandpass and similar in both preferred spatial frequency (2.56 ± 1.26 cyc/° and 2.09 ± 1.00 cyc/° respectively) and in bandwidth (2.05 ± 0.70 octaves (full width, half height) and 2.96 ± 0.69 octaves respectively).

Figure 6

Double-opponent cells in V1 from Johnson et al (2008). The spatial organization of an orientation-selective, spatial-frequency-bandpass, double-opponent neuron’s receptive field (after Johnson et al 2008). A: shows a schematic receptive field with side-by-side spatially antagonistic regions with opponent cone-weights. The weighting above the horizontal plane is “ON”, where an increment of light will evoke an increase in response, whereas the weighting below the line is “OFF” where a decrement will result in a response. B: shows the two-dimensional spatial map obtained from a neuron in V1 by means of the subspace reverse correlation technique (Ringach et al, 1997) with L-cone isolating grating stimuli. C: the map obtained with M-cone isolating stimuli. At the starred location in B, the L-cone map is decrement excitatory, whereas in C, at the same location the M-cone map is increment excitatory, and vice versa for the location marked by the open circles. The schematic in A is a three dimensional representation of the overlay of the two cone maps to give an overall profile. A is not to scale with respect to B and C.

Figure 7

V2 stripe selectivity from Gegenfurtner (2003). The proportions of cells selective for color, orientation, direction of motion and size in different cytochrome oxidate (CO) compartments (thick stripes, thin stripes and interstripes) of macaque monkey area V2. The data are from six studies 37(DeYoe and Van Essen, 1985), 64(Peterhans and von der Heydt, 1993), 68 (Levitt et al, 1994), 75 (Roe and Ts’o, 1995), 76(Gegenfurtner et al, 1996), 80(Shipp and Zeki, 2002). The heavy black lines represent the means across all six studies. Despite the different methods used in these studies, the results show remarkable agreement.

Figure 8

Human color centers – fMRI from Mullen et al (2007). Average t-statistical map (n = 8) comparing Achromatic and Chromatic conditions, displayed on average unfolded cortical surfaces (from Mullen et al 2007). The oblique medial views of the left and right hemispheres are shown on the left and right, respectively. On the averaged surfaces, locations of the parietal–occipital sulcus (POS) and corpus callosum (CC) are indicated to facilitate orientation on the surfaces. Black-and-white dashed lines indicate the average visual area and border locations for V1, V2, V3, VP, V3A, hV4 and hMT+. The stars indicate the cortical representations of the fovea in each hemisphere based on the average of eight subjects. Significantly stronger responses to Achromatic than to the average of the two Chromatic stimuli are indicated by positive t-values (red–yellow scale) and significantly stronger responses to the average of the two Chromatic than to Achromatic stimuli are indicated by negative t-values (purple–blue scale).