Primary visual cortex (V1)

In early studies of the primate primary visual cortex, the proportion of chromatically responsive cells was estimated to be relatively low (Hubel and Wiesel, 1968). A few years later, it was found that many cells that respond to luminance variations also respond to color variations, bringing the overall proportion of color-selective cells to about 50% in the striate cortex of macaque monkeys (Gouras, 1974; Dow and Gouras, 1973; Johnson et al., 2001; Thorell et al., 1984; Yates, 1974). These results are supported by studies using functional magnetic resonance imaging (fMRI), which showed a strong color-opponent response in the primary visual cortex of human subjects (Engel et al., 1997; Kleinschmidt et al., 1996).

The chromatic properties of V1 cells show both differences from and similarities with those at earlier stages of visual processing (retinal ganglion cells or parvo cells of the lateral geniculate nucleus, pLGN). A number of studies showed that in V1, unlike in the pLGN, the distribution of the cells' preferred colors does not obviously cluster around particular directions in color space (Lennie et al., 1990; Yoshioka et al., 1996). While most color-selective pLGN cells prefer stimuli modulated either along a roughly red-green or blue-yellow direction, those in the primary visual cortex can have preferences for many other directions. However, Lennie et al. (1990) also found that pLGN and V1 cells have similar color tuning properties. They showed that a model that successfully describes the tuning properties of pLGN cells (Derrington et al., 1984) also fits the responses of most V1 neurons. This model postulates that the receptive field of cells can be summarized as a linear combination of the inputs from the three different cone classes. In other words, Lennie et al. showed that although V1 neurons, as a whole, sample color space more evenly than pLGN cells, individual cells in V1 are not more selective for color than pLGN cells. Other investigators have reported V1 cells with a narrow color selectivity that deviates significantly from the linear model (Cottaris and De Valois, 1998; Gouras, 1974; Yates, 1974), but overall, the proportion of such narrowly tuned cells appears to be small in V1.

A number of reports suggested that the color signals within V1 are carried by a special dedicated population of unoriented cells (Livingstone and Hubel, 1984; Roe and Ts'o, 1999; Ts'o and Gilbert, 1988). These results have been challenged more recently. In particular, Leventhal et al. (1995) found that most cells in the superficial layers of V1 are sensitive to both the orientation and color of a visual stimulus. In addition, many of these cells also signal the stimulus' direction of motion. More recently, Johnson et al. (2001) showed that V1 cells can simultaneously encode both the chromatic and spatial characteristics of a stimulus. These important findings raise serious doubts about the notion that color information is treated separately from other visual attributes within area V1.

While the contribution of V1 cells to color constancy has not been studied systematically, several results bear on that issue. In particular, a number of studies reported the existence of a population of double-opponent cells in the primary visual cortex of primates (Livingstone and Hubel, 1984; Michael, 1978a, 1978b, 1978c, 1979). These cells have a spatially and chromatically antagonistic center-surround organization, and their properties could lead them to play an important role in achieving color constancy (Zeki, 1980). Although some studies reported only a very low incidence of such cells in V1 (Lennie et al., 1990; Ts'o & Gilbert, 1988), their existence has been confirmed by more recent reports (Conway, 2001; Johnson et al., 2001). Finally, a possible role of V1 cells in color constancy is supported by their ability to adapt during prolonged exposure to a habituating stimulus (Lennie et al., 1994), while LGN neurons do not (Derrington and Lennie, 1984). Similar results have been reported by Engel and Furmanski (2001), who used fMRI to investigate the adaptability of the human primary visual cortex to chromatic stimuli. While these results suggest that the response properties of V1 cells could contribute to color constancy, they are by no means conclusive proof that color constancy is achieved in V1.