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response was identified and then presented in three different versions, color, grayscale and black-and-white (B/W).
Resulting from the earlier connections between the P and M pathways, dorsal structures show also mixed sensitivity to different visual attributes. One clear example comes from MT neurons. It has been described that direction-sensitive neurons in this area modulate their responses depending on color although they do not show isolated color responses (Charles & Logothetis, 1989; Saito et al., 1989; Dobkins & Albright, 1990, 1991, 1994; Albright, 1992; Gegenfurtner et al., 1994).
The following table summarizes the main studies showing combined responses for color and some other visual attributes at different stages along the visual pathway.
Table 1. Mixed responses to color and other visual attributes in human and monkey studies. Information about the specific areas considered is included, showing the intercommunication observed all along different visual stages.
2.2. Evidences For and Against a Specialized Color Centre in the Primate
Most of classical studies in color processing suggested the existence of a color centre in the primate brain. Such a critical area, involved in high chromatic analyses, was located in V4, and subdivided into two main regions, an anterior one, called V4α, and a posterior one, simply named V4, and localized at the posterior fusiform circumvolution (Zeki & Bartels, 1999). However, the exact location of this area seems to vary for every subject, extending from the collateral sulcus, at the fusiform circumvolution, to the lingual gyrus (Beauchamp et al., 1999).
Area V4 performs higher level color analyses, including the comparison of wavelength differences with surrounding objects (Lueck et al., 1989; Zeki et al., 1991; Zeki & Marini, 1998). It has been suggested that the role played by this structure would not be related with simple color processing, but more to color and shape interactive analyses of objects (Heywood & Cowey, 1987; Schiller & Lee, 1991; Walsh et al., 1992a; Merigan, 1996;
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Merigan & Pham, 1998; De Weerd et al., 1996, 1999; Barrett et al., 2001). Furthermore, area V4 is an important region for visual attention, as attentional modulation appears to improve the spatial selectivity in this area (Moran & Desimone, 1985; Haenny et al., 1987; Maunsell et al., 1991; Motter, 1994; McAdams & Maunsell, 1999) and its selective lesion disrupt performance in attentionally demanding visual searching tasks (Schiller and Lee, 1991; Schiller, 1995; De Weerd et al., 1999).
In the macaque, V4 is one of the largest visual areas, occupying about 10% of the visual cortex and 5% of the neocortex (Felleman & Van Essen, 1991). Situated as an intermediate structure in the ventral visual stream (Ungerleider & Mishkin, 1982), this area receives direct inputs from V2, and projects primarily to the posterior IT cortex (area TEO) (Felleman & Van Essen, 1991). Neurophysiological studies have shown that macaque area V4 contains a high proportion of color selective cells (Schein & Desimone, 1990; Zeki, 1975, 1983b). As the complex analyses developed by these cells largely exceed the chromatic processing observed in earlier visual areas, V4 has been suggested to play an important role in color constancy (Zeki, 1980; Zeki et al., 1999). However, pure achromatopsia can be derived from different lesions at several visual structures (Cowey & Heywood, 1995; Heywood et al., 1995; Hadjikhani et al., 1998; Heywood & Cowey, 1998), and therefore, simple damage in V4 is not enough to explain the whole deficit (Kölmel, 1988; McKeefry & Zeki, 1997).
In humans, whereas ventral V4 (V4v) has been localized next to VP (V3v) (Sereno et al., 1995; De Yoe et al., 1996), its dorsal subdivision (V4d) has not been yet clearly identified, contributing to maintain the current debate on the functional equivalence between human and non-human primate area V4 (Tootell & Hadjikhani, 2001). To solve the homology problem, Zeki and colleagues (1991) proposed the fusiform and the lingual gyri in the human cortex as the equivalent areas to V4 in the monkey brain. Later on, this group suggested the posterior fusiform gyrus as a more precise location for human V4 (McKeefry & Zeki, 1997). In agreement with this idea, functional Magnetic Resonance Imaging (fMRI) studies have shown that patients with cerebral achromatopsia often present damage at this structure, together with, in some particular cases, specific damage of the lingual gyrus and the basal temporal cortex (Meadows, 1974; Green & Lessell, 1977; Lapresle et al., 1977; Damasio et al., 1980; Damasio & Frank, 1992; Allison et al., 1993; Lee et al., 2000; Girkin & Miller, 2001). The simultaneous lesion of these three structures is common in subjects affected by visual hallucinations and prosopagnosia (Damasio et al., 1982; Lee et al., 2000).
Similarly, selective lesions of the fusiform gyrus may affect face and object recognition as well as color perception (Puce et al., 1996; Kanwisher et al., 1997; Girkin & Miller, 2001). A small face-selective area has been described in the right lateral middle fusiform gyrus, (Halgren et al., 1999; Haxby et al., 1999; Rossion et al., 2000, 2003), in homology to the IT cortex (Tootell et al., 2003).
The reported data highlight the relevance of V4 and the fusiform gyrus in color processing. However, the observed color sensitivity of cells at different cortical stages has opened a debate about the existence of a possible color centre in the primate brain. In a recent study, Gonzalez and collaborators (2006) showed that the neuronal activity evoked in the human fusiform gyrus is strongly dependent on the stimulated hemifield (Gonzalez et al., 2006). This hemifield dependence indicates the early activation of this structure, suggesting that higher cortical areas can be required to combine the information from both visual hemifields. This new evidence supports the idea of a multistaged cortical system for color processing (Zeki & Marini, 1998). In agreement with this idea, it has been shown that color
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categorization can still occur after V4 ablation in the macaque (Walsh et al., 1992b). Additionally, lesion studies in patients with posterior cerebral infarcts demonstrated that color discrimination can be independent of color memory, reinforcing the assumption of multiple areas involved in color perception (Schoppig et al., 1999). From the same perspective, several authors found a left-dominant but mainly bilateral multistage activation of color-related areas in the human brain (Zeki et al., 1991; Corbetta et al., 1991; Howard et al., 1998; Zeki & Marini, 1998; Beauchamp et al., 1999; Barrett et al., 2001). These authors indicated that different visual areas could be selectively recruited for different chromatic analyses depending on the specific requirements of the task.
Finally, as in earlier chromatic visual areas, cells in V4 and the fusiform gyrus respond to complex combinations of visual parameters. Several neurophysiological studies in human and non-human primates have demonstrated that these cells are not only sensitive to color, but also to some other properties of the stimulus, such as the stimulus orientation (Mendola et al., 1999), and shape (Desimone & Schein, 1987; Gallant et al., 1993, 1996; Rizzo et al., 1993; Kobatake & Tanaka, 1994; Wilson et al., 1997; Allison et al., 1999; James et al., 1999; Pasupathy & Connor, 1999). In humans, Gonzalez and colleagues (2006) have found combined responses to color and texture in the fusiform gyrus. In their study, functional evoked potentials were recorded from subdural electrodes implanted in a patient suffering from occipital epilepsy. During simple fixation, dynamic squares of colorful dots were presented to the patient in both, left and right visual hemifields (contraand ipsilaterally to the affected hemisphere). Following this procedure fusiform activation was found after dynamic-textured squares but not solid squares (Figure 4).
Figure 4. Visual evoked responses recorded in the right fusiform gyrus of a patient suffering from occipital epilepsy (bipolar recording; BOT strip). The stimuli used consisted of solid figures and textured squares composed by dynamic random dots, all surrounded by a dark background. Only texture-related images evoked responses in the fusiform gyrus while no activation was observed for the solid stimuli. The thick line on the abscissa indicates the time the stimulus was on. On the left side, lateral and coronal views of the brain are shown, signaling the exact location of the electrode arrays implanted.