The location of the human cerebral color center and the visual field representation within it

The notion that color may be the function of a specialized cortical area was hinted at several times before Louis Verrey (1888) published his paper entitled Hémiachromatopsie droite absolue (absolute right hemiachromatopsia). Verrey's advantage over his predecessors was that he had been able to examine the lesion that had led to the syndrome of acquired achromatopsia (cerebral color blindness). Apart from some involvement of the body of the corpus callosum, the lesion was confined to the fusiform and lingual gyri and was thus located in the inferior part of the occipital lobe (Fig. 67.1). Every word of Verrey's title, together with the figure representing the lesion in the brain of his achromatopsic patient, is worth studying. Together they tell a great deal about the organization of the visual brain even today, though much of this is not mentioned by Verrey and is read by me into his evidence with hindsight. Foremost among the lessons to be learned is something about the topographic organization of the human visual brain. Given that the lesion producing cerebral hemi-achromatopsia was located in the lingual and fusiform gyri, the title implies that a center located in the lower part of the occipital lobe controls color vision in both the upper and lower parts of the entire contralateral visual hemifield.

Figure 67.1..  

The sites of the lesions in the brain examined by Louis Verrey. (From Verrey, 1888.)

The discovery of a visual area lying outside the striate cortex was an embarrassment at the time (see Zeki, 1990, 1993, for reviews). Henschen and after him Holmes had concluded, correctly, that the lower part of the calcarine cortex (V1) represents the upper visual field and the upper part of the lower visual field. They had concluded, also correctly, that the calcarine cortex, which Henschen referred to as the “cortical retina” and Holmes as the “visuosensory” cortex, and which we now call the primary visual cortex or area V1, was coextensive with the striate cortex. This led both Henschen and Holmes to conclude, incorrectly, that V1 was the only visual center in the brain and therefore had to receive all visual “impressions,” including color impressions (see Zeki, 1993, for a review).

From his single case of achromatopsia, Verrey had concluded, correctly, that there is a color center in the brain, but he had also supposed, incorrectly, that this is part of the “visuosensory” cortex. The implication was obvious: that the “visuosensory cortex” or “cortical retina” of the brain was larger than that supposed by Henschen and by Holmes, that is, it was not confined to the striate cortex. Verrey implied that the primary visual receptive cortex had a specialized subdivision dealing with color. Verrey's conclusions about the cortical site for color processing (le centre du sense chromatique), together with his observation that both upper and lower contralateral quadrants were compromised in his unilaterally lesioned patient, implied that both quadrants are mapped in the lower part of the occipital lobe. Such an implicit supposition (which Verrey himself did not explicitly make) obviously cast a doubt on the way that Henschen and Holmes had supposed the visual field is mapped in the occipital lobe. Both Henschen and Holmes dealt with this in the same way, by brushing aside Verrey's evidence or ignoring it altogether, until it vanished from the literature (for reviews see Zeki, 1990, 1993).

There was a price to be paid for ignoring the significance of the finding that an area located in the lower occipital cortex controls color vision in both contralateral quadrants. That peril existed until well into the 1990s. Actually, it is probably with us even today. This is surprising because in 1980, Damasio alluded to it explicitly. He wrote: “one single area in each hemisphere controls color processing for the entire hemifield. This is so regardless of the fact that such an area is eccentrically located, in the lower visual association cortex, classically related to upper quadrant processing only. . . . The classic concept of a concentrically organized visual association cortex no longer appears tenable.” No one took much notice of what Damasio said then, and I don't think that anyone takes much notice of it today either.

There is probably a good explanation for this intellectual scotoma. With time, and with the discovery that “areas 18 and 19” (Brodmann, 1905; von Bonin and Bailey, 1951), or areas V2 and V3 (Cragg, 1969; Zeki, 1969), form concentric rings around V1 (Fig. 67.2), it became customary to consider that the upper part of the visual field is represented in the lower occipital lobe and vice versa. A new habit developed of tagging on the letter “v” or “d” to areas to indicate that they are located in the lower occipital lobe (“v”) and therefore represent upper fields or that they are located in the upper occipital lobe (“d”) and therefore represent lower visual fields. This terminology begged for confusion and trouble, which was not long in coming. It was based on an implicit assumption that had already been discounted, namely, that the upper contralateral quadrant is represented in the lower occipital lobe and vice versa. Verrey (1888) had shown that an area located in the lower occipital cortex must represent both contralateral quadrants (otherwise, how would one account for the complete contralateral hemiachromatopsia produced from a unilateral lesion in the lower occipital lobe?), and physiological evidence had shown that that an area located in the upper occipital lobe can represent both contralateral quadrants, as does area V3A (Van Essen and Zeki, 1978) or that it may be located somewhere between the two halves and still do the same, as does area MT in the owl monkey (Allman and Kaas, 1971). Indeed, Allman and Kaas had introduced the more neutral designations of + and − to indicate upper and lower field representation, respectively, without making either explicit or implicit assumptions about whether upper contralateral quadrants are represented only in the lower occipital lobe (Baker et al., 1981). It is unfortunate that their more sensible designations were not more widely used. If they had been, we might have avoided some of the present difficulties, though even that is not certain. At any rate, with implicit assumptions imposing themselves, if an area was found in the lower occipital cortex, “v” was hastily tagged on to it, irrespective of whether a dorsal counterpart could be found for it; if it was located in the upper occipital lobe, “d” was tagged on to it, again irrespective of whether a ventral counterpart could be found for it. It was but one step from this to describing what Jon Kaas (1993) has called “improbable” areas, ones that represent only one quadrant, with no representation for the other corresponding quadrant. But what kind of visual information is restricted to only one quadrant that it alone should have a cortical representation, without a companion area to represent the same information for the “unrepresented” quadrant? If the proponents of this bizarre terminology thought about it at all, they were not telling. A good example related to color vision is provided by area “VP.”

Figure 67.2..  

Brodmann's cytoarchitectonic map of the brain. Brodmann numbered the areas according to the sequence in which he studied them. Note how areas 18 and 19 form rings around area 17. (From Brodmann, 1909.)