Ординатура / Офтальмология / Английские материалы / The Neuropsychology of Vision_Fahle, Greenlee_2003

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many times that disorders, such as colour anomia (Oxbury et al. 1969) and colour agnosia (Beauvois and Saillant 1985), and deficits of colour imagery and memory (Kinsbourne and Warrington 1964; Luzzatti and Davidoff 1994), are quite distinct. Equally, the loss of colour vision as a result of brain damage can occur as a strikingly selective disorder. Whether colour constancy can be selectively impaired is less clear and will be discussed.

Visual pathways in the primate brain

It is now established that the primate brain contains multiple visual areas, although both their precise number and perceptual roles are far from clear. It is unnecessary to dwell at length on the organization of the primate visual system, which is described in Chapter 5, this volume and reviewed extensively elsewhere (see Livingstone and Hubel 1987a,b; Zeki and Shipp 1988; Schiller et al. 1990; Zeki 1990a,b). In brief, areas in the parietal and temporal lobes are associated with ‘dorsal’ and ‘ventral’ streams of visual processing. Dorsal stream areas play a crucial role in the visual control of action and are functionally distinct (which is not to say that they never interact) from those in the ventral stream, which convey information about colour and form to the temporal lobe (Milner and Goodale 1995). Moreover, electrophysiological studies have distinguished between P- and M-channels of visual processing, which cannot, however, be assigned to the two distinct groupings of visual cortical areas in a straightforward and exclusive manner.

The M- and P-channels originate in the P and P ganglion cells of the primate retina, respectively. These different classes of cells send their axons to different laminae of the dorsal lateral geniculate nucleus (dLGN), the magnocellular and parvocellular layers, from which the channels derive their name. The M- and P-channels convey different properties of the visual image to primary visual cortex. Whereas the M-channel chiefly relays low-contrast, achromatic visual information at high temporal frequencies, the P-channel is principally concerned with the chromatic properties of the image and the processing of higher spatial, and lower temporal, frequencies.

More recently, a third pathway has been identified, arising from blue/yellow bistratified ganglion cells, and dubbed the koniocellular (K) pathway (Hendry and Yoshioka 1994; Dacey 1993: Dacey and Lee 1994). The interlaminar K-cells are much more numerous than previously thought and may be as common as the M-cells. It has been suggested that they play a major role in aspects of colour vision, but this remains to be established (for reviews see Dacey 1993, 2000; Hendry and Reid 2000).

The segregation between the retinocortical visual pathways of primates, so prominent in the dLGN, continues up to primary and secondary visual cortical areas. The parvocellular layers of the dLGN project to layer 4C of V1 and then to the so-called ‘blob’ and ‘interblob’ regions in primary visual cortex, revealed by labelling with the metabolic marker, cytochrome oxidase. The blobs also receive a direct projection from interlaminar dLGN cells of the K-channel. The cells in the cytochrome oxidase blobs are selective for wavelength, but not orientation. In contradistinction, orientation, but

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not wavelength selectivity, is common in cells in the interblobs. The blobs and interblobs of V1 project to cytochrome oxidase-rich thin stripes and cytochrome oxidase-deficient interstripes in area V2, which, in turn, project to area V4.

In contrast, the magnocellular channel in dLGN projects primarily to layer 4C of area V1 and from there to layer 4B. Layer 4B projects both directly and, via the cytochrome oxidase-rich thick stripes in V2, to cortical area MT.

In summary, the blob and interblob regions provide two arms of the P-channel that project to visual areas assigned to the ventral stream. As the response properties of their constituent neurons suggest, the blob and interblob regions code wavelength and form, respectively. The orientation and direction selectivity of cells in the M-channel, along with their high luminance contrast gain, suggests that it plays a role in conveying motion and form information to visual areas in the parietal lobes.

Area V4 and colour

While the properties of single neurons cannot unambiguously provide a reliable indicator of the perceptual role of the visual area in which they reside (Cowey 1994), it has been argued that area V4 plays a pivotal role in colour processing, particularly in colour constancy (Zeki 1990b). This proposal is based on the early observation that V4 contains a relatively high proportion of cells that code colour (Zeki 1973). The later demonstration (Zeki 1983) that cells in V4, unlike those in V1, respond to the colour of a surface in a complex chromatic scene, regardless of the wavelength composition of the reflected light, i.e. that they appear to achieve colour constancy, has bolstered this view. There are, however, some detractors. For example, successive studies have, more recently, reported ever-declining estimates of the proportion of colour-coded cells in area V4 (see below). Furthermore, it has been suggested that cells exhibiting colour constancy are just as evident in V1 as long as the stimuli used to examine it are scaled to match the smaller receptive field in V1 (Wachtler et al. 1999). Notwithstanding, this conflicting evidence has not prevented V4 from being termed the ‘colour area’. Certainly, the large receptive fields of cells in V4, and their widespread callosal connections, suggest this area engages in long-range processes of the sort required for mediating colour constancy. Such processes are thought to include the calculation of the relative ratios of the intensity of light of different wavebands from different surfaces. Ratios are independent of the absolute intensities, and therefore of the illuminant. Thus V4, the ‘colour area’, has been identified as an area where such ratios are computed and constant colours are assigned to surfaces.

If area V4 is critical for the ratio-taking processes outlined above, then its destruction should lead to a selective failing of colour constancy. The chromatic vision of the monkey should then rely on colour processes earlier in the visual pathway, namely, those in areas V1 and V2, where cells respond to the wavelength distribution of light falling in their receptive fields. The monkey should retain the ability to tell colours apart but the colour appearance of a surface will depend on the spectral power distribution of the illuminant. We shall return to this issue below but suffice it to say that the evidence that

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Fig. 8.2 To the left is a chromatic Mondrian pattern and, to the right, its achromatic counterpart. (See Plate 6, colour plate section.)

bilateral ablation of simian V4 results in colour impairment, especially of colour constancy, is slim. Meanwhile, it should be noted that there was a further reason that encouraged area V4 to be functionally dubbed the ‘colour area’.

An early interpretation of the roles of multiple visual areas was that each is relatively specialized for the processing of a different perceptual attribute. However, attempts to assign perceptual functions to visual areas of the brain, either on the basis of the response properties of their cells, or from inferences made from the behavioural effects of selective ablation, have encountered considerable difficulties (see Cowey 1994 for review). In stark contrast to the absence of compelling evidence for selective visual disorders following the ablation of any single visual area in monkeys, naturally occurring brain lesions in man occasionally produce disorders that are strikingly selective. Most notable among these is the clinical condition of cerebral achromatopsia, where medial occipitotemporal damage can abolish colour vision (Brill 1882; Meadows 1974; Albert et al. 1975; Green and Lessell 1977; Heywood et al. 1987; Victor et al. 1989; Zeki 1993). The selectivity of the disorder is consistent with the notion of functional specialization within different regions of extrastriate visual cortex. The advent of neuroimaging allowed for a further supposition.

An early study demonstrated a hotspot of activation in the region of the lingual and fusiform gyri when normal observers passively viewed a display of coloured rectilinear patches (called a Mondrian; Fig. 8.2) compared with the viewing of an identical, but achromatic scene of equivalent lightnesses (Zeki et al. 1991).

The activation was located within the region invariably damaged in the brains of achromatopsic patients, albeit their lesions are a great deal more extensive. It was a short step to equate this ‘colour centre’ with the macaque colour area identified by other means, and designate it ‘human V4’. The step may have been premature.

Cerebral achromatopsia

Cerebral achromatopsia refers to the loss of colour vision as a result of brain damage. Patients retain three functional cone mechanisms (Mollon et al. 1980) as shown by the increment threshold technique of Stiles (1978) and the deficit is clearly of central origin. Patients are unable to match, discriminate, sort, or name colours and perform poorly on the Farnsworth–Munsell 100-Hue test, which requires placing in chromatic

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Fig. 8.3 An Ishihara plate is composed of small circles with random luminance variation. The numeral is defined by colour difference. (See Plate 7, colour plate section.)

order a number of equiluminant coloured chips (at least they are equiluminant for the average, young, male observer). The deficit exists in varying degrees of severity where in cases of incomplete achromatopsia there is frequently a greater loss of blues and greens and a relative sparing of reds (Pearlman et al. 1979). On another conventional test of colour vision, the Ishihara pseudoisochromatic plates (Fig. 8.3), results are variable. Some patients are able to read some or all of the plates (Meadows 1974; Victor et al. 1989), while others only succeed under particular testing conditions, notably viewing distance (Green and Lessell 1977; Albert et al. 1975; Heywood et al. 1987).

It is often stated that patients complain that their visual world is drained of colour and consists of ‘dirty’ shades of grey. However, it is unclear and, to our knowledge, never yet discussed whether such subjective reports of visual phenomenology are possible only in cases of incomplete loss, the so-called dyschromatopsias. Just as a severe visual field loss may go unreported, the complete absence of the processing system that underlies our visual phenomenology may render an achromatopsic patient incapable of reporting the absence of a perceptual attribute that is normally the product of the missing neural machinery. This may account for the strange reluctance on the part of patients to assign labels to their perceptions of chromatic or achromatic surfaces, unless their achromatopsia affects only one hemifield, in which case the normal hemifield preserves their conceptual knowledge about colour. There is little reason to suppose that their phenomenal experience is akin to a chromatic image stripped of colour variation, i.e. as a normal observer may experience a monochrome display. Indeed, the putative mechanisms that have been lost are presumed to undertake computations just as essential for determining the greyness of a surface as any other colour tone. Some patients retain visual imagery of colours (Shuren et al. 1996), and it is unknown whether such sparing relates to a greater readiness to describe the nature of their colourless world.

Achromatopsia is frequently, though not invariably (Duvelleroy et al. 1997), accompanied by impaired facial recognition (prosopagnosia) and altitudinal visual field defects (Meadows 1974). This is a straightforward consequence of the proximity of the ‘colour centre’ to face-processing regions in the fusiform gyrus and the lip and lower bank of area V1, which topographically represents the upper visual field. However, there are occasional reports where the impairment is restricted to the perception of colour (Mackay and Dunlop 1899; Kölmel 1988; Damasio el al. 1980; Sacks et al. 1988). Without doubting any of the observations made in these reports it should not be forgotten that the examination of non-chromatic vision was hardly extensive.

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As noted by Verrey (1888), achromatopsia can be confined to one hemifield or a single quadrant (Wilbrand 1884; Kölmel 1988). In such cases patients may be unaware of their loss, again implying that the activity normally elicited in the damaged region perhaps mediates attention to colour, or is the neural correlate of conscious colour experience.

It is becoming increasingly clear that, while achromatopsia patients have depleted colour vision, they can nevertheless use wavelength variation to determine other aspects of the visual scene. In this respect, those with complete achromatopsia are particularly informative and one such patient, M.S., has been studied extensively. An early indication that, paradoxically, the loss of colour vision does not prevent the segmentation of the visual scene on the basis of colour differences was provided by Mollon et al. (1980). Patient M.S. was unable to read the Ishihara pseudoisochromatic plates at conventional reading distance but could do so when they were presented at 2 m. The test requires the identification of a numeral that is defined by coloured dots embedded in similar dots of varying lightness. At normal reading distance, the chromatic border that defines the numeral is masked by the luminance contour of individual dots. At a distance where the latter can no longer be resolved, or when the plate is optically blurred (Heywood et al. 1991), M.S. can detect the now dominant chromatic boundary and report the concealed figure. In a further test (Heywood et al. 1991), M.S. was presented with two rows of equiluminant coloured patches. In each row the colours abutted each other, but in one row they were in chromatic order and in the other they were jumbled (Fig. 8.4(a)). M.S. could tell the difference between jumbled and ordered arrays, presumably by detecting, and distinguishing the salience of, chromatic boundaries. In the jumbled array, adjacent equiluminant hues were inevitably more widely separated in colour space and the greater chromatic contrast presumably made them more salient. Chromatic borders between two equiluminant hues are therefore visible to M.S. even when the two hues cannot be told apart. And when the colours were all moved a few mm apart, creating a conspicuous white border between all adjacent colours, he became unable to discriminate the ordered from disordered series (Fig. 8.4(b)). It would be interesting to see whether the widely

(a)

(b)

Fig. 8.4 (a) The upper figure is a row of abutting equiluminant patches ordered in chromaticity. Below, the identical patches are presented as a jumbled array. Although M.S. was unable to discriminate between any of the constituent patches, he was able to discriminate between the ordered and jumbled arrays. In (b) the patches no longer abut and M.S. can no longer tell the arrays apart. (See Plate 8, colour plate section.)

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Fig. 8.5 The figure is composed of an achromatic checkerboard (draught board) in which a green cross is embedded. When the luminance of each square is rapidly varied from moment to moment, M.S. effortlessly detects the location of the green cross. The rapid fluctuation in luminance, to which the M-channel is sensitive, would render it ineffective in detecting the chromatic contour. Detection must presumably be mediated by a preserved P- or K-channel. (See Plate 9, colour plate section.)

used Farnsworth–Munsell 100-Hue test would become possible for achromatopsic patients if the prominent black border round every colour were removed!

These abilities are consistent with the properties of broad-band cells in the M-channel, i.e. those that sum the output of longand middle-wavelength cones, rather than acting in an opponent fashion, which can signal chromatic contour without coding information about the constituent colours (Saito et al. 1989). One possible interpretation of achromatopsia is that it results from selective destruction of the P-channel. However, several lines of evidence argue against this attractively simple proposal. The introduction of rapid and spurious spatial and temporal luminance fluctuations (luminance noise) into chromatic visual displays prevents the broad-band system from distinguishing between chromatic and luminance contrast. Such random luminance masking did not prevent M.S. from segregating figure and ground on the basis of chromatic cues alone (Fig. 8.5), suggesting preservation of the colour-opponent P-channel and/or the K-channel (Heywood et al. 1994). Thus, M.S. can use wavelength to extract form despite lacking any phenomenal experience of colour itself. Moreover, M.S. has essentially normal chromatic contrast sensitivity for the detection of sinusoidally modulated equiluminant chromatic gratings, i.e. he can detect gratings composed of colour differences he cannot tell apart (Heywood et al. 1996). A similar dissociation has been reported in cases of incomplete achromatopsia (Barbur et al. 1994). Unlike in normal observers, thresholds for the detection of colour change differ from those for revealing chromatic form suggesting that different and independent processes contribute to perceived object colour and form derived from chromatic signals.

A second reason to suspect P-channel involvement stems from measurements of spectral sensitivity (Heywood et al. 1991). As illustrated in Fig. 8.6, M.S. does not show the single peak at ~550 nm characteristic of the sensitivity of the broadband channel, but shows sensitivity peaks at three different wavelengths, indicative of colouropponent mechanisms of the P-channel (Sperling and Harwerth 1971). One consequence of colour-opponency is that mixtures of red and green light result in a yellow

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Fig. 8.7 The figure shows four successively presented frames of an equiluminant display where the phase of the pattern is shifted a quarter of a cycle. The direction of motion (left-to-right) can only be ascertained by matching successive green/red borders. If red/green and green/red borders cannot be distinguished, the direction of motion will be ambiguous. (See Plate 10, colour plate section.)

even though he was unable to tell apart the constituent colours of the grating (Heywood et al. 1994).

There are two further reports of spared motion processes in achromatopsia. In the first (Cavanagh et al. 1998), three achromatopsic patients were presented with moving, high-contrast, equiluminant chromatic gratings. It was possible to measure the strength of the preserved motion response based on colour by gauging the equivalent luminance contrast countermotion required to null it. Unlike M.S., these achromatopsic patients had grossly impaired sensitivity to chromatic contrast. Nevertheless, high-contrast equiluminant gratings produced a robust motion response equivalent to that of normal observers. The response was five to ten times stronger than that expected from the chromatic mechanism identified with area MT and was presumably mediated elsewhere. The second report (Heywood et al. 1998) provides indirect evidence for an intact P-channel contribution to motion in achromatopsia.

The ‘slow’ chromatic motion pathway is highly sensitive to chromatic contrast but does not code velocity veridically. This perhaps accounts for the phenomenon of ‘motion slowing’, where drifting, sinusoidal chromatic gratings are perceived as moving considerably more slowly than an achromatic grating drifting at the same speed. When sinusoidal gratings are constructed by the addition of middleand longwavelength light in spatial antiphase (as in Fig. 8.8(a)), the effects of brightness subadditivity will result in unintended brightness variation. This is most conspicuous midway between the red and green peaks, where red and green are mixed in equal proportion. The slow-motion channel receives a colour-opponent input and will therefore be susceptible to the sort of subadditive brightness responses described above, i.e. it is plausible that such brightness variation might influence perceived speed. When this brightness variation was corrected, by the addition of an appropriate amount of frequency-doubled luminance (Fig. 8.8(b)), there was a further reduction in the apparent speed of the grating in 10 observers with normal colour vision (Heywood et al. 1998). However, the same occurred for patient M.S., indicating processing of slow equiluminant chromatic motion even when, for M.S., the colours are indistinguishable.

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colours are assigned prior to subsequent processing to extract motion and form, then residual abilities based on spectral processing in cases of cortical colour blindness are unexpected. Instead, they propose that phenomenal colour is a secondary consequence of these several dissociable spectral processes, damage to which could delete some, but not all, aspects of conscious visual experience. These proposals are consistent with the nature of residual chromatic processing, described above, in a case of complete achromatopsia, patient M.S. (Heywood et al. 1994). They are also in agreement with accounts elsewhere (Cowey and Heywood 1997; Heywood et al. 1998), where we argued that residual abilities are mediated, not by what remains of a damaged ‘colour centre’, but by other independent spectral processes that use wavelength differences to derive other visual attributes. Each of these remaining processes has a conscious correlate.

The studies described above suggest that wavelength variation in the visual scene can be used, not only to produce colour experience, but also to determine further attributes such as form and motion. In achromatopsia, colour experience can be obliterated while the latter remain intact. Such cases provide important clues about the organization of the colour pathways, which, more recently, have been more closely examined by imaging the brains of normal observers viewing a variety of chromatic displays.

Functional neuroimaging of the colour pathways

The location of an extrastriate focus of activation concerned with chromatic processing has now been confirmed in a number of neuroimaging studies using markedly different paradigms. They can broadly be divided into those that entail passive viewing of chromatic displays, where residual cortical activation (as revealed by cerebral blood flow) after appropriate subtraction of an achromatic reference condition identifies regions responding to chromaticity, and those that involve a discrimination task in each of the two conditions. In the first category, the study mentioned earlier (Zeki et al. 1991) used positron emission tomography (PET) and required subjects to passively view ‘Mondrian’ patterns composed of chromatic patches of different hue and brightness. The reference condition was an identical arrangement of grey patches with the same corresponding luminance (Fig. 8.2). The activation of the fusiform gyrus revealed by PET has been demonstrated in several subsequent studies. Sakai et al. (l995) replicated this finding using functional magnetic resonance imaging (fMRI), where a focal signal increase in the posterior part of the fusiform gyrus correlated with the percept of colour, most notably with the perception of afterimages. Activation in response to the passive viewing of an array of coloured circles was compared with that in response to an identical array of achromatic circles, equiluminant with their coloured counterparts. Activation was bilateral in some subjects and unilateral in others. Similarly, Kleinschmidt et al. (1996) demonstrated bilateral activation, using fMRI, in the collateral sulci and extending into the lingual and fusiform gyri, when subjects viewed equiluminant chromatic modulation, but not isochromatic luminance modulation, and the reference condition was a uniform field