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

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(a)Behavioural procedure: same/different orientations

Fig. 5.4 Effects of V4 and MT lesions on orientation discrimination. (a) Psychophysical testing procedure. Monkeys fixated a small spot for 1 s to initiate the trial. The orientation of the sample was chosen at random from a set of six orientations and the orientation of the test was the same as, or orthogonal to, that of the sample. (b) Contrast sensitivity. Only the contrast of the sample was varied; the test was set to 51% contrast. Spatial frequency, 1 c/deg; temporal frequency (counterphase flicker), 5 Hz. (c) Signal-to-noise thresholds. The grating was masked by adding 3 3 pixel two-dimensional noise. The noise levels masking the sample were varied. The test grating contained no noise and was set to 51% contrast, and the task was identical to that shown in (b). The area V4 lesion reduced contrast sensitivity and elevated signal/noise thresholds, while MT/MST lesions had no significant effect on orientation discrimination. Lesions of areas V4 and MT/MST were unilateral and were made by multiple injections of ibotenic acid. Representative data are shown for a single monkey with a V4 lesion and from another with an MT/MST lesion. The MT/MST lesion data were adapted from Rudolph and Pasternak (1999). The V4 lesion data were adapted from Rudolph (1997, University of Rochester, doctoral dissertation).

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Perception of complex form

Involvement of the ventral pathway in the perception of complex forms was initially suggested by physiological findings of shape selectivity in IT cortex (Gross et al. 1979). These results led to an extensive series of studies of the effects of IT lesions on form and other discriminations (e.g. Cowey and Gross 1970), which generally supported the idea that IT lesions affected shape discriminations. Subsequent physiological studies confirmed the extraordinary shape selectivity of IT neurons for such features as faces and hands (Desimone et al. 1984) as well as moderate shape tuning in V4 neurons (Kobatake and Tanaka 1994; Gallant et al. 1996; Pasupathy and Connor 1999).

Lesions of area V4

Many studies have shown that V4 lesions cause transitory disruption of moderately difficult shape discriminations. Walsh and his colleagues (1992a) found little effect of V4 lesions on a square–triangle discrimination, but did find an increase in the number of trials needed to relearn more complex form discriminations, including rotated letters and numbers. Heywood and Cowey (1987) reported that monkeys with V4 lesions required an increased number of trials to reach criterion (90% correct) on shape and face discriminations that had been trained before the lesions were made.

Other studies have found strong evidence for permanent shape discrimination deficits after V4 lesions. DeWeerd et al. (1996) reported consistent and pronounced deficits in orientation difference thresholds, using contours created by illusory contours, or texture differences. On the other hand, orientation thresholds for luminance, colour, or motion shear contours showed much less effect.

Heywood et al. (1992) examined visual search for the odd stimulus among nine stimuli presented on each trial. Monkeys with V4 lesions could perform the task when the odd stimulus differed in colour from the distractors, but when form discrimination was tested with alphanumeric characters, the discrimination ability was severely impaired.

Subsequently, Merigan (2000) used the approach of extended testing, one discrimination at a time, to try to uncover stimuli that could not be discriminated after V4 lesions. A wide range of line–element segmentation and grouping tasks, three-dimensional object discriminations (see Figs 5.3(a),(b) and 5.7), and discriminations involving illusory contours (see Fig. 5.3(c)), were tested under conditions designed to identify any residual discrimination ability that survived the lesion. Those discriminations that could not be easily performed at the visual field locus of the lesion were subsequently presented with added visual cues that were intensified or eliminated, under a staircase procedure, to aid discrimination. Also, these discriminations were initially presented at the edge of the affected portion of the visual field, and gradually moved toward the lesioned location dependent on the performance of the monkey. Despite these efforts, the monkeys were never able to relearn the grouping, illusory contour, and three-dimensional form discriminations. Those discriminations, unlike many

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predictable by varying either the size of the sample stimulus or by transforming the match stimuli and, under these conditions, matching dropped to near chance levels.

These results demonstrate an enduring deficit in shape discrimination or shapematching after V4 lesions that, in the studies that used controlled fixation testing, was confined to the region of the visual field corresponding to the lesion.

Lesions of IT cortex

Numerous studies have compared the effects of IT cortex and prestriate (largely V4) lesions on form discriminations (Gross 1973), and they have found a disruption of both initial learning and relearning of discriminations. For example, Cowey and Gross (1970) studied the effects of IT and prestriate lesions, and found deficits in both the initial learning and the retention of form discriminations after both IT and V4 lesions with both single and concurrently presented sets of visual stimuli.

Weiskrantz and Saunders (1984) used an unusual intervention to make object discriminations difficult. They trained monkeys to choose one of the two objects in nine pairs of objects, and then altered the appearance of the positive objects by ‘transforming’ their size, three-dimensional orientation, or the direction of lighting of an intense spotlight. They found that prestriate (largely V4) and IT lesions resulted in similarly large deficits in discriminating both the untransformed and transformed objects. In all cases, however, the monkeys could discriminate the transformed objects given sufficient practice.

The effects of IT lesions on shape perception have also been also examined by measuring thresholds, rather than trials to criterion. Blake et al. (1977) measured thresholds for discriminating right angles (90 ) from smaller, acute angles after IT lesions. They found that, although monkeys with IT lesions learned the discrimination more slowly, their final thresholds were not elevated. In a recent study, Huxlin et al. (2000b) tested shape distortion thresholds for simple geometric shapes (see Fig. 5.6(c)) before and after IT lesions. They found a relatively transient disruption in shape distortion thresholds. These results show that, when shape discrimination is assessed by measuring thresholds using procedures that usually involve extensive testing, it does not appear to be permanently disrupted by ventral pathway lesions.

Interpretation of these findings as a selective effect of ventral pathway lesions on the discrimination of complex form requires clear evidence that form discriminations are disrupted, while other discriminations are unaffected. Several of the studies described above have shown such a dissociation. For example, DeWeerd et al. (1996) found marked threshold elevations only for those contours that required complex form-processing. Luminance and colour contours, as well as those created by motion shear, were much less affected. Merigan (2000) reported that only a few form discriminations were severely affected by V4 lesions. Others, including the one illustrated in Fig. 5.3(b), were unaffected.

Thus, both V4 and IT lesions can cause an increase in the number of errors committed while learning or relearning complex form discriminations. Permanent disruption of complex form discriminations or elevation of thresholds measured with them, has been more pronounced after V4 than after IT lesions. These results confirm an

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important role for V4 neurons in complex form discriminations. The failure to find equally severe effects of IT lesions could be due to postlesion reorganization.

The studies described above can be divided into two groups. The first group assessed the effects of lesions by measuring either speed of learning of new discriminations or the postlesion retention of previously learned discriminations that were relatively easy. These studies have commonly reported a disruption in the performance of previously learned discriminations, or slowed learning of new discriminations, followed by subsequent recovery. The second group used more difficult discriminations and in some cases measured visual thresholds. When such studies have involved IT lesions, they have often reported no permanent performance or threshold deficits, while those involving V4 lesions have consistently reported a permanent, but variable, decrease in performance.

Colour vision

It has long been accepted that the ventral cortical pathway in primates is central to colour-processing. This view initially emerged from the findings of Zeki (1983a,b) that chromatic selectivity was particularly prominent in area V4 neurons. It was augmented by the later findings of strong colour components in the responses of both V4 (Schein and Desimone 1990) and IT neurons (Komatsu et al. 1992; Kobatake and Tanaka 1994). It has also been shown that the input to the colour-responsive regions within V4 comes from colour-tuned regions within V2 (thin stripes), which in turn receive input from the colour-responsive blobs of area V1 (Xiao et al. 1999). Based on the physiological evidence of colour selectivity, many studies have looked at the effect of V4 and IT lesions on basic colour discriminations (often hue difference thresholds or visual detection based on colour). A few studies have also examined the effect of V4 lesions on more complex colour discriminations.

Lesions of area V4

V4 lesions frequently cause a transitory disruption of colour vision, as indicated by an increase in the number of errors made while learning or relearning colour discrimination. Walsh and colleagues (1992b, 1993) trained monkeys after bilateral V4 lesions to make pairwise discriminations of colours (Munsell patches) and found slower learning of colour discriminations in those monkeys with V4 lesions. In the first experiment of a subsequent study, the same group (Walsh et al. 1993) found that monkeys with V4 lesions also showed an increase in the number of trials required to relearn a previously mastered pairwise colour discrimination.

Another way of assessing loss in colour vision involves the use of thresholds as a measure of performance, and numerous studies have examined thresholds for hue and chromatic contrast sensitivity after V4 lesions. No disruption of hue thresholds by bilateral V4 lesions was reported in several studies (Dean 1979; Wild et al. 1985; Heywood et al. 1988, 1992; Walsh et al. 1993; see also Chapter 6, this volume) or later in a study that used controlled fixation testing in monkeys with quadrant V4 lesions (Merigan 1996). An experiment that had earlier found small, but consistent, elevations of hue thresholds after V4 lesions (Heywood and Cowey 1987) was

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repeated by the same laboratory with somewhat different parameters (Heywood et al. 1988, 1992), and found no hue threshold elevations. On the other hand, chromatic contrast sensitivity was tested along red–green and blue–yellow colour axes in four monkeys with unilateral V4 lesions (Merigan 1996), and found to be decreased by about a factor of two. Schiller (1993) also reported a series of threshold measures of colour sensitivity, hue difference, colour saturation, and colour contrast after V4 lesions. Although substantial effects were observed in all of these thresholds, the results are difficult to directly compare with the above studies, because they represent comparisons of stimulus appearance at lesioned and unlesioned visual field locations (see above).

Lesions of IT cortex

The effects of IT lesions on colour-related discriminations can be much more dramatic than those of V4 lesions, but they range in severity, in different studies, from virtually no effect to profound disruption of colour vision. Minimal effects of IT lesions include the slight increase in errors to criterion found in two studies (Heywood et al. 1988; Aggleton and Mishkin 1990) for performance of colour discriminations, and the recovery to normal hue difference thresholds after IT lesions in a third study (Dean 1979). The first report of a severe loss of colour vision was that of Heywood and colleagues (1995). This study included three groups of monkeys with different sizes and locations of IT lesions, and the magnitude of colour loss was closely related to the lesion extent. All the monkeys in the group with the largest lesions lost the ability to perform hue discriminations, while colour discrimination loss was found in only two of four in the group with intermediate lesions, and in none of the monkeys in the group with the smallest lesions. This effect was specific to colour, since the same monkeys had no difficulties performing achromatic (grey) discrimination.

From the above results, it appeared that the major factor governing the magnitude of colour vision loss might be the size of the IT lesion. However, a subsequent study (Buckley et al. 1997) demonstrated that marked colour effects could be produced even by lesions smaller than those that caused almost no colour loss in the Heywood study. The lesions in the Buckley study included only a portion of IT, but the colour task was more difficult, and the monkeys were profoundly impaired on the colour discrimination.

Recently, Huxlin et al. (2000b) tested the effects on hue discrimination of bilateral IT lesions similar to the large lesions of the Heywood study. They, too, found a complete loss of the ability to discriminate large hue differences that had been easily learned before the lesions. By adding large luminance cues to the hue discrimination, it was possible to laboriously re-train the lesioned monkeys to make colour discriminations. However, even after extensive training, during which luminance cues were made irrelevant, these monkeys still showed moderate elevations of hue difference thresholds (see Fig. 5.6(d)).

These studies show that colour vision can be profoundly disrupted by IT lesions, provided that the damage is extensive or that relatively difficult discriminations are used to assess the effect. It is not clear why IT lesions can cause such disproportionately greater colour loss than that caused by V4 lesions. It is noteworthy that large IT lesions, of the type that cause the most marked colour vision change, also produce more

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generalized behavioural effects, such as the ‘Kluver–Bucy’ syndrome of emotional alterations, as well as some colour preferences that show up as stimulus bias during discrimination testing (Merigan, unpublished). Evidence that IT lesions interact with stimulus biases is described in the next section. Further studies are needed to determine if these are the basis of the greater colour vision alterations after IT lesions.

Finally, one study demonstrated that, even when colour discriminations are not disrupted by V4 or IT lesions, some features of performance may be substantially changed. Walsh and colleagues (2000) found that monkeys with V4 or TEO lesions could perform a colour pop-out discrimination with no apparent deficit. However, these monkeys did not show the normal priming, i.e. a latency advantage when the correct stimulus occurs on consecutive trials. This loss of priming probably reflects a memory deficit, a type of loss that has been little studied after V4 lesions.

In summary, V4 lesions appear to transiently disrupt colour discrimination learning and to slightly elevate chromatic contrast thresholds, but not to permanently disrupt discrimination of hue differences. This result would be surprising if the alternative cortical stream, the dorsal pathway, were completely devoid of colour responsivity. However, recent evidence suggests a more balanced view of the two pathways with respect to colour processing, with the growing awareness of substantial chromatic sensitivity in the dorsal pathway (Dobkins and Albright 1994; Gegenfurtner et al. 1994; Seidemann et al. 1999; Wandell et al. 1999) of both macaque and human. There is evidence that the function of colour-processing in the dorsal pathway may be primarily to subserve the perception of motion meditated by moving colour patterns (Wandell et al. 1999), whereas that in the ventral pathway may be more related to object recognition and segmentation by colour. Thus, differences in the sensitivity of dorsal and ventral pathway chromatic vision (Gegenfurtner et al. 1994) might simply reflect the stimulus conditions (e.g. spatiotemporal profile) most appropriate to the different uses of the colour information (Wandell et al. 1999). In any case, the substantial colour sensitivity found in the dorsal pathway may help account for the failure to find large, permanent colour vision loss after V4 lesions.

Lesions of IT can cause permanent and/or profound losses of colour vision. Such effects typically result from more extensive damage but, for some especially complex colour discriminations, smaller IT lesions can also cause permanent colour loss.

Learning

In recent years, the idea that cortical neurons may be involved in visual learning (e.g. Crist et al. 1997) has become widely accepted. The basis of this view is the consistent finding that perceptual learning has features that could only come from cortical neurons, such as orientation specificity and interocular transfer (Fiorentini and Berardi 1980; Schoups et al. 1995; Ahissar and Hochstein 1996). The fact that such abilities as orientation discrimination and face recognition show perceptual learning (Schoups et al. 1995; Gold et al. 1999) suggests an involvement of the ventral pathway.