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

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session of 100 trials. Control monkeys learned the discriminations quickly, rapidly reaching approximately 90% correct, whereas monkeys with IT lesions took much longer to reach an equivalent level of performance. Although the magnitude of the deficit was gradually reduced by training within each individual learning set, the deficit was persistent across problems, lasting for the full 60 sets of postoperative learning.

Fortunately, the characteristics of the IT lesion learning deficit have been examined in many studies, so there is now a good understanding of the conditions under which it is found. First, it is apparently confined to visual discriminations, since IT lesions cause no disruption in the learning of discriminations involving audition, touch, or olfaction (Dean 1975). Curiously, however, the disruption of visual learning by IT lesions is related, not to the type of visual stimuli being discriminated, but rather to the difficulty of the discrimination (Gross 1973). Thus, the learning of colour discriminations (Heywood et al. 1988) can be as severely impaired as the learning of complex object discriminations (Butler 1969) if the former discrimination is as ‘difficult’ as the latter (i.e. the number of trials needed to learn the discrimination is as high in normal monkeys).

This observation raises some concerns about the basis of this effect, since we might expect difficulties in discrimination learning to be specific to the complex discriminative features evident in the response of IT neurons. Clearly, it is important to determine whether the visual learning deficit is general to all learning situations. One feature of learning studies is that the monkey is usually required to reverse pre-existing stimulus biases, and it is possible that IT lesions may interfere with this reversal. In the Gaffan et al. (1986) study described above, it was noted that the monkeys often strongly preferred one of the pair of stimuli during the first few presentations of a pair. In subsequent testing, the strength of this preference was a good predictor of the number of errors made by the monkey during the remainder of the test session. Thus, it appears that IT lesions reduce the monkey’s ability to reverse stimulus preferences, and that this may be a major component of the disruption of learning by such lesions.

The importance of stimulus preferences in IT lesion effects was reflected in an earlier study (Holmes and Gross 1984) that examined the postoperative learning of monkeys with IT lesions using two types of stimulus pairs. The first type were standard form stimuli, in which the two patterns were different and, with these stimuli, the monkeys showed the typical deficit in learning. In the second type of discrimination, the two patterns were identical, but one was rotated by at least 60 from the other. With the latter stimuli, the authors found no learning deficit after IT lesions. This is one of the few instances in which IT-lesioned monkeys showed no visual learning deficit compared to controls, suggesting that the lack of strong stimulus preference when using identical, but rotated, stimuli may have been the reason.

These results suggest that an altered ability to reverse stimulus preferences could be an important component of IT lesion effects. Such an effect could be considered cognitive, but may have an important perceptual component, since one study found that the impaired learning was confined to one part of the visual field. Butler (1969) demonstrated

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that monkeys with a unilateral lesion of IT showed the visual learning deficit only in the visual field contralateral to the IT lesion. This unusual deficit was revealed by combining a unilateral IT lesion with a split optic chiasm and forebrain commissure so that monocular vision covered only one hemifield. When testing object learning, the designation of correct or incorrect object was made after the animal’s first choice, with the object not chosen designated correct for the rest of testing. This required that the monkey reverse any stimulus preference it showed on the first trial and, when the monkeys used the lesioned hemisphere, they required roughly three times as many trials to learn (i.e. reverse their stimulus preference) as when they were using their non-lesioned hemisphere. Since the impaired learning was confined to half of the visual field, it could not be due to a non-visual behavioural change, such as decreased motivation, perseveration, or a general cognitive decline. This conclusion also pertains to the two studies of V4 lesions described above (Schiller 1995; Merigan 1996) that found retinotopic alterations in learning.

Another study that used unusual stimuli also found an atypical effect of IT lesions on the learning and retention of form discriminations (Britten et al. 1992a). In this study, monkeys were required to learn or retain form discriminations, in which the form was conveyed in one set of stimuli by the usual luminance variation, but in a second set of stimuli by relative motion. With both types of discriminations, the monkeys showed the typical deficit in retention of discrimination performance after IT lesions. IT lesions also caused impaired acquisition of new form discriminations when form was conveyed by luminance variation. However, when form information was conveyed by relative motion, the IT-lesioned monkeys showed no impairment in learning new form discriminations. This study supports the rather general finding that ventral pathway lesions typically spare motion discriminations. However, it also suggests that even form discriminations may be partially spared from the effects of ventral pathway lesions when the form is conveyed by motion.

Finally, we should mention a study that may have important implications for the nature of ventral pathway lesion effects on learning. Manning (1971) found that monkeys with IT lesions learned pattern discriminations as quickly as control monkeys if they received a shock when they made errors in addition to being rewarded with food for correct responses. On the other hand, the same monkeys showed the typical impaired visual pattern learning when they were only rewarded with food for correct responses. It is unlikely that the learning impairment found when no shock was delivered could be attributed entirely to a motivational decrease caused by IT lesions, given that the effect of an IT lesion on learning in the Butler study described above (Butter and Hirtzel 1970) was confined to one part of the visual field. Clearly, more research is needed to examine the implications of this result for both IT lesions and perceptual learning.

In summary, ventral pathway lesions impair visual learning in ways that imply a major perceptual alteration. Stimulus–response learning is especially degraded, although other forms of learning are also affected (Merigan 1996), suggesting that the ventral pathway is central to many forms of visual learning.

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Attention

It is well established that visual attention plays an important role in the response of macaque V4 and IT neurons (Maunsell et al. 1992; Motter 1993; Connor et al. 1997; Chelazzi et al. 1998; Reynolds et al. 2000). These physiological studies have shown that the response of V4 and IT neurons depends strongly on the visual field location or stimulus type the monkey is attending to. These observations raise the possibility that V4 or IT lesions could alter visual performance by changing the allocation of visual attention to different locations of the visual field or different stimulus types.

One of the first reported attentional effects of ventral pathway lesions was an alteration of search performance in monkeys at the visual field location that corresponded to a V4 lesion (Schiller and Lee 1991). The monkeys viewed 4 to 64 stimuli presented symmetrically around fixation and then made an eye movement to the single odd stimulus. V4 lesions severely disrupted the ability to detect a less salient (smaller, less coarse, etc.) odd stimulus, but had less effect on the ability to detect a more salient (larger, coarser) odd stimulus. This result is consistent with current views that V4 may be part of the circuitry involved in the control of attention.

In a recent paper, DeWeerd and colleagues (1999) described a very different effect of V4 and TEO lesions in macaques that also suggested mediation by altered attention. Monkeys performed an orientation discrimination for a single circular patch of grating, presented a few degrees from a fixation stimulus. Curiously, when three irrelevant circular distractors were placed around the grating patch, orientation thresholds were elevated more at the site of the V4 and TEO lesion than at the control visual field location. Furthermore, as predicted by a model of the role of attention in ventral pathway neural responses (Desimone and Duncan 1995), the degree of threshold elevation was proportional to the contrast of the distractors. This result supports the possibility that V4 lesions can alter perception by disrupting the role of attention in separating visual targets from distractors (Braun 1994).

These findings suggest that attention, an important determinant of visual function that is inherently an element of top–down neural control, may be involved in some aspects of ventral pathway lesion effects. Clearly, further study is needed to determine the role of attention, both in the normal function of visual cortex and following cortical lesions.

Dorsal pathway

The dorsal pathway has been called the ‘motion’ pathway because of the selectivity of its neurons for the direction of stimulus motion. This property, while present in only limited numbers of neurons in area V1 (Hawken et al. 1988), becomes more prominent in area V3 (Felleman and Van Essen 1987; Gegenfurtner et al. 1997) and is present in a majority of neurons in area MT (Maunsell and Van Essen 1983; Albright 1984). At subsequent stages of processing in the dorsal pathway, neuronal tuning becomes more complex. Neurons in the middle superior temporal (MST) area show selectivities to expanding versus contracting motion, and clockwise versus counterclockwise rotation (Duffy and

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Wurtz 1991; Graziano et al. 1994). Neurons in parietal cortex, such as those in areas 7a and lateral inter parietal (LIP), integrate information from several sensory modalities with motor output, as well as constructing an extrapersonal representation of space (Andersen 1997; Read and Siegel 1997; Siegel and Read 1997). This specialization for the processing of motion suggests that lesions early in the dorsal pathway are likely to result in deficits in the ability to perform various types of motion discriminations. The spatial orientation and sensorimotor integration responses of neurons within parietal cortex suggest that damage to this region will cause deficits in behaviours that utilize these properties. Indeed, the data reviewed below support the notion of specialization of the dorsal pathway for processing of image motion. They also suggest that the dorsal pathway is important for the integration of motion information to construct a representation of space that can be used in navigation and other motor behaviours.

Area MT lesions

Area MT has become the area of choice for examining the effects of lesions within the dorsal pathway, primarily because of its high incidence of directionally selective neurons, its clearly defined borders within the superior temporal sulcus (STS) and its precise retinotopy. The first studies involving lesions of areas MT and MST used ibotenic acid, and examined the effects of MT and MST lesions on eye movement responses. Wurtz and his colleagues reported that MT and MST lesions resulted in retinotopically specific deficits in smooth-pursuit eye movements (Newsome et al. 1985; Dursteler et al. 1987; Dursteller and Wurtz 1988). The monkeys had been trained to pursue moving targets but, after MT lesions, were unable to match the speed of their smooth-pursuit eye movements to the speed of the target. The animals also had problems adjusting the amplitude of their saccadic eye movements to compensate for target motion, but had no problems making saccades to stationary targets. Since these effects reflected difficulties in matching the velocity of visual targets, without evidence of motor abnormalities, they were interpreted as impaired perception of stimulus velocity. A similar deficit in smooth-pursuit eye movements was later reported (Schiller and Lee 1994). Subsequently, the studies described below examined the effects of damage to area MT on motion perception more directly. In most of these experiments, the monkeys judged differences in the direction or speed of stimulus motion.

Discrimination of stimulus direction

In the first study in this series, Newsome and Paré (1988) examined the perception of image motion with displays in which the proportion of coherently and randomly moving dots was adjusted to measure threshold. The monkeys reported whether the stimulus moved up or down by making a saccade to one of two small targets on the screen. The lesion was made by injecting ibotenic acid into sites in MT that were physiologically identified while the monkey was performing the discrimination task. Severe deficits in motion coherence thresholds were observed when stimuli were placed in the portion of the visual field affected by the lesion. A similar inability to extract coherent

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motion in the presence of noise was subsequently reported after MT/MST lesions by Pasternak and Merigan (1994), who tested monkeys with bilateral damage to MT/MST produced by multiple injections of ibotenic acid.

More recently, Rudolph and Pasternak (1999) used a match-to-sample task to examine in greater detail the MT lesion-induced inability to extract motion from directional noise. They compared the effects of unilateral MT/MST lesions on the ability of monkeys to discriminate the direction of motion of random-dots or of drifting gratings masked by noise (Figs 5.5(c) and 5.9(a)). On each trial, the monkeys indicated whether the two sequentially presented stimuli, sample and test, moved in the same or in different directions (Fig. 5.5(a)). The delay separating the two comparison stimuli was very brief (200 ms). Thus, the task imposed only minimal requirements on the ability to remember the preceding stimulus. Deficits in direction discrimination were found with both types of stimuli (Fig. 5.5(c), left). On the other hand, no permanent deficits were found in contrast thresholds for discriminating the direction of drifting gratings measured in an identical task (Fig. 5.5(b) left). This selectively increased susceptibility to noise was specific to the domain of motion perception, since the same monkeys showed no deficit in discriminating the orientation of gratings masked by two-dimensional noise (Fig. 5.4). Moreover, visual deficits after V4 lesions, measured with the same tasks, were limited to discriminations of stimulus orientation, and were not found when the monkeys were required to discriminate stimulus direction, even when the motion stimulus was masked by noise (Rudolph 1999; Rudolph and Pasternak 1999; Figs 5.4 and 5.5). These selective results demonstrated the importance of MT/MST neurons for the ability to discriminate motion direction in the presence of noise.

Direction integration

In addition to an increased susceptibility to noise, MT/MST lesions result in deficits in the integration of local motion vectors (Pasternak and Merigan 1994; Rudolph and Pasternak 1996; Bisley and Pasternak 2000). To measure motion integration, individual, randomly positioned dots were displaced in a range of directions, and the speed of stimulus motion, which depended on the size of the displacement, remained constant throughout each session (Fig. 5.9(b)). The maximal range of directions in the ran- dom-dot stimulus at which the monkeys could reliably judge the overall direction of motion was taken as a measure of the integration of local directional signals (Williams and Sekuler 1984; Watamaniuk et al. 1989). Unilateral MT/MST lesions resulted in a deficit in motion integration thresholds (see Figs 5.9(b) and 5.10(b)). Although this deficit was most pronounced early in postlesion testing and decreased with continued training, some loss persisted throughout the several years of postlesion testing.

Remembering stimulus direction

The task used by Bisley and Pasternak (2000) required that the monkeys not only process information about stimulus direction, but also remember that direction for a brief period of time. They used the same task that Rudolph and Pasternak (1999; see

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effects of MT/MST lesions depended upon both the demands of the task and the nature of the visual motion stimuli. These results suggest that MT/MST contributes to the retention of visual motion information only if it is involved in its encoding.

Discrimination of stimulus speed

Three studies have examined the discrimination of stimulus speed after MT lesions. Pasternak and Merigan (1994) made bilateral ibotenic acid lesions involving areas MT and MST, and measured the accuracy of speed discrimination using gratings moving at a speed of 2 /s over a range of contrasts. They found a 2–3-fold elevation of speed difference thresholds over a broad range of stimulus contrasts. With additional training (see below), this deficit decreased. The improvement was unlikely to be due to the monkeys relying on cues other than speed, such as differences in temporal frequencies, since the accuracy of discrimination of differences in flicker rates, measured with counterphase gratings, was lower than that measured with drifting gratings (also see Pasternak 1987). Orban et al. (1995) used bilateral aspiration to measure the effects of lesions of areas MT and MST in monkeys trained to discriminate differences in speed. They found a loss in the accuracy of speed discrimination over a broad range of base speeds. Schiller and Lee (1994) examined the effect of MT lesions on speed discrimination with an oddity task, in which the monkeys viewed eight small targets arranged around a fixation target, one of which moved with a speed different from the other stimuli. The monkeys were required to saccade to the odd stimulus, and made the most errors when the odd stimulus was placed in the hemifield affected by the MT lesion and when the differences in speed were relatively small. These monkeys were also impaired in discriminating differences in flicker rate, a result that confirms earlier findings after damage to the visual motion system in cats (Pasternak 1987; Pasternak et al. 1989).

Relative motion and structure-from-motion

Only a few studies have explored the effects of MT lesions on other aspects of the processing of complex motion. Andersen and Siegel (1989) tested the effects of MT lesions on the perception of relative motion, and found deficits in the detection of motion shear. This deficit was transitory, and they found nearly complete recovery within a few days of continued training. This study also measured the effects of MT lesions on the detection of structure-from-motion in a single monkey, and reported severe deficits that lasted longer, and were more pronounced, than the deficit in perceiving relative motion.

Recovery of function after MT lesions

The data cited above demonstrate that lesions of areas MT/MST lead to selective deficits on a variety of motion discrimination tasks, as well as tests of smooth pursuit eye movements. However, equally striking in the above studies, is the extent to which many lesion-disrupted visual functions recover. The early studies by Wurtz and his colleagues reported essentially complete recovery in smooth pursuit after small MT or MST lesions (Newsome et al. 1985; Dursteler et al. 1987; Dursteler and Wurtz 1988;

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Yamasaki and Wurtz 1991). Subsequently, Yamasaki and Wurtz (1991) examined this recovery in greater detail, and found residual deficits only when the lesion was larger and included both MT and MST. Newsome and Paré (1988) also reported rapid and nearly complete recovery of motion coherence thresholds for discriminating opposite directions of motion.

On the other hand, Pasternak and her colleagues (Rudolph and Pasternak 1999; Bisley and Pasternak 2000), despite finding substantial postlesion improvements on several motion discriminations, generally found permanent, albeit subtle, residual deficits on most studied tasks. Residual vision motion deficits following MT lesions have also been reported by other laboratories (see above), only some of which addressed the question of functional recovery directly (e.g. Andersen 1989). The relatively rapid and complete recovery observed by Wurtz and his colleagues is in stark contrast to the observations of residual deficits detectable years after the lesion. The most likely explanation for this apparent discrepancy is the time at which threshold measurements began in the lesioned portion of the visual field. In studies where recovery was observed within days after the lesion (Dursteler et al. 1987; Dursteler and Wurtz 1988; Newsome and Paré 1988; Yamasaki and Wurtz 1991), the damage to a retinotopically localized portion of MT was produced while the monkey was performing a behavioural task in the corresponding portion of the visual field. Thus, immediately after the lesion and in the days that followed, the animal received extensive behavioural training in the damaged visual field. On the other hand, in the experiments by Pasternak and her colleagues (Pasternak and Merigan 1994; Rudolph and Pasternak 1999; Bisley and Pasternak 2000) this type of training occurred many days or even months after the lesion, and improvements in performance became apparent only after the initiation of training on a given task in the affected portion of the visual field (Rudolph and Pasternak 1999). This suggests that a necessary condition for partial or complete recovery after lesions is behavioural training within the lesioned portion of the visual field.

It is generally thought that the partial or complete recovery of a visual function following localized cortical damage reflects the assumption of processing by other cortical areas (e.g. Newsome and Pare´ 1988; Pasternak and Merigan 1994). It is also possible that motion processing normally involves a wide network of many cortical areas, and that recovery represents an adaptation of those not damaged. However, little is known about the mechanisms underlying recovery of function after extrastriate cortical lesions, although efforts are currently underway in elucidate its histochemical and anatomical basis (e.g. Eysel and Schweigart 1999; Huxlin and Pasternak 1999, 2001; Huxlin et al. 2000a).

Lesions of parietal cortex

Within parietal cortex, the neuronal properties of areas LIP and 7a have been studied most extensively. Such studies indicate that neurons in these areas integrate visual, somatosensory, auditory, and vestibular signals that reflect the observer’s location (Andersen 1997). They are also active before and during saccadic eye movements (Andersen et al. 1990) and