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

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Recognition of multiple objects is impaired even if these appear not strictly simultaneously, but in sequence: performance is determined by the total period available for processing (Kinsbourne and Warrington 1962; Levine and Calvanio 1978). Location pre-cues improve performance while postcues have no effect (Levine and Calvanio 1978).

Both types of simultanagnosiacs are often considered as suffering from a special type of apperceptive agnosia (see e.g. Farah 1990). Instead, I would argue that simultanagnosia should be considered as a class in-between associative agnosias and neglect (and Balint’s syndrome), given the fact that recognition of single objects is possible in simultanagnosia (influenced by top–down influences), while not in apperceptive agnosia. In particular, the unilateral ventral type of defect (ventral simultanagnosia) shares the quality of an apparent deficit in ‘attentional’ allocation with the neglect syndrome, and may be better called ‘bradygnosia’ rather than agnosia (from Greek: brady, slow), since the most prominent symptom seems to be a problem of disengaging attention from an object, thus slowing down the progress of visual search (e.g. Posner et al. 1984; Baynes et al. 1986).

Blindsight and neglect

Failure of failed analysis within scotomata: blindsight

Legally, blindness of a part of the visual field is defined as an absolute scotoma in this part of the visual field. This means that patients are not able to consciously perceive a stimulus presented in this part of the visual world. However, as demonstrated in Chapter 9, this volume, at least some patients may still be able to react in a goal-directed way to stimuli presented within this blind part of the visual field. In this sense, the visual analysis fails, but in another sense, it succeeds (fails to fail) since the patient is still able to detect, localize, and analyse the stimulus, even if this analysis is not available to conscious insight. Patients usually are not pleased at all if asked to respond to stimuli that they do not subjectively see. As a new method of alleviating this problem when testing patients, we presented either two or three dots sequentially in the visual field and asked patients to discriminate between the directions of motion (Stoerig and Fahle 1995). In this task, the patient always saw two dots that were presented within the intact visual field and hence had no exceptional problem answering the question regarding motion direction between these two dots, even if the direction was not obvious. As to be expected, normal observers achieved significantly better results in this task when three dots were displayed rather than just two dots. The same was true for a patient suffering from a large scotoma caused by a brain trauma even though the additional third point was presented in the middle of his scotoma and hence was never consciously perceived (Fig. 7.18; Stoerig and Fahle 1995). However, in two other patients, suffering from large absolute scotomata due to cerebral infarctions, we did not find any sign of blindsight with this task (Spang and Fahle, unpublished). Hence, the gift of blindsight is not evident in all patients suffering from (absolute) visual field defects.

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(a)

Fig. 7.18 Blindsight for motion direction. (a) The patient was asked to discriminate between upwards versus downwards motion. A least two stimulus dots were presented, one above and the other below the patient’s scotoma (that had been caused by traumatic brain injury). The two dots were presented in sequence, with either the upper or the lower dot presented first. Presenting the upper dot first produced apparent motion downwards, starting with the lower dot resulted in the impression of upwards motion. In half of the presentations, a third dot was displayed midway between the outer dots, and at the appropriate time. Adding the third dot significantly improved direction discrimination in normal observers, and the same held true for the patient, in spite of him never consciously perceiving the middle dot that appeared in the middle of his scotoma. (b) So while the patient was unable to discriminate consciously between presentations containing two dots versus three dots, he nevertheless yielded better motion discrimination in the latter case even in the temporal field, with the third dot presented in his absolute scotoma. (From Stoerig and Fahle, unpublished.)

Neglect

Seeing but not perceiving: visual neglect

Visual neglect is a fascinating and still only partially understood phenomenon that has received renewed interest in recent years. Neglect, it must be said, probably is not just one homogeneous syndrome but a class of deficits with similar but distinct symptoms caused by defects in different parts of the brain but this view is by no means undisputed. It is impossible to give a full review of all the facets of this clinical syndrome here (such as discussions on compression of ‘contralesional’ subjective space (Bisiach et al. 1994),

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interactions with hemianopia (Doricchi 2002, and many more), but, fortunately, this is not necessary since a simultaneous publication from Oxford University Press covers in detail the topic of neglect (Karnath et al. 2002). The reader interested in a (far) more detailed account on neglect is referred to this book.

There is at least one common feature in blindsight, the ability to react to visual stimuli presented in a blind part of the visual field, and neglect (as well as Balint’s syndrome and, to a certain degree, simultanagnosia), the failure to react to stimuli presented in a part of the visual field that is not blind. This common feature is the discrepancy between the status of the visual field (seeing versus blind) on one side, and the reaction to stimulus presentation within this part of the visual field (appropriate reaction to stimulation of the blind field, missing reaction to stimulation of the intact field (see the subsection ‘Relation between neglect, hemianopia, and blindsight’)). Neglect was described in patients as early as 1885 by Oppenheim (cf. also Poppelreuter 1917), is relatively common in patients with defects of the occipito-parietal-temporal zone, and is often accompanied by scotomata. The assessment of neglect in patients is greatly complicated by the coincidence of visual field defects and neglect—hence the resulting problem to decide whether the failure of visual stimulation to elicit a response is due to purely sensory factors such as blindness or else due to partly cognitive or attention-related factors as in neglect.

A definition and basic symptoms of neglect

Neglect is a failure of perception on the highest, supramodal level, namely, conscious perception, that is relatively common after strokes involving the (right) parietal and/or temporal brain hemisphere. As we will see in the following, most of the processes of visual pattern analysis discussed so far seem to be intact in these patients, and yet they behave as if they were blind in part of the visual field. Even worse: these patients behave as if the contralesional part of the world no longer existed; they seem not to be aware of it and not to explore it at all. Not surprisingly, this defect is quite disabling for the patient, much more so than an hemianopia. Neglect patients are unable to explore the neglected (sic!) part of the world while patients suffering from visual field defects can still explore the blind regions by using eye movements. Problems are greatest for those (not so rare) cases with large lesions leading to both sensory deficit (hemianopia or large scotomata) and neglect.

Unilateral neglect is thus characterized by a reduced ability of a patient—usually suffering from a lesion in the right hemisphere, thalamus, and/or basal ganglia—to detect and subsequently report stimuli presented to the contralesional, i.e. usually left half of the world. Neglect occurs for all sense modalities—hearing, touch, seeing, even pain—and, as mentioned above, involves an inability to explore the neglected space, corresponding well to the finding that patients very often are not aware of their deficit. In the present context, we will only deal with visual neglect.

Neglect has a unique role among the disorders on higher levels of processing. Like a scotoma, it prevents perception of all stimulus attributes—not just, e.g. their colour, or form. The object as a whole is not available to conscious perception, unlike in patients suffering from indiscriminations, or apperceptive or associative agnosias. Hence

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neglect, in a way, includes the symptoms of these other disorders. Neglect, therefore, is the most surprising of all failures of visual perception—a failure of conscious perception in spite of largely preserved visual pattern analysis. The neglect syndrome involves one of the basic categories of perception, one of the a priori of all perception and thinking in Kant’s sense, namely, a partial loss of the concept of space—for the patient, a part of space no longer exists. In a way, the concept of the left part of the world for a neglect patient seems to be what the fourth dimension may be for a physicist: He or she knows that it must be there, but lacks a concept of what it looks like.

Relation between neglect, hemianopia, and blindsight

Contrasting neglect with blindsight and hemianopia leads to a better understanding of all three syndromes. As outlined above, neglect in a way is the reverse of blindsight. In blindsight, the primary visual cortex is defective (leading to hemianopia, see ‘Complete failure to see: blindness and scotomata’), but patients can nevertheless detect and analyse stimuli presented in their scotoma (usually without a corresponding subjective awareness of the stimuli; see Chapter 9, this volume). It should be noted that blindsight is possible only in hemianopic patients with intact retinae and optic nerves. In severe neglect, the primary visual cortex is intact, but patients are nevertheless unable to react to stimuli in the contralesional visual field. Another difference is that the border of the scotoma is rather clear-cut in hemianopia and blindsight, reflecting the usually sharp border of the visual field defect, while no such sharp border exists in neglect, but rather a gradient (see Fig. 7.19). A third difference is the dependence on eye, head, and body posture. The defect in hemianopia and blindsight is defined strictly in retinotopic coordinates, while it depends on head and body posture in neglect where the defect seems to be in egocentric or even allocentric coordinates (see e.g. Pouget et al. 1993). This difference is due to the fact that neglect involves a defect on a higher level of representation than the retinotopic lesion that leads to a scotoma and may leave blindsight within the scotoma intact. The fourth difference concerns the dependence on additional stimuli in the intact visual field. These seem to have only marginal influence on perception in all blindsight patients. Patients suffering from mild forms of neglect, on the other side, can usually detect a stimulus displayed in the neglected portion of the visual field if the ipsilesional visual field is empty, i.e. homogeneous. However, presentation of stimuli in the ipsilesional visual field usually ‘extinguishes’ perception of stimuli presented in the neglected, contralesional part of the visual field. A fifth difference, again underlining the higher level of underlying defect in neglect, is the occurrence of neglect for nearby objects only (Halligan and Marshall 1991b), or else for far objects only (Vuilleumier et al. 1998), indicating that there may be different cortical representations for the space immediately accessible to grasping movements versus space farther away. This finding is in line with differences in response qualities of single neurons in the parietal cortex of monkeys, some of which code for nearby objects only (Colby and Goldberg 1999; Berti and Frassinetti 2000). A sixth difference is that scotomata are strictly visual and patients will react to auditory stimuli in the contralesional side of the outer world, while neglect

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often involves several sense modalities. A seventh difference is that neglect may also concern the contralesional side of objects and places recalled from memory from a specific vantage point (Bisiach and Luzzatti 1978; see the subsection ‘Spatial neglect in allocentric, object-centred coordinates and for remembered landscapes’).

Given all these differences, the reader may wonder what blindsight, cortical scotoma and neglect have in common at all. The answer is quite straightforward: all three types of patients are not normally reacting to stimuli presented to their contralesional side. They behave in a standard ophthalmological test as if they were blind or had defective vision, in the contralesional visual field. Moreover, blindsight and neglect share the property that considerable visual processing and analysis of the visual input occurs without reaching awareness (unlike in patients suffering from a retinal scotoma). In several ways, hemianopias caused by defects of the visual afferents and neglect are similar, since patients do not consciously perceive objects in the defective part of the world. But while hemianopia in patients without blindsight does not lead to any detectable effects of the stimuli on the cortex, this is not true in neglect nor in hemianopia caused by cortical defects for the patients showing blindsight.

Symptoms typical of visual neglect

We have already given an overview of the typical symptoms present in neglect patients. In the following, a more detailed account follows, while the reader is again referred to an even more detailed account in the book by Karnath et al. (2002; see also Heilman et al. 1993).

Neglect, as we know, is characterized by a lack of responsiveness to visual stimulation in the contralesional visual field in the absence of scotomata or at least with scotomata not covering the whole contralesional hemifield. Typically, the patients ignore all stimuli on the contralesional side, both visual stimuli and those from other sense modalities. Symptoms are usually far more severe after lesions of the right cortical hemisphere and hence in the left half-field. (As we will see in the subsection ‘Neuronal and neuropsychological mechanisms of spatial neglect: deficit of attention versus representation?’, the right hemisphere may contain a representation not only of the left side of the outer world, but also at least a rudimentary representation of the right side.) The cortical lesions underlying neglect seem to bias perception towards fine local details of visual scenes, leading to a loss of overview over more global properties and to a centripetal bias in addition to a horizontal (left/right) bias (Robertson et al. 1988; Lamb et al. 1990; Halligan and Marshall 1991a,b, 1993). Patients suffering from neglect caused by right hemispheric lesions may only eat the food on the right side of their plate and complain of having not enough food, while the left part of the plate is still not emptied. Just rotating the plate, thus exchanging its right and left sides, can satisfy them. Patients may read only the right side of a newspaper, or of isolated words, or describe and copy only the right half of a figure. When searching through a page of paper and marking all lines, or all shapes of a specific form, they may mark only those lines or shapes on the

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ipsilesional side of the paper. Anecdotal reports include a woman who after suffering a stroke and coming back from the hospital put formidable make-up on her face, but only on one side. Patients sometimes develop surprising strategies to search for objects, e.g. by turning to the right until the required object might turn up in their right visual field, i.e. shortly before they finish a complete circle.

Generally, neglect patients are not aware of and have little or no insight into their deficits, especially shortly after the injury and for large insults, a symptom sometimes called anosognosia (cf. already Redlich and Bonvicini 1909; Babinski 1914).

Graduation of spatial neglect and extinction of stimuli

Defects of the primary visual cortex, or in the pathways leading there, usually cause reasonably sharply delineated scotomata, reproducibly testable by perimetry. This is not the case for the failure of analysis observed in neglected parts of the outer world. There is no sharp spatial divide between positions where stimuli are consciously perceived and those where they are neglected, but rather a gradient in probability of detection and perception. In the most severe cases, stimuli in the neglected half are completely invisible for the patient, even if there are no simultaneous stimuli in the ipsilesional visual field, as is the case during perimetric testing. The probability of detecting a stimulus increases for stimuli presented more towards the ipsilesional side. For less severe neglect, the overall probability of stimulus detection in the contralesional visual half-field increases, but a gradient between the contraand ipsilesional sides persists. As detailed in the next section, the gradient may also shift in horizontal direction depending on the position of eyes, head, and body.

Probability of stimulus detection also depends on whether other stimuli are simultaneously displayed, and where. The defect of spatial vision as evidenced in neglect is most obvious during competition between stimuli. Generally, the stimulus presented more to the contralesional side will not be perceived. It is suppressed or extinguished by the stimulus further towards or further within the ipsilesional field. Natural scenes usually contain a multitude of objects, so suppression will occur permanently, leading to extinction of objects on the neglected side, possibly due to attraction of attention by the objects on the ipsilesional, usually right side. As we will discuss in detail (in the subsection ‘Evidence for preserved processing of visual input’), suppression of some stimuli occurs even in healthy observers if their attention is focused on other objects— we cannot consciously perceive all objects that are processed at least up to primary visual cortex. The extinction observed in neglect may be a special case of the suppression also experienced in healthy observers due to a limited conscious visual capacity, just with a strong spatial bias. However, healthy observers still have the concept that there are objects outside their focus of attention, while at least some neglect patients seem to lack the very concept of space on their contralesional side. A related phenomenon is simultanagnosia, a strong restriction in the number of objects that a patient simultaneously perceives (see the eponymous subsection; Holmes and Horrax 1919; Rafal 1997; cf. also Gorea and Sagi 2000).

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subsection, there is no sharp border in neglect between those spatial locations attended to and those where stimuli are neglected, but rather a gradient, with stimuli further towards the ipsilesional side detected more often than those shifted more towards the contralesional side (even if both stimuli lie in the same hemifield).

Surprisingly, the gradient is not defined in retinal coordinates, but more in egocentric ones. When the eyes are moved, the gradient may stay almost constant in the outer world. This is to say that it depends on the location of objects relative to the body, whether or not they are neglected, not on their location on the retina, as is the case in patients with scotomata (Fig. 7.19). So, rotating the body in a contralesional direction while simultaneously moving the eyes in the opposite direction, keeping the gaze on the same object, may switch a near-midline part of the visual field from the ‘neglect’ mode to a ‘perception’ mode. In the new body position, this visual field position belongs to the ipsilesional part of the outer world, and the stimuli it receives are far less neglected, though they fall of the same part of the retina.

Basically, the same holds true for movements of the head. Turning only the head rather than the body also shifts the gradient of neglect in retinal terms (either by shifting the entire reference system or predominantly the subjective straight ahead). This is even true for intended, rather than real head movements or if a head movement is simulated by stretch reflexes of the neck muscles (Karnath et al. 1991). Hence, it is, to a first approximation, body posture more than eye or head position that determines whether a stimulus at a given location succeeds or fails to reach awareness in a neglect patient: egocentric rather than retinotopic localization is the crucial parameter.

Spatial neglect in allocentric, object-centred coordinates and for remembered landscapes

Another symptom that strongly sets apart the failure of visual stimulation as measured by object identification in neglect from that in scotomata is the dependence of neglect on object-centred coordinates. The left side of a flower may be neglected, irrespective of whether it is presented in vertical orientation (left side is neglected, cf. Driver 1999) or rotated clockwise, to a horizontal orientation (upper side is neglected). This astonishing symptom can be understood in the framework of neglect as a disorder of objectcentred spatial representations and/or of spatially selective attention. This is to say that some type of constancy-mechanism (see ‘Failures to achieve object constancy’) readjusts the object to the normal, upright position, and only thereafter may the neuronal mechanisms underlying conscious perception come into full play.

The ground-breaking experiments of Bisiach and colleagues (e.g. Bisiach and Luzzatti 1978) demonstrated convincingly that spatial neglect is not caused by sensory deficits or by deficits in memory consolidation or recall. Patients were asked to imagine standing on one side of a square they knew well in Milan, looking at the opposite side of the square. Their task was to name all the buildings they saw. Patients suffering from a neglect caused by a right-sided brain lesion would only name buildings located in the right half of the patient’s imagined visual field. Then, patients were asked to imagine

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standing on the opposite side of the square, looking at the location they had just imagined to be. Again, they tried to name all the buildings they perceived with their mind’s eye. This time, they would name only buildings on the opposite side of the square— again the ones in the right part of the visual field of their mind’s eye. This experiment clearly shows that neglect is not primarily a defect of information-processing and storage, but of information retrieval by the aware subject.

Evidence for preserved processing of visual input

Three lines of evidence support the claim that neglected stimuli failing to reach conscious perception nevertheless are processed in some detail in the patient’s visual system. This evidence relies on: (1) the clear effects of grouping and priming by neglected stimuli; (2) the presence of visually evoked sum potentials; as well as, (3) the evidence for stimulus-evoked changes of cortical blood oxygenation levels as evidenced by functional magnetic resonance imaging (fMRI).

Neglect (as well as simultanagnosia) can be considered as a severe form of the inability even of normal observers to process more than about five stimuli presented simultaneously, just with a spatial bias in the case of neglect. Grouping the stimuli presented in the neglected part of the visual field with others presented in the ipsilesional field into a single object should alleviate the suppression in the neglected hemifield. And suppression indeed decreased when two stimuli in the neglected half-field represented corners of a large illusory square whose other two corners were located in the normal half of the visual field. Hence, some type of grouping and categorization is still possible, including that of stimuli presented in the neglected part of the visual field. The grouping process has to be pre-attentive since, per definition, attentive vision is defective in the neglected half-field (Mattingley et al. 1997; Ward et al. 1994; cf. also Davis and Driver 1998; Gilchrist et al. 1996; cf. Luria 1959; Berti et al. 1992; Vuilleumier et al. 2001; Godwin-Austen 1965, for similar effects in simultanagnosic patients).

This finding strongly argues for a model of neglect as a competition between object representations rather than between retinotopic locations (see ‘Neuronal and neuropsychological mechanisms of spatial neglect: deficit of attention versus representation?’). The same holds true for the fact that some patients asked to enumerate multiple objects presented simultaneously in both hemifields were able to take into account the stimuli in the neglected hemifield, while they suppressed and hence ignored these stimuli when asked to indicate their position in bilateral displays (Vuilleumier and Rafal 1999). Presented with the picture of a house with smoke coming from the contralesional side of the roof, the patients would not appreciate anything unusual with this house. Yet, when presented with two houses, one normal and one burning on the contralesional side, they would nevertheless choose the normal one if asked where they would prefer to live (Marshall and Halligan 1988). However, this result is not undisputed.

Priming effects of neglected (or suppressed) stimuli are evident in a number of experimental situations. One such effect is the decrease of reaction times after bilateral

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stimulus presentations as compared to unilateral presentations. This is to say that patients responded faster to stimuli presented to both hemifields than to stimuli presented to the ipsilesional hemifield alone—even if they were not aware of the stimulus in their contralesional field, this stimulus increased their speed of responding (Marzi et al. 1996). Not only can the presence of a stimulus in the contralesional visual field (unconsciously) influence reaction times but also rather complex features of this neglected stimulus such as its shape and colour may have an influence, as well as its identity and even its semantic contents do (Audet et al. 1991; Cohen et al. 1995; di Pellegrino and de Renzi 1995; Berti and Rizzolatti 1992; cf. also Baylis et al. 1993; McGlincheyBerroth et al. 1993; Ladavas et al. 1993; 1997).

Processing of neglected stimuli does not only lead to improvement of reaction times. Patients suffering from neglect and extinction of contralesional stimuli were also able to discriminate between same and different stimulus presentations in both hemifields and hence could identify the stimulus in the neglected hemifield (Volpe et al. 1979; Berti et al. 1992; cf. Farah et al. 1991). Stroop effects, i.e. an interference of a coloured stimulus with reading a colour name, are exerted by stimuli in the neglected hemifield, similar to the effects in healthy observers—though the stimuli themselves are neglected (cf. Logan 1980; MacLeod 1991; Berti et al. 1994; Sharon et al. 1999). Presentation of stimuli in the neglected halffield, moreover, may lead to perceptual learning, i.e. improvement of perceptual capabilities for the stimuli displayed. To sum up, stimuli presented in the neglected hemifield can influence the response of the patient even though they are not consciously perceived and their effect may differ from that exerted by stimuli presented in the ipsilesional hemifield.

Objects and faces that were presented in the contralesional hemifield and were not subjectively perceived nevertheless evoked ERPs in sum potential recordings on the scalps of patients suffering from neglect. First, unspecific potentials arise about 100 ms after stimulus onset, followed at 170 to 200 ms latency by potentials specific for, e.g. presentation of faces. The potentials evoked by presentation in the contralesional visual field, however, sometimes differ considerably from those evoked by stimulus display in the ipsilesional field (Spinelli et al. 1994; Angelelli et al. 1996; Vallar et al. 1991; Sagiv et al. 2000; Bentin et al. 1996; Eimer 1998; cf. however Marzi et al. 2000; Hämäläinen et al. 1999; Deouell et al. 2000; Doricchi et al. 1996; Viggiano et al. 1995). This difference between the potentials evoked in the ipsiversus contralateral hemifields is not surprising given the fact stressed in the subsection ‘Visual informationprocessing in the cortex: parallel processing and feedback’ that visual informationprocessing involves strong feedback connections. Thus, defects of ‘higher’ stages of processing will also have detrimental influences on the performance of ‘lower’ areas—unlike in a strictly hierarchical feedforward system.

Presentation of objects and faces in the contralesional hemifield also significantly increased fMRI signal strength in the primary visual cortex of neglect patients as well as in early extrastriate areas and the fusiform region of the lesioned cortical