cognitive rehabilitation for unilateral neglect

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Cognitive rehabilitation for unilateral neglect:Review

Tom Manly

Addenbrookes Hospital, Cambridge, UK

Unilateral spatial neglect, a striking difficulty in paying attention to one side ofspace, is a common consequence of cerebro-vascular disease. Although mostpatients appear to recover from this deficit relatively quickly, chronic formsof the disorderusually resulting from right hemisphere damage and affectingleft spaceare associated with slowed motor recovery, poor response torehabilitation, and difficulties in many everyday activities. This article reviewsthe theoretical underpinnings andefficacyof rehabilitation techniques including;behavioural training in leftward visual scanning, eye-patching, encouragingmovement of the left limbs, and interventions designed to increase generalalertness.Recenthighly positive results frombrief adaptation trainingwithprism

lenses are discussed. Neglect is a heterogeneous cluster of deficits that canarise following damage to a variety of brain structures. It is not yet clear whetherone rehabilitation technique will be appropriate for all patients/manifestations ofthe disorder, or whether combining different interventions may produce additivebenefits. There is growing evidence that chronic neglect is associated withindeed possibly fostered bylimitations in a number of non-spatial attentionalcapacities. Whether reduction of the spatial bias is sufficient, in itself, to improveoverall outcome for patients remains an open question.

INTRODUCTION

Unilateral spatial neglect is a curious difficulty in detecting, acting on or even

imagining information from one side of space that cannot be fully explained by

basic sensory loss. Numerous studies now show that its presence is associated

Correspondenc e should be sent to Tom Manly, MRC Cognition and Brain Sciences Unit,

Box 58 Addenbrookes Hospital, Cambridge CB2 2EF, UK.

Email: [email protected], Tel: + 44 1223 355 294, Fax: + 44 1223 516630

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with grossly impaired everyday functioning and, importantly, with slowed

recovery in apparently unconnected functions, including non-spatial attention

and motor skills (Ben-Yishay, Diller, Gerstman, & Haas, 1968; Blanc-Garin,

1994; Cherney et al., 2001; de Seze et al., 2001; Denes, Semenza, Stoppa, &

Lis, 1982; Paolucci, Antonucci, Grasso, & Pizzamiglio, 2001a; Paolucci,

Grasso, Antonucci, et al., 2001b; Robertsonet al., 1997; Rode,Rossetti, Badan,

& Boisson, 2001; Sea, Henderson, & Cermack, 1993). Developing and

evaluating interventions that might ameliorate the condition (or the effects of

the condition on everyday activities) are therefore important clinical aims.

Well over a thousand scientific papers on unilateral neglect have been

published in the last 20 years, many focused on the careful analysis of different

neglect phenomena and their relevance for understanding normal perceptionand attention. Although there is a degree of well-justified scepticism about the

links between basic cognitive neuropsychological research and rehabilitation,

it seems almost inconceivable that at least some of these findings would not

provide useful pointers for intervention.

UNILATERAL SPATIAL NEGLECT: PRESENTATION,

AETIOLOGY, AND NATURAL HISTORYMost readers will be familiar with the striking presentation of unilateral

neglect. Patients with apparently intact visual pathways1may fail to find visual

targets presented on the left side of a page, may draw only the right half of a

remembered image, copy the right half of a picture, or squash the numbers from

1 to 12 into the right half of a drawn clock. They may fail to respond to auditory

stimuli originating from the left, or to tactile stimuli presented to the left limb

or the left side of a limb (Mattingley & Bradshaw, 1994). Famously, their

recollection of well-known scenes (learned prior to the injury) may be strongly

determined by their imagined point of view, omitting information on their left

that they can subsequently recall when it is imagined on the right (Bisiach &

Luzzatti, 1978). Motorically, patients may ignore their own left limbs or have

difficulty reaching to the left (Mattingley & Driver, 1996; Mattingley, Phillips,

& Bradshaw, 1994b). It is important to note, however, that patients vary enor-

mously in the details of presentation and that neglect should not be viewed as

a unitary disorder, but rather as a cluster of deficits characterised by lateralised

spatial bias (Halligan & Marshall, 1994c; Robertson & Halligan, 1999). The

implication of this diversity for rehabilitation (i e whether one technique

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considered to dateindeed the majority of studies considered here have

primarily examinedvisualneglect for an area immediately in front of the

patient.

Neglect has been observed following damage to a variety of brain regions

including the parietal cortex (particularly the posterior region: Vallar & Perani,

1986), frontal cortex (Damasio, Damasio, & Chang Chui, 1980; Mesulam,

1981), basal ganglia (Bradshaw & Mattingley, 1995; Damasio et al., 1980),

striatocapsular (Chung et al., 2000), putamen (Hier, Davis, Richardson, &

Mohr, 1977), caudate (Kumral, Evyapan, & Balkir, 1999), and thalamus

(Velasco, Velasco, Ogarrio, & Olvera, 1986). Recent analyses suggest that

lesionswithin paraventricularwhite matter in the temporal lobe (Samuelsson et

al., 1997) or superior temporal cortex (Karnath, Ferber, & Himmelbach, 2001)are most closely associated with the disorder. However, Hillis et al. emphasise

that the location and extent of clearly lesioned tissue is not always the best

predictor of disability (Hillis et al., 2000). In their study, the extent of

blood hypoperfusion within cortical regions (the ischemic penumbra), in

fact formed the better predictor of neglect. Given this diversity, neglect may

be better understood as a cluster of lateralised spatial problems that can

arise following damage toor dysfunction ina network of brain regions

and normal psychological functions involved in the allocation of attention andrepresentation of space (Mesulam, 1981; Robertson & Halligan, 1999).

Aspects of neglect have been reported in a surprisingly high proportion of

stroke patients within the acute phase. When assessed 23 days post-stroke,

Stone, Halligan, and Greenwood (1993) found evidence of neglect in 82% of

right hemisphere patients and65%of left hemisphere patients (see also Stoneet

al., 1991; Stone, Patel, Greenwood, & Halligan, 1992). The great majority of

patients showing this acute form of neglect apparently recover rather quickly

fromthe spatial biasalthough it should benoted that this is generally based ona relatively limited range of measures (Campbell & Oxbury, 1976).

The group of patients who show more chronic forms of the disorder almost

invariably have right hemisphere lesions and neglect left space. The reasons for

this asymmetric recovery pattern remain controversial. It has been suggested,

for example, that the left hemisphere is responsible for the allocation of

attention to the right half of space, while the right hemisphere is capable

of driving attention to the left or the right (Weintraub & Mesulam, 1987).

Damage to the right hemisphere therefore leads to domination of a rightwardbias from the intact left hemisphere. The specialisation of regions of the left

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attentional bias (e.g., towards right-sided targets on cancellation tasks) and

failure todetect and orient to the wider spatial context. While helping to explain

the chronic hemispheric asymmetry of neglect, these types of account are less

useful in thinking about the presence of neglect in the acute stage in many left

hemisphere patients, and the rapid recovery in some, but not all, patients with

right hemisphere damage. An alternative (although not contradictory) view

emphasises the role of damage to non-spatial right hemisphere capacities (see

below) that may form the setting conditions that allow neglect to persist

(Posner, 1993; Robertson & Manly, 1999). This account has drawn heavily on

observed differences between right hemisphere patients who recover and those

who do not (see Robertson & Halligan, 1999).

The question of how patients recover is important in thinking about rehabili-tation. A number of studies suggest that some forms of apparently spontaneous

recovery may in fact reflect behavioural compensation rather than a genuine

reduction in the underlying spatial distortion. Goodale, Milner, Jakobson, and

Carey (1990) analysed the reaching trajectories of right hemisphere patients

who no longer showed neglect on standard bedside tests. Although the patients

were able to reach towards targets with a similar accuracy to that of a control

group, significant deviations into right space during the reach were still

apparent. Similarly, a bias was apparent if the patients were given the morechallenging task of pointing to the midpoint between two objects (i.e., to a

spatially-defined, rather than object-defined, region: see also Mattingley,

Bradshaw, Bradshaw, & Nettleton, 1994a). Bartolomeo (2000) compared the

performance of right hemisphere patients who currently showed neglect,

patients who had recovered from neglect, and healthy age-matched controls on

a computerised spatial task. As might be expected, while the neglect patients

produced slow or inaccurate responses to left-sided targets, the recovered

patients and the controls showed no consistent bias. When, however, theparticipants were asked to perform the task while simultaneously performing a

second attentionally demanding (although non-spatial) test, a lateralised

pattern re-emerged in the recovered patients (see also Robertson & Frasca,

1992).The results suggest that, whatever the precise mechanism ofbehavioural

adaptation in this group (e.g., compensatory voluntary leftward eye move-

ments: Ladavas, Carletti, & Gori, 1994) these seem to require limited capacity

top-down attentional resources. One obvious consequence of this is that

patients with co-occurring difficulties in mobilising these resources are morelikely to show chronic spatial bias.

If diff b i h ff i l

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TRAINING LEFTWARD SCANNING AS A HABIT

Many neglect patients can become aware of a left-sided stimulus or make some

leftward eye or head movements if they are cued to do so (e.g., Riddoch &

Humphreys, 1983). The difficulty is that such cuesas with simply informing

the patient that they are missing things on the lefttend to have only very tran-

sitory effects (Halligan & Marshall, 1994b). From at least the 1960s, therefore,

therapists have tried to develop very systematic, behavioural programmes to

encourage these behaviours. Perhaps the simplest example is in the context of

reading. In reading text, neglect patients may miss the words on the left side of

each line (see Young, Newcombe, & Ellis, 1991 for discussion of other forms

of neglect dyslexia). A useful strategy is therefore to train patients to habitu-ally find the left side of the page before attempting to read each line (i.e., using

the additional object on the left to re-frame the left side of the text line as an

object on the right). This may be assisted byusing a highly salient cue (e.g., a

red book-mark)as an attentional anchor at the left of the sheetand systemat-

ically fading this cue as performance improves (Diller & Weinberg, 1977;

Weinberg et al., 1977). Such training indeed appears to be successful in

reducing left-word omissions. The problem is that very little spontaneous

generalisation seems to occur. Lawson (1962), for example, describes how apatients improved readingwasso context-specific that it did not generalise to a

different edition of the same book.

Another quite widelyused technique has been to encourage patients to track

a light that moves from right into left space, with the degree of leftward

movement increasing as patients progress (Antonucci et al., 1995; Diller &

Weinberg, 1977; Pizzamiglio et al., 1992; Ross, 1992; Wagenaar et al. 1992;

Webster et al., 1984; Weinberg et al., 1977; Zihl, 2000). Again, although eye

movements during the exercise improve, generalisation has been ratherdisappointing (Robertson, Gray, & McKenzie, 1988; Ross, 1992; Wagenaar et

al., 1992; Webster et al., 1984). The results appear to concord with a general

principle in rehabilitation that it is usually better to train real activities that are

useful for patients (where a lack of generalisation is less important) rather than

rely on transfer from abstract tasks (Wilson, 1996). Webster et al. (2001), for

example, have shown that training that is specific to the task of navigating a

wheelchair around complex environments produces very practical benefits.

However, as neglect permeates so many aspects of a patients life, and trainingeach of these activities may be beyond the resources of most services, seeking

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over a wide area) patients were initially given highly salient cues and therapist

encouragement to look to the left. The cues were progressively faded as aware-

ness of left space increased. As might be expected, performance on the trained

tasks showed significant gains. Unlike previous studies, however, improve-

ments were also noted on untrained tests and, crucially, on structured everyday

activities. The reason for these positive results (which have been replicated in a

fully randomised design: Antonucci et al., 1995) in comparison with previous

studies is unclearalthough the authors suggest that the sheer duration of the

training may have been a crucial factor.

Many neglect patients show a curious lack of awareness foror outright

denial oftheir disabilities (anosognosia). This has clear implications for their

motivation to takepart in rehabilitationand their ability todetect progress. In aninteresting case study, Zoccolotti et al. (1992) have shown that the techniques

developed in Rome (Antonucci et al., 1995; Pizzamiglio et al., 1992) can

produce positive behaviour changes without necessarily effecting the patients

acknowledgement of their difficulties.

Although neglect can operate on object-based co-ordinates (the left side of

an object being neglected regardless of the objects location: Driver &

Halligan, 1991), for many patients the bodys midline appears to be a crucial

marker of what is left and what is right. A potential alternative approach totraining leftward eye movements is, therefore, to train patients to rotate their

torsos to the left in relation to their headposition. In this manner, when a patient

looks straight ahead, more of the visual scene will fall to the right of the body

midline. Remarkably, this simple intervention (trunk rotated left by 15) hasbeen shown to significantly reduce neglect (Karnath, Schenkel, & Fischer,

1991). The difficulty is that, as with eye movements, patients are unlikely to

spontaneously make such rotations, preferring to orient the eyes, head and

trunk to the right.The rehabilitation studies discussed so far haveencouragedpatients to look

(or turn) to the left duringsometrained activities. A different approach which,

given the difficulty in achievinggeneralised results, has some merit, is to essen-

tiallyforcepatients to look to the left duringallactivities.

EYE PATCHING STUDIES

Butter and Kirsch (1992) explored the value of using a patch to cover the right

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a dynamic relationship (activation in one hemisphere inhibits activity in the

other). Damage to one hemisphere could therefore create an uneven competi-

tion leading to a persistent orienting bias towards ipsilesional space (neglect).

Unlike the visual pathways of the cortex, each colliculus primarily receives

stimulation from the contralateral eye rather than hemifield. Preventing stimu-

lation to the intact left superior colliculusbypatching the right eyemight, there-

fore, release the right colliculus from this competitive inhibition and allow

residual function to be better expressed (a benign form of the Sprague effect:

Sprague, 1966).

Butter and Kirsch asked 13 patients to wear right eye patches as they

performed various spatial tasks. Significant reductions in spatial bias on those

tasks were reported in 11 of the group. To potentially enhance this effect byincreasing stimulation to the right hemisphere, right eye patching was

combined with a flickering visual stimulus on the left (dynamic left-sided

visual cues had previously been shown to reduce neglect on computerised

tasks). A study of 18 patients suggested that the combination of these tech-

niques indeed produced greater reductions in neglect than either used in

isolation.

Subsequent work has provided rather more mixed results. Walker, Young,

and Lincoln (1996) found improvements in three patients, no change intwo patients, andpoorerperformance in four of the patients in their study.

Barrett, Crucian, Beversdorf, and Heilman (2001) also found that right eye

patching could worsen neglect, and (in a single case study) that patching of the

left eye could, bizarrely, produce improvements. The results stress the impor-

tance of ruling out non-specific effects of interventions (e.g., heightened

arousal caused by novelproceduressee later).They may also represent a case

where one rehabilitation technique has considerable value for some patients,

while being ineffective or counterproductive for others. Further work exam-ining which patients are likely to benefit (e.g., in terms of their presentation of

neglect, their primary lesion location, time since injury or comorbidity) is

required.

Beis, Andre, Baumgarten, and Challier (1999) examined the effect of

blocking information from the right hemifieldrather than the right eye. Patients

were asked to wear glasses with the right half of each lens masked off for

approximately 12 hours a day over 3 monthsthat is well over 1000 hours.

When compared with right eye patching, the patients showed significantlyincreased spontaneous eye movements to the left and, encouragingly, signifi-

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external stimulation, is in a poorer position to competitively suppress residual

activity in the right.

RE-DISTORTING SPACE

Prism lenses

It has been demonstrated that some of the phenomena associated with neglect

can be related to a distorted or rotated sense of ones location within space

(Karnath et al., 1991). Accordingly, researchers have examined the effect of

using interventions that, in healthy individuals, produce a similar distortion,and using these to correct the pathological bias of neglect.

Wearing prism glasses creates an immediate distortion of space. If they are

worn for long enough, however, the brain adapts (particularly if actions

are performed). Subsequent removal leads to a refractory period during which

the perception of space (as indexed by accuracy in reaching) is distorted in the

opposite direction. In a randomised group design, Rossetti et al. (1998) asked

patients to wear prism lenses that distorted space to the rightessentially

giving them a form of hyper-neglect.After about five minutes of beingaskedtomake reaches towards targets, the lenses were removed.Thepatients showed

the adaptation effect, their straight ahead reaches now being to the left of

the pretreatment baseline. Remarkably, this brief exposure was sufficient to

improve performance on neuropsychological tests relative to thecontrol group.

These improvements were still apparent when both groups were re-tested

2 hours later. Rossetti et al. suggested that the very strong error signal that

resulted from the patients observing their own inaccuracy while wearing the

prism lenses may have been sufficient to effectively re-set the perceptual/motoric representation of space.

These positive effects have been replicated in a recent controlled study that,

in addition to using a wider range of measures, examined the persistence of the

gains at intervals up to 5 weeks post-treatment. Frassinetti et al. (2002) offered

seven right hemisphere patients with chronic neglect 20 sessions of prism

adaptation therapy (two per day over 2 weeks, each of 20 minutes duration). At

the beginning of each therapy session, before wearing the prism lenses, the

patients were asked to point to 60 visual targets presented at midline and tothe left and right of midline. Subsequently, when wearing the prism spectacles

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stages of each session revealed a significant leftward deviation in pointing

attributable to prism adaptation for six of the seven patients.

When compared with a pretreatment baseline, significant reductions in

neglect were apparent on Conventional and the Behavioural subtests of the

Behavioural Inattention Test (Wilson, Cockburn, & Halligan, 1987), a reading

measure (Ladavas, Shallice, & Zanella, 1997), and tasks requiring patients to

name objects located around a room and to reach for objects on a table. A trend

for improvement was also apparent on the Fluff Test (in which patients,

while blindfolded, are asked to find stickersplacedon the left sideof theirbody:

Cocchini, Beschin, & Jehkonen, 2001). These improvements were apparent at

re-tests administered two days, one week and five weeks after treatment.

Evidence in support of a specific effect of the prisms camefrom a control group(based at another hospital, but otherwise matched on age, time since insult and

Behavioural Inattention Test [BIT] performance) who showed no significant

improvements despite being re-tested at the same intervals. The fact that

performance gains were also absent in the treatedpatient whofailedto show the

normal adaptation effects to the prisms is also consistent with a rather specific

effect. Importantly, this study shows that the benefits of prism therapy are not

limited to the control of motor behaviour but appear to exert a more general,

higher level effect upon patients representation of space. If this pattern ofresults is apparent in other studies, this very practical intervention should

clearly have a major impact on clinical approaches to neglect.

Optokinetic stimulation, caloric vestibularstimulation, and neck muscle vibration

Exposure to a background display of coherently moving dots causes involun-

tary eye movements (nystagmus) and a distortion to the subjective midline.Pizzamiglio et al. (1990) have shown that the performance of neglect patients

on spatial tests canbe significantly enhanced by such optokinetic stimulation

although the effects appear to be broadly restricted to when the movement is

actually present. Other routes to inducing temporary subjective shifts in

midline include caloric vestibular stimulation (in which warm and cold water

are used to create a temperature imbalance between the ears: Cappa, Sterzi,

Vallar, & Bisiach, 1987; Rubens, 1985), and posterior neck muscle vibration

(thought to create a motor illusion that the head is turned: Karnath, 1994;Karnath, Christ, & Hartje, 1993).

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LIMB ACTIVATION

The term attention is usually used with reference to some form of limited

capacity selectionin other words mechanisms that can promote a subset of

available stimuli to dominate awareness (e.g., because they are task relevant orinherently salient) while suppressing that which is irrelevant or unchanging. In

accounting for why a potentiallyhighly parallel perceptual system is ultimately

reduced toa narrow channelof awareness, a numberofauthorshave argued that

its key role lies in allowing coherentaction(e.g., Allport, 1992; Rizzolatti &

Camarda, 1987). As we are generally only capable of responding to one or two

objects at a time (not least because of the limited number of limbs at our

disposal), selection is a necessary aspect of the system. In line with this

argument, our awareness of where things are may be modulated by what weare intending to do, or what we are intending to do it with. In the context of

neglect, for example, Robertson, Nico, and Hood (1995a) found that spatial

bias could be modulated by whether a patient intended to pick up, or to point to,

an object.

The finding that has been most relevant to rehabilitation was that (at least

some) neglect patients showed marked reduction in neglect if they used their

left hands to perform a task (Halligan, Manning, & Marshall, 1990; Halligan &

Marshall, 1989; Joanette & Brouchon, 1984; Joanette, Brouchon, Gauthier, &Samson, 1986). In a series of single case and group studies, Robertson and

colleagues (Robertson & North, 1992, 1993, 1994; Robertson, North, &

Geggie, 1992; Robertson, Tegnr, Goodrich, & Wilson, 1994a) subsequently

showed that:

1. The reduction invisualneglectdid not depend on the patient being able to

see the moving left hand.

2. The left hand did not need to be performing the spatial task for the effectto occur. Repeated finger movements of the left hand facilitated a purely

perceptual test of naming letters in a spatial array.

3. An interaction of movement of the left hand and thelocationof that

movement to the left of the body midline appeared to be necessary to

generate the effect (movement of the left hand in right space, or

movement of the right hand in left space did not produce significant

gains).

4. Simultaneous bi-manual movements (regardless of the location of thehands) abolished any benefits of left hand movement on spatial

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6. Although initial results in which the experimenter moved the fingers on

the patients left hand suggested that passive movements did not produce

benefitssubsequent research with larger amplitude passive movement

of the arm has reported positive results (Frassinetti, Rossi, & Ladavas,

2001)

7. Left limb activation effects have not be found in all patients (see also

Brunila et al., 2002)

The results of these studies have been useful in clarifying the potential mecha-

nisms of the left limb activation effect. The benefits of unseen movements,

for example, clearly suggest that the effect is not simply one ofvisualcueing to

the left. The failure to show benefits in the bi-manual movement conditionsimilarly suggest that a generalised alerting (caused by the difficulty or novelty

of using the left hand) forms an unlikely account (see later for discussion of

alerting effects on neglect). If there were a simple facilitation of awareness

from intended movement in a particular location, it might be expected that

moving therighthand within left space would also produce advantages

which was not the case. It seems likely, therefore, that the additive effects of

hand and location of movement are necessary, perhaps in inducing a more

general activating effect within the right hemisphere (Robertson et al.,1994a; see also Kinsbourne, 1993).

Many patients with neglect have dense left-sided hemiplegia. Left limb

activation is therefore unlikely to hold much rehabilitative value for this group.

For other patients, however, there may be under-use of residual function in the

left limbs for attentional reasons (motor neglect: Sterzi et al., 1993). Encour-

aging use of the left limb for these patients may produce benefits for both

perceptual and motor function.

Robertson et al. (1992) developed a portable neglect alert device to cuepatients to move their left hands. The device consisted of a hand-held button

which, if not pressed within a particular interval (generally around 8 s) would

trigger a buzzer. In a series of case studies using the device (Robertson, Hogg,

& McMillan, 1998a; Robertson et al., 1992), improvements across a range of

tasks (both spatial tests and everyday activities) were demonstrated. Encourag-

ingly, for some of the patients, the improvements were well maintained

following the end of formal training. A lasting effect was also observed by

Wilson, Manly,Coyle, andRobertson (2000).Here, the patienthaddifficulty inadequately completing his morning self-care routine (often failing to wash or

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maintained for at least another 10 days, and the patient appeared to be making

more spontaneous use of his left hand. It is possible, therefore, that the

increased awareness of left space induced by the limb movement itself

promotes greater use of the left hand,establishing a beneficial feedbackloop.

If patients have some movement in their left hand or arm, and if the

movement does not cause excessive discomfort, there are a number of advan-

tages to this rehabilitation technique. Firstly, it is a very concrete activity to ask

a patient toperform, and one that is clearly observable. It is therefore possible to

get an estimate of whether it is likely to be beneficial in any given case through

looking for improvements on spatial tasks concurrent with the onset of

movement. It also lends itself to the automaticmonitoring and cueing described

by Robertson et al. (1992) and to the verbal encouragement of therapists andcarers. Most importantly, it seems to lead to improvements in underlying

spatial awareness that generalise to different tasks. Beneficial effects for the

recovery of hemiplegic limbs have resulted from restraint therapy in which

the patients unaffected limbs are temporarily restrained to prevent their use

(Taub & Wolf, 1997). The value of these techniques for rehabilitation in

neglect, through encouraging greater use of the left arm, has not yet been fully

addressed.

Although many of the studies reviewed in this article have focused on aspecific technique that allows clear interpretation of positive results, this

should not be taken to imply that the best clinical outcome is likely to emerge

from the application of anyof the techniques in isolation. Accordingly, Brunila

et al. (2002) recently examined the effect of combining limb activation training

with a progressive visual scanning programme. Four patients were encouraged

to move either their left arm or hand (or if that was not possible, shoulder)

during exercises including naming objects in a spatial array and cancellation

tasks. Compared with a nine week repeated assessment baseline, the 12sessions of therapy produced significant improvements in reading, letter

cancellation and in copying a complex figure, that were well maintained over

the next 3 weeks. Again, the authors note considerable variability in the

patients response, strongly suggesting that careful evaluation of the potential

benefits of any technique for a given patient shouldbeexplored at the outset.

TARGETTING NON-SPATIAL FUNCTIONS

Right hemisphere lesions are associated with disproportionate problems with a

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Shallice, & McCarthy, 1987). There is, furthermore, a degree of convergence

between neuropsychological and functional imaging literature on the particular

importance of a right hemisphere fronto-parietal network in mediating these

functions (Knight et al., 1981; Lewin et al., 1996; Pardo, Fox, & Raichle, 1991;

Rueckert & Grafman, 1996; Sturm et al., 1999; Wilkins et al., 1987). On this

basis, it would be expected that many patients with persistent neglectwho

almost always have right hemisphere lesionswould be vulnerable to these

problems. This certainly seems to be the case. Many patients appear to be

drowsy, unresponsive and to have difficulty in maintaining their focus on any

task, regardless of its spatial content. These clinical observations have been

confirmed in experimental studies. Robertson et al. (1997) asked a large group

of patients (57 with right- and 30 with left-hemisphere lesions, mainly fromstroke), and age-matched controls, to perform a particularly tedious nonspatial

tone counting measure (Robertson, Ward, Ridgeway, & Nimmo-Smith, 1994b;

Robertson, Ward, Ridgeway, & Nimmo-Smith, 1996; Wilkins et al., 1987).

Although all patients were mildly impaired relative to the control group, it was

the right hemisphere patients with neglect who performed disproportionately

poorlyindeed it was possible to make a good guess as to which right hemi-

sphere patients would show neglect based on the score on this test alone.

Similarly, it has been shown that neglect patients, when compared withrighthemispherepatients without neglect, have difficulty in mentally bridging the

intervals between a cue and a target in reaction time tasks (Samuelsson et al.,

1988).

Neglect is a rather volatile condition, changing in apparent severity not

simply on different tasks but on the same task at different times (sometimes to

the exasperation of experimental psychologists looking for reliable effects).

This variability is consistentwith factors (suchas level of arousal/alertness)not

simply being associated with neglect at a general level, but exerting adirectmodulatory influenceon spatial awareness2.

This conclusion receives some support from a recent pharmacological study

in which apparently recovered stroke patients (including three patients with


2 This raises the intriguing possibility that other groups with low levels of alertness may also

be vulnerable to spatial bias. In fact there is growing evidence that at least some children with the

diagnosis of attention deficit hyperactivity disorder (in which poor sustained attention/lowarousal are central features) may show exactly this pattern of left-sided inattention (Nigg,


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right hemisphere lesions) were given midazolam (a GABA antagonist) that

produces mild sedation. The period of the drugs effect (about 2 hours) was

associated with significant increases in left neglect and, interestingly, in left

hemiplegia (Lazar et al., 2002).

Robertson and colleagues examined the link between arousal and neglect

behaviourally using a prior entry computerised task. If healthy individuals

are cued to attend to the side of a display onto which two simultaneous

lateralised targets are subsequently presented, despite maintaining a central

fixation, they will tend to report the stimulus on the attended side as having

occurred firstin other words attention gives that stimulus prior entry into

subsequent processing (Stelmach & Herdman, 1991). This technique has been

used to calibrate the pathological attentional bias of neglect (Rorden,Mattingley, Karnath, & Driver, 1996). In their study Robertson, Mattingley,

Rorden, and Driver (1998b)preceded occasional trials of the computerised task

with a loud, alerting tone. Although the tone had no predictive value for the

stimulus presentation order, its presence was associated with an abolitionor

even reversalof neglect. Heilman, Watson, Valenstein, and Goldberg (1987)

have suggested that there are two routes to developing and maintaining an

alert or ready-to-respond state. The first is exogenously driven by the

detection of intense, novel or salient stimuli. The second, suggested by recip-rocal cortical projections to the brain stem, involves the internal (endogenous)

self-generation and maintenance of this state. Robertson et al.s results with

loud tones suggests that, for neglect patients, the former may be relativelyintact

while the second is deficient.

Although it may be possible to use some form of external alerting during the

performance of tasks (e.g., through presenting tones or the encouragement of a

therapist of carer), as the technique appears to rely on the novelty as well as the

salience of the tones, this may not be practical as a long-term solution. Twopotential alternatives for harnessing this effect are to try and train patients in

self-maintaining an alert state during an important activity, and, given the

results of Lazar et al. (2002), to use medication that boosts rather than reduces

alertness.

Robertson and colleagues (1995b)explored the first possibility, adapting a

technique for the verbal regulationof attention firstdescribed byMeichenbaum

and Goodman (1971; see also Luria, 1963; Meichenbaum & Cameron, 1973).

During training, patients with neglect were asked to perform a number of rathertedious tasks (e.g., sorting coins or shapes). With their prior consent, every

40 d h h i ld l d i b b i h d k d

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the phrase out loud, and finally to internalise this instruction. Although there

was no on-line monitoring (e.g., EEG) of the effect on alertness levels,

improvements in performance on a nonspatial tone-counting sustained

attention task, consistent with such enhancement, were found. Most import-

antly, as a group the patients showed significant improvements on a number of

untrained spatial neglect measures.

MEDICATION

In animals, behaviours analogous to unilateral neglect are associated with

disruption to the dopamine system (Corwin, Burcham, & Hix, 1996). Fleet,

Valenstein, Watson, and Heilman (1987) administered bromocriptine (adopamine agonist) to two patients. This stimulant was associated with

improvements in some, but not all neglect measuresimprovements that

tended to reverse when the medication was withdrawn. In a more recent case

study, Hurford, Stringer, and Jann (1998) compared the effects of methyl-

phenidate with bromocriptine. They report that, although methylphenidate

produced benefits compared with the no-treatment condition, bromocriptine

produced the stronger results. These preliminary studies suggest that stimulant

medication may indeed have a role within rehabilitation for neglect, althoughclearly larger fully controlled trials are required.

FUTURE DIRECTIONS

Although most patients who show unilateral neglect in the acute post-stroke

phase recover, the presence of chronic neglect in the less fortunate minority

is associated with slowed recovery and poor outcome. This review has consid-

ered broad approaches to the rehabilitation of neglect; training (or forcing)leftward scanning behaviour, prism adaptation, left limb activation; and inter-

ventions designed to improve general alertness. Each has produced positive

results that have shown some generalisation to untrained tasks. It is notable, in

terms of the potential mutual benefits between cognitive neuropsychology and

rehabilitation, that at a number of these approaches have emerged from studies

of the underlying nature of the disorder (rather than direct treatment of the most

salient symptoms)and have furthermore raised interesting questions for

further academic study. A number of important questions, however, remain.In order for these effects to be considered rehabilitation, it is necessary to

h fi l h h i i li h f k h i



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effects of distraction and dual tasking on apparently recovered neglect have

been elegantly demonstrated by Bartolomeo (2000). Secondly, it is necessary

to show that the effects last. The majority of studies have to date shown effects

lasting for some weeks but the longer-term consequences of the interventions

remain largely unknown.

In discussing the negative consequences of neglect on recovery and

outcome, the assumption has been that it is theneglectthat is mediating this

effect. As discussed, however, neglect is associated with a cluster of other

deficits, perhaps particularly with the nonspatial attention systems of the right

hemisphere. Whether a reduction in the ostensive behavioural manifestations

of neglectwithout improvements in these other systemsis sufficient to

produce real changes in prognosis remains an open question. There is certainlygrowing evidence on the role of more general executive or attentional

capacities in mediating recovery and functional adaptation following brain

injury. It may well be that improvements in our understanding of these areas

will offer new insights into the persistence and remediation of spatial and other

deficits.

In the majority of studies presented here, there has been considerable indi-

vidual variation in responses to the interventions. It is also true that few of the

studies have directly contrasted one technique with another at a group levelor examined possible additive effects of combining treatments. As discussed,

neglect is a very heterogeneous condition that can arise following damage to a

variety of brain structures. While the practicalities of applying the different

approaches clearly suggests a sensible order in which to investigate their

usefulness, an experimental suck-it-and-see approach with each individual

patient remains the best policy.

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