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MAJOR REVIEW

Visual Neglect Following Stroke: Current Concepts and Future Focus

3 , 4 , 5

Darren S.J. Ting, MBChB, 1 Alex Pollock, PhD, 2 Gordon N. Dutton, MD, FRCOphth,

Fergus N. Doubal, MRCP, 6 Daniel S.W. Ting, MBBS, 7 Michelle Thompson, BSc (Hons), 6 and Baljean Dhillon, FRCPS, FRCS, FRCOphth 8

1 Victoria Infirmary, Glasgow, UK; 2 Nursing, Midwifery, and Allied Health Professionals (NMAHP) Research Unit, Glasgow Caledonian University, Glasgow, UK; Tennent Institute of Ophthalmology, Gartnavel General Hospital, Glasgow, UK; 4 Royal Hospital for Sick Children, Glasgow, UK; 5 Department of Vision Sciences, Glasgow Caledonian University, Glasgow, UK; Western General Hospital, Edinburgh, UK; 7 Royal Perth Hospital, Western Australia, Australia; and 8 Princess Alexandra Eye Pavilion, Edinburgh, UK

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Abstract. Visual neglect is a common, yet frequently overlooked, neurological disorder following stroke characterized by a deficit in attention and appreciation of stimuli on the contralesional side of the body. It has a profound functional impact on affected individuals. A assessment and management of this condition are hindered, however, by the lack of professional awareness and clinical guidelines. Recent evidence suggests that the underlying deficit in visual attention is due to a disrupted internalized representation of the outer world rather than a disorder of sensory inputs. Dysfunction of the cortical domains and white-matter tracts, as well as inter-hemispheric imbalance, have been implicated in the various manifestations of visual neglect. Optimal diagnosis requires careful history-

taking from the patient, family, and friends, in addition to clinical assessment with the line bisection test, the star cancellation test, and the Catherine Bergego Scale. Early recognition and prompt rehabilitation employing a multidisciplinary approach is desirable. Although no treatment has been definitively shown to be of benefit, those with promise include prism adaptation, visual scanning therapy, and virtual reality--based techniques. Further high quality research to seek optimum short- and long-term rehabilitative strategies for visual neglect is required. ( Surv Ophthalmol 56 :114--134,

2011. 2011 Elsevier Inc. All rights reserved.)

Key words. assessment dorsal stream neglect rehabilitation spatial representation stroke unilateral neglect ventral stream visual neglect

I. Introduction

Visual neglect (VN) is a neurological disorder characterized by a deficit in attention to stimuli on one side of the body, almost invariably contra- lateral to the side of the cerebral lesion. 95 The term has been used loosely and interchangeably with hemispatial neglect, unilateral neglect, and visual inattention. Its adverse impact on day-to-day

2011 by Elsevier Inc. All rights reserved.

functioning and stroke rehabilitation outcome is well established. Stroke, whether ischemic or hemorrhagic, is a de- bilitating and disabling condition that can impair cognition, visuospatial, language, and motor func- tion. 36 Motor rehabilitation following stroke is well recognized, but rehabilitation for visual neglect, a common and dramatic consequence of stroke, 105

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0039-6257/$ - see front matter doi: 10.1016/j.survophthal.2010.08.001

VISUAL NEGLECT FOLLOWING STROKE

has received limited attention, as it can be difficult to identify, and there is currently no consensus con- cerning optimal assessment and treatment of this condition.

II. Epidemiology

A US study 141 of 1,281 stroke patients reported

a prevalence rate of VN of 43% and 20% following

right and left hemispheric stroke, respectively. This asymmetry in prevalence of VN is consistent with other literature 4,13,21 and probably occurs because the right hemisphere tends to allocate attention to both hemispaces, but the left hemisphere accords attention more selectively to right hemispace. 66,116 Also, VN patients with right hemispheric stroke generally have a worse prognosis than those with left hemispheric stroke. 13,46,131 Despite the high prevalence rate, 61% of patients with VN were overlooked during hospital admission in the US, 40 and only 13% of stroke patients were assessed with standardized neglect assessments in

a Canadian study. 114 This low detection rate could be explained by insufficient awareness of this condition or may reflect inherent difficulties in diagnosing neglect in the presence of other more

acute and readily recognizable features of stroke like dysphagia, dysphasia, hemianopia, or hemiplegia. In the UK, the documented prevalence rates of VN post-stroke vary between 8% 164 and 82% 162 as

a result of heterogeneous patient cohorts, inconsis-

tent definition, non-standardized assessment methods, and different timings of the assessment. Increased age has also been shown to be associated with a higher incidence and severity of VN. 57,141 This could be attributed to prior cerebral atrophy or a physiologically dampened reaction time in the elderly population during visual search-

ing activities, especially when intensive visual atten-

Other demographic factors

tion is required.

like sex 111,141 and handedness 141 have no significant

influence on the occurrence of VN.

57,102

III. Varieties of Neglect

A wide range of neglect variants have been described as a consequence of the discrepant classifications adopted. Conceptually, it can be considered under the following headings. 169

A. MODALITY (INPUT/OUTPUT)

Neglect can be divided into sensory (input) and premotor (output) neglect. Sensory neglect is characterized by unawareness of sensory stimuli of different modalities—including tactile/somatosen-

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sory, auditory, and visual or visuospatial in contrale- sional hemispace. Premotor neglect is described as failure to orientate the limbs towards contralesional hemispace despite awareness of the stimulus. VN has been primarily considered part of the spectrum of sensory neglect; recent studies, however, suggest that the underlying deficit primarily is a disrupted internal computation of the spatial representation of the external world rather than a true sensory deficit (see section V. Pathophysiology in this review) This has important implications in for- mulating optimal assessment and rehabilitation strategies.

B. SPATIAL REPRESENTATION

Spatial representation, which depends on the frame of reference, has also been used to distinguish between different neglect subtypes, namely, egocen- tric (viewer-centered) VN and allocentric (stimulus or object-centered) VN. Egocentric VN is described as failure to orientate or attend to the stimuli on the contralesional hemispace with respect to the mid- sagittal plane of the body, head and eye. In contrast, allocentric VN refers to the inability to attend to the one side of the stimulus irrespective of the relative position of the stimulus with respect to the viewer. Egocentric VN has a higher reported incidence than allocentric VN as a sequel to a cerebrovascular event. As a result, the terms ‘‘visual neglect’’ or ‘‘unilateral neglect’’ primarily refer clinically to egocentric VN; however, these neglect subtypes exist as separate entities with distinct neural bases 58,109,113 (see section V.E Clinico-anatomical correlations of visual neglect, herein). VN is a heterogeneous disorder that involves various neurocognitive re- gions, and broader consideration needs to be taken for each neglect subtype.

C. RANGE OF SPACE

According to the classification by ‘‘range of space’’, VN can be divided into personal, periperso- nal, and extrapersonal neglect. This classification has been widely adopted as part of VN assessment of the functional performance in clinical practice.

IV. Functional Impact

VN results in a range of functional impairments, with severe neglect being associated with a poor prognosis. 79,163 Those with left VN fail to attend to their left side, with features ranging from those affecting personal, through peripersonal, to extrap- ersonal space ( Table 1 ). Each subtype of neglect may either manifest as a separate entity or be associated with other subtypes. For instance, a

116 Surv Ophthalmol 56 (2) March--April 2011

TING ET AL

TABLE 1

Definitions and Examples of Personal, Peripersonal, and Extrapersonal Neglect

Personal space the space occupied by one’s body combing, grooming, shaving, recognizing the right half of the body only 17,90 and anosagnosia (a feature in which the patient is unable to recognize his or her own deficit) 14,18 Peripersonal space the space surrounding one’s body, within arm’s reach eating food from the right half of the plate and neglecting the food on the left, reading the right half of the two pages of an open book 28 Extrapersonal space the space surrounding one’s body, beyond arm’s reach failing to identify meaningful stimuli and people on the left, colliding into objects on the left while mobilizing or using a wheelchair

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patient affected by peripersonal neglect does not necessarily also manifest extrapersonal neglect. 59,173 It is important, however, to recognize that this classification concerns the external observers’ in- terpretation rather than the nature of the distur- bance of the internalized, virtual representation of the external world that characterizes human vision/ visuospatial perception. Also, VN may be associated with other forms of neglect, including tactile, auditory, and motor neglect.

V. Pathophysiology

VN is a multifaceted disorder. The anatomical, physiological, and conceptual models of cortical visual processing have always been highly conten- tious scientific issues. As mentioned, VN can be conceptually divided into several categories accord- ing to the modality (input/output), the spatial representation, and the range of space. Although various mechanisms and models have been pro- posed and examined, none has fully and successfully captured the entire spectrum of this heterogeneous disorder. We attempt a systematic overview of pathophysiology and clinico-anatomical correlations of VN from different perspectives.

A. PHYSIOLOGY OF VISUOSPATIAL PERCEPTION

It is becoming increasingly apparent that our brain operates and processes visual information via two distinct, but complementary, higher neural processing pathways, namely, the dorsal stream and ventral stream (as proposed by Milner and Goodale). 56,119,120 They suggested that the dorsal stream, which connects the visual cortex with the superior parietal lobe and the intraparietal sulcus, subconsciously assimilates incoming visual informa- tion in order to bring about immediate ‘‘on-line’’, visually guided movements through the virtual images in the mind, which constitute an internal and subconscious egocentric spatial representation of the multidimensional external world. By contrast, the ventral stream, which bridges the visual cortex

and the inferior temporal lobe, is accountable for our conscious, object-based visual perception and recognition. Dysfunction of dorsal stream results in optic ataxia (impaired visual guidance of move- ment), and dysfunction of ventral stream causes visual agnosia (impaired recognition of visual

stimuli), respectively. Although this model provides

a comprehensive explanation for various compo-

nents of visuospatial perception and visuomotor function, the manifestation of VN, which normally

follows the damage of inferior parietal lobe, has yet

to be fully considered in the context of this dorsal--

ventral dichotomy. 156 Also, the double dissociation

between VN and optic ataxia or visual agnosia has suggested separate underlying disorders of the

neural substrates. Instead of the occipito-parietal and occipito- temporal pathways, the dorsal--ventral dichotomy variant proposed by Corbetta and Shulman 32 focused on the attentional basis of the frontopar- ietal networks, namely, the dorsal and ventral frontoparietal pathways. The bilateral ‘‘dorsal’’ pathways, which connect the superior parietal lobes and the intraparietal sulci with the dorsal frontal lobes, including the frontal eye fields, are involved in goal-directed, top--down attentional selection. 32 This top--down attention facilitates visuospatial exploration in the context of prior knowledge of what to search for or what the task is. 33 In contrast, the right lateralized ‘‘ventral’’ pathway, which links the temporal parietal junction (TPJ), inferior parietal lobe (IPL), and ventral frontal lobe, is associated with stimulus-driven, bottom--up atten- tional selection. 32 This bottom--up attention simply refers to the ability to capture an event occurring in the surrounding world—salience detection. 33 In view of the overlap between the neural basis of VN and their proposed ‘‘ventral’’ network, Corbetta and Shulman infer that VN is associated with a bottom-- up attentional deficit. 32 Also, their proposed right lateralized ventral pathway helps explain the higher incidence of VN following right posterior parietal damage.

73,133

VISUAL NEGLECT FOLLOWING STROKE

In addition, consistent activation of both frontal and parietal regions, as evident from imaging

during tasks requiring spatial atten-

studies,

tion and visuomotor function have supported the

neural basis of this fronto-parietal model. Nonethe- less, there is emerging evidence showing that patients with VN may exhibit deficits of both attentional components, including sustaining atten-

tion (goal-directed)

and salience detection

(stimulus-driven), 23,33 which suggests that a combi-

nation of both of the described conceptual frame- works is required to explain this complex disorder.

52,134,157

24,74

B. SPATIALLY LATERALIZED DYSFUNCTION OF VISUAL NEGLECT

According to the original definition, VN is a disorder characterized by the failure of orientating or attending towards the stimuli on one side of the hemispace; it is a form of spatially lateralized dysfunction. For instance, patients with ‘‘egocentric’’ VN can exhibit complete inattention (perceptual/ input neglect) or impaired visuospatial exploration (premotor/output neglect) confined to contrale- sional hemispace, with normal visuospatial percep- tion within ipsilesional hemispace. This spatially lateralized dysfunction of VN has been well demon- strated by both clinical observation and the VN assessment tools (see subsequent discussion). Heilman et al 66 hypothesized that the right posterior parietal cortex, which is highly specialized for spatial attention, allocates attention to both hemispaces, whereas the left posterior parietal cortex allocates attention, more selectively, to the right hemispace. This explains why VN is more commonly reported following right rather than left hemispheric damage. 13,21,141 This is also why the affected in- dividual exhibits deficits on the contralesional side as well as the ipsilesional side, to a milder extent, 12,149 when the right hemisphere is affected. Moreover, the common paradoxical observation of contralesional limb apraxia (inability to activate limb) following left IPL damage, but the development of VN following right IPL damage, underlines the organizational and functional asymmetry between both IPLs, at least in the context of spatial attention. 54 On the other hand, Kinsbourne 96 suggested that allocation of spatial attention towards both hemi- spaces is balanced by the reciprocal inhibition from each hemisphere, with left hemisphere allocating attention towards the right hemispace and vice versa. Therefore, when there is a right hemispheric damage, the unopposed left hemisphere becomes relatively hyper-attentive towards the right hemi- space, subsequently leading to left VN. This model is further reinforced by Koch et al 100 that describes

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relative electroencephalographic hyperexcitability in the left posterior parietal cortex (PPC) of the neglect patients with right hemispheric stroke, resulting in rightward attention bias (or left visual neglect). Improvement of VN was observed in 7 of 10 patients following the application of repetitive transcranial magnetic stimulation (r-TMS) over the unaffected PPC. In a similar vein, Oliver et al 128 reported beneficial effect in patients with VN following the application of r-TMS on the un- affected PPC. An explanatory mechanism is that r-TMS disrupts the integrated neural activity of the intact side, dampening the attention to the ipsile- sional side, and thereby restoring the orientation balance between both hemispheres.

C. NON-SPATIALLY LATERALIZED DYSFUNCTION OF VISUAL NEGLECT

Until recently, VN was thought strictly to be attributable to lateralized disruption of the spatial attention on one side of the visual space; however, there is emerging evidence proposing that VN is not necessarily confined to one hemispace. It can

comprise both spatially lateralized and non--spatially lateralized dysfunctions. 74 In other words, patients with VN may completely neglect the contralesional hemispace (spatially lateralized) while demonstrat- ing global inattention to stimuli regardless of the location of the target (non-spatially lateralized). Both the IPL and the ventral frontal region— which, when damaged, are frequently associated with VN—have been shown to exhibit functions related to non-spatial attention including sustained

attention and salience detection.

patients, with damage to the IPL, may demonstrate these non-spatial attentional deficits. This can be assessed by techniques including the oddball para- digm, 31,38 which requires the patient to detect target stimuli interspersed with non-target stimuli at the same area, and attentional blink paradigm, 75 a mea- sure that assesses the ability of salience detection and perception of each stimulus among a series of rapidly changing stimuli at one spatial location. A delayed ‘‘attentional-blink’’ response is suggestive of an attentional deficit. Although non-spatial inatten- tion may be doubly dissociable from VN, 150 the presence of a non-spatial attentional deficit aggra- vates the severity of VN. These intriguing findings enhance understanding of the pathophysiology of VN and, more impor- tantly, facilitate the development of potentially more effective therapies including sustained attention measures and pharmacological intervention di- rected towards improving general non-spatial attention. 107

74

Similarly, VN

75

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Surv Ophthalmol 56 (2) March--April 2011

D.

ROLE OF NON-VISUAL AFFERENT INPUTS

In addition to visual afferent input, egocentric multidimensional internalized spatial mapping re- quires multiple afferent inputs from non-visual receptors, including neck muscle 19 and extra- ocular muscle proprioceptors, 75 and the tactile and the vestibular systems. 125,127 This afferent pro- prioceptive feedback maintains the required stabil- ity and perception of the location of the visual images by maintaining correct egocentric localiza- tion of the body despite head and eye movement. There is evidence that patients who have altered

extraocular muscle proprioception 175 —either from surgery, 25,161 forced ductions with a suction contact lens, 48 or dysfunction of the trigeminal nerve 26,171 — demonstrate errors in spatial localization and visually guided movement.

demonstrated the role of neck muscle

proprioception in maintaining egocentric spatial localization. He observed that the ipsilesional de- viation of neglect patients when looking straight ahead can be ameliorated by the application of vibration to the contralesional neck, 87,152 modi- fying the afferent input from the neck muscle proprioceptors. In addition, the role of the vestibular system in body orientation and egocentric spatial localization has long been recognized. The vestibular input contributes to spatial orientation mainly via the vestibulo-ocular reflex, which involves the trans- mission of afferent inputs from the vestibular nuclei to the ocular motor nuclei and higher cortical

centers via the medial longitudinal fasciculus. 125,127 Following integration of the afferent inputs in the higher cortical centers, efferent outputs are trans- mitted along vestibulospinal projections for head, eye, and body orientation—the internal ‘‘plumb line,’’ which accords balance and our knowledge of

the vertical, and hence, spatial localization. This concept has been further reinforced by the use of vestibular caloric stimulation (irrigation of the ear canal with either warm water ipsilaterally or cold water contralaterally), which transiently reduces the orientation bias in VN and can restore the egocen- tric spatial reference frame. 88,147 Longer term interventions, designed to ‘‘deceive’’ the sensory input of the visuospatial perception rather than addressing the underlying lack of awareness, re- mains elusive.

125,127

Karnath

87

E. CLINICO-ANATOMICAL CORRELATIONS OF

VISUAL NEGLECT

Several factors challenge clinicians and researchers investigating the neural basis of VN. First, patients with VN often manifest extensive brain damage, which

TING ET AL

hinders precise anatomical correlation. Second, pure assessment of VN is problematic in the stroke patient who has co-existing cognitive impairment, causing difficulty in recruiting ‘‘ideal’’ VN patients for further

investigation. Also, the lack of detailed classification of the different neglect subtypes can lead to over- generalization of the neural basis of VN. For example, the distinction between egocentric VN and allocentric VN, which can occur independently, 58,109 has not been made in many studies. Various cortical regions serving visuospatial atten- tion have been identified by high quality functional brain imaging like functional magnetic resonance imaging and positron emission tomography. These regions comprise, in particular, the inferior parietal

the superior temporal

lobe and the

gyrus,

85 and the frontal lobe, including the medial

and inferior frontal gyri. 75,76 In contrast, the pre- viously controversial role of the subcortical regions implicated in VN has been refuted by recent studies, suggesting that, instead of the subcortical infarction itself, VN is associated with hypoperfusion of the overlying cortex and that subcortical infarction alone does not result in VN. 70 The neuroanatomical findings can be influenced by the timing of assessment. For instance, Mort et al, 123 who investigated the neural basis of VN during the chronic phase (63 days post-stroke), have reported that VN is most strongly associated with angular gyrus (part of the inferior parietal lobe) infarction. In contrast, Karnath et al 84 examined their patients at 8 days post-stroke and had observed the superior temporal gyrus is the most common implicated region in VN. Moreover, the development of diffusion tensor imaging, which provides the facility to track white- matter tracts, has led to a quantum leap in the understanding of the neuro-anatomical correlation of VN. Various white-matter tracts have been identified, particularly in the fronto-parietal net-

and their dysfunction can lead to the

‘‘disconnection syndrome’’ underlying VN. 11,37 This observation is in accordance with the anatomical and theoretical model proposed by Corbetta and Shulman, 32 who focused on the attentional basis of the fronto-parietal network. This suggests that spatial attention operates in a multi-level network that requires intact neurocognitive cortical regions and the underlying connections between them. Interestingly, VN results from both anterior and posterior circulation strokes, depending on the affected corresponding white-matter tracts. 15,37 In addition, VN has been classified according to the site of neuroanatomical damage, which chiefly comprises three areas: the parietal lobes, the frontal eye fields, and the cingulate regions. 117 Each of the

work, 11,15,37

TPJ, 64,70,123,170

VISUAL NEGLECT FOLLOWING STROKE

TABLE 2

119

Summary of Neuroanatomical Classification and the Functional Consequences of VN

Type

Function of Each Area

Presentation

Parietal neglect

The posterior parietal lobes integrate afferent stimuli of any modality including visual stimuli, transforming external space into an internalized representation

Loss of subconscious synthesis of the internalized representational space, resulting in unawareness of the visual stimuli in contralesional hemispace, even one’s own body (a form of anosagnosia) Failure of limb orientation towards contralesional hemispace in the absence of hemiparesis, even when using the unaffected limb on the ipsilesional side, which suggests the abnormality lies in motor output instead of sensory input; 34,65 this is probably secondary to a defect in the internalized representation of motor programming towards the contralesional side Spends a disproportionately long period attending to the greater motivational event, omitting the others which have less impact

Frontal neglect

The frontal eye fields interact with the parietal lobes in selecting salient information and filtering irrelevant information, thus planning meaningful visually guided movement

Cingulate neglect

Provides limbic integration, responsible for allocating directed attention according to motivation 130

Data from Mesulam et al. 117

neuro-anatomical neglect subtypes exhibits some

degree of site-specific variation ( Table 2). Although this classification provides useful insights into the complex neuroanatomical correlation of VN, it does not include the underlying complex disorders of function. Also, the differentiation of these subtypes can be difficult in clinical practice. As discussed earlier, spatial representation takes into account different frames of reference, primarily viewer-centered (egocentric) and stimulus-centered

examined the neural basis

of VN subtypes and observed distinct physiology and

neural correlates underlying both subtypes with the aid of high quality functional brain imaging. They have reported that egocentric VN primarily follows

and, to some

damage to the inferior parietal

extent, the posterior inferior frontal gyrus, 70 which

are implicated in the ventral frontoparietal network proposed by Corbetta and Shulman. 32 Similar asso- ciation between egocentric VN and dysfunction of the supramarginal gyrus (part of the inferior parietal lobe) has been observed by Medina et al. 113 On the other hand, allocentric VN is more commonly observed following injuries to the temporal regions,

the ventro-

including the superior temporal gyrus,

medial temporal area, 58 and the posterior inferior temporal gyrus. 113 This is consistent with Milner and Goodale’s proposal that the temporal or ventral pathway is highly accountable for object- based perception and recognition; therefore, dys- function of this pathway leads to allocentric VN. The functional differences and the interactions among various intra-temporal regions have yet to be further investigated.

(allocentric). Hillis et al

70

lobe 69,70

70

Although the neural correlates of left VN have been well studied, right VN following left hemispheric

stroke has received limited attention. Kleinman et al 98 focused on the neural correlates of VN subtypes following left, instead of right, hemispheric stroke and reported a higher proportion of allocentric VN than egocentric VN, which contrasts with the findings

These findings, once again, suggest

of Hillis et al.

that both hemispheres are organized and function in distinct ways in the context of spatial attention.

In view of the heterogeneity of VN, we emphasize that all studies should be interpreted with caution because they are influenced by the type of VN included in the study, the assessment methods used, and the timing and type of brain imaging instituted.

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F. CLINICAL SYNDROMES ASSOCIATED WITH VISUAL NEGLECT

VN has been found to be associated with other complex parietal lobe syndromes that affect visuo- spatial comprehension and attention, such as Gerstmann and Balint syndromes. Gerstmann syn- drome results from a focal lesion affecting the

angular and supramarginal gyri near the TPJ, usually on the left, and is characterized by inability to perceive an object properly (agnosia), dysgra- phia, dyscalculia, and left--right disorientation. 132 Balint syndrome, first reported in the early 20th century, 9 is an uncommon disorder that classically results from bilateral posterior parietal pathology and comprises a constellation of symptoms: unilateral visuospatial inattention (left hemineglect), deficits in visually guided movement despite normal limb

120 Surv Ophthalmol 56 (2) March--April 2011

strength (optic ataxia), and the inability to shift gaze voluntarily to objects of interest despite normal eye movements (ocular apraxia). 9,63 The spatial disorder of attention emphasized by Balint was further regarded as ‘‘disturbance of visual orientation’’ by Holmes 71 and simultanagnosia by Wolpert. 177 Based on his observation of six soldiers with bilateral parietal-occipital lobe injury particularly affecting the angular gyri, Holmes concluded that damage to the angular gyri can lead to what he called a ‘‘distur- bance of visual orientation’’ 71 and results in difficul- ties in precise determination of the multidimensional position of an object or relative positions of objects (optic ataxia) and in learning the new surroundings and in transferring attention from one object to another (ocular apraxia). On the other hand, the term ‘‘simultanagnosia’’, coined by Wolpert, 177 refers to the inability to perceive and integrate all the components of a visual scene. Each element of Balint syndrome—left hemineglect, optic ataxia, and ocular apraxia—may manifest independently. 34 Refer to Rizzo and Vecera’s 142 study for further elaboration.

VI. Assessment of Visual Neglect

A. CURRENT CLINICAL GUIDELINES

Recommendations concerning the specific assess- ment methods of VN remain limited. US 39 and UK 77,154 guidelines consistently recommend that visuo-perceptual function, including the potential for VN, should be assessed in patients in stroke units employing a multidisciplinary approach. Mini- Mental State Examination and Addenbrooke’s Cognitive Examination (2005) are the two most well-recognized general cognitive assessment batter- ies in current clinical practice in the UK. 47,121 The limitation of both tests is that VN is only assessed by drawing and copying objects ( Table 3 ). No specific assessment tool is recommended in the US. On the other hand, the UK guidelines 77 recommend the use of Behavioral Inattention Test whereas the Canadian 27 guidelines recommend the use of specific assessment tools for VN, comprising the Comb and Razor Test, the Line Bisection Test (LBT), and the Behavioral Inattention Test with the alternatives of the Rivermead, Ontario Society of Occupational Therapy Perceptual Evaluation and the Motor Free Visual Perceptual Test.

B. HOW IS VISUAL NEGLECT ASSESSED?

The results of an extensive literature search concerning the assessment of VN and the underlying rationale, assessment profiles, with strengths and weaknesses of the more common tests of VN are

TING ET AL

summarized in Table 3 . The assessment methods comprise four main groups: pencil-and-paper tests, behavioral assessment, clinical observation, and more recent techniques.

1. Pencil-and-paper Tests

VN can be sought by the cancellation test, the LBT, and the copying and drawing test. 144 The cancellation task ( Fig. 1) requires the patient

to delete multiple identical visual target symbols on

a paper sheet. Incomplete or disproportionate de-

letion on one side indicates VN. There is robust evidence showing that this type of test, particularly

interspersed with distracters, has the best sensitivity of the pencil-and-paper tests. 60,61,97,110 Common vari- ants include the star cancellation test, the letter cancellation test, and the bell cancellation test. Moreover, structured observation of cancellation test performance, taking into account the location of the initial commencing point 2 (deemed to be the most sensitive measure) along with the scanning pattern, the search time, and the number of re-cancellations of the same target, 55,108,167 provide useful qualitative information in addition to quantitative scores. The LBT ( Fig. 1 ) requires the patient to estimate and bisect the midline, thereby determining left- ward/rightward orientation bias. Despite limitations, the construct validity, 110 reasonable sensitivity and reliability, and ease of administration render this

a good supplementary pencil-and-paper test. 8 The

minimal time required for administration is a major advantage for clinicians. On the other hand, copying and drawing tasks ( Fig. 1 ) are the least satisfactory pencil-and-paper tests in terms of sensitivity, reliability, and validity, 8 but have a place in gaining an understanding of the nature of the morbidity. Lindell et al 104 and Jehkonen et al 80 have highlighted the benefit of combining several tools in yielding a higher detection rate and better characterization of VN. On the basis of the available evidence, the star cancellation test, coupled with the line bisection test, are recommended as screening tools for all patients with hemispheric stroke.

2. Behavioral Assessment Tools

Azuovi et al found that behavioral assessment has

a much higher sensitivity than pencil-and-paper tests

(96% vs 65%). 5 This finding is in accordance with other similar studies. 6,61 Therefore, behavioral assessment is essential to enhance VN detection rate and, more importantly, to determine and evaluate the nature and level of functioning. 4 The BIT and the Catherine Bergego Scale (CBS) are two of the most frequently used tests. The BIT 176 is

VISUAL NEGLECT FOLLOWING STROKE

TABLE 3

Synthesis of Various Types of Assessment of VN

Tests

Brief Description/Rationale

Strength

Limitation

Cancellation

Refer to a

Patient is asked to cross out the visual targets on a paper sheet Looking for disproportionate omission of visual targets on one side of hemispace

Star cancellation has the best sensitivity (76.4% 60 to 100% 110 ) among the three forms of pencil-and- paper tests Good construct validity Greater reliability than line bisection test 110 Qualitative interpretation enhances the detection

rate

55,108,167

110

Line Bisection Required to estimate and bisect the middle of straight lines Deviation towards the ipsilesional side suggests orientation bias and, hence, potential visual neglect

Drawing and

Required to draw and copy objects

copying task Leaving out one side of the given object or cramming everything in one side of the figure is suggestive of VN

Easy to administer Good validity Reasonable sensitivity 115 (60% 43 to 76.4% 8 ) Comparable reliability to cancellation test May help distinguish between motor and sensory neglect with modification of test

Assesses for representational neglect, which may suggest the presence of orientation bias and potentially, VN

False positive results may be produced secondary to hem- ianopia/handedness 43 Sometimes non-standardized Difficult to interpret the result Refer to a

Poor sensitivity and validity 8 Interpretation of outcome lim- ited by subjectivity and other cognitive impairment Refer to a

Comb and

Asked to comb hair and shave side of the face

Razor test

Looking for omission of one

Behavioral

Consists of six pencil-and-paper tests and nine behavioral subtests

Inattention

test 62

Catherine

A checklist of 10 items that assess normal functioning in daily

Bergego

Scale 5

living

Clinical

observation

Continuous observation during the delivery of care, looking for signs indicative of VN, for instance, eating food from one side of the plate, colliding repetitively with obstacles on the same side

Good supplementary test for behavioral inattention as Only assesses personal space

it assesses attention for personal space

Assesses functional performance Provides quantitative and objective assessment

Good predictive measure of functional performance

in daily living

62,115

May be confounded by other stroke conditions (e.g., hemiparesis)

Does not evaluate personal space Time consuming

Assesses all three conceptual spaces including the functional performance in daily living Assesses patient’s self awareness of own deficit (anosagnosia score) 7 Good validity, reliability and sensitivity 5,115

Allows continuous assessment of VN, which might be Does not provide quantitative

missed earlier on Improves the detection and assessment of VN when used as a supplementary method to clinical VN

Scoring of the outcome does not differentiate the neglect subtypes

and objective assessment Cannot differentiate between motor neglect and VN Non-standardized

tests 81,164

individuals 78 may vary

There is no robust evidence on

the validity, sensitivity, and reliability of this test Does not assess personal space

perception in space

the

of validity, is

and reliability

Focuses on peripersonal

virtual environment

Limitation

evaluation

sensitivity,

Visuospatial

required

between

Further

as manual the exploration

patient’s visual search pattern and develop better understanding of the nature of VN

scanning pattern, Presence of eye trackers aid the assessor to record

Allows assessment in a simulated environment re- lating to daily life Creates a more interactive, versatile and safer

motor

et al. 137 for peripersonal space and cannot differentiate between input and output neglect.

which of thus VN excludes

environment for assessment of VN

component/premotor neglect

Strength

assessment

is not pure required,

Table 3 ( continued )

Allows

Looking for orientation bias towards the ipsilesional side which indicates VN

Oculography 30 Requires image or the task patient to focus at the midpoint of a given object,

head-mounted display), eye

Enables the users to explore real-time virtual images while

and analyzed

head motion,

Brief Description/Rationale

are recorded

hardware (i.e., sensor

orientation including

Plummer attention

trackers, a set and of head-position

and spatial information

is modified only from evaluate

relevant

Virtual reality Requires

a This These table investigations

Tests

122 Surv Ophthalmol 56 (2) March--April 2011

TING ET AL

a 15-item checklist, which comprises six conventional

tests (line crossing, letter cancellation, star cancella- tion, figure copying, line bisection, and free drawing) and nine behavioral tests (picture scanning, tele- phone dialing, menu reading, article reading, telling and setting the time, coin sorting, address and sentence copying, map navigation, and card sorting). There is consistent evidence showing that BIT serves as a good predictive measure of functional perfor- mance in daily living. 62,115 The major limitation of this battery is that it does not formally assess the personal space. This is imperative because each of the neglect subtypes (personal, peripersonal, and extrap- ersonal) can manifest as a separate entity. On the other hand, the CBS is a 10-item checklist that focuses on functional performance of activities of daily living. These include grooming and shaving

the left part of the face, wearing the left sleeve or slipper, eating food on the left side of the plate, cleaning the left side of the mouth after eating, spontaneous leftward gaze, ‘‘knowledge’’ of the left part of the body, auditory attention to stimuli from

the left, collisions with objects on the left, leftward navigation in familiar places, and locating familiar items on the left. Although this test was originally designed for the assessment of left VN, it should be applicable to right VN. We prefer CBS over BIT because CBS considers all three conceptual spaces, includes anosognosia scoring, 7 and has fine psycho- metric properties, including validity, sensitivity, and reliability. 5,115 Anosognosia scoring serves as an

important indicator of VN severity. We recommend that all patients who demonstrate spatial orientation bias on VN screening test should undergo some form of behavioral assessment like BIT or, preferably, CBS.

7

51,137

3. Clinical Observation and History-taking from

the Patient and the Near Contacts

Skilled clinical observation should increase the

detection rate of VN, 81 which may be missed because of the false negative result of the standard- ized tests and VN’s inherently subtle and fluctuating course. 2 Family and friends who are familiar with

a patient’s normal behavior may also play a signifi-

cant role in picking up subtle neglect behavior. VN may be missed during the acute phase of stroke but may be picked up later by other allied health professionals or at home by the near contacts.

4. Recent Development of Assessment

Technique

One of the main shortcomings of the pencil-and- paper tests is the inability to differentiate between sensory/input and premotor/output neglect, as

VISUAL NEGLECT FOLLOWING STROKE

123

VISUAL NEGLECT FOLLOWING STROKE 123 Fig. 1. Examples of patient with VN neglecting the stimuli on

Fig. 1. Examples of patient with VN neglecting the stimuli on the left hemispace in: ( A ) a cancellation task; ( B) a line bisection task; and ( C ) a copying and drawing task. (Adapted from http://ahsmail.uwaterloo.ca/ waktse/assessment. html .)

these tests require both visual attention and manual exploration. Chiba et al 30 have proposed the use of oculography for the midpoint-fixation task, which removes the manual component. Virtual reality (VR) based techniques may poten- tially overcome the shortcomings of traditional assessment methods. 94 The use of VR systems not only helps to establish a better assessment and understanding of the nature of VN, but also creates

a safe, versatile, and multimodal virtual environ-

ment to assess the patient’s functional performance

in a range of daily living tasks. Conventional tests including the line bisection test, the cancellation test, and daily living tasks have all been incorpo- rated into a VR system. 166 However, the VR assessment focuses on use of peripersonal and, to

a certain extent, extrapersonal space and further

evaluation is required to determine its sensitivity,

cost-effectiveness, and practicability.

C. DISTINCTION BETWEEN VISUAL NEGLECT AND OTHER VISUAL PROBLEMS

VN is commonly associated with other visual problems, including visual extinction and homony-

mous hemianopia (HH). Therefore, understanding of the nature of these visual problems and the distinct features of each visual condition should facilitate assessment and diagnostic process. Visual extinction is described as the failure of identifying one of two simultaneous stimuli, while retaining the perception of a stimulus presented

singly in either hemispace. 169 Unlike VN, the allocation of attention in the context of visual extinction is largely task-dependent. 172 For instance, the ability to localize stimuli on bilateral display can be markedly impaired (similar to neglect), but with retained normal reporting of numerical stimuli on

Extinction may also occur

bilateral presentation.

when both stimuli are presented simultaneously

within the same hemifield.

extinction has been described as a cardinal sign indicative of a deficit in attention, 16,139 or as part of neglect disorder. 67 Clinically, visual extinction should be sought during neurological examination, as visual extinction and neglect are commonly, but not in- variably, associated. 49 This can be done by asking the patient to point to the examiner’s moving finger, initially one side at a time and then bilaterally inmirror

172

172

Nonetheless, visual

124 Surv Ophthalmol 56 (2) March--April 2011

image quadrants. The ability to identify a single stimulus, but not simultaneous stimuli, defines extinc- tion. In addition, Hillis et al 68 have shown that visual, tactile, and motor extinction involve mainly the visual association cortex, the inferior parietal lobe, and the superior temporal gyrus, respectively. These anatom- ical findings, which considerably overlap with the neural underpinnings of VN, help explain the frequent co-occurrence of both VN and extinction. Involvement of ophthalmologists and orthoptists is of potential value, as ‘‘egocentric’’ visual neglect may occasionally coexist with, or masquerade as, a visual field defect, 101 despite their distinct patho- physiology. Egocentric VN is characterized by in- attention toward the contralesional hemispace, which is independent of the direction of gaze, whereas HH is the actual loss of visual field of contralesional hemispace, which can be compen- sated by the head and eye movements. Scanning behavior, which relies on spatial attention, serves as the primary distinguishing factor. Patients with VN can have profound difficulties in surveying and navigating the visual scene in affected hemispace and cannot consciously compensate for within the neglected hemispace. In contrast, HH poses a less significant impact on the affected individual’s scanning behavior because spatial attention of one side of the visuospatial world is retained, thereby allowing compensatory movement of the eye, head, and body towards the affected visual field. There- fore, behavioral assessment can be very useful in differentiating these two disorders. In addition, VN, but not HH, is commonly associated with visual extinction. 49 Also, other modalities such as somatosensory, auditory, and motor neglect may coexist with VN, whereas HH is strictly a visual deficit. Visual evoked potentials (VEPs) are increasingly used to differentiate VN and HH. Patients with VN usually have a near normal response on VEPs, 160 whereas patients with HH commonly demonstrate marked disparity be- tween the normal and affected hemifields. 90 In addition, various alternative methods have been proposed to distinguish these conditions 93 ( Table 4 ). Such differentiation may be difficult, as they may overlap or be compounded by a condition called hemianopia anosognosia, which is characterized by unawareness of the visual field loss. 18,29

D. SUMMARY AND RECOMMENDATIONS FOR THE ASSESSMENT OF VISUAL NEGLECT

Despite a lack of consensus regarding neglect assessment, we recommend that health professionals routinely assess for personal, peripersonal, and extrapersonal neglect, and, more importantly, the

TING ET AL

level of independence in activities of daily living. We recommend that the star cancellation test and the line bisection test should form part of the routine cognitive assessment battery. This approach is best coupled with the Catherine Bergego Scale and continuous clinical observation via multidisciplinary teamwork. Application of virtual reality--based assess- ment may be of potential value in future practice. In addition, it is imperative to distinguish VN from other visual problems, especially homonymous hemianopia.

VII. Rehabilitation of Visual Neglect

There is an extensive body of literature concern- ing the effectiveness of the rehabilitation of VN. In order to minimize the selection bias and enhance the level of evidence, we have, therefore, centered analysis on high-quality literature such as systematic

reviews and randomized controlled trials. Relevant evidence 3,20,50,82,103,106,136,140 regarding the effec-

tiveness of rehabilitation is summarized in Table 6 .

A. CURRENT CLINICAL PRACTICE

Clinical guidelines 77,154 recommend a multidisci- plinary approach in managing cognitive impairment including visual neglect but there is no clear and specific guidance on the choice of interventions. As a result, heterogeneous interventions are applied by different institutions, depending on the local guidelines, health professionals’ clinical experience, and clinical resources.

B. TYPES OF REHABILITATION

Interventions include utilizing remaining intact brain function (compensation), adaptation to the impairment by using prosthetic devices or environ- mental modification (substitution), or retraining of the impaired function (restitution). 92 Although certain interventions involve more than one mech- anism, some fall outside this classification. We summarize available interventions ( Table 5 ) and their effectiveness ( Table 6 ). Traditionally, rehabil- itation focused upon the compensatory and sub- stitutive interventions as the brain was thought to have limited regenerative ability. However, recent evidence suggests that the brain has the ability to reorganize and reconstruct following damage ( neuroplasticity ), 22,78,91,112 suggesting the possibility of success of restitutive rehabilitation.

1. Compensatory

Visuospatial perception relies on intact internal subconscious computation of the outer world along with feedback from different sensory

VISUAL NEGLECT FOLLOWING STROKE

125

TABLE 4

How to Distinguish Visual Neglect from Homonymous Hemianopia

Criteria

Visual neglect

Homonymous Hemianopia

Visual behavior

Lack of attention to contralesional hemispace, independent of the direction of gaze Usually unaware of own deficit

Loss of visual field of contralesional hemispace, with respect to the position of the head and eyes Usually retains awareness to a certain extent Usually within the territory of the posterior cerebral artery Strictly confined to visual modality

Awareness of deficit

Location of lesion

Usually within the territory of the middle cerebral artery May associate with other modalities

Uni- vs multi-modal deficit

Extinction Drawing from memory

Visuospatial disorder Line bisection Attentional ‘‘cueing’’ strategies

Specific perimetric techniques

VEP and eye movement registration

like auditory, tactile and motor Frequently associated 49 Less commonly associated

Commonly leave out the details on the affected hemispace

More commonly affected Usually not affected

Ipsilesional deviation Presence of cueing may ameliorate neglect (usually transiently) Difficulty in maintaining central fixation Near normal response to stimulation on both sides but prolonged latency may be demonstrated on the affected side 160

Normal and symmetrical

Usually contralesional deviation 122 Presence of cueing does not modulate the disorder Good control of central fixation

Marked disparity between the normal and affected hemifield 90

VEP 5 visual evoked potentials. This table is modified from Kerkhoff et al. 93

modalities. 19,75,125,127,175 The compensatory, bot- tom--up approach of rehabilitation focuses on the modulation of the afferent inputs towards the central internalized process of the inner mind by utilizing the remaining intact brain function and various afferent/sensory modalities, including vi- sual, tactile, vestibular, extraocular, and neck muscle proprioception. This type of intervention does not address the underlying lack of self-awareness of the deficit by the affected individuals, resulting in only short-lived improvement. Some interventions, such as feedback training and r-TMS, may involve more than one mechanism ( Table 5).

2. Substitutive

This form of rehabilitation involves neither mod- ulation of afferent inputs nor enhancement of self- awareness, but rather adaptation to the underlying visual neglect with the aid of rehabilitative measures such as prism adaptation, visual scanning therapy, and environmental modification. These methods potentially impact VN more than pure compensatory interventions, as the improvement of VN relies on both adaptation and subconscious active learning, taking advantage of neuroplasticity. 145 Also, the affected individuals may sometimes benefit from ‘‘substitutive’’ measures rather than ‘‘restitutive’’ methods as they are so severely affected that the underlying deficit cannot be appreciated ( Table 5).

3. Restitutive

This form of rehabilitation focuses on retraining of the impaired function 92 and the modulation of the internalized perception of the outer world, rather than altering the afferent inputs. This may be achieved by increasing self-awareness with mental imagery, transcranial magnetic stimulation, virtual reality--based space remapping, and, potentially, feedback training ( Table 5 ).

C. CURRENT EVIDENCE ON THE EFFECTIVENESS OF REHABILITATION

As a result of our literature search, eight systematic reviews 3,20,50,82,103,106,136,140 concerning

the effectiveness of rehabilitation were identified; they are summarized in Table 6. Visual scanning therapy (VST) and prism adapta- tion are the two best-studied neglect rehabilitative interventions, probably on account of the ease of administration, cost-effectiveness, and easily repro- ducible positive results. Jutai et al, 82 Luaute et al, 106 and Pizzamiglio et al 136 recommend the use of VST in patients with VN. Generalization of task-specific effects to a functional level has been documented by Geusgen et al. 50 However, the role of additional passive sensory stimulation in the context of VST is inconclusive. 136,153 There is strong evidence demonstrating that prism adaptation helps rehabilitate VN. 3,106 Long-term beneficial effects can be achieved via a short period

126 Surv Ophthalmol 56 (2) March--April 2011

TING ET AL

TABLE 5

Summary of Underlying Rationale/Concepts for Various Types of Rehabilitation for Unilateral Neglect

Types

Interventions

Brief Descriptions/Proposed Rationale

Compensation

Visual scanning therapy 174,178

Re-develop an organized scanning pattern by learning systematic right-to-left search Induce left pursuit movement with the aid of leftward

Activate attention on the neglected side with ‘‘cueing’’ stimuli (visual, auditory or tactile) Re-center the spatial egocentric frame of reference by modifying the afferent neck proprioceptive inputs relative to the position of the head to the trunk Re-center the spatial egocentric frame of reference by modifying the afferent information relative to the position of the head to the trunk Induce nystagmus towards the affected side with cold contralesional or warm ipsilesional caloric stimulation Increase leftward saccades by occluding the unaffected

Improves spatial attention by generating general arousal

Optokinetic stimulation 124

moving background targets Limb activation 143 Improve attention on the neglected hemifield by moving the contralesional limb in the neglected hemispace

Training with ‘‘cueing’’ 174

Neck muscle vibration 86,88,152

Trunk rotation 44,88

Caloric stimulation 147

Eye patches 44,179

right hemifield Fresnel prisms 148 Shift the affected visual hemifield towards the unaffected ipsilesional egocentric frame of reference

Sustained attention training 144

system Substitution Prism adaptation 3,118,146 Recalibrate the midline of the egocentric reference frame by using prism adaptation and successive visuo-motor actions; an after-effect of leftward shift towards the neglected hemifield following prism removal may improve VN

Minimize the required visual attention during visual scene navigation by reducing the background and foreground

environmental distracters Restitution Pharmacological treatment 107 Improve general non-spatial attention by using dopamine and norepinephrine agonists

Improve representational (imagery) neglect by using visual or movement imagery Remap the egocentric reference frame towards the affected hemifield by using VR system Increase patients’ self awareness (restitution) with feedback sessions (video, mirror, verbal, visuomotor) following certain tasks, point out their neglect behavior, and teach them the ‘‘compensatory’’ strategies to improve functional performance Disrupt the integrated neural activity of the intact side, dampen the attention to the ipsilesional side and thereby restore the orientation balance between both hemispheres (compensation), 99,128 or alternatively, induce the process of neuroplasticity (restitution) Stimulate cognitive function via sensory and emotional stimulation

Compensation and

Diminished background

pattern and

foreground clutter 35

Mental imagery 158

VR space remapping 1

Feedback training 159

Restitution

r-TMS/direct polarization 99,128,129

Music therapy 53

129

Unknown

VR 5 virtual reality; r-TMS 5 repetitive transcranial magnetic stimulation.

of prism adaptation 42 and ongoing improvement has been observed even 5 weeks after the active phase of rehabilitation. 45 Such long-term effects do not occur with passive Fresnel prism exposure, 118 demonstrat- ing that improvement relies on more than just modulating the afferent inputs, and requires the feedback loop of rewarded motor activity. Nonetheless, the vast majority of the prism adapta- tion studies are case reports or small case series. A

recent single-blind randomized controlled pilot trial of 34 neglect patients conducted by Turton et al 168 has shown that prism adaptation does not provide any beneficial effect on the functional performance of the VN patients, as measured by CBS and BIT, despite the improvement of pointing behavior. The inconsistent effect of prism adaptation observed across different studies may be influenced by the inconsistency of prism adaptation methods used, the disparity of

VISUAL NEGLECT FOLLOWING STROKE

127

TABLE 6

Synthesis of Reviews of Evidence of Effect of Interventions for Visual Neglect 3,20,50,82,103,106,136,140

Reviews

Included Studies

Aims

Key Findings

Limitation of Evidence

Arene 2007 3

31 studies—mixed trials of different quality

Assess mainly the effectiveness of passive sensory stimulation, prism adaptation, visual scanning therapy, and pharmacological treatment

Passive sensory stimula- tion only confers short- lived improvement

Some of the interventions were not included

 

Majority of the included

Prism adaptation demon- strated long term func- tional gain

studies are not of high quality

 

Visual scanning therapy has no significant impact on overall function

Riggs 2007 140

27 studies—11 RCTs, 3 non- RCTs, 13 case studies

Assess the effectiveness of visuoperceptual therapy, prism adaptation, eye patches, and visuomotor feedback

Improvement was ob- served with hemifield eye patching, prism adapta- tion, and visuomotor feedback, mainly by means of standardized neglect test like line bi- section tests and cancel- lation tests

Effectiveness of other ne- glect rehabilitative inter- ventions remains uncertain

 

Majority of the improve- ment not measured at the functional level

 

Lack of long-term follow- up

Geusgen 2007 50

7 studies—1 RCT, 3 single subject, 2 pre-test post-test, 1 case control

Evaluate the ‘‘transfer’’ of the effect of visual scanning strategies from trained tasks to daily tasks or daily living

Almost all confer positive impact on daily tasks or daily living but three of

seven were not statistically tested

Lack of long-term follow- up

Only visual scanning strategy was evaluated

Bowen 2007 20

12 studies—all RCTs

Assess overall effectiveness of cognitive rehabilitation for visual neglect on independence of activities of daily living

Only spatiomotor cue-

Many neglect rehabilita-

 

ing

83

confers statistically

tive interventions were not included as they are not RCTs

significant improvement on performance in standardized neglect assessment

Lincoln 2006 103

None showed statistical significance in functional performance

 

25 studies—12 RCTs of above and 13 CCTs

Assess overall effectiveness of various interventions relating to visual neglect

Rehabilitation observed slight immediate and persisting improvement on standardised neglect test

Effect on functioning was statistically insignificant, for either immediate or persisting effects

Many neglect rehabilita- tive measures were not included as they are nei- ther RCTs nor CCTs

(continued on next page )

128

Surv Ophthalmol 56 (2) March--April 2011

TING ET AL

 

Table 6 ( continued )

Reviews

Included Studies

Aims

Key Findings

Limitation of Evidence

Luaute 2006 106

54 studies -- RCTs, controlled trials, crossover, case- control, single-case, and case reports

Assess the effectiveness of various interventions relating to visual neglect

Improvement has been observed following VST, mental imagery and video feedback training

There is need for further high quality evidence to confirm the effect

Pizzamiglio

2006

136

Jutai 2003 82

12 studies— group studies and

single cases

32 studies, including RCTs, crossover, cohorts, and single group designs

Assess the effectiveness of visual scanning therapy with and without additional passive sensory stimulation

Investigate effectiveness of a variety of interventions relating to visual neglect

TR and NMV is partially effective when coupled with visual scanning therapy

Fresnel prism and passive sensory stimulation do not afford positive func- tional impact

VST serves as a useful neglect rehabilitative intervention

No beneficial effect gained with additional peripheral sensory stimulation

There is strong evidence that rehabilitation specif- ically targeting visual ne- glect and visual scanning improves functional performance

There is moderate evi- dence that Fresnel prisms and hemifield patching improve performance in standardized neglect tests

There is limited evidence in favor of TENS, limb activation, dopamine ag- onist therapy, caloric stimulation improving vi- sual neglect

Only assesses limited re- habilitative interventions

Lack of quality appraisal and meta-analysis

Majority of included studies are not of high quality

CCT 5 controlled clinical trial; NMV 5 neck muscle vibration; RCT 5 randomized controlled trial; TR 5 trunk rotation; VST 5 visual scanning therapy; TENS 5 transcutaneous electrical nerve stimulation.

VISUAL NEGLECT FOLLOWING STROKE

number and duration of therapeutic sessions in- stituted, and the difference in outcome measures applied. This study did not address the anatomical regions involved in their neglect patients. This is important because some studies have suggested that any potential beneficial effects of prism adaptation may be lesion site--specific. 151,155 The effectiveness of rehabilitation based on passive sensory stimulation, such as eye patches, Fresnel prism, trunk rotation, neck muscle vibra- tion, limb activation, vestibular stimulation, and optokinetic stimulation, remain inconclusive or unsatisfactory. 3,106 Although it seems logical that longer-term benefits may be achieved with restitutive rehabilitation, the

evidence is limited. Within the context of restitutive rehabilitation, Luaute et al 106 considermentalimagery and feedback training, as Grade B interventions, 135 largely because the evidence of benefit is only based on

a case study of two patients. 158 The efficacy of

pharmacological treatment (dopamine and norad- renergic agonists), transcranial magnetic stimula- tion 128 or direct current polarization, 99 virtual reality--based space remapping, 1 and music therapy must be deemedinconclusive. 158 There are conflicting

results from single case reports of the use of dopamine and norepinephrine agonists to improve general

attention.

Virtual reality--based space remapping

has shown to be of potential value, but has been restricted to patients who have normal inferior parietal/superior temporal lobes. 1 The systematic reviews of Bowen et al 20 and Lincoln et al 103 have concluded that none of the interventions lead to a positive impact on functional performance. They excluded the majority of the research trials because of unsatisfactory levels of evidence, highlighting the pressing need for high quality research.

3,10,72

D. SUMMARY AND RECOMMENDATION FOR REHABILITATION OF VISUAL NEGLECT

The overall efficacy of rehabilitation remains

uncertain. Based on the best available evidence, we feel that visual scanning therapy and prism adapta- tion warrant consideration. In our experience, education and training of family and close friends

to understand the nature of VN and how to assist VN

patients on a daily basis are equally important.

VIII. Prognosis

A few studies have observed spontaneous recovery in patients with mild to moderate visual neglect, especially during the acute phase, 41 and recovery has been seen up to 90 days post-stroke. 126

129

Unresolved visual neglect predicts poorer functional

and rehabilitation outcome in post-stroke pa- tients. 79,89,163,165 Longer-term follow-up is required,

there has been no systematic reported evaluation of outcome beyond 1 year.

as

79

IX. Conclusion

VN is a common, but frequently overlooked, condition. Greater awareness and understanding of this condition should improve the quality of life of post-stroke patients. Detection is by combination of pen-and-paper tests, behavioral assessment tools, clinical observation and history taking and, poten-

tially, virtual reality assessment. Although there is lack of robust evidence of the efficacy of VN rehabilitation, visual scanning therapy and prism adaptation warrant consideration. There is a press- ing need for well designed, high quality research, particularly randomized controlled trials, to demonstrate the clinical efficacy of current rehabil- itation strategies. Increasingly sophisticated neuro- imaging tools, including magnetic resonance scanning coupled with detailed clinical observation and neuro-ophthalmic examination, will improve understanding of the nature of VN, enabling

a deeper appreciation of how an individual with

VN recognizes, organizes, and orients ‘‘self’’ in

relation to the external environment.

X. Method of Literature Search

Multiple electronic databases (EMBASE, Cochrane library, and Medline) were searched, reference lists were hand-searched, and experts in the field were contacted to identify peer-reviewed literature con- cerning visual neglect. Key literature which addresses the functional impact, neuroanatomical causes, assessment, and treatment of visual neglect was identified. Certain keywords were used during the literature search, including visual neglect, unilateral neglect, visual inattention, and hemispatial neglect .

XI. Disclosure

The authors reported no proprietary or commer- cial interest in any product mentioned or concept discussed in this article. Alex Pollock is employed by the Nursing Midwifery and Allied Health Profes- sionals (NMAHP) Research Unit, which is funded by the Scottish Government’s Chief Scientist’s Office.

1.

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Reprint address: Dr Darren SJ Ting, MBChB, Victoria In- firmary, Langside Road, Glasgow G42 9TY, U.K.

134 Surv Ophthalmol 56 (2) March--April 2011

Outline

TING ET AL

I. Introduction

II.

Epidemiology

III.

Varieties of neglect

A. Modality (input/output)

B. Spatial representation

C. Range of space

IV.

Functional impact

V.

Pathophysiology

A. Physiology of visuospatial perception

B. Spatially lateralized dysfunction of visual neglect

C. Non-spatially lateralized dysfunction of vi- sual neglect

D. Role of non-visual afferent inputs

E. Clinico-anatomical correlations of visual neglect

F. Clinical syndromes associated with visual neglect

VI.

Assessment of visual neglect

A. Current clinical guidelines

B. How is visual neglect assessed?

1. Pencil-and-paper tests

2. Behavioral assessment tools

3. Clinical observation and history-taking from the patient and the near contacts

4. Recent development of assessment technique

C. Distinction between visual neglect and other visual problems

D. Summary and recommendations for the assessment of visual neglect

VII. Rehabilitation of visual neglect

A. Current clinical practice

B. Types of rehabilitation

1. Compensatory

2. Substitutive

3. Restitutive

C. Current evidence on the effectiveness of rehabilitation

D. Summary and recommendation for reha- bilitation of visual neglect

VIII. Prognosis

IX. Conclusion

X. Method of Literature Search

XI. Disclosure