NeuroRehabilitation An Interdisciplinary Journal
ELSEVIER
NeuroRehabilitation 5 (1995) 115-128
Unilateral spatial neglect: assessment and rehabilitation strategies Anjan Chatterjee Department of Neurology and the Alzheimer's Center, University of Alabama at Birmingham, 454 Sparks Center, 1720 7th Avenue South, Birmingham, Al 35294-0017, USA
accepted 16 December 1994
Abstract Unilateral spatial neglect is one of the most striking disorders of cognition. Focal brain lesions, more commonly on the right, produce profound deficits in the awareness of contralateral self and space. This article reviews the assessment and current theoretical explanations of neglect, in light of rehabilitation. The presence of neglect is a predictor of poor functional recovery. No treatment protocols have been demonstrated to unequivocally aid the rehabilitation of these patients. However, based on a growing understanding of underlying mechanisms in the neglect syndrome, several promising treatment strategies have emerged. Group studies designed to establish the efficacy of these therapeutic options are urgently needed. Keywords: Attention; Recovery; Stroke
1. Phenomenology Unilateral spatial neglect is one of the most striking disorders of cognition. Patients with this syndrome act as though whole regions of space contralateral to their lesions have vanished from existence. These patients do not orient toward, respond to, or act upon meaningful stimuli in contralateral space [1]. It is common for these patients to appear lethargic in the first few days after brain damage. Even when alert, they often
lie in bed with their head and eyes deviated ipsilaterally. They seem to be unaware of objects that lie in the contralateral side of their environment and may only eat food on the ipsilateral half of their plate. Despite being able to hear sound emanating from contralateral space, they may search ipsilaterally for its source. If able to ambulate, or if navigating a wheelchair, they may hit contralateral objects, or take circuitous routes to their destination by preferentially making ipsilateral turns. In the early stages, patients may also neglect parts of their own body, and deny owner-
1053-8135/95/$09.50 © 1995 Elsevier Science Ireland Ltd. All rights reserved. SSDI 1053-8135(94) 0110-T
116
A. Chatte7jee / NeuroReh~bilitation 5 (I995) 115-128
ship of their contralateral limb. When dressing they might not clothe the contralateral side of their body. They may fail to groom their contralateral side and not comb their hair or shave parts of their faces. Occasionally, the denial of the contralateral side of their body is accompanied by an intense dislike of this side [2]. Despite being functionally devastated and frequently having accompanying motor and sensory deficits, these patients appear unconcerned or peculiarly resigned to their condition. Neglect is more common and severe after right than left hemisphere damage [3-5]. For the sake of clarity, in this paper, neglect will refer to left-sided neglect. Analogous right-sided symptoms sometimes occur after left hemisphere damage. Neglect is frequently a consequence of stroke and brain tumors and occurs occasionally after head trauma. Lesions producing neglect may also result in other neurologic deficits such as visual field defects, contralateral somatosensory loss, or hemiplegia. However, primary sensory or motor abnormalities do not produce neglect. The associated neurological deficits occur because of the proximity of sensory and motor cortices to neural structures critical for spatial awareness. Since most patients with neglect have relatively intact language abilities, they may be able to carry out reasonable conversations about their life, current events and factual information. This generally preserved intellectual functioning presents a marked contrast to their sometimes bizarre behavior and poor insight into their own obvious disabilities. For example, Bisiach and Geminiani described a patient who thought that her left hand did not belong to her. She claimed that this hand had in fact been left in the ambulance by a previous patient. She was unable to explain why her rings appeared on this alien hand. A few days later, when asked to pick up a series of cubes laid out horizontally in front of her, she started at the right most cube until arriving at her mid sagittal plane. At that point she pushed the remainder of the cubes leftward even as she verbally claimed there were no more cubes [6]. The fact that a discrete brain lesion can produce such deep fissures within the very structure of our awareness
and beliefs poses a serious challenge to designing remediation strategies. 2. Assessment A number of bed side tasks have been developed to assess neglect. The more commonly used tasks will be briefly described below. These tasks help clarify the quality of the deficit and provide means to quantify neglect severity. 2.1. Line bisection tasks Line bisection tasks are simple to administer. Patients are presented with horizontal lines, traditionally presented centered at their mid sagittal plane. They are asked to place a mark at the mid point of the line. The task is generally administered without restricting head or eye movements and without time limitations. Patients with leftsided neglect place their mark to the right of the true mid position (Fig. 1) [7]. Patients make larger errors with longer lines [8,9]. If stimuli are placed in space contralateral to their lesion patients frequently make larger errors [10]. Thus, the most sensitive measure of left-sided neglect using line bisection tasks would be the use of long lines (generally greater than 20 cm) placed in left space. 2. 2. Cancellation tasks
In cancellation tasks, sheets with arrays of targets are placed before patients. Patients are asked to place a mark, or 'cancel' each of the targets. Similar to line bisections, cancellation tasks are generally administered without restricting head or eye movements and without time limitations. Patients with left-sided neglect cancel targets on the right side of arrays and neglect targets on the left (Fig. 2) [11]. Sometimes patients cancel the same right-sided targets repeatedly. Increasing the number of targets may uncover neglect not evi: dent on arrays with fewer targets [12]. Arrays may
Fig. 1. Line bisection performance by a 33 year-old woman, BT, with unilateral spatial neglect, who suffered an ischemic infarct in the distribution of the right middle cerebral artery.
A. Chatterjee / NeuroRehabilitation 5 (J 995) 115-128
V
S
L
•G
A II
A
G
II
S
II
B
~
A
A
A
II
II
C
L
A .'
_/
L
(i)
B
C
(.'
I
A
8
S
@
M
0
A C
(j
G
S
0 C
•
0
D
s
C
~/
8
L
L
@
B
B
II
s
C
Q)
~
0
~,
~
0
0
II
M
8
G
117
G
5
M
~/
Fig. 2. Cancellation performance by BT. She was asked to circle all the 'A's.
also be constructed with distractor stimuli interspersed among targets. The sensitivity of cancellation tasks may be increased by presenting arrays in which targets are difficult to discriminate from distractor stimuli [13]. 2.3. Drawing tasks
Neglect may be assessed by having patients copy drawings or draw from memory. In copying tasks various combinations of two general patterns may be observed [14]. When asked to copy stimulus arrays with multiple objects, or complex objects with multiple parts, patients may neglect left-sided objects in the array (Fig. 3) and/or neglect the left side of individual objects, regardless of where they appear in the array. Items commonly used in drawing from memory are clock drawings, or simple figures like a daisy. In clock drawings, when patients place numbers 1 to 6 on the right side of the clock face and nothing on the
left, they are clearly demonstrating neglect. However, when they place all 12 numbers on the right or inaccurately space left-sided numbers, the interpretation is less obvious. Such behavior may represent poor strategic planning rather than neglect per se. When patients with neglect draw simple objects like a daisy they may leave leftsided petals or leaves out of their drawings (Fig. 4), or depict left-sided features with less detail than right-sided features. 2. 4. Reading
When patients with left-sided neglect read text, they sometimes have trouble bringing their gaze to the left margin of the page. As a consequence they may read lines starting at points in the middle of the page resulting in sequences of words or sentences that do not make sense. When reading single words they may either omit leftsided letters or substitute them with confabulated
118
A. Chatterjee / NeuroRehabilitation 5 (J995) 115-128
Fig. 3. Copy of drawing by BT.
letters. Thus the word 'walnut' might be read as either 'nut' or as 'peanut'. This reading disorder is called neglect dyslexia [15]. 2.5. Double simultaneous stimulation. Many patients with neglect also demonstrate extinction to double simultaneous stimulation. Extinction refers to the unawareness of stimuli, which can be perceived in isolation, when competing stimuli are simultaneously presented [16,17]. In left sided neglect right-sided stimuli preferentially penetrate consciousness at the expense of awareness of left-sided stimuli of equivalent intensity. Extinction may occur in visual, auditory or tactile modalities. At the bedside, extinction may be tested by asking patients to count fingers presented to one or both hemifields, snapping fingers at one or both ears, and touching one or both hands. When presented with stimuli on both sides patients with neglect preferentially report
Fig. 4. Drawing of a flower by BT.
only the right-sided stimulus. Extinction cannot be adequately tested in the presence of a primary sensory disorder such as a visual field defect, unilateral hearing loss or lateralized somatosensory loss. However, manifestations of neglect may occasionally masquerade as a primary sensory loss [18-20]. 2.6. Comment Many patients with right brain damage demonstrate neglect on the above tasks. However, patients who manifest neglect on some but not other tasks used in the assessment are being
A. Chatterjee / NeuroRehabilitation5 (1995) 115-128
reported [21-24]. Such observations have led some investigators to question the notion that neglect refers to a single coherent neuropsychological entity [25]. Rather, 'neglect' may be more meaningfully viewed as referring to a family of symptoms, analogous to the sense in which 'aphasia' refers to a family of language disorders. For assessment purposes it is important to recognize that a patients may demonstrate neglect on some, but not other tasks. The Behavioral inattention test is a published neuropsychological test which incorporates some of the above bedside measures that can be used to quantify the severity of deficit in neglect, and be used to follow patients [26]. 3. Theory
The phenomenology of neglect is puzzling and profoundly disturbing. These patients behave in ways that offend our common sense intuitions of self and space. That a focal brain lesion can cause profound abnormalities of awareness, consciousness and beliefs has intrigued neurologists and neuropsychologists, and more recently cognitive psychologists, connectionist modelers and even philosophers. Contemporary explanations of the neglect syndrome focus on underlying attentional, intentional and representational mechanisms. Table 1 lists the major behavioral manifestations of attentional, intentional and representational deficits. Table 1 Behavioral manifestations as a result of disruption of underlying mechanisms in unilateral spatial neglect. (1) Attentional deficits.
(a) extinction to double simultaneous stimulation (b) ipsilateral orientation bias (c) limited attentional capacity (2) Intentional deficits. (a) akinesia (b) directional hypokinesia (c) motor extinction (d) motor impersistence (3) Representational deficits (a) anterograde contralateral memory deficits (b) retrograde contralateral memory deficits (c) contralateral confabulation
119
3.1. Attentional theories Patient with neglect demonstrate a number of attentional deficits. They tend to have a bias in orienting spatial attention ipsilaterally. They also seem to have a diminished attentional capacity and may have a breakdown of specific elementary attentional operations. A major issue in neglect is understanding why neglect is more common and more severe after right than after left brain damage [4]. Kinsbourne postulates that each hemisphere generates a vector of spatial attention directed towards contralateral space, and that this attentional vector is inhibited by the opposite hemisphere [27,28]. He further posits that the left hemisphere's vector of spatial attention is powerfully directed, in contrast to the right hemisphere which only produces a weak vector. As a consequence of this neural organization of spatially directed attention, after right hemisphere damage, the left hemisphere's unfettered vector of attention produces a powerful orientation bias to the right. Since the right hemisphere's intrinsic vector of attention is only weakly directed, after left hemisphere damage, there is not a powerful orientation bias to the left. Thus, right-sided neglect is less common and not as severe. Heilman and co-workers, in contrast to Kinsbourne, propose that the right hemisphere is dominant for arousal and spatial attention [29]. Patients with right brain damage have greater electroencephalographic slowing than those with left brain damage [30]. They also demonstrate diminished galvanic skin responses than normal controls or patients with left hemisphere damage [31]. They suggest that the right hemisphere is capable of directing attention into both hemispaces, while the left hemisphere directs attention only into contralateral space. Thus, after right brain damage, the left hemisphere is ill-equipped to direct attention into left hemi-space. However, after left brain damage, the right is capable of directing attention into both hemispaces and neglect does not occur with the same severity as after right brain damage. Positron emission tomographic studies confirm the notion that the right hemisphere is capable of attending to stimuli in both hemispaces [32]. The right hemisphere's
120
A. Chatterjee / NeuroRehabilitation 5 (J 995) 115-128
dominance for arousal may also account for the diminished attentional capacity seen after right brain damage. Although neglect is characteristically seen after right parietal damage [33], it may also occur after lesions to the dorsolateral frontal cortex [34,35], cingulate cortex, [36] thalamus, [37] putamen [38] and the mid brain [39]. Such clinical observations led Heilman and co-workers to propose that an anatomically distributed network mediates spatially directed attention [34,37]. Mesulam has also proposed a similar model, emphasizing that different regions within this large scale network implement different aspects of an individual's interaction with his/her spatial environment [40,41]. For example, the parietal lobes are postulated to be involved in sensory attentional aspects of neglect, the frontal lobes in motor exploratory behaviors and the cingulate cortex in motivational aspects of spatially-directed behavior. Posner and colleagues have also emphasized the role of neural networks in spatial attention [42]. They propose that spatially-directed attention can be decomposed into elementary operations, such as 'engage', 'disengage' and 'shift'. Posner and Rafal reported that patients with right parietal damage are selectively impaired at disengaging attention from right-sided stimuli in order to shift and engage left sided stimuli [43]. This 'disengage deficit' underlies some aspects of the neglect syndrome, most likely the phenomenon of extinction to double simultaneous stimulation. 3.2. Intentional theories
Heilman, Watson and colleagues also advanced the idea that premotor, or intentional aspects of behavior contribute to the deficit observed in the neglect syndrome [44]. They have argued that patients with neglect may have a disinclination to . initiate movements, or move towards or in contralateral hemispace [10]. Intentional disorders may present in a variety of ways, such as akinesia, hypokinesia, motor extinction and motor impersistence [45]. In most situations, attention and intention are inextricably linked, since attention is usually directed to objects on which one acts. It .is not always easy to dissect intentional from
attentional contributions to the neglect syndrome. Coslett and co-workers had patients perform line bisections in right and left hemispace. However, their visual feedback for the task was restricted to a video monitor which could be placed in either right or left hemispace. Thus, by dissociating the locus of attention (location of the monitor) from the locus of intention (location of their movements), they were able to demonstrate that some patients' errors were primarily influenced by the intentional rather than attentional demands of the task [46]. Bisiach and co-workers, using a set of pulleys, were able to dissociate the direction in which attention and intention were moved in a line bisection task, and also confirmed the intentional influences on the deficits in some patients [47]. Tegner and Levander, using mirrors set at right angles to each other, were also able to dissociate attentional from intentional variables in cancellation tasks [48]. Patients viewed targets directly or through mirrors. In the mirror condition, targets that were seen on the right (reflection in the mirror) actually lay on the left, and vice versa. They demonstrated that some patients had attentional neglect, others intentional neglect, and others a combination of both. Intentional neglect tends to be associated with frontal lesions. However, there are exceptions to this trend, such as the recent report of a patient with relatively pure intentional neglect produced by a lesion confined to the parietal lobe [49]. Heilman and colleagues have suggested that frontal sub-cortical circuits mediate intention. One loop involves projections from the supplementary motor area to the putamen to the globus pallidus/substantia nigra to the ventralis anterior and ventralis lateralis thalamic nuclei back to the supplementary motor area. The other loop involves projections from the prefrontal cortex to the caudate to the globus pallidus/substantia nigra to the medial thalamic nuclei, back to the prefrontal cortex [45]. Mesulam has similarly emphasized the role of frontal-sub cortical circuits in mediating contralateral motor exploratory behavior [41], and Posner has also proposed an 'anterior attentional circuit' responsible for the preparation for actions [42] .
A. Chatterjee / NeuroRehabilitation 5 (1995) 115-128
3.3. Representational theories Bisiach and co-workers have emphasized that since neglect can be demonstrated in the absence of external stimuli or movements, and suggest that neglect occurs primarily at a representational level [50,51]. He proposes that these patients' inabilities to form contralateral mental representations of space underlie their observable behavioral deficits. Denny-Brown had previously described a patient who, after discharge from the hospital, only recalled patients to her right and when asked to describe the corridor from the ward, only reported right-sided structures [17]. The importance of this casual observation was not underscored and it remained buried in the literature. A quarter of a century later, Bisiach and Luzzatti made similar observations in two patients asked to imagine the Piazza del Duomo in Milan, Italy from two perspectives: looking into the square towards the cathedral, and from the cathedral door looking into the square away from the cathedral [52]. The patients only reported structures to the right of their imaginal space, resulting in the reporting of different structures, in both conditions. Similar findings have been replicated [50,53] and even extend to the imaginal descriptions of routes that would be used by patients going from one point to another [54]. By preferentially reporting right tunis, patients may describe circuitous and bizarre routes to locations that could be reached more directly if left turns were used. Patients with neglect may also have difficulties forming contralateral representations in an anterograde manner. Bisiach and co-workers had neglect patients view pairs of abstract cloudlike shapes as they were moved through a narrow slit centered at the mid sagittal plane. They were asked to decide if the two shapes were similar or different. In order to do the task patients had to imagine the form of the shape since they never saw entire shapes at one time. Patients with neglect were inaccurate when these judgments relied on distinguishing features only on the left side of these shapes [55]. In addition to having difficulties forming contralateral representations, patients may also form misrepresentations. These
121
misrepresentations may result in confabulations of contralateral stimuli [56]. Representational theories of neglect are generally presented in opposition to attentional and intentional theories. This distinction may not be warranted. Farah points out that attention is not allocated to stimuli, but, rather to representations [57]. In vision, elementary features such as edges, orientation and color are processed pre-attentively at different locations within the visual cortex [58]. Representations are formed by the binding of these elementary features into percepts. This means that attention is allocated to nascent topographic representations, derived from stimuli in space rather than the stimuli themselves. Bisiach, in recent writings has suggested that attentional processes are linked to the intrinsic dynamic activity of circuits dedicated to spatial representations [51]. Attentional (and intentional) and representational accounts of neglect may be explanations aimed at different levels of analysis.
3.4. Some recent theoretical issues Neglect is usually described along the horizontal (left/right) axis. Recent reports have expanded the concept of spatial neglect to multiple coordinate systems. Our spatial environment also encompass altitudinal (up-down) and radial (nearfar) coordinates. Patients have been described that have neglect of either upper or lower space, and of either near or far space [59-61]. One patient has also been reported who had left neglect in near space, but not in far space [22]. Objects in space are also represented by different reference frames [62]. These frames are generally divided into viewer centered, object centered and environment centered coordinate systems. For example, imagine a chair in an office. An individual views the chair relative to his/her own location. This viewer centered reference frame locates the chair with respect to the viewer: left/right, near/far and above/below. Viewer-centered coordinates change with movement of either the viewer or the object. Environment-centered reference frames refer to an objects relationship to the environment, such as the chair's location with reference to its surrounding
122
A. Chatterjee / NeuroRehabilitation 5 (1995) 115-128
topography: where in the room, relationship to other fixed objects, or relationship to geographic coordinates. These coordinates are unaffected by changes in the viewer's location, but are altered by changes in the chair's location. Object centered coordinates refer to the intrinsic spatial coordinates of the object itself, such as the chair's top-bottom, left-right and front-back. Object centered reference frames remain stable irrespective of movements of the viewer or object. Changing positions of the viewer or the chair within the office does not alters the chair's object centered coordinates. Our ability to construct this coordinate system allows us to recognize familiar objects viewed from unfamiliar vantage points. Several recent reports suggest that neglect may occur in any of these reference frames [14,63-68]. Recent reports reveal interesting quantitative relationships between the amount of stimuli presented to patients with neglect and the extent of their awareness. For over a century it has been known that the subjective experience of sensations is mathematically related to objective measures of sensory magnitude [69]. In other words, the way in which normal individuals experience the sensory environment is lawful and orderly and can be described by psychophysical laws. These psychophysical laws constrain the nervous system's organization of its sensory environment. Stevens and colleagues have shown that for any sensory modality a power function (1jJ = K
ELSEVIER
NeuroRehabilitation 5 (1995) 115-128
Unilateral spatial neglect: assessment and rehabilitation strategies Anjan Chatterjee Department of Neurology and the Alzheimer's Center, University of Alabama at Birmingham, 454 Sparks Center, 1720 7th Avenue South, Birmingham, Al 35294-0017, USA
accepted 16 December 1994
Abstract Unilateral spatial neglect is one of the most striking disorders of cognition. Focal brain lesions, more commonly on the right, produce profound deficits in the awareness of contralateral self and space. This article reviews the assessment and current theoretical explanations of neglect, in light of rehabilitation. The presence of neglect is a predictor of poor functional recovery. No treatment protocols have been demonstrated to unequivocally aid the rehabilitation of these patients. However, based on a growing understanding of underlying mechanisms in the neglect syndrome, several promising treatment strategies have emerged. Group studies designed to establish the efficacy of these therapeutic options are urgently needed. Keywords: Attention; Recovery; Stroke
1. Phenomenology Unilateral spatial neglect is one of the most striking disorders of cognition. Patients with this syndrome act as though whole regions of space contralateral to their lesions have vanished from existence. These patients do not orient toward, respond to, or act upon meaningful stimuli in contralateral space [1]. It is common for these patients to appear lethargic in the first few days after brain damage. Even when alert, they often
lie in bed with their head and eyes deviated ipsilaterally. They seem to be unaware of objects that lie in the contralateral side of their environment and may only eat food on the ipsilateral half of their plate. Despite being able to hear sound emanating from contralateral space, they may search ipsilaterally for its source. If able to ambulate, or if navigating a wheelchair, they may hit contralateral objects, or take circuitous routes to their destination by preferentially making ipsilateral turns. In the early stages, patients may also neglect parts of their own body, and deny owner-
1053-8135/95/$09.50 © 1995 Elsevier Science Ireland Ltd. All rights reserved. SSDI 1053-8135(94) 0110-T
116
A. Chatte7jee / NeuroReh~bilitation 5 (I995) 115-128
ship of their contralateral limb. When dressing they might not clothe the contralateral side of their body. They may fail to groom their contralateral side and not comb their hair or shave parts of their faces. Occasionally, the denial of the contralateral side of their body is accompanied by an intense dislike of this side [2]. Despite being functionally devastated and frequently having accompanying motor and sensory deficits, these patients appear unconcerned or peculiarly resigned to their condition. Neglect is more common and severe after right than left hemisphere damage [3-5]. For the sake of clarity, in this paper, neglect will refer to left-sided neglect. Analogous right-sided symptoms sometimes occur after left hemisphere damage. Neglect is frequently a consequence of stroke and brain tumors and occurs occasionally after head trauma. Lesions producing neglect may also result in other neurologic deficits such as visual field defects, contralateral somatosensory loss, or hemiplegia. However, primary sensory or motor abnormalities do not produce neglect. The associated neurological deficits occur because of the proximity of sensory and motor cortices to neural structures critical for spatial awareness. Since most patients with neglect have relatively intact language abilities, they may be able to carry out reasonable conversations about their life, current events and factual information. This generally preserved intellectual functioning presents a marked contrast to their sometimes bizarre behavior and poor insight into their own obvious disabilities. For example, Bisiach and Geminiani described a patient who thought that her left hand did not belong to her. She claimed that this hand had in fact been left in the ambulance by a previous patient. She was unable to explain why her rings appeared on this alien hand. A few days later, when asked to pick up a series of cubes laid out horizontally in front of her, she started at the right most cube until arriving at her mid sagittal plane. At that point she pushed the remainder of the cubes leftward even as she verbally claimed there were no more cubes [6]. The fact that a discrete brain lesion can produce such deep fissures within the very structure of our awareness
and beliefs poses a serious challenge to designing remediation strategies. 2. Assessment A number of bed side tasks have been developed to assess neglect. The more commonly used tasks will be briefly described below. These tasks help clarify the quality of the deficit and provide means to quantify neglect severity. 2.1. Line bisection tasks Line bisection tasks are simple to administer. Patients are presented with horizontal lines, traditionally presented centered at their mid sagittal plane. They are asked to place a mark at the mid point of the line. The task is generally administered without restricting head or eye movements and without time limitations. Patients with leftsided neglect place their mark to the right of the true mid position (Fig. 1) [7]. Patients make larger errors with longer lines [8,9]. If stimuli are placed in space contralateral to their lesion patients frequently make larger errors [10]. Thus, the most sensitive measure of left-sided neglect using line bisection tasks would be the use of long lines (generally greater than 20 cm) placed in left space. 2. 2. Cancellation tasks
In cancellation tasks, sheets with arrays of targets are placed before patients. Patients are asked to place a mark, or 'cancel' each of the targets. Similar to line bisections, cancellation tasks are generally administered without restricting head or eye movements and without time limitations. Patients with left-sided neglect cancel targets on the right side of arrays and neglect targets on the left (Fig. 2) [11]. Sometimes patients cancel the same right-sided targets repeatedly. Increasing the number of targets may uncover neglect not evi: dent on arrays with fewer targets [12]. Arrays may
Fig. 1. Line bisection performance by a 33 year-old woman, BT, with unilateral spatial neglect, who suffered an ischemic infarct in the distribution of the right middle cerebral artery.
A. Chatterjee / NeuroRehabilitation 5 (J 995) 115-128
V
S
L
•G
A II
A
G
II
S
II
B
~
A
A
A
II
II
C
L
A .'
_/
L
(i)
B
C
(.'
I
A
8
S
@
M
0
A C
(j
G
S
0 C
•
0
D
s
C
~/
8
L
L
@
B
B
II
s
C
Q)
~
0
~,
~
0
0
II
M
8
G
117
G
5
M
~/
Fig. 2. Cancellation performance by BT. She was asked to circle all the 'A's.
also be constructed with distractor stimuli interspersed among targets. The sensitivity of cancellation tasks may be increased by presenting arrays in which targets are difficult to discriminate from distractor stimuli [13]. 2.3. Drawing tasks
Neglect may be assessed by having patients copy drawings or draw from memory. In copying tasks various combinations of two general patterns may be observed [14]. When asked to copy stimulus arrays with multiple objects, or complex objects with multiple parts, patients may neglect left-sided objects in the array (Fig. 3) and/or neglect the left side of individual objects, regardless of where they appear in the array. Items commonly used in drawing from memory are clock drawings, or simple figures like a daisy. In clock drawings, when patients place numbers 1 to 6 on the right side of the clock face and nothing on the
left, they are clearly demonstrating neglect. However, when they place all 12 numbers on the right or inaccurately space left-sided numbers, the interpretation is less obvious. Such behavior may represent poor strategic planning rather than neglect per se. When patients with neglect draw simple objects like a daisy they may leave leftsided petals or leaves out of their drawings (Fig. 4), or depict left-sided features with less detail than right-sided features. 2. 4. Reading
When patients with left-sided neglect read text, they sometimes have trouble bringing their gaze to the left margin of the page. As a consequence they may read lines starting at points in the middle of the page resulting in sequences of words or sentences that do not make sense. When reading single words they may either omit leftsided letters or substitute them with confabulated
118
A. Chatterjee / NeuroRehabilitation 5 (J995) 115-128
Fig. 3. Copy of drawing by BT.
letters. Thus the word 'walnut' might be read as either 'nut' or as 'peanut'. This reading disorder is called neglect dyslexia [15]. 2.5. Double simultaneous stimulation. Many patients with neglect also demonstrate extinction to double simultaneous stimulation. Extinction refers to the unawareness of stimuli, which can be perceived in isolation, when competing stimuli are simultaneously presented [16,17]. In left sided neglect right-sided stimuli preferentially penetrate consciousness at the expense of awareness of left-sided stimuli of equivalent intensity. Extinction may occur in visual, auditory or tactile modalities. At the bedside, extinction may be tested by asking patients to count fingers presented to one or both hemifields, snapping fingers at one or both ears, and touching one or both hands. When presented with stimuli on both sides patients with neglect preferentially report
Fig. 4. Drawing of a flower by BT.
only the right-sided stimulus. Extinction cannot be adequately tested in the presence of a primary sensory disorder such as a visual field defect, unilateral hearing loss or lateralized somatosensory loss. However, manifestations of neglect may occasionally masquerade as a primary sensory loss [18-20]. 2.6. Comment Many patients with right brain damage demonstrate neglect on the above tasks. However, patients who manifest neglect on some but not other tasks used in the assessment are being
A. Chatterjee / NeuroRehabilitation5 (1995) 115-128
reported [21-24]. Such observations have led some investigators to question the notion that neglect refers to a single coherent neuropsychological entity [25]. Rather, 'neglect' may be more meaningfully viewed as referring to a family of symptoms, analogous to the sense in which 'aphasia' refers to a family of language disorders. For assessment purposes it is important to recognize that a patients may demonstrate neglect on some, but not other tasks. The Behavioral inattention test is a published neuropsychological test which incorporates some of the above bedside measures that can be used to quantify the severity of deficit in neglect, and be used to follow patients [26]. 3. Theory
The phenomenology of neglect is puzzling and profoundly disturbing. These patients behave in ways that offend our common sense intuitions of self and space. That a focal brain lesion can cause profound abnormalities of awareness, consciousness and beliefs has intrigued neurologists and neuropsychologists, and more recently cognitive psychologists, connectionist modelers and even philosophers. Contemporary explanations of the neglect syndrome focus on underlying attentional, intentional and representational mechanisms. Table 1 lists the major behavioral manifestations of attentional, intentional and representational deficits. Table 1 Behavioral manifestations as a result of disruption of underlying mechanisms in unilateral spatial neglect. (1) Attentional deficits.
(a) extinction to double simultaneous stimulation (b) ipsilateral orientation bias (c) limited attentional capacity (2) Intentional deficits. (a) akinesia (b) directional hypokinesia (c) motor extinction (d) motor impersistence (3) Representational deficits (a) anterograde contralateral memory deficits (b) retrograde contralateral memory deficits (c) contralateral confabulation
119
3.1. Attentional theories Patient with neglect demonstrate a number of attentional deficits. They tend to have a bias in orienting spatial attention ipsilaterally. They also seem to have a diminished attentional capacity and may have a breakdown of specific elementary attentional operations. A major issue in neglect is understanding why neglect is more common and more severe after right than after left brain damage [4]. Kinsbourne postulates that each hemisphere generates a vector of spatial attention directed towards contralateral space, and that this attentional vector is inhibited by the opposite hemisphere [27,28]. He further posits that the left hemisphere's vector of spatial attention is powerfully directed, in contrast to the right hemisphere which only produces a weak vector. As a consequence of this neural organization of spatially directed attention, after right hemisphere damage, the left hemisphere's unfettered vector of attention produces a powerful orientation bias to the right. Since the right hemisphere's intrinsic vector of attention is only weakly directed, after left hemisphere damage, there is not a powerful orientation bias to the left. Thus, right-sided neglect is less common and not as severe. Heilman and co-workers, in contrast to Kinsbourne, propose that the right hemisphere is dominant for arousal and spatial attention [29]. Patients with right brain damage have greater electroencephalographic slowing than those with left brain damage [30]. They also demonstrate diminished galvanic skin responses than normal controls or patients with left hemisphere damage [31]. They suggest that the right hemisphere is capable of directing attention into both hemispaces, while the left hemisphere directs attention only into contralateral space. Thus, after right brain damage, the left hemisphere is ill-equipped to direct attention into left hemi-space. However, after left brain damage, the right is capable of directing attention into both hemispaces and neglect does not occur with the same severity as after right brain damage. Positron emission tomographic studies confirm the notion that the right hemisphere is capable of attending to stimuli in both hemispaces [32]. The right hemisphere's
120
A. Chatterjee / NeuroRehabilitation 5 (J 995) 115-128
dominance for arousal may also account for the diminished attentional capacity seen after right brain damage. Although neglect is characteristically seen after right parietal damage [33], it may also occur after lesions to the dorsolateral frontal cortex [34,35], cingulate cortex, [36] thalamus, [37] putamen [38] and the mid brain [39]. Such clinical observations led Heilman and co-workers to propose that an anatomically distributed network mediates spatially directed attention [34,37]. Mesulam has also proposed a similar model, emphasizing that different regions within this large scale network implement different aspects of an individual's interaction with his/her spatial environment [40,41]. For example, the parietal lobes are postulated to be involved in sensory attentional aspects of neglect, the frontal lobes in motor exploratory behaviors and the cingulate cortex in motivational aspects of spatially-directed behavior. Posner and colleagues have also emphasized the role of neural networks in spatial attention [42]. They propose that spatially-directed attention can be decomposed into elementary operations, such as 'engage', 'disengage' and 'shift'. Posner and Rafal reported that patients with right parietal damage are selectively impaired at disengaging attention from right-sided stimuli in order to shift and engage left sided stimuli [43]. This 'disengage deficit' underlies some aspects of the neglect syndrome, most likely the phenomenon of extinction to double simultaneous stimulation. 3.2. Intentional theories
Heilman, Watson and colleagues also advanced the idea that premotor, or intentional aspects of behavior contribute to the deficit observed in the neglect syndrome [44]. They have argued that patients with neglect may have a disinclination to . initiate movements, or move towards or in contralateral hemispace [10]. Intentional disorders may present in a variety of ways, such as akinesia, hypokinesia, motor extinction and motor impersistence [45]. In most situations, attention and intention are inextricably linked, since attention is usually directed to objects on which one acts. It .is not always easy to dissect intentional from
attentional contributions to the neglect syndrome. Coslett and co-workers had patients perform line bisections in right and left hemispace. However, their visual feedback for the task was restricted to a video monitor which could be placed in either right or left hemispace. Thus, by dissociating the locus of attention (location of the monitor) from the locus of intention (location of their movements), they were able to demonstrate that some patients' errors were primarily influenced by the intentional rather than attentional demands of the task [46]. Bisiach and co-workers, using a set of pulleys, were able to dissociate the direction in which attention and intention were moved in a line bisection task, and also confirmed the intentional influences on the deficits in some patients [47]. Tegner and Levander, using mirrors set at right angles to each other, were also able to dissociate attentional from intentional variables in cancellation tasks [48]. Patients viewed targets directly or through mirrors. In the mirror condition, targets that were seen on the right (reflection in the mirror) actually lay on the left, and vice versa. They demonstrated that some patients had attentional neglect, others intentional neglect, and others a combination of both. Intentional neglect tends to be associated with frontal lesions. However, there are exceptions to this trend, such as the recent report of a patient with relatively pure intentional neglect produced by a lesion confined to the parietal lobe [49]. Heilman and colleagues have suggested that frontal sub-cortical circuits mediate intention. One loop involves projections from the supplementary motor area to the putamen to the globus pallidus/substantia nigra to the ventralis anterior and ventralis lateralis thalamic nuclei back to the supplementary motor area. The other loop involves projections from the prefrontal cortex to the caudate to the globus pallidus/substantia nigra to the medial thalamic nuclei, back to the prefrontal cortex [45]. Mesulam has similarly emphasized the role of frontal-sub cortical circuits in mediating contralateral motor exploratory behavior [41], and Posner has also proposed an 'anterior attentional circuit' responsible for the preparation for actions [42] .
A. Chatterjee / NeuroRehabilitation 5 (1995) 115-128
3.3. Representational theories Bisiach and co-workers have emphasized that since neglect can be demonstrated in the absence of external stimuli or movements, and suggest that neglect occurs primarily at a representational level [50,51]. He proposes that these patients' inabilities to form contralateral mental representations of space underlie their observable behavioral deficits. Denny-Brown had previously described a patient who, after discharge from the hospital, only recalled patients to her right and when asked to describe the corridor from the ward, only reported right-sided structures [17]. The importance of this casual observation was not underscored and it remained buried in the literature. A quarter of a century later, Bisiach and Luzzatti made similar observations in two patients asked to imagine the Piazza del Duomo in Milan, Italy from two perspectives: looking into the square towards the cathedral, and from the cathedral door looking into the square away from the cathedral [52]. The patients only reported structures to the right of their imaginal space, resulting in the reporting of different structures, in both conditions. Similar findings have been replicated [50,53] and even extend to the imaginal descriptions of routes that would be used by patients going from one point to another [54]. By preferentially reporting right tunis, patients may describe circuitous and bizarre routes to locations that could be reached more directly if left turns were used. Patients with neglect may also have difficulties forming contralateral representations in an anterograde manner. Bisiach and co-workers had neglect patients view pairs of abstract cloudlike shapes as they were moved through a narrow slit centered at the mid sagittal plane. They were asked to decide if the two shapes were similar or different. In order to do the task patients had to imagine the form of the shape since they never saw entire shapes at one time. Patients with neglect were inaccurate when these judgments relied on distinguishing features only on the left side of these shapes [55]. In addition to having difficulties forming contralateral representations, patients may also form misrepresentations. These
121
misrepresentations may result in confabulations of contralateral stimuli [56]. Representational theories of neglect are generally presented in opposition to attentional and intentional theories. This distinction may not be warranted. Farah points out that attention is not allocated to stimuli, but, rather to representations [57]. In vision, elementary features such as edges, orientation and color are processed pre-attentively at different locations within the visual cortex [58]. Representations are formed by the binding of these elementary features into percepts. This means that attention is allocated to nascent topographic representations, derived from stimuli in space rather than the stimuli themselves. Bisiach, in recent writings has suggested that attentional processes are linked to the intrinsic dynamic activity of circuits dedicated to spatial representations [51]. Attentional (and intentional) and representational accounts of neglect may be explanations aimed at different levels of analysis.
3.4. Some recent theoretical issues Neglect is usually described along the horizontal (left/right) axis. Recent reports have expanded the concept of spatial neglect to multiple coordinate systems. Our spatial environment also encompass altitudinal (up-down) and radial (nearfar) coordinates. Patients have been described that have neglect of either upper or lower space, and of either near or far space [59-61]. One patient has also been reported who had left neglect in near space, but not in far space [22]. Objects in space are also represented by different reference frames [62]. These frames are generally divided into viewer centered, object centered and environment centered coordinate systems. For example, imagine a chair in an office. An individual views the chair relative to his/her own location. This viewer centered reference frame locates the chair with respect to the viewer: left/right, near/far and above/below. Viewer-centered coordinates change with movement of either the viewer or the object. Environment-centered reference frames refer to an objects relationship to the environment, such as the chair's location with reference to its surrounding
122
A. Chatterjee / NeuroRehabilitation 5 (1995) 115-128
topography: where in the room, relationship to other fixed objects, or relationship to geographic coordinates. These coordinates are unaffected by changes in the viewer's location, but are altered by changes in the chair's location. Object centered coordinates refer to the intrinsic spatial coordinates of the object itself, such as the chair's top-bottom, left-right and front-back. Object centered reference frames remain stable irrespective of movements of the viewer or object. Changing positions of the viewer or the chair within the office does not alters the chair's object centered coordinates. Our ability to construct this coordinate system allows us to recognize familiar objects viewed from unfamiliar vantage points. Several recent reports suggest that neglect may occur in any of these reference frames [14,63-68]. Recent reports reveal interesting quantitative relationships between the amount of stimuli presented to patients with neglect and the extent of their awareness. For over a century it has been known that the subjective experience of sensations is mathematically related to objective measures of sensory magnitude [69]. In other words, the way in which normal individuals experience the sensory environment is lawful and orderly and can be described by psychophysical laws. These psychophysical laws constrain the nervous system's organization of its sensory environment. Stevens and colleagues have shown that for any sensory modality a power function (1jJ = K
