Prospects for the Rehabilitation of Unilateral Neglect
Medical Research Council Applied Psychology Unit, Cambridge, UK
Rivermead Rehabilitation Centre, Oxford, UK
Neuropsychology Unit, Radcliffe Infirmary, Oxford, UK
Why Consider Rehabilitation?
For two main reasons, few previous books on neglect have tackled the issue of rehabilitation. The first is that many experimentalists have not regarded rehabilitation questions as theoretically interesting or informative about the fundamental phenomenon; the second is that clinicians often tend to assume that the phenomenon is transient and of little therapeutic relevance. We argue that both of these views are wrong and that the issue of rehabilitation should have a central place in both theoretical and clinical thinking in this area.
That the rehabilitation of neglect can yield theoretically interesting results is shown by Robertson, North and Geggie (1992), who found that limb activation procedures designed to cue visual scanning to the neglected side appear to have therapeutic effects even when the instruction to scan to the neglected side was omitted. This led on to experimental studies (Robertson & North, 1992) demonstrating that visual scanning was irrelevant to the improvements in performance observed during rehabilitation; the crucial element of rehabilitation appeared to be the presence of voluntary movements by one of the affected limbs in the neglected hemispace (these studies will be described in greater detail below).
That unilateral neglect is of practical clinical importance is demonstrated by a number of studies. At least five have found the presence of neglect to predict poor recovery in everyday life functioning (Denes, Semenza, Stoppa, & Lis, 1982; Fullerton, McSherry, & Stout, 1986; Henley, Pettit, Todd-Pokropek, & Tupper, 1985; Kinsella & Ford, 1980; Wade, Skilbeck, & Langton Hewer, 1983). Indeed, Denes et al. found that the presence of neglect a mean of 53 days post-stroke was the only significant predictor of activities of daily living (ADL) functioning: Severity of lesion, dysphasia and intellectual capacity all failed to show a significant relationship with ADL.
The Role of Theories of Neglect in Determining the Nature of Rehabilitation
Most attempts at rehabilitation of neglect have hitherto relied on relatively atheoretical attempts to induce patients to scan the neglected hemifield. These studies are based largely on explicit or implicit principles of behaviour therapy. One or two examples of theoretically driven attempts at rehabilitation will be considered later, but the question remains as to whether theory has anything to offer the rehabilitationist.
The most obvious potential contribution relates to fractionation of neglect phenomena, and the chapters in this volume amply demonstrate the complexities and subtypes of neglect which exist. If ways can be developed to reliably assess these subtypes, then it is possible that advances may be made in rehabilitation through tailoring specific treatments to specific subtypes of the disorder (Halligan & Marshall, 1991). Furthermore, it may be the case that some types of neglect are less fundamentally remediable than others, depending, for instance, on the level of representation in the visual system which is hypothesised to be impaired (see, for instance, Caramazza & Hillis, 1990).
The question of non-lateralised attentional loss (see Chapter 8, this volume) is also relevant to clinical issues. If it is the case that neglect patients are particularly limited in their dual-tasking capacity, then requiring them to scan left at the same time as they try to learn new motor and other skills may result in a situation of continual information overload; this in turn may help explain the fact that neglect predicts poor recovery in everyday life functions.
Effectiveness of Rehabilitation 1
One of the earliest studies of attempts to remediate visual neglect was by Lawson (1962). He treated two cases of neglect by frequently reminding the patients to “look to the left”, and also to use their fingers to guide their vision while reading. They were also encouraged to find the centre of a book or food-tray by using touch and then to use their finger position as a reference point from which to explore systematically the page or tray. It is important to note that Lawson reported that generalisation to untrained tasks was poor.
The New York Studies
Weinberg et al. (1977) carried out a controlled study which involved 20 h of training with 25 right CVA patients suffering from left hemi-inattention, defined by a range of cancellation, reading and other tests. The performance of these patients was compared with that of a randomly selected group of 32 patients satisfying similar criteria. The mean time post-stroke was 10 weeks, though the range was considerable. The control subjects received the same normal occupational therapy programme as the experimental subjects, and no attempt was made to control for the non-specific effects of being in a novel treatment programme.
The experimental treatment consisted of a number of tasks designed to “compensate for faulty scanning habits” (ibid., p. 481). These included, among others, the use of a “scanning machine”, reading and cancellation tasks in which the subjects were provided with a thick red vertical line down the left side of the page, and which they were taught to use as an “anchor” by always bringing it into vision before beginning the task in hand. Performance on a wide range of reading, cancellation and other tests showed significant benefit to the treated group relative to the controls, particularly for the group showing severe neglect.
In a partial replication of this study using identical selection criteria, Weinberg et al. (1979) carried out a further randomised trial, in this case with the control group being given an extra hour of occupational therapy each day to match the extra treatment time given to the treatment group. The procedures were similar to the previous study, with the addition of two extra training tasks relating to tactile-location training and length estimation training. The treated group did better than the controls on a number of neuropsychological tests, and again this was particularly prominent among the severe group.
A further partial replication of this type of training procedure was carried out by Young, Collins and Hren (1983), whose results suggested a significant treatment effect. Gordon et al. (1985) attempted a further replication of the training procedures developed by Weinberg et al., though this time not using a randomised design. Instead, one institution supplied the control group for one period, and another institution supplied the experimental group. The two institutions then alternated between control and treatment conditions on an unspecified number of occasions. The experimental (n = 48) and control (n = 29) subjects were well matched on all neurological and neuropsychological measures. A total of 35 h of training showed the experimental group performing significantly better than the control group on cancellation, arithmetic, reading comprehension, line bisection and on a search task. By four months, however, there were only two significant differences between the two groups, namely the control group showed significantly less lateral bias on Raven’s Coloured Progressive Matrices, and the treatment group reported significantly less anxiety and hostility.
Poor Generalisation in Attempted Replications of the New York Studies
In yet another attempt at a replication of Weinberg and co-workers’ methods, Webster et al. (1984) used a multiple-baseline by subject single case design with three males showing left neglect. That is, treatment onset was staggered for the three subjects, in order to determine whether improvements in neglect corresponded with the onset of treatment. The outcome measure was performance in navigating an “obstacle course” in wheelchairs, based upon the number of collisions with markers on the course. The training relied on the scanning machine used by Weinberg et al., and lateral scanning was trained while moving in the wheelchair. Significant improvements in wheelchair navigation appeared in each case, though only for frontal collisions with the obstacles, and not with collisions with the rear of the wheelchair.
In replicating this study, Gouvier et al. (1984) reported similar results, though improvement on wheelchair and scanning board performance did not generalise to letter cancellation performance. Another study by this group (Gouvier, Bua, Blanton, & Urey, 1987) supported the view that the effects of training were much more consistently observed in tasks similar to the training procedure. For instance, training using a “light board” (detecting lights on a 2-m wide board) produced improvements on this measure, but not on cancellation, while training in cancellation resulted in improvements in cancellation tests but not on light board performance.
Failure of Computerised Versions of the New York Methods
Robertson Gray, Pentland and Waite (1990) carried out a randomised controlled trial of computerised training with 36 patients suffering from unilateral neglect. One group of 20 subjects received a mean of 15.5 ± 1.8 h of computerised scanning and attentional training, which drew on many of the methods of the New York group (e.g. perceptual anchoring); a second group of 16 subjects received a mean of 11.4 ± 5.2 h of recreational computing selected in order to minimise scanning and timed attentional tasks.
The training consisted of computerised procedures such as matching to sample tasks, where the computer would not accept a response before the subject pressed an “anchor bar” on the left of the touch-sensitive screen. Blind follow-up at the end of training and 6 months follow-up revealed no statistically or clinically significant results between the groups (which were extremely well matched prior to training) on a wide range of relevant tests. This was not because of large improvements on the part of the control group, as neither group showed dramatic improvements in neglect over 6 months.
Conclusions from Early Studies of Neglect Rehabilitation
The rehabilitation of hemi-inattentional disorders is probably the most researched area of neuropsychological rehabilitation outside the domain of the language disorders. The results have tended to be positive, but closer inspection of the data suggests the following:
Effectiveness of Rehabilitation 2: Behavioural Training of Stimulus-Specific Responses
The limitations of the New York-based studies have been turned into a virtue in a few other studies of neglect rehabilitation. In other words, the New York studies are viewed as being successful in producing specific responses (compensatory saccades) to specific situations (largely reading/writing tasks). Such improvements are of fundamental importance to the rehabilitation of individuals, given the importance of reading and writing in everyday life.
A few subsequent studies have eschewed the ambitious aims of Diller and his colleagues and contented themselves with inducing specific response changes to specific stimuli without aiming to produce generalised and spontaneously initiated changes in scanning behaviour. One example of this is the case of Seron, Deloche and Coyette (1989), who attempted to use the New York methods with a severely neglecting patient, and failed to produce improvement. They also attempted self-instructional training and failed with this also. Their final attempt at therapy was, however, successful in reducing the handicapping effects of neglect on the patient’s everyday life functioning. The treatment involved a “mental prosthesis”, namely a device the size of a cigarette packet which gave a high-pitched buzz at random intervals between 5 and 20 secs. This was placed in the patient’s left shirt pocket, and he was encouraged to explore space to find the machine and switch it off. The result was a significant improvement in everyday functioning, where none had been obtained by the previous methods.
Robertson and Cashman (1991) reported a 29-year-old woman with left sensory and visual neglect in the context of frontal lobe difficulties who presented problems in physiotherapy because she walked with her left foot heel-up in a highly unstable planarflex position. She completely failed to learn to lower her heel on walking, which as a result could have led to an eversion injury, despite the fact that she could lower her heel to the floor on command. This was partially attributable to a unilateral left neglect (as well as frontal problems). A pressure-sensitive switch attached to a buzzer on her belt was inserted under her left heel, and a walking programme instituted, with time of heel contact during a 4-m walking test being gradually increased through a process of charting progress and setting goals. Improvements in her walking were charted, which appeared to generalise to everyday life.
Lennon (in press) trained a patient with severe left visual neglect to avoid collisions in the physiotherapy gymnasium by placing large coloured paper markers on the edges of tables, corners, etc., with which he habitually collided. This method is analogous to Weinberg and co-workers’ anchoring procedure for reading. The patient was trained to look for these markers, which he learned to do, and also to skirt around the obstacles with which he habitually collided. This he also learned. Once the markers were removed, the improved behaviour was maintained, though it did not generalise beyond the precise topography of the gymnasium and its furniture.
When this patient went home, he made as many collisions as before in the new environment. The procedure was therefore repeated in the home, with markers being placed on the edges with which he habitually collided. The treatment worked as before, and the effects persisted after removal of the paper markers. However, the behaviour change was again limited to the precise topography of his home and there was no further generalisation.
In another study, Lennon (1991) showed how teaching a neglecting person to verbally regulate the steps involved in transferring from a wheelchair produced significant improvement in this functionally important activity.
In summary, the above series of cases illustrates the potential remediability of specific responses to specific stimuli. But the conclusions of the previous section still hold, namely that generalised scanning improvements in unilateral neglect as a result of training remain elusive.
Effectiveness of Rehabilitation 3: Spatio-Motor Cueing
Theoretical Background: Limb Activation in Visual Neglect
Joanette and Brouchon (1984) described a 64-year-old woman who suffered a right brain CVA and who tended to point to stimuli on her left as if she had seen them on her right. Interestingly, an interaction appeared between the side of space upon which the stimulus appeared and the arm which was used. Only when the right arm was used in response to a left-sided stimulus did the allaesthesia appear. When the other arm was used in response to the same stimulus on the same side, there was no allaesthetic response; performance was reasonably accurate. A subsequent series of cases (Joanette, Brouchon, Gauthier, & Samson, 1986) found that it was not only allaesthetic problems which revealed such an interaction. In a standard stimulus identification procedure, neglect was less severe when the limb contralateral to the lesion was used to point to the target stimuli than when the limb ipsilateral to the lesion was used. In a single case study, Halligan and Marshall (1989) also found that use of the left arm for a cancellation and line bisection task resulted in less neglect.
These findings are in line with the theoretical position of Rizzolatti and Camarda (1987), who propose that spatial attention is based upon a series of circuits largely independent from one another which programme motor plans in a spatial framework. Spatial attention is not seen as a supraordinate function controlling whole-brain activity, but as a property intrinsically linked to pre-motor activity and distributed among a range of centres.
Subsequently, however, Halligan, Manning and Marshall (1991) showed in a series of experiments that the advantage of arm use in reducing neglect was better explained by a spatio-motor cueing process than by an hemispheric activation hypothesis. More specifically, they found that the advantage of left arm use in line bisection was eliminated by having the subject begin the task on the right side of the line, i.e. with the arm crossed over the body midline. This finding does not exclude the possibility that any hypothesised activation effect may be dependent upon limb activation within left hemispace, as opposed to limb activation per se.
Such results lead to a clear clinical question in the rehabilitation of unilateral left neglect; Is there a stimulus which is reliably present in all the different situations in which the sufferer must operate? One answer to this is the person’s left arm. In short, the question posed in these studies is whether left arm activation and perceptual anchoring can produce enduring and therapeutic improvements in neglect.
A caveat to the approach in question is necessitated by the high incidence of hemiplegia often associated with unilateral neglect. However, Robertson (1991) has reported one case of severe left hemiplegia where use of the hemiplegic left arm aided by the right arm (and including some minimal left shoulder movement) resulted in a significant reduction in inattention to the left compared to standard right arm performance. Furthermore, in two of the three cases reported below, patients did have severe hemiplegias: The movements required were the kind of residual minimal responses which are often possible in hemiplegic patients. Finally, even where there is no movement whatsoever in the left arm, the possibility of using the left arm as a passive perceptual anchor remains.
The first study (reported in Robertson et al., 1992) used a combination of perceptual anchoring training with left arm activation procedures in a case of severe left neglect. Specifically, the patient was trained always to place his partially hemiparetic left arm to the left margin of any activity, and to locate it visually during every stage of concurrent activity (e.g. shaving, eating, reading). The training was associated with improvements in reading, telephone dialling and letter cancellation, without improvement on an untrained task, namely digit backward span.
In the second case reported by Robertson et al., the same basic procedure was used, with one additional element—a device which, like Seron’s buzzer, emitted a loud noise at variable intervals. In this case, however, the subject had to prevent the noise being triggered by pressing a large switch with the hemiplegic hand, something which she managed despite her partial hemiplegia. The results of this training were positive. In addition, the woman’s husband made daily ratings (baseline and training) of her mobility difficulties arising from the neglect. These ratings improved as the training commenced, and the patient also showed improvements on cancellation tests. The improvements thus generalised to everyday life as well as to formal testing.
In the third case reported by Robertson et al., the treatment was again similar to the previous case, with the exception that this patient was not told to scan for his left arm. In other words, this study emphasised only the limb activation aspects of the treatment. Despite this constraint, the treatment produced therapeutic gains on cancellation tests (both visual and touch-based), and also improved ratings of mobility in everyday life.
Theoretical Implications of the Spatio-Motor Cueing Treatment
The therapeutic effects of left arm activation on neglect in the last of the above three case studies were experimentally examined by Robertson and North (1992). Left hand finger movement was compared with an instruction to visually anchor perception on the left arm during letter cancellation. Only the finger movements significantly reduced neglect. Another comparison was between “out of sight” finger movements of the left hand in left and right hemispace, respectively. Only left hemispace “blind” finger movements significantly reduced neglect compared to the standard condition. Thirdly, blind left finger movements in left hemispace were compared with passive visual cueing (reading a changing number) and again it was found that only the finger movements reduced neglect. Finally, right finger movements in left hemispace were compared with left finger movements in left hemispace: only the latter reduced neglect. This suggests that, in the last of the three treatment cases at least, the potent effect of treatment was not the perceptual anchoring on the left arm, but rather the fact of mobilising a part of the hemiplegic side. Robertson and North interpreted these results by reference to the work of Rizzolatti and his colleagues (Rizzolatti & Berti, 1990).
Rizzolatti and co-workers suggest that multiple and dissociable spatial frames of reference exist in both humans and animals, and these may be selectively impaired. Rizzolatti has demonstrated in monkeys that space is coded in dissociable ways by different brain centres, and that damage to one centre may result in unilateral neglect for one spatial system but not another. For instance, frontal eye field neurons use visual information to control purposeful eye movements, while inferior area 6 neurons use somatosensory and peripersonal visual information to organise purposeful somatic movements. Lesions in these different areas produce corresponding different types of spatial deficit. A recent case study demonstrates related dissociations between neglect for peripersonal and locomotor space in man (Halligan & Marshall, 1990).
Rizzolatti proposes the existence of multiple representations of space by these different spatial systems, interacting together to produce a coherent spatial reference system against which purposeful motor movements are calibrated and organised. It is the parallel activity of these different perceptuo-motor neural maps which produces the representation of space and, conversely, it is their breakdown which creates distorted representations. Applying this theory to the case reported by Robertson and North (1992), the subject may have been suffering neglect with respect to at least two independent but nevertheless integrated spatial systems—a “personal” space related in some way to some somatosensory representation of his body, and a peripersonal or “reaching” space within which he manifested such deficits as neglecting the left in letter cancellation.
By inducing the subject to make voluntary movements with his left hand in left hemispace, it is possible that the left half of the somatosensory spatial sector was in some way activated or enhanced. Because of the integration of the somatosensory and peripersonal spatial sectors, this in turn produced enhanced activation of the impaired half of peripersonal space. Such is the interpretation which would follow from Rizzolatti’s work. But why did not left hand movements in right hemispace similarly activate the left side of peripersonal space? After all, though left hemispace may not have been activated, the left side of the body was activated. One possibility is that reciprocal activation of more than one corresponding spatial sector of the closely linked neuronal maps in the brain must be activated to overcome the deficit in representing the left side of space.
In other words, cueing/recruitment of the hemispatial system was inadequate on its own. So also for the hemi-corporeal (“personal”) system. Only when both were activated simultaneously did some improvement of spatial perception of the left arise, possibly by reciprocal activation across the related neuronal systems.
Possible Future Directions in Neglect Rehabilitation
Dynamic Stimulation
Butters, Kirsch and Reeves (1990) argued in favour of a polymodal distributed spatial attention system similar to that proposed by Rizzolatti (described above). They argue that some aspects of this polymodal system, particularly some of the brainstem components, may be intact, and that if these are stimulated, then they in turn may increase functioning in related areas of the brain. The result is an overall increase in attention to the neglected side.
Butters and his colleagues reported that transient stimuli, particularly those moving in a jerky manner, are potent activators of neurons in the deep layers of the superior colliculus. They therefore proposed that dynamic stimulation on the neglected side should reduce neglect more than static stimuli. In a series of experiments, they demonstrated that this was indeed the case, using line bisection on a computer screen, with static and moving stimuli on the left side. Both stimuli reduced neglect over baseline, but the dynamic stimuli more so. However, the effects were transient and had no carry-over beyond the time of stimulation.
Butters et al. speculated that placing light-emitting diodes (LED) on the left frame of patients’ spectacles might produce effects transferrable to everyday life. When they tried this during task performance, however, they found that there was no reduction in neglect. There was, however, a reduction in neglect when the same LEDs were placed to the immediate left of the sheets of paper containing the line bisection tasks, leading the authors to argue that dynamic stimuli must be mounted in the region where the patients perform the task and not just on the neglected side of space.
Butters et al. (unpublished) evaluated a second type of manipulation of visual neglect, based on a suggestion by Posner and Rafal (1987), that patching the eye ipsilateral to the lesion in neglect patients should reduce neglect. This was predicted because retinal inflow to the right and left superior colliculi arises primarily in the contralateral eye. Hence, it is argued for cases of left neglect, patching the right eye should reduce retinal inflow (and hence activation) to the left superior colliculus. This would reduce the amount of inhibition that it exerts on the right superior colliculus, rendering the latter relatively “stronger” and hence more able to direct eye movements and attention to the left side.
Butters et al. went on to show the benefits of eye-patching in 11 of 13 patients with left neglect (in at least 1 of 5 tests in each case), though, as with the previous method, the effects lasted only as long as the manipulation (the eye-patch) was in place. In a subsequent experiment, Butters et al. combined eye-patching with dynamic stimulation and found that the combined effects were more powerful in reducing neglect than either method on its own.
Caloric (Vestibular) Stimulation
When around 20 cc of iced water is squirted into a neglect patient’s left ear for approximately 1 min, dramatic improvements in visual and personal neglect are observable in many, but not all, cases and a similar result is obtained when a similar amount of warm water is inserted into patients’ right ears (e.g. Cappa, Sterzi, Vallar, & Bisiach, 1987; Rubens, 1985; Vallar et al., 1990). Vallar et al. also found temporary remission of hemianaesthesia following vestibular stimulation.
The precise mechanisms for this effect are at present unknown, though arguments that it is attributable to induced ocular deviation are now hard to sustain given the evidence that hemianaesthesia may be reduced by the process (see Chapters 3 and 5 this volume, for further discussion). As with eye-patching, however, the effects are relatively transitory and tend to disappear 15–30 mins post-caloric stimulation, though there have been no controlled longitudinal follow-up studies.
Optokinetic Stimulation
Pizzamiglio et al. (1990) demonstrated that neglect could be reduced when line bisection was performed against a leftward moving background. Such a continuous movement produces a slow nystagmus in the direction of movement not dissimilar from that produced by caloric stimulation; indeed, Pizzamiglio and his colleagues argue that the two phenomena may share some common mechanisms. As with caloric stimulation, however, the beneficial effects only lasted as long as the stimulation was present.
Fresnel Prisms
Fresnel prisms produce a displacement of a retinal image to the right or left, depending on the orientation of the prism. Rossi, Kheyfets and Reding (1990) attached such prisms to the spectacles of 18 stroke patients who were said to have either homonymous hemianopia or unilateral neglect. The patients with field or neglect problems to the right were given prisms which displaced peripheral images on the right to a more central location in the visual field, with the reverse for patients with field or neglect problems on the left.
The patients wore these spectacles during the day for 4 weeks and were tested on a number of perceptual tasks at the end of this period while still wearing the prisms. Compared to a control group, the prism group performed better on a number of perceptual tasks, though their overall everyday life functioning was not significantly different. The effects on the patients’ performance of removing the prisms were not reported.
Overview
The five methods described—dynamic stimulation, eye-patching, caloric stimulation, optokinetic stimulation and fresnel prisms—are among a number of manipulations which appear to reduce visual neglect in the short term, but which provide no carry-over after the manipulations are ended. Future research may establish ways of increasing the carry-over from such methods so as to increase general performance in everyday life. Clearer theoretical delineation of different types of unilateral neglect may lead to more sophisticated treatment procedures which are more closely tied to theory, and it is to be hoped that the chapters in Part II of this book will help provide the foundation of such an enterprise.
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