Rehabilitation of Unilateral Neglect: Improving

Neuropsychological Rehabilitation

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Rehabilitation of Unilateral Neglect: Improving Function by Contralesional Limb Activation Ian H. Robertson , Karen Hogg & Tom M. McMillan To cite this article: Ian H. Robertson , Karen Hogg & Tom M. McMillan (1998) Rehabilitation of Unilateral Neglect: Improving Function by Contralesional Limb Activation, Neuropsychological Rehabilitation, 8:1, 19-29 To link to this article: http://dx.doi.org/10.1080/713755556

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NEUROPSYCHOLOGICAL REHABILITATION 1998, 8 (1), 19–29

Rehabilitation of Unilateral Neglect: Improving Function by Contralesional Limb Activation Ian H. Robertson MRC Applied Psychology Unit, Cambridge, UK

Karen Hogg and Tom M. McMillan Wolfson Rehabilitation Centre, Atkinson Morley’s Hospital and St George’s Healthcare, Copse Hill, Wimbledon Unilateral neglect predicts poor motor recovery following right hemisphere stroke. Contralesional limb activation has previously been shown to reduce neglect of the left side of space (Robertson & North, 1992), and it is proposed that this happens in part due to overcoming inhibition from competitor perceptuomotor circuits in the undamaged left hemisphere. Application of this principle to clinical rehabilitation results in improvements in neglect and in everyday function (Robertson, North, & Geggie, 1992). The present study extends and replicates this finding with a case of severe unilateral neglect, whose statistically significant improvement in measured neglect is confined to near peripersonal space, and not to personal space nor far peripersonal space. The theoretical implications of this finding for understanding recovery from unilateral neglect are discussed.

INTRODUCTION Unilateral left neglect, a lack of attention or responses to the left side of space which is linked with right hemisphere parietal lobe lesions (Vallar, 1993), is one of the single best predictors of poor functional recovery following stroke (Denes, Semenza, Stoppa, & Lis, 1982; Gialanella & Mattioli, 1992; Kinsella & Ford, 1980; Sea, Henderson, & Cermack, 1993). Unilateral neglect is, however, notoriously difficult to rehabilitate and many studies aimed at training Requests for reprints should be sent to I H Robertson, MRC Applied Psychology Unit, Rehabilitation Research Group, Box 58, Addenbrooke’s Hospital, Hills Road, Cambridge CB2 2QQ, Tel: 01223 355192 extn 354, Fax: 01223 516630, Email: ian.robertson@ mrcapu.cam.ac.uk. The authors would like to acknowledge gratefully the help of Ian Nimmo-Smith for statistical advice and Julia Darling for preparation of the manuscript.

Ó 1998 Psychology Press Ltd

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ROBERTSON, HOGG, McMILLAN

patients to scan leftwards as a compensatory strategy have found no positive results (Seron, Deloche, & Coyette, 1989; Wagenaar et al., 1992; Webster et al., 1984); although a few studies have found some therapeutic effects of intensive therapies which include scanning training as a component of training (Antonucci et al., 1995; Weinberg et al., 1977). One alternative approach to rehabilitation of neglect has been that of limb activation (Robertson & North, 1992, 1993, 1994; Robertson et al., 1992; Robertson, Tegnér, Goodrich, & Wilson, 1994). This is based on the assumption that limb activation of the left limb in left hemisphere causes changes in lateral attention or spatial representation (possibly, although not necessarily, associated with reduction in inhibitory competition from the left hemisphere). We have previously shown that unilateral left neglect can be significantly improved in the short term by inducing patients to make even small movements with some part of the left side of their body (Robertson & North, 1992, 1993, 1994; Robertson et al., 1992, 1994). We have argued elsewhere that the movement of a left part of the body in left hemisphere produces sufficient activation to overcome inhibition from the undamaged left hemisphere, in line with the findings of Sprague (1966). Furthermore,we find that bilateral movements of both hands simultaneously abolish the beneficial effect of a single left movement by a left limb in left hemisphere. We have subsequently established that these short-term improvements in neglect can be converted into longer term therapeutic improvements (Robertson et al., 1992), with neglect patients showing reduced neglect as well as increased functional performance in everyday life, several weeks after the end of training. We hypothesise that the mechanism underlying this improvement rests on an increased awareness of left body space contingent upon making movements with the left side of the body. Once awareness of the left side of the body increases, then the probability of making further movements spontaneously increases. This further improves awareness and activation of the lesioned hemisphere, which again results in greater use, and so on in a positive feedback loop. The viability of this hypothesis is strengthened by findings such as those by Sterzi et al. (1993) who found that right hemisphere lesions resulted in a significantly greater proportion of apparently primary sensory, motor, and limb position sense problems than left hemisphere lesions. Clearly this is anatomically not viable, and they concluded that a proportion of apparently primary sensory and motor deficits following right brain damage were actually attentional in origin. If this is the case, then it is likely that at least some of the motor deficits in unilateral neglect may be secondary to impaired attention to the left side of the body. The positive feedback loop between increased motor use and increased awareness of the left side seems a plausible mechanism in this context. The present study reports an extension and replication of our previous research showing enduring positive changes in unilateral neglect over time,

REHABILITATION OF UNILATERAL NEGLECT

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contingent upon a limb activation procedure. The present study extends our previous observations by (1) significantly increasing the number of baseline and post-baseline assessments, and (2) applying rigorous interrupted time series analysis statistics to test the causal relationship between treatment and behavioural changes. In selecting repeated measures of spatial behaviour sensitive to neglect, we attempted to sample from three theoretically and empirically distinct domains of spatial attention. It is now clearly established that neglect for body space, reaching or peripersonal space, and far or locomotor space can be dissociated, each from the other (Guariglia & Antonucci, 1992; Halligan & Marshall, 1991; Rizzolatti & Camarda, 1987). It is therefore important in assessing the effects of manipulations or rehabilitation strategies in neglect to attempt to sample from these three domains, and the methods used are described below.

METHOD Subject The subject was a 22-year-old man who suffered an extremely severe traumatic brain injury. The computed tomography (CT) scan showed that he had sustained a right parieto-occipital skull fracture and right extra and subdural haematomas. The haematomas were evacuated following craniotomy. He was unconscious for 6 –7 weeks. Later, hydrocephalus developed and a ventriculoperitoneal shunt was inserted. Post-traumatic epilepsy developed 4 months after the trauma. On admission for rehabilitation to the Wolfson Centre some 18 months post-injury, he had a left-sided weakness and partial hemiplegia. He was independently mobile and independent for most activities of daily living, other than some washing/dressing tasks made difficult by his hemiplegia. Tested 18 months post-injury, just prior to the training procedure described below, he showed the following profile. His estimated premorbid verbal IQ was 108 (National Adult Reading Test—Nelson, 1982), and his age-scaled scores on selected Wechsler Adult Intelligence Scale—Revised subtests (Wechsler, 1982) were as follows: Comprehension 9, Similarities 13, Block Design 8, and Digit Symbol 2. He scored 32 out of 36 on copying the Rey figure (Rey, 1964), but on recall remembered only seven out of the original 32 items. On the Benton FAS verbal fluency test, he scored a total of only 10, while on the Wisconsin Card Sorting Test (Nelson, 1976), he achieved only one category, and made 35 errors, of which 37%were perseverative. He showed significant left neglect on two subtests of the Behavioural Inattention Test (Wilson, Cockburn, & Halligan, 1988), namely line bisection (score 8 out of maximum 9) and star cancellation (score 42 out of maximum 52). He also showed neglect during everyday activities on the hospital ward.

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Procedure The patient was assessed on three different target measures over a baseline period of 13–20 daily sessions (depending on the measure), followed by identical assessments carried out prior to training on 18 training days, followed by a follow-up period of 9 days (8 days in the case of the combing task). During the training phase, the assessment was always carried out prior to training, and so any changes in behaviour during the training phase reflected effects which lasted at least 24 hours, and were not immediate effects of training. Of course, the training procedure was never implemented during testing, in any of the experimental phases. Assessment and training were carried out by different individuals, and the assessor was blind as to which phase of the single case study was in effect in each test session. The data were analysed using an interrupted times series model (Gottman & Glass, 1978) with a first order autoregressive model for the errors. The software used was the AREG procedure in SPSS Release 4.0 for Apple Macintosh. The auto-regressive model makes a modest allowance for the type of serial temporal dependencies that may be encountered in repeated testing. The procedure can be thought of as a type of multiple regression analysis with two ‘independent’ variables: (1) a dummy variable indicating whether the trial was pre- (0) or post- (1) intervention, and (2) the score for the immediately preceding trial, or equivalently as a modified t- test between the two groups of scores for the pre- and post-intervention trials, allowing for serial dependencies. The test statistic has a t-distribution under the null hypothesis that there is no effect of the intervention on mean test score (Box & Jenkins, 1970; Gottman & Glass, 1978). Rehabilitation procedure

Training involved the use of a “Neglect Alert Device”. This consists of a small metal box, roughly 12 × 8 × 2 cm, with a switch attached via a cable. The device can be set such that it emits a loud buzzing noise if the switch is not pressed within a predetermined, and variable, time interval. A red light is also mounted on the box, which remains on as long as the buzzer is not activated. Both box and switch are sufficiently light and mobile that they can be used in a variety of situations. The pressure required to activate the switch can also be adjusted on a continuous scale. The subject was required to press the switch to turn off the buzzer during the performance of a range of therapy activities, including self-care instruction, reading, card sorting, and other activities which constituted routine treatment during the occupational therapy programme at the rehabilitation centre. This therapy continued through all phases of the experiment, including baseline and post-training, and hence any changes in behaviour could be attributed to the onset and withdrawal of the limb activation procedure.


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The alert device was set on an 8-second fixed interval schedule. He used his left hand to turn off the buzzer. Assessment procedure

Three target measures were used which assessed spatial behaviour in three distinct domains which have been isolated as dissociable (Guariglia & Antonucci, 1992; Halligan & Marshall, 1991; Rizzolatti & Berti, 1990; Rizzolatti & Camarda, 1987). To measure personal or body space neglect, we used a variant of the Hair Combing Task (Zoccolotti & Judica, 1992), for far space or locomotor neglect, we used a specifically tailored measure of navigation through a fixed route in the hospital, and for neglect within near or “reaching” space, we used the Baking Tray Task (Tham & Tegnér, 1996).

Combing Task. Neglect of the left side of the body is known to dissociate from neglect of the left side of extrapersonal space (Guariglia & Antonucci, 1992). Zoccolotti and Judica (1992) developed a measure of personal neglect, which we adapted into a more quantitative form, by giving the patient a comb and asking him to comb his hair, normally with his right hand. The number of strokes on the right and left side of the head respectively in a fixed 30-second period was counted. From this, the proportion of left to total strokes was calculated and used as a measure of personal neglect. Navigation Task. A fixed route was constructed through the hospital, which comprised a total of seven doorways and three corridors. Above each doorway, an unobtrusive mark defined the centre of the door, and at each doorway it was recorded whether the patient was to the left of this mark, centrally positioned under the mark, or to the right. Previous research has shown that patients with unilateral neglect all veer to the right when passing through doorways (Robertson et al., 1994). In each corridor, the patient was assessed as walking “centrally”, if, at any point within that particular corridor, he walked within the central 2 m, irrespective of whether he veered to the left or right before or after this. In other words, in a particular corridor, the patient was only assessed as walking “right”, if the walking trajectory was consistently on one side, and never entered the central 2-m area of the corridor. This walking circuit resulted in a total of 20 assessment points, namely seven doorways and three corridors, each assessed twice, namely during the outgoing circuit, as well as during the return. Baking Tray Task. The Baking Tray Task (Tham & Tegnér, 1996) requires subjects to place 16 blocks of wood (“buns”) onto a 50 × 75 cm piece of hardboard (“the baking tray”) in as symmetrical a layout as possible, as if they were buns being placed on a baking tray so that they cooked properly and

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equally in the oven. In their study, patients with unilateral neglect tended to place more blocks on the right side of the tray, and no control placed any less than seven blocks on the left side. The score is simply the number of blocks placed to the left of the tray midline, and any score less than 7 is abnormal and indicative of neglect.

RESULTS Within training results. During the 18 days of training, the therapist recorded the number of times the patient correctly responded to the neglect alert device by switching off the switch, the number of times the patient did so after nonspecific prompting (“what are you supposed to be doing?”), and the number of times there was no response whatsoever. During each training session the subject correctly responded to the neglect alert device 101 times on averag e (SD = 27.2). The subject required prompting on 5.3 times/session on averag e (SD = 3.2), and failed to respond at all on 15.3 times/session on average (SD = 10.8). Personal neglect (hair combing). Figure 1 shows the hair combing performance (proportion of all strokes which were made to the left of the head) over the three phases of the experiment). An interrupted time series analysis using ARIMA (auto-regressive integrated moving average) models (Box & Jenkins, 1970; Gottman & Glass, 1978) was used to estimate within test significance of change in performance following onset of treatment. The treatment effect between baseline and onset of training for the hair combing task was highly significant [t(44) = 3.68; P < .001]. Scrutiny of Fig. 1 shows, however, that the significant improvement in performance during the training phase declines to around baseline levels in the follow-up period. Locomotor space (circuit walking). There was a statistically significant improvement in performance on the circuit coinciding with the onset of training [t(41) = 2.08, P < .05] (see Fig. 2). Similar to the personal neglect measure, however, the body positioning performance on the circuit gradually declined in the nine sessions of post-training unit it returned to near baseline levels. Reaching space performance (baking tray task). There was a statistically significant improvement in baking tray performance coinciding with the onset of training [t(38) = 5.74; P < .001]. Figure 3 shows performance on this test, and, unlike the previous two measures, the improvements were maintained after the end of training.


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FIG. 1. Performance in hair combing over baseline, training and follow-up (Personal space).

DISCUSSION As predicted, all three measures of three different types of neglect—locomotor/far space, personal/body space, and peripersonal or reaching space—showed very significant improvements coinciding with the onset of limb activation training, replicating previous findings. Only the peripersonal/ reaching space measure of neglect showed maintained improvements after the end of training. This finding does, however, confirm previous findings that limb activation treatments can produce persisting improvements which extend beyond the training situation. Possible reasons for the return to baseline in the two non-reaching space measures are discussed below. The fact that two measures returned to baseline after the end of training constitutes a very strong argument for the causal relationship between the training and the change in behaviour. While all of the changes in behaviour coinciding with the onset of training were statistically significant according to a time series analysis, there is always the concern that some undetected

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FIG. 2. Performance in body positioning during walking, baseline training, and follow-up (Locomotor/Far space).

correlated variable accounts for the changes rather than the onset of training itself. This argument is untenable when withdrawal of training results in return to baseline, as it did in two out of three of the tests. On the other hand, the maintenance of training effects on a task performed within reaching space confirms previous findings regarding the therapeutic benefits of this procedure. One possible explanation for why only peripersonal space measures showed an effect beyond the end of training is that the effects of limb activation are confined to this domain of spatial attention. This is, however, not a tenable explanation because the limb activation effects did preclude temporary changes in locomotor spatial performance, something which we have confirmed in other studies (Robertson et al., 1994). The present study, in actual fact, suggests that limb activation influences all three areas of space—personal, reaching, and far—as would be predicted from the theoretical explanations for this phenome-


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FIG. 3. Performance in baking tray task, baseline, training and follow-up (Near peripersonal space).

non (Robertson & North, 1992). What has to be explained, therefore, is the failure of long-lasting effects for the non-reaching space measures. If the limb activation generalisation effects are indeed secondary to increased use of the contralesional side of the body, which in turn results in improved activation of the lesioned hemisphere, then one would have to put forward an argument as to why such post-training limb activation would be more likely spontaneously to occur in reaching tasks such as the Baking Tray Task than in the Walking or Hair Combing Tasks. It is conceivable that the Walking and the Hair Combing Tasks are more effortful for a patient suffering unilateral motor and sensory problems, and that the inherent task difficulty of these tasks for this patient reduced the likelihood of spontaneous movements by the contralesional side of the body. This is, however, purely speculative and cannot be established without more detailed observational data of patient behaviour while performing such tests.

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Whatever the reason for the different patterns of generalisation on the test, the fact is that a simple limb activation procedure carried out as a non-obtrusive addition to existing therapy, produced significant improvements on all three tests of functionally relevant behaviours, and indeed produced enduring improvements even after the end of training on one of these, namely a test carried out within peripersonal space.

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