POSTURAL CONTROL IS organized to build up and update

Transcription

1 440 Transcutaneous Electric Nerve Stimulation Reduces Neglect-Related Postural Instability After Stroke Dominic Alain Pérennou, MD, PhD, Catherine Leblond, MD, Bernard Amblard, PhD, Jean Paul Micallef, PhD, Christian Hérisson, MD, Jacques Yvon Pélissier, MD ABSTRACT. Pérennou DA, Leblond C, Amblard B, Micallef JP, Hérisson C, Pélissier JY. Transcutaneous electric nerve stimulation reduces neglect-related postural instability after stroke. Arch Phys Med Rehabil 2001;82: Objective: To test the existence of a neglect-related component of postural imbalance in some stroke patients to determine whether neglect patients (1) show worse postural control compared with nonneglect patients and healthy subjects and (2) have latent postural capacities that could be unmasked by an appropriate somatosensory manipulation. Design: Intervention study with and without transcutaneous electric nerve stimulation (TENS). Setting: Rehabilitation center research laboratory. Participants: Twenty-two stroke patients (mean age, yr; average days since stroke, 83.2d) and 14 age-matched healthy subjects. Stroke patients were subdivided into 3 groups: 6 with spatial neglect and 16 without (8 with left lesion, 8 with right lesion). Interventions: All participants were subjected to a dynamic balance task, performed while sitting for 8 seconds on a laterally rocking platform. Seated on this mobile support, they were asked to maintain actively an erect posture, sitting as still as possible. In patients, TENS was applied on the contralesional side of the neck during the postural task. An effective stimulation (intensity corresponding to the threshold of perception, TENS ) was compared with a placebo stimulation (.01 threshold of perception, TENS ). Main Outcome Measures: Postural performance in each trial was monitored by using 2 criteria: the number of aborted trials caused by loss of balance, and the angular dispersion of the support oscillations in roll. The latter criterion, which increased with body instability, was defined as 2 standard deviations of the angular distribution. Results: Patients showing neglect displayed pronounced postural instability compared with other patients and controls. Although dramatic postural instability in the neglect patients was spectacularly and systematically reduced with TENS, no effect was observed in patients without neglect. Conclusion: This is among the first studies to provide clinical evidence supporting the postural body scheme concept. Key Words: Balance; Cerebrovascular accident; Posture; Rehabilitation; Transcutaneous electric nerve stimulation. From the Départment de Médecine Physique et Réadaptation du CHU de Nîmes, Unité de Rééducation Neurologique (Pérennou, Micallef, Pélissier), Le Grau du Roi; Service de Rééducation Fonctionnelle, Hôpital Gui de Chauliac, CHU Montpellier (Pérennou, Leblond, Micallef, Hérisson); and UPR Neurobiologie et Mouvements du CNRS (Amblard), Marseille, France. Accepted in revised form June 20, No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the author(s) or upon any organization with which the author(s) is/are associated. Reprint requests to Dominic A. Pérennou, MD, PhD, Dépt de Médecine Physique et Réadaptation du CHU de Nîmes, Unité de Rééducation Neurologique, Centre Médical, Le Grau du Roi, France, perenn@iurc1.iurc.montp.inserm.fr /01/ $35.00/0 doi: /apmr by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation POSTURAL CONTROL IS organized to build up and update body orientation and to ensure that balance is maintained. 1 This spatially oriented behavior is thought to be organized on the basis of an internal model, ie, the postural body scheme. 2,3 Internal models may represent a general neural process to resolve sensory ambiguities, to synthesize information from disparate sensory modalities, and to combine efferent and afferent information, 4 and thus may support anticipation in motor behaviors. The postural body scheme could take into account not only the body geometry and orientation with respect to gravity, but also borders between bodily and nonbodily spaces, as well as body dynamics. According to this concept, cerebral lesions that induce a pronounced disruption in the processing of spatial information should impair the internal representation of the body in space and consequently the postural control. Recent studies performed in stroke patients seem to confirm this assumption. 5,6 When such lesions are located in the right hemisphere (in right handed people), they often entail spatial neglect that represents an alteration in the construction of the bodily and/or the nonbodily space. 7 Because the left side of the body is often underused in patients with left neglect, 8 it is not surprising that spatial neglect has been found to be among the most important factors influencing postural capability in individuals with hemiplegia. 9,10 These 2 studies, which confirmed the clinically accepted existence of a strong link between impairment in spatial cognition and impairment in postural control, provide some of the earliest clinical evidence in favor of a cognitive component of postural control. Amblard et al, 11 and more recently others, 12 have suggested the existence of 2 separate mechanisms that control body orientation and stabilization. In the clinical study mentioned earlier these 2 domains of postural control were assessed together without distinction between orientation and stabilization. We have investigated both body orientation in a previous study 13 and postural stability in this study. Stabilizing the body consists of regulating the positions of body segments either with respect to each other, or to the external support, or to the absolute space. One may assume that this function relies on multiple representations of the body subserving the building up of the postural body scheme. These intermediate spatial representations (eye-head, head-trunk, body-environment) are especially interesting with regard to neglect, which has been hypothesized to be the consequence of a mismatch between different afferent information integrated into an egocentric space representation. 14 This model predicts that neglect patients should display increased postural instability compared with nonneglect brain-damaged patients (and a fortiori to healthy individuals). Our first objective was to verify this point. Most manifestations of unilateral neglect may be temporarily reduced by appropriate sensory manipulation. Such effects have been obtained with vestibular, visual, or somatosensory

2 TENS AND NEGLECT-RELATED INSTABILITY, Pérennou 441 stimulation. 15 Sensory manipulations, when appropriate, may compensate for the distortion in processing spatial information. Their efficiency in reducing neglect is usually temporary and may be the result of recruiting intact systems to produce the observed result, rather than a specific boosting of the impaired representational systems. However, an after effect 16 as well as an improvement in daily life 17 have been reported. Although most manifestations of spatial neglect may be reduced by appropriate sensory manipulation, this remained to be shown with respect to postural instability. The main goal of our study was to test the hypothesis that latent postural capacities could be unmasked in neglect patients. The contribution of each sensory modality to the elaboration and updating of different domain of space representation (bodily, nonbodily) may vary. Consequently, the effects of sensory manipulation may differ in quality and in intensity, depending on the task. Regarding postural control, the reference for maintaining a given vertical posture is supposed to be constructed from multiple sources, and the main role is often attributed to proprioception. 18,19 When a dysfunction of postural control is induced by a peculiar hemispheric cerebral lesion associated with neglect, somatosensory stimulation seems a good candidate for modulating the neural systems implicated in postural impairment. It is well known that somesthetic input elicited from the neck plays a crucial role in body stability, in both animals 20,21 and humans. 22 Much evidence has also been gathered about the powerful effects of neck muscle stimulation on body posture. 18,23-30 Based on this, we decided to apply the somatosensory stimulation at the neck level. Two forms of somatosensory stimulation are efficient in reducing neglect: vibration and transcutaneous electric nerve stimulation (TENS). TENS was used in this study with a view to improving postural stability in neglect patients. TENS is a safe and well-established procedure that can be delivered over prolonged periods, via cutaneous electrodes glued to the skin. This technique consists of stimulating superficial cutaneous nerve fibers of large diameter, 31 by using an electric current of relatively short-pulse duration and intensity below the motor threshold. 32 Because TENS stimulates Ia fibers, as does vibration, the theoretical background of both somatosensory stimulations differs slightly. There is thus no reason to apply TENS to the same location as that used to vibrate spindle muscles. As previously described, 13 TENS was applied at the emergence of the superficial cervical plexus over the posterior part of the sternocleidomastoid muscle contralateral to the lesion (fig 1). This area is known to contain a subcutaneous network with a high density of sensitive fibers. 33 TENS was delivered while patients performed the postural task. Data obtained under baseline and TENS conditions were compared. METHODS Patients Patients enrolled in the study provided informed consent in accordance with the guidelines of the local ethics committee. They were younger than 75 years old, had suffered a unique supratentorial cerebrovascular accident, and were able to perform the postural task. Patients with psychiatric disorders or dementia, patients who had previous sensory or orthopedic diseases that could affect balance, and patients with a pacemaker were not included. Twenty-two patients participated in the study (16 men, 6 women; mean age standard error of the mean [SEM], yr; mean height, cm; mean weight, kg). Thirteen had right-sided brain-damage and 9 had left brain-damage. Twenty of these patients were right-handed, 1 was left-handed, and 1 was ambidextrous on Fig 1. Schematic view of the superficial cervical plexus, which is a dense subcutaneous network of sensitive fibers. The middle part of the sternocleidomastoid muscle corresponds to the subcutaneous emergence of this plexus from the deep neck areas. This site is a good candidate for TENS, with a view to activating the contralesional hemisphere. the basis of the Edinburgh Inventory. 34 Their postural performances were recorded with a mean time interval of days between stroke onset and the experiment. The clinical examination included assessment of weakness, tone, tactile sense of discrimination, visual deficits, and spatial neglect (table 1). A trained practitioner examined patients at the moment of their inclusion in the study, a few days before the first experimental session. Weakness of the lower limb was assessed by a standard examination of muscle strength adapted to patients with central neurologic disorders. 35 Eight anatomic functions were assessed manually for each patient at hip (flexion, extension, abduction, adduction), knee (flexion, extension), and ankle (flexion, extension) levels. Each of these functions was assessed on a 6-point scale and the motor function of the paretic lower limb was then assessed on a global scale ranging from 0 (no contraction) to 40 (normal strength). Synergistic limb movements were also considered. Spasticity was assessed at the lower limb by using the Ashworth scale. 36 Five muscle groups were tested (psoas, hip adductors, quadriceps, hamstring, triceps surae), giving a total score ranging from 0 (no spasticity) to 20 (severe and diffused spasticity). As has been previously proposed, 13 the somatosensory threshold was assessed by an investigation of pressure sensitivity at the pulp of the big toe by using the Semmes-Weinstein aesthesiometer. 37 We used a set of 20 calibrated nylon filaments. Filaments were equal in length but varying in diameter, each implanted at 1 end of a plastic rod. As suggested in the standard method, the value of the force needed for a given patient to perceive the stimulus applied to the skin was then submitted to a log transform to obtain a 20-point linear increasing scale. Patients with neuropathy were not included in the study and any sensory loss was caused by the stroke itself. The presence of visuospatial neglect was assessed by the Bells test. 38 Patients were considered as having visuospatial neglect if they omitted at least 6 targets in the contralesional part of the test sheet. In addition, bodily neglect was assessed by using a scale derived from that proposed by Bisiach et al. 39 Only 6 patients who displayed both visuospatial and bodily neglect were classified as having neglect (N ). Five of them (all right-handed) had a right lesion, the other (left-handed) had a left lesion. Among the 16 patients who did not shown neglect (N ), 8 patients had a right (RN ) and 8 a left (LN )

3 442 TENS AND NEGLECT-RELATED INSTABILITY, Pérennou Table 1: Patients Demographic and Clinical Characteristics N (n 6) RN (n 8) LN (n 8) Age (yr) Gender (men/women) 5/1 6/2 5/3 Delay from stroke onset (d) Muscular strength (0 40) Spasticity (0 20) Tactile hypesthesia ( ) Number of targets omitted in the Bells test Lesion features Corticosubcortial Cortical Subcortical NOTE. Data are presented as mean SEM except for gender and numbers of lesions. hemispheric lesion. Within the 22 patients, neglect severity was quantified by the total number of targets omitted in the cancellation task (Bells test). Demographic, clinical, and anatomic data of each group are presented in table 1. N patients had greater muscular weakness (t 2.2, p.05), spasticity (t 2.3, p.03), and sensitivity loss (t 2.4, p.04) than those who were N. They omitted many more targets in cancellation tasks (t 8,5, p.001) than N. With N, the lesions were more extensive than in the N patients, always involving the temporoparietal junction (cortex and white matter in 5 cases, deep lesion and white matter in 1 case). Lesion location was more variable in N, with more subcortical lesions. Healthy Subjects Fourteen healthy subjects who participated in the study were age-matched to patients. This control group was made up of 9 men and 5 women, aged years. Their mean height was cm and their mean weight was kg. Task and Surroundings An experimental apparatus was designed to analyze dynamic balance in the frontal plane. We used a rocking platform paradigm, adapted to sitting posture. 6,13,44,45 It has the advantage of supporting a self-regulated, unperturbed, dynamic task that can be performed by disabled people. A self-regulated task means that the subjects themselves are responsible both for imbalance and active correction. A rigid plane support was mounted on a seesaw with a horizontal rotation axis parallel to the subject s sagittal plane; safety armrests at the sides prevented falls (fig 2). Subjects and patients sat centrally on the laterally unstable rocking platform. They were asked to maintain an upright sitting posture, sitting as still as possible while looking straight ahead and fixing a target for 8 seconds. This duration might appear rather short as regards usual investigation of balance control in erect stance on stable support (eg, force platform). In fact, this duration was the best compromise between the difficulty of the task and the postural ability of the most impaired patients. A previous study found that less than half of patients (not selected) could successfully complete this test 1 month poststroke onset, whereas most of them became able to perform the task 3 months poststroke. 6 During the trials, their hands were crossed, resting on the thighs. The height of the sitting support was adjustable so that the subjects legs were freely hanging. The sitting position and the radius of the seesaw (22cm) were selected to suit to hemiplegics showing balance impairment (fig 2). Subjects and patients were placed at the center of an open vertical cylinder (diameter, 170cm; height, 190cm), covering about 2.6rad of visual field. The inner wall of the cylinder was covered with a rectangular grating consisting of blue and white vertical stripes. A fixation point was centrally positioned on the visual pattern at gaze level. Data Collection The kinematics of the support oscillations reflecting the subject s imbalance were analyzed by means of an accelerometer a fixed under the platform and used as an inclinometer at a sampling frequency of 50 frames/s. The characteristics of the sensor used were the following: 2G, frequency response 0 to 400Hz, damping factor 0.7, accuracy 0.2% span, and transverse sensitivity 1% span. The sensitive axis of the accelerometer was horizontal, so when tilting, its voltage output was proportional to the sine of the tilt angle. To linearize and extract the angle value, the raw data were stored and then transferred to Excel b where the arcsin function was used. After filtering the first data with a low-pass Bessel fourth-order filter, with a cutoff frequency of 10Hz, it was noted that the quality of the captured signal did not impose a filtering procedure on the variables analyzed. Two criteria were taken into account to evaluate the postural performance in each trial. First, the number of trials needed for a patient to succeed in the task in each condition. The support Fig 2. (A) Rocking platform paradigm adapted for analyzing dynamic lateral balance of neurologic patients in a sitting posture. Patients sat on a rigid plane support, mounted on a seesaw with a horizontal rotation axis parallel to the subject s sagittal plane. (B) Safety armrests were located at the sides to prevent falls. (C) Oscillations in roll of the unique base of support with respect to the horizontal were measured by means of an accelerometer used as an inclinometer. Body stability was quantified with the angular dispersion, which was 2 SDs of its angular distribution about the roll axis. Two conditions of balance were compared: BASE and TENS applied on the neck contralateral to the brain lesion. Row data of a given patient are displayed showing a better body stabilization with TENS than with BASE.

4 TENS AND NEGLECT-RELATED INSTABILITY, Pérennou 443 Table 2: Correlation Coefficients Between Clinical Characteristics and Postural Indices (Average, 4 trials) Age Height Weight Muscular Strength Spasticity Sensory Loss Number of aborted trials caused by balance loss * Angular dispersion * p.01. p.05. p.001. Neglect Severity tilt (the mechanical constrain of the apparatus) was limited to 17. Trials in which the support tilt reached 17, ie, the support had been suddenly stopped, were ruled out and classified as aborted trials. This criterion gave us a first indication on the difficulty encountered by the patients in performing the task. The aborted trials caused by balance loss were rejected for the quantitative analysis of body stability. Second, as previously proposed, 6,44,46 body stability was quantified with the angular dispersion of the support, which was 2 SDs of its angular distribution about the roll axis in each trial (fig 2). An increase in angular dispersion thus reflects an increase in body imbalance. The reliability and accuracy of these measurements were verified in some trials with the help of a Vicon opto-electronic system. c A mild overestimation of the angular dispersion was noted with the accelerometer ( a compared with the Vicon system ( v ). This was probably caused by the capture of both rotation and translation with the accelerometer, whereas only rotations were computed with the Vicon system. A strong correlation was noted, however, between these 2 measurements of the oscillation amplitudes ( v.69 a.34, R 2.99). This methodologic approach confirms the reliability of measuring body stability by using accelerometric signals with a view to analyzing balance performance. Experimental Conditions and Procedure Each healthy subject performed 4 trials in a single session. Because they were presumed to display normal postural performances, no additional trial was performed under stimulation. Two conditions of stimulation were compared for patients, differing by their intensity: TENS and baseline (BASE). Patients were informed that they may or may not feel any sensation. Two surface electrodes (roughly 2cm apart) applied TENS. These electrodes were attached to the skin over the dorsal part of the sternocleidomastoid muscle contralateral to the damaged hemisphere. We used a manufactured device d tuned to deliver biphasic rectangular stimulation at a frequency of 100Hz with a pulse width of 200 s. The intensity of the TENS stimulation was individually adapted up to a level (roughly 10mA) where the patient perceived a mild tingling sensation. An extremely weak stimulation (.01 threshold of perception) served as placebo in the BASE condition. Each patient performed 8 trials in 2 sessions, 1 week apart. There were 2 successive repetitions per condition (TENS, BASE) in each session. Half of the patients in each group conducted their first session in the order TENS then BASE and their second session in the reverse order; and vice versa for the other patients. Any stimulation started 10 minutes before the beginning of the first trial and lasted up to the end of the second successful trial. Statistical Analysis Data were analyzed by using the Number Cruncher Statistical System. e Nonparametric correlation was used to test possible relationships between the clinical characteristics of patients and their postural indices (averaged value of the 4 trials per condition). When required, multiple regression was also used. Proportions were compared by using chi-square and Fisher s exact test when required. Comparisons between groups were made by using either the Wilcoxon test or analysis of variance (ANOVA) with repeated measures. TENS efficiency was tested by ANOVA with repeated measures. The.05 level of significance (2-tailed test without other mention) was adopted throughout data analysis. Data are given as mean standard error of mean (SEM). RESULTS Regarding the correlation between the 2 postural indices, a positive correlation was found in patients between angular dispersion and the number of balance losses (r.62, p.002). The highest was the angular dispersion in successful trials; the most frequent were the number of aborted trials because of balance loss. Taken together, the 2 postural indices provide congruent and complementary information about postural stability of patients. Comparisons Between Patients and Healthy Subjects Aborted trials caused by balance loss were much more frequent in patients than in healthy subjects ( vs ; p.01), indicating that the task was performed easily by able-bodied subjects but with some difficulty for patients after a stroke. Angular dispersion was smaller in healthy subjects than in patients ( vs ), confirming an impaired body stability in sitting for the latter. Influence of Clinical Characteristics on Body Stability The following results concern only data obtained in patients in the BASE condition. The correlation between individual number of aborted trials caused by balance loss and age, body height and weight, muscular strength, spasticity, sensitivity loss, and neglect severity were investigated in the 22 patients (table 2). The main result to emerge was a strong link between this index and neglect severity. A trend for the influence of age on the number of aborted trials was also noted, but this effect did not reach significance. No other significant correlation was noted. To classify the effects noted earlier, a stepwise regression was made including all variables tested. Severity of neglect was found to be the best contributing variable to the model, explaining alone 33% of the variability in the number of aborted trials (table 2). The number of aborted trials caused by balance loss in N and N patients was then compared with the Wilcoxon rank test. N patients failed their trials much more often than N patients ( vs ; p.01). These results stress the dramatic influence of neglect in performing a self-regulated lateral balance task while sitting. Correlation between angular dispersion and age, body height, weight, muscular strength, spasticity, sensitivity loss,

5 444 TENS AND NEGLECT-RELATED INSTABILITY, Pérennou patients were plotted (fig 3), showing a postural improvement as constant as spectacular. Finally, there was no effect of order between TENS and BASE, suggesting that the effect of TENS on body stability was only transitory, lasting less than 20 minutes. Fig 3. Body stabilization in neglect patients, patients without neglect, and healthy subject. Patients with neglect showed greater postural imbalance than others. Patients showing neglect improved spectacularly by TENS (average, 27%), whereas no significant change was induced in other patients. Individual behavior in response to TENS (inset) attests that improvement in body stability was constant in neglect patients. Values presented as mean support angular dispersions SEM., TENS ;, TENS. and neglect severity were investigated in the 22 patients (table 2). Both age and sensitivity loss were positively related to body imbalance. The main result to emerge was a strong link between the neglect severity and the angular dispersion of the support (body instability). No significant influence of body height, weight, muscular strength, or spasticity was noted on body balance. Combined effects of neglect severity and age explained 40% of angular dispersion variability. Only a further 1% in angular dispersion variability was explained by injecting sensibility loss in the previous model, presumably caused by the high correlation between neglect severity and sensitivity loss (r.66, p.001). The ANOVA showed that angular dispersion was higher in N patients than in those with LN (F 1, ; p.001) and RN (F 1, ; p.01) (fig 3). Although patients with N displayed more severe deficits than N because of a more extended lesion, these results taken together stress again the crucial influence of neglect on the lateral postural imbalance of brain-damaged patients. Reducing Postural Instability with TENS The same postural indices used in the BASE condition were used to assess the stimulation effect. Because we hypothesized that patients will improve their balance with TENS, it was possible to subject the number of aborted trials caused by balance loss to a 1-tailed paired t test. For the 22 patients, there were fewer balance losses with TENS than with BASE (1 0.3 vs 2.4 1; t 9.86, p.04), which gave a first indication of the TENS efficiency on postural stability. The TENS effect on angular dispersion was first tested by using a 2-factor ANOVA (TENS, 3 groups) with repeated measures (fig 3). A strong group effect (F 2, ; p.001) and a TENS effect (F 1, ; p.02) were noted, with an interaction between these 2 factors (F 2, ; p.03). The TENS effect was then analyzed separately for patients in N, LN, and RN groups. No TENS effect was noted in the RN (F 1,48.06; p.80) or in LN (F 1,48 2.2; p.15) groups, whereas TENS strongly improved in N (F 1,36 9; p.005). Individual responses to TENS of N DISCUSSION The relation between body posture and spatial cognition has been emphasized by Paillard, 47 who hypothesized that the postural space coordinate system has the advantage of being physically anchored to the invariant direction of gravity, which provides, at least on Earth, the unique absolute frame of reference. There is increasing evidence that body posture influences the degree of spatial neglect Conversely, much less is known about the influence of neglect on posture, and especially of posture on gravity. We addressed this question by using a postural paradigm suited to analyzing the sitting equilibrium of disabled people. Because the innervation of trunk and girdle muscles is bilateral, 54,55 the dysfunctioning of the crossed corticospinal pathway induced by a focal hemispheric lesion could have a minor influence on the active maintenance of sitting posture. In our study, neither weakness nor spasticity was shown to influence postural stability, which emphasizes the relevance of our paradigm for analyzing the sensory contribution to postural control in neurologic patients. This dynamic self-regulated balance task was chosen to increase the sensory contribution to body balance, 11 to reveal the effects of sensory deficits on postural control. Because the axis of rotation did not pass through the supporting surface, the movements of the rocking platform combined rotations around an anteroposterior axis and lateral translations (fig 2). With the apparatus used in this study, the lateral displacement of the line of contact between seesaw and the supporting plane was about 3.8mm/degree, indicating that lateral translations were not negligible. Consequently, no absolute stable tactile frame of reference was available to perform the task that still increased the role of the body scheme representation as well as visual and vestibular inputs. Angular dispersion was highly correlated to the number of balance losses, which indicates the relevance of this index for quantifying body imbalance. Moreover, nearly half of the variance of angular dispersion was explained by the clinical features considered. This means that pelvic stability closely reflects the general body stability. Findings in Baseline Condition Although N patients were analyzed later than N, their postural imbalance was apparent both by their frequent loss of balance and increased angular dispersion compared with other patients. This disadvantage cannot be explained by the greater severity of their elementary deficits (ie, spasticity, muscular weakness) because no correlation was found between these deficits and the postural indices. We found that body instability was roughly proportional to sensitivity loss (hypesthesia). Because somatosensory deficits may also be attributed to neglect, 56 our study showed a strong relation between spatial neglect and impairment in lateral stabilization. Postural control could be organized on the basis of an internal model 2,3 that closely deals with the body scheme, originally defined in 1911 as a combined standard against which all subsequent changes of posture are measured and which intervenes in organising spatially oriented activities. 57 Neglect may be associated with a disruption of, or failure to attend to, the body scheme. 58 Despite abundant literature on postural control after a cerebrovascular accident, 59,60 little attention has been paid to the alteration in the cognitive control

6 TENS AND NEGLECT-RELATED INSTABILITY, Pérennou 445 of posture induced by a hemispheric lesion. It has been suggested that the recovery of posture in hemiparetic patients implies not only the recovery of motor and somatosensory deficits but also of spatial cognition. 60,61 To explain why patients with left hemiparesis show greater sway area and lateral displacement of the center of pressure toward the ipsilesional side than those with right hemiparesis, Rode et al 61 hypothesized that the cause was a distortion in the postural reference. According to Rode, 61 the postural reference could be shifted toward the lesion, like the midsagittal plane representation in neglect patients. They reported that, compared with right hemiparetics, left hemiparetics continued to overload the nonparetic leg though manifestations of neglect had disappeared at the time of the experiment. This led them to dissociate the persistent distortion of a spatial postural representation from neglect-related manifestations. 61 In contrast, the high correlation noted between neglect severity and postural impairment, in a previous study 10 as well in this study, argues for a strong relation between spatial neglect and postural disability. This apparent discrepancy could be because, as postulated by Gainotti et al, 62 only automatic orienting of attention toward stimuli arising in the contralesional hemispace could be disrupted in unilateral spatial neglect, whereas controlled, volitional orienting could more or less be completely spared. Body stabilization is organized mainly on the basis of nonvolitional mechanisms. The apparent dissociation between the recovery of spatial neglect and the persistence of postural imbalance could reflect the persistence of a disturbed automatic orientation of attention toward the contralesional hemibody, despite some integrity (or recovery) of the volitional orientation of attention toward the contralesional extracorporal space. On the basis of previous studies 9,10 as well as findings from this one, we suggest that the pronounced postural imbalance of some stroke patients is a basic manifestation of spatial neglect. This manifestation referring to the bodily domain of neglect may be termed postural neglect. 10 Rather than a concept of a unitary representation of egocentric space, 63 the concept of multiple representations of space appears now more convenient to account for numerous disorders that are known at present to affect spatial cognition. Stabilizing the body consists of regulating the position of body segments, either with respect to each other, or to external support or to absolute space. One may assume that this function relies on multiple intermediate body representations (eg, eyehead, head-shoulders, shoulders-pelvic, pelvis-supporting platform in the paradigm we used) subserving the building-up of the postural body scheme. The transformation of the coordinates of various body segments in intermediate representations is just a high-risk process in patients showing neglect. 14 Accordingly, we hypothesize that the postural instability of neglect patients could be the result of a mismatch in the multisegmental coordination of the body in space. This conception has the advantage of explaining why neglect patients display such a dramatic postural instability. The multisegmental coordination has not been quantified in this study but would have to be considered in further investigations. Beyond the role of spatial neglect on body stabilization, the idea of a hemispheric asymmetry for postural control is an emerging concept, congruent with the right hemisphere dominance for spatial attention and/or representation. The neglect group of our study was made up of 5 right-handers with a right lesion and 1 left-hander with a left lesion. In this group, all the lesions involved the temporoparietal junction. Our data suggest that the right hemisphere cortex (in right-handers) could be especially suited to process the sensorimotor information subserving lateral postural control. This view is in line with previous reports, based either on studies of postural performances in patients with brain injury 10,61,64-66 or in healthy subjects. 44 Why Use TENS to Induce a Neuromodulation? Although the precise physiologic mechanisms of TENS neuromodulation are still a matter for debate, some beneficial effects are emerging in the literature, including behavioral improvements in patients with brain injury. For instance, TENS-like stimulation has been successfully used to improve the functional outcome after a stroke, 67 possibly through an improvement of postural control. 68 A reduction of the bias in the postural vertical has also been obtained in some patients with brain injury. 13 It has been also shown that TENS can be used to reduce some neglect manifestations. Improvements have been obtained in tactile perception, 69 spatial exploratory tasks, and purely mental representation. 73 According to this literature, it seemed particularly relevant to test the efficacy of TENS on postural control in patients showing neglect. TENS has some technical advantages compared with other sensory manipulation. First, this somatosensory stimulation can be applied easily without any constraint on patient mobility, and for as long as necessary. Indeed, if vibration is a unique method for performing basic works in research laboratories, it might appear less reliable in a clinical context. In particular, the effects of vibration seem very sensitive to the precise location of the vibrator probe on the vibrated muscle. For example, Taylor and McCloskey 74 reported that very small changes in the position of the vibrator could cause large alterations in the magnitude of the illusory movement of the light and could even reverse its direction. Second, most patients with neglect reported a tingling sensation only in the first minutes of stimulation and then lost the conscious perception of the stimulation. Because they were not aware of their stimulation, it was possible to use a placebo procedure, the effects of which could be compared with those induced by the actual stimulation. We used this placebo procedure in our study. Improving Postural Control in Neglect In neglect, both somatosensory 69,75,76 and motor deficits 77,78 can be reduced with appropriate sensory manipulation, whereas no such changes are usually observed in nonneglect patients. This argues for the existence of a cognitive-related component of these deficits. Our findings show that TENS may unmask latent postural capacities in neglect patients. Several explanations are conceivable. Even if the intensity of the TENS stimulation was individually adapted to reach a level that corresponded to a subliminal intensity of contraction of the sternocleidomastoid, a mild contraction of this muscle could not be excluded. Because the head was free, the action of the sternocleidomastoid muscle could have associated a contralateral turning with an ipsilateral tilt of the head. This action is not compatible with orienting attention overtly (by eye and head movement toward the neglect side), which excludes this explanation. Karnath et al 48 have shown that a 15 trunk rotation toward the neglect side reduces some neglect manifestations. Because patients were instructed to look straight ahead in our study, we cannot exclude that a mild contraction of the sternocleidomastoid might have induced a trunk rotation toward the neglect side, thus, reducing the severity of the spatial neglect and subsequently improving postural control. Given the mass of the trunk and the low level of the stimulation, however, it is unlikely that the sternocleidomastoid moved it. TENS activates afferent nerve fibers, which convey stimuli to the contralateral hemisphere. The effect of TENS may rely

7 446 TENS AND NEGLECT-RELATED INSTABILITY, Pérennou on a cerebral activation under the pressure of stimuli artificially delivered. Various afferent nerve fibers are presumably activated by transcutaneous neural stimulation. Consequently, the pattern of sensory activation related to TENS is not confined to proprioceptive input. The effect of TENS on neglect manifestations has been discussed in terms of specificity of the stimulation location. 71,79 In our study, we are unable to provide additional arguments because we decided a priori to stimulate the lateral side of the neck given the engagement of this body segment in postural control. Nevertheless, we have reported a spectacular neglect-related effect of TENS on body stability. This improvement may reflect the modulation of some higher order representation of space by an afferent somatosensory pathway. This effect was observed in patients whose lesion involved the temporoparietal junction. If we take into account the limits of the topographic identification of large and sometimes not very well delimited vascular lesions on computed tomography scans, this area can be said to correspond in humans to the parietal-insular-vestibular area found in monkeys by Grüsser et al. 80,81 This last area contains neurons responding to vestibular, visual, and somesthetic stimulation in particular from the neck. Grüsser 80,81 reported that nearly all the neurons of the parietalinsular-vestibular cortex (PIVC) responded to adequately selected somatosensory stimuli and that rotation of the body while the head was fixed in space was the most effective somatosensory stimulus activating PIVC neurons. These polymodal vestibular units may contribute to the building up and updating of trunk and head position in space, 80,81 and also could contribute to the control of spatially oriented behavior. Our study suggests that TENS applied to the neck facilitates the reorganization or improves the functioning of the neural network, including the polymodal sensory area. This leads to an improvement in the regulation of positions of head and trunk, either with respect to each other, or to external support, or absolute space. The dramatic impairment in postural stability of N patients is compatible with an insufficient compensation for the effects of the lesion. The sustained artificial stimulation delivered somatotopically at the neck level could thus be active through a transient mechanism of substitution, based on the activation of undamaged parts of the neural network underlying multisensory integration. In this way, various stimulation could be active in view of experimentally restoring body balance. Optokinetic stimulation could facilitate the restoration of a standing posture in patients with vestibular deficits. 82 A reduction of the weight-bearing asymmetry has been obtained in patients with right brain damage by using caloric vestibular stimulation. 83 Together with ours, these studies bring evidence that balance restoration can be experimentally induced with an appropriate sensory substitution. This sensory stimulation could be delivered either from visual, 82 vestibular, 83 or somesthetic inputs, as in our study. Because of the technical advantages of TENS, including its portability and prolonged duration of stimulation, this technique could be used as a sensory prosthesis. As in most studies analyzing the effects induced by sensory manipulations in patients with brain damage, the number of patients with neglect was quite small in our experimental study. The possible clinical interest of TENS for restoring body balance must be confirmed by studies on larger groups of patients. CONCLUSION Our study is among the first to stress neglect s crucial influence on body stabilization against gravity. In addition, we show how it is possible to modulate this postural instability by an appropriate somatosensory manipulation. The fact that the gain in body stability was spectacular and systematic in neglect patients and null (on average) in others strengthens the idea of a neglect-related component in the postural imbalance of the former. TENS has some technical advantages compared with other sensory manipulations, ie, it is a specific somatosensory stimulation, it is portable, and can be applied easily for as long as necessary. Furthermore, the tingling sensation induced by TENS is only transitory in neglect patients who rapidly lose the conscious perception of the stimulation. 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