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Motor strategies of postural control after hemispheric stroke
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REVIEW/MISE AU POINT
Motor strategies of postural control after hemispheric stroke Stratégies motrices du contrôle postural après AVC hémisphérique S. Tasseel-Ponche a,∗, A.P. Yelnik b,c, I.V. Bonan d a
Service de médecine physique et de réadaptation, université Picardie-Jules-Verne, CHU d’Amiens, avenue René-Laënnec, Salouel, 80054 Amiens cedex 1, France b Service de médecine physique et de réadaptation, université Paris-Diderot, groupe hospitalier Saint-Louis-Lariboisière-F. Widal, AP—HP, 200, rue du Faubourg-Saint-Denis, 75010 Paris, France c COGNAC G (COGNition and Action Group), université Paris-Descartes, CNRS, UMR 8257, 45, rue des Saints-Pères, 75270 Paris cedex 06, France d Service de médecine physique et de réadaptation, université de Rennes 1, 2, rue Henri-Le-Guilloux, 35000 Rennes, France Received 5 September 2015; accepted 7 September 2015
KEYWORDS Stroke; Posture; Strategies; Balance; Standing; Rehabilitation; Adaptation
∗
Summary After stroke, the causes of balance disorders include motor disorders, sensory loss, perceptual deficits and altered spatial cognition. This review focuses on motor strategies for postural control after stroke. Weight-bearing asymmetry, smaller surface of stability, increased sway, body tilting and sometimes pushing syndrome are observed. Weakness and sensory impairments account only for some of these disturbances; altered postural reactions and anticipated postural adjustments as well as abnormal synergistic muscular activation play an important part. These disorders are often linked to cognitive impairments (visuospatial analysis, perception of verticality, use of sensory information, attention, etc.), which explain the preeminent disorders of postural control seen with right rather than left-hemisphere lesions. Most of the motor changes are due to an impaired central nervous system but some could be considered adaptive behaviors. These changes have consequences for rehabilitation and need further studies for building customized programs based on the motor comportment of a given patient. © 2015 Elsevier Masson SAS. All rights reserved.
Corresponding author. E-mail address: [email protected] (S. Tasseel-Ponche).
http://dx.doi.org/10.1016/j.neucli.2015.09.003 0987-7053/© 2015 Elsevier Masson SAS. All rights reserved.
Please cite this article in press as: Tasseel-Ponche S, et al. Motor strategies of postural control after hemispheric stroke. Neurophysiologie Clinique/Clinical Neurophysiology (2015), http://dx.doi.org/10.1016/j.neucli.2015.09.003
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MOTS CLÉS AVC ; Posture ; Stratégies ; Équilibre ; Debout ; Adaptation ; Rééducation
Résumé Les troubles de la posture et de l’équilibre résultent de déficiences sensorimotrices, de troubles perceptifs sensoriels et/ou d’altération de la cognition spatiale. Cette revue de la littérature se focalise sur les stratégies motrices du contrôle postural après accident vasculaire cérébral (AVC). La diminution de la surface de la stabilité, l’asymétrie d’appui entre les deux membres inférieurs, les oscillations posturales et l’inclinaison posturale voire le « Pusher syndrome » peuvent être observés chez ces patients. Le déficit hémicorporel sensitivomoteur n’explique qu’en partie les troubles de la posture assise et debout. L’altération des stratégies posturales, des ajustements posturaux anticipés et les coactivations musculaires synergiques y participent aussi. De plus il existe des interactions entre ces stratégies motrices et les troubles de la cognition spatiale (négligence visuospatiale, bais de perception de la verticalité, préférences sensorielles, troubles attentionnels. . .). Les mécanismes des troubles posturaux prédominent chez les sujets avec lésion hémisphérique droite du fait d’une prédominance de celui-ci dans le contrôle spatial. La majorité des stratégies motrices posturales observées après un AVC sont secondaires à l’atteinte des réseaux neuronaux du système nerveux central mais certaines peuvent aussi être considérées comme des comportements adaptatifs. Comprendre les stratégies motrices d’un sujet donné est primordial pour construire des programmes de rééducation posturale personnalisés. © 2015 Elsevier Masson SAS. Tous droits réservés.
Introduction Postural control is the ability to control posture in order to maintain an upright stance during functional activities and to compensate for external and internal body perturbations to avoid falls. Impaired balance was found to be a predictor of falls in community-dwelling older women after stroke [37]. Balance and postural disorders are among the most prevalent consequences, affecting 50% of post-stroke patients in France [12]. They are responsible for medical and surgical complications due to falls, social isolation and impaired quality of life [10,63]. Rapid and optimal improvement of postural control in stroke patients is essential to ensure their independence, social participation and overall health. The mechanisms of post-stroke balance disorders are diverse [25,56]. This postural disturbance may involve motor weakness, asymmetrical muscular tone, sensory loss, perceptual deficits and altered spatial cognition with reference to the postural body scheme. However, compensation strategies to stabilize posture could be developed. After stroke, the postural control would be more sensory-driven rather than anticipatory [29] because the anticipatory mechanism involves many cerebral structures: cortical (supplementary motor area and premotor area), subcortical (central gray nuclei and thalamus) and subtentorial (vestibular nuclei and cerebellum) [45]. Different postural strategies could be controlled by the central nervous system (CNS) to coordinate muscle activity against destabilizing forces applied to the body (extrinsic destabilization) or with self-induced movements (intrinsic destabilization). This review focuses on studies of post-stroke motor strategies involved in the recovery of postural control during both quiet standing balance control and dynamic conditions.
Sitting posture Impaired sitting posture is by itself a major cause of dependency because trunk control is required for the control of
more complex activities such as voluntary movements of the upper limb or standing posture or gait [22]. After stroke, the automatic axial muscle tonus and voluntary strength of the trunk are bilaterally impaired, most prominently on the paretic side [3]. Besides the paresis, other components in trunk control may be impaired, depending on the side of the lesion: ‘‘postural instability’’ would be significantly more frequent among patients with right-hemisphere lesions, and ‘‘apraxic responses’’ would be predominant among those with left-hemisphere lesions [3,65]. Indeed, the voluntary trunk control involves cognitive functions such as visuospatial exploration and mental representation ability for postural adaptation and the construction of the postural body schema [57,13]. Hemineglect and bias of the subjective vertical are important causes of postural asymmetry and instability [57,58,52,34,54,4]. Contraversive pushing, called ‘‘Pusher syndrome,’’ is the most serious postural impairment [55]. It is a perceptual disorder observed with acute stroke, whereby patients lean towards the affected side and actively resist any attempt to correct this posture [33]. Pushing has been linked to biased verticality and hemispatial neglect, more common among patients with right — rather than left-hemisphere lesions [55].
Quiet standing balance control Quiet standing postural control requires maintaining the center of gravity (CoG) within limits of stability. Center of pressure (CoP) measures are commonly used to assess this control by measuring the body position and the amount of body sway. After stroke, stabilometry is used to assess a surface of stability, which is smaller than for healthy subjects, beyond which the CoG cannot move without exposing the hemiparetic patient to loss of balance [51]. Weight-bearing asymmetry (WBA) The quiet standing posture of hemiplegic patients after stroke is characterized by WBA, a shift in the mean position of the CoP toward the unaffected side and increased
Please cite this article in press as: Tasseel-Ponche S, et al. Motor strategies of postural control after hemispheric stroke. Neurophysiologie Clinique/Clinical Neurophysiology (2015), http://dx.doi.org/10.1016/j.neucli.2015.09.003
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Motor strategies of postural control after hemispheric stroke body sway as compared with age-matched healthy people. WBA is very common, predominant with right-hemisphere lesions [58,51]. However, the shift toward the non-paretic lower limb is not systematic. Mansfield et al. studied the prevalence of stance asymmetry 1 year after stroke: 48% of patients were asymmetric, favoring the non-paretic lower limb; 12% favored the paretic lower limb; and 40% were symmetric [42]. Hence, the behavior favoring the paretic lower limb is unusual and could reflect a strategy learned during rehabilitation to favor the paretic lower limb or may represent a pre-planned strategy to permit a rapid compensatory step with the non-paretic limb in the event of instability. WBA diminishes considerably during the 4 first weeks after stroke. A substantial degree of WBA persists during the eighth week and increases during attention-demanding arithmetic tasks, such that weight-bearing symmetry can never become fully automated [11]. The paresis after stroke explains in part the coordination difficulties of each body segment with WBA. Patients with severe motor impairments of the paretic lower limb seem to use this strategy more systematically than do less severely impaired patients [60]. The CoP could shift towards the non-paretic side during standing to minimize instability due to unilateral lower limb impairment [60,59,24]. Sway is greater when loading the paretic than non-paretic lower limb during quiet standing [62]. Sensitivity impairment is another major cause of WBA, as we have observed in our daily clinical practice, although studies devoted to this issue are surprisingly few [60,8]. The abnormal CoP displacement under the paretic lower limb, recorded with a dual-force platform, reflects impaired stabilization control of the paretic lower limb. Patients seem to be constrained in developing an adaptive strategy with greater involvement of the non-paretic lower limb. However, the non-paretic lower limb alone seems unable to compensate for the postural impairment [24]. WBA has also been related to neglect and more generally spatial cognition disturbances [58,52,54,4,53]. Postural control is organized on the basis of internal models that closely deal with the body scheme. Distortions in the coordinates used to distribute the body weight over the two lower limbs during standing could be disrupted, especially with right-hemisphere lesions. The right hemisphere is indeed devoted to spatial processing and is the site of processing for multisensory integration. The right-hemisphere lesion that induces a pronounced disruption in the processing of spatial information is also likely to impair the internal representation of the body in space and, consequently, postural control [57]. A contralesional rotation in the representation of the longitudinal axis could also be involved in the WBA [1] as well as misrepresentation of the midsagittal plane [52,66]. The crucial role of the right hemisphere would thus account for the lateral CoP deviation in such patients [57,51]. The degree of WBA during quiet standing has been associated with the level of independent self-care and length of hospital stay [62]. WBA is strongly related to several gait variables such as gait velocity, cadence, and duration of a single support phase, as if the degree of asymmetry of weight distribution is maintained during gait [47]. However, WBA may not be the main target of rehabilitation programs aimed at restoring standing balance after stroke, especially in patients with the most motor impairment [60,24]. The
3 compensatory role of the non-paretic lower limb should be accepted and the balance rehabilitation program should focus on intensive destabilizing exercises, rather than the quality of the posture and movement during gait, specifically for the most-impaired patients [73]. More than asymmetry of the body weight, tilt and instability should be a concern. The same disorders with standing are seen with sitting and can disrupt balance, especially among pushers [55,33]. Bias of verticality and spatial cognition disorders are often associated with sensorimotor impairments that disrupt standing posture [4,55]. Body sway After stroke, the amplitude of body sway is increased, in particular in the frontal plane [11,50]. With body instability, significant improvement, particularly in the frontal plane, requires more time than with WBA [71]; the condition is negatively associated with gait velocity and is related to risk of falling [62]. In addition, postural sway can distinguish between fallers and non-fallers in community-dwelling older adults [40]. Nevertheless, an increase in sway for some patients could be, at least in part, a necessary comportment to increase sensory feedback [9,5,72].
Postural strategies for maintaining standing posture in dynamic conditions Deviations from a set position are regulated by postural adjustments relying on both feedback, with extrinsic perturbation, and a feedforward control mechanism when the movement can be anticipated for intrinsic perturbations. Intrinsic perturbations During self-initiated movements, internal perturbations must be counteracted automatically to maintain balance by anticipated postural adjustments. Weight-shifting ability. The ability to execute a selfgenerated weight shift within the base of support without adjusting the foot position is crucial, notably in the frontal plane, when rising from a chair, transferring, walking, turning or stair climbing. When leaning the body as far as possible in a specific direction, stroke patients have difficulties in all planes but mostly in the direction of the paretic lower limb [15,26,67]. Voluntary weight shifting to one limb while standing [27] or during dynamic tasks such as rising from a chair [21,28,7] is compromised after stroke. During voluntary displacements, patients use only part of their base of support [35]. Weight-shifting ability during different dynamic tasks is correlated [20]. Poor weight-bearing ability may result from an impaired concentric knee muscle component specific to the task of rising [20]. Interestingly, although subjects can shift more than half of their body weight onto the paretic limb during a voluntary weight shift in any direction, they spontaneously bear less than half of their body weight on the paretic limb during the static task of standing or the dynamic task of rising from a chair. The ability to transfer body weight laterally or forward onto the paretic lower limb while standing is indicative of walking performance [15]; this impaired ability contributes to falls after stroke [7]. Weight-bearing ability can be
Please cite this article in press as: Tasseel-Ponche S, et al. Motor strategies of postural control after hemispheric stroke. Neurophysiologie Clinique/Clinical Neurophysiology (2015), http://dx.doi.org/10.1016/j.neucli.2015.09.003
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improved with rehabilitation [11], with positive impact on rising from a chair and bilateral standing symmetry [70,14]. Limits of stability (LoS). In standing posture, LoS are defined when the CoP displaces voluntarily to the outer limits of the base of support. Post-stroke patients have greater difficulty than control subjects in displacing the CoP in both the forward and backward directions [27]. However, in our experience, the limits of stability do not reflect the efficiency of balance control but rather the fear of falling and the mental representation relating to supposed balance performance [73]. This situation is especially true for post-stroke patients: besides the possible difficulty in understanding the task, the hip strategy post-stroke patients often use reduces the displacement of the CoP; moreover, neglect patients often show larger limits of stability despite a greater risk of falling. Anticipatory postural adjustments (APAs). APAs are muscular responses to stabilize posture before movement. Preparatory muscle activity serves to compensate for the disturbing forces due to displacements by sequential activations [32,6]. The failure to coordinate postural muscle adjustments may contribute to the instability of patients with hemiparesis [32,23]. After stroke, the ability to perform adequate APAs is related to good balance performance, assessed by the Berg Balance Scale [23], and the acquisition of APAs associated with a newly learned task is impaired [44]. When normal subjects raise their right arm, left paraspinal and right biceps femoris activity is usually initiated before right deltoid activity. In hemiparetic patients, the sequence of hip, back, and shoulder muscle activation is the same as in control subjects when the speed of arm movement is similar, but muscle activation is delayed and reduced, particularly on the paretic side [64]. Some patients raise their arm very slowly as compared with controls, then spatial and temporal muscle activation becomes more variable and the timing of postural muscle activity changes. Some muscles with normal early activity before rapid movement show no measurable activity during slower movement [32,23]. One explanation for this observation is that lesions of the CNS decrease APAs, especially for the paretic lower limb [32,6]. Hemiplegic patients avoid excessive use of the muscles in the paretic lower limb even when the task requires it [64]. Indeed, healthy subjects with postural instability show attenuated APAs. The reduced speed of self-initiated arm movements in hemiparetic patients as compared with controls could be a compensatory strategy to decrease intrinsic perturbations of posture [32,23]. Considering that APAs represent preprogrammed activity due to the central initiation of the motor command, the contralateral supplementary motor area is involved [68]. Chang et al. showed that a unique premotor cortex lesion impairs APAs of both the contralateral and ipsilateral lower limbs during stepping [6].
Extrinsic perturbation Investigation of feedback systems typically involves comparison of physiological or biomechanical responses to externally applied perturbations or manipulations of the sensory environment. To study feedback control, some dynamic platforms produce a rhythmic oscillatory
destabilization, and others produce a single unpredictable destabilization. Phasic disturbance. Hocherman et al. studied postural reactions to disturbances imposed by reciprocal movement of an oscillatory platform [29]. The posture of hemiplegic patients differed from the reactions of controls by longer tonic and periodic activation of the gastrocnemius or tibialis anterior muscles. With oscillatory movements of the platform, both muscles often showed co-contractions without synchronization [29,17]. The periodic muscular contractions in hemiplegic patients could be due to abnormal postural strategies such as fixation of the ankles rather than oscillatory contraction of ankle muscle groups [29] or spasticity. Postural reactions after perturbation. After stroke, patients poorly tolerate unexpected external perturbation in an upright position and during walking [38], in particular in the frontal plane toward the paretic side [30]. Platform translations are used to study postural reactions. They provoke a coordinated activation of ankles, hips and trunk muscles [48,49]. During rotational (toe up/down) and horizontal perturbations (fore and back) in the sagittal direction, two distinct muscle responses are observed: • an initial long-latency response (LLR) of the muscles lengthened by perturbation; • a subsequent antagonist response (AR) in the opposing muscles passively shortened by the movement stimulus [16]. The pattern observed is classically a coordinated muscle synergy, with distal to proximal activation and intralimb coupling. This efficient postural response maintains upright stability following a platform translation. Temporal level. After stroke, postural reflexes show delayed, temporally disrupted and weakened short-latency [16] as well as medium — and long — latency leg-muscle responses on the paretic side when reacting to movements of the support surface [29,16]. The same pattern is observed during simultaneous bilateral [16] and unilateral lower-limb perturbations during standing [19]. The delayed inter-limb coupling between the two lower limbs prevails in the distal portion of the paretic limb with the AR, which is shifted later in time as compared with the non-paretic extremity. The delayed paretic-muscle onset latencies combined with impaired modulation of ankle dorsiflexor postural reflexes may contribute to the instability and frequent falls observed after stroke [43]. Spatial level. The activation pattern of muscle could be altered in hemiplegic patients. The rapid motor-response pattern is not consistently graded or sequential [19]. Simultaneous activation of proximal and distal muscles during the initial response and the AR demonstrates a loss of fine motor coordination in both paretic and non-paretic lower extremities. Horak hypothesized that the coactivation was due to the integrity of the polysynaptic spinal reflexes dependent on the supraspinal control [32]. In spastic paresis, this control is impaired, firstly lacking inhibition of monosynaptic stretch reflexes followed by reduced facilitation of polysynaptic spinal reflexes [32,2]. This observation raises the question of the muscle co-contraction mechanism, which is explained in part by the spasticity but also by an ‘‘in mass’’ strategy (cf. below).
Please cite this article in press as: Tasseel-Ponche S, et al. Motor strategies of postural control after hemispheric stroke. Neurophysiologie Clinique/Clinical Neurophysiology (2015), http://dx.doi.org/10.1016/j.neucli.2015.09.003
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Motor strategies of postural control after hemispheric stroke A lack of knee flexion was observed among faller patients during platform translation [43]. In contrast, the large knee flexion observed among non-fallers may have facilitated their recovery response. Thus, differences in the latency of postural reflexes and the resulting changes in kinematics among faller patients contributed to the large number of fall episodes in this group. During standing, hemiparetic patients fall more frequently when the trunk has a faster backward displacement at the end of the platform translation. Altered muscle reflexes result in a recoil of the trunk further behind the ankle axis [43]. Useful compensatory reaction?. Excessive support on the non-paretic lower limb. Excessive support on the non-paretic lower limb could stabilize posture in reaction to movements of the support surface. Coupling strategy of agonist and antagonist muscles. Coactivation of distal and proximal synergist muscles (intralimb coupling of triceps — quadriceps or gastrocnemius — hamstrings) is more frequent in the paretic lower limb of hemiplegic patients than controls [43]. The increased incidence of distal—proximal coactivation during the AR for within-limb synergy in vascular hemiplegic patients also parallels similar findings of synergistic coactivation in patients with cerebral palsy lesions [49]. Lower-limb synergistic coactivation could be considered a mechanism to increase postural stability because of the additional recruitment [18]. However, in response to forward platform translations, paretic and non-paretic intralimb coupling durations are longer for faller than non-faller patients [43]. The activation of the antagonist response (AR) is frequently activated earlier with respect to the initial long-latency response (LLR). This brief within-limb LLR-AR separation seen in both lower limbs of hemiplegic patients creates excessive stabilization of the lower extremities by contracting agonists and antagonists together. A cerebral lesion increases the likelihood of competing muscle contraction, which renders the lower limb rigid or excessively stable [49]. Hip strategy. A hip strategy, defined by a hip flexion in response to an external destabilization, can be observed [31,61]. After sideways-induced sway, the pattern of muscle activity is modified during standing to compensate for the hemiparesis [69]. Healthy adductors are recruited early and with greater amplitude than in normal controls. This hip strategy compensates for the weak and delayed response of the hemiparetic muscles [36]. Kirker et al. described 4 different hip muscular activations; patterns 1 and 2 could reveal compensatory adductor activity of the non-paretic lower limb and patterns 3 and 4 could reveal physiological recovery in response to standardized sideways perturbations. Stepping responses. A stepping response strategy is defined by the ability to make fast and multidirectional stepping responses to unexpected perturbations [39]. In the absence of external support to the trunk or the arms, the posture-control system may no longer be able to rely on reactive postural adjustments to keep the CoG within the limits of the base of support. Instead, the system may need to execute a stepping response to adjust the base of support to the movement of the CoG to prevent a fall [39,46]. In hemiparetic patients, the step would be executed
5 predominantly with the non-paretic limb [41]. However, the initiation of paretic hip muscles while taking a voluntary step is relatively preserved in patients with chronic stroke as compared to the same muscle activity during automatic equilibrium reactions of a compensatory stepping response [36].
Conclusion Post-stroke patients show many changes in motor strategies for postural control, mainly body weight asymmetry, delayed and reduced anticipatory postural adjustments, synergistic muscle coactivation and abnormal postural tilt. Most of the changes are due to an impaired CNS, but some could be considered adaptive comportments. The consequences for rehabilitation are important and the topic needs further study for developing customized programs based on an understanding of the motor comportment for a given subject. The important link between these disorders and cognitive impairments (visuospatial analysis, perception of verticality, use of sensory information, attention, etc.) deserves another specific review.
Disclosure of interest The authors declare that they have no competing interest.
References [1] Barra J, Chauvineau V, Ohlmann T, Gresty M, Perennou D. Perception of longitudinal body axis in patients with stroke: a pilot study. J Neurol Neurosurg Psychiatry 2007;78:43—8. [2] Berger W, Horstmann GA, Dietz V. Spastic paresis: impaired spinal reflexes and intact motor programs. J Neurol Neurosurg Psychiatry 1988;51:568—71. [3] Bohannon RW, Smith M, Larkin P. Relationship between independent sitting balance and side of hemiparesis. Phys Ther 1986;66:944—5. [4] Bonan IV, Guettard E, Leman MC, Colle FM, Yelnik AP. Subjective visual vertical perception relates to balance in acute stroke. Arch Phys Med Rehabil 2006;87:642—6. [5] Bottaro A, Casadio M, Morasso PG, Sanguineti V. Body sway during quiet standing: is it the residual chattering of an intermittent stabilization process? Hum Mov Sci 2005;24:588—615. [6] Chang WH, Tang PF, Wang YH, Lin KH, Chiu MJ, Chen SH. Role of the premotor cortex in leg selection and anticipatory postural adjustments associated with a rapid stepping task in patients with stroke. Gait Posture 2010;32:487—93. [7] Cheng PT, Liaw MY, Wong MK, Tang FT, Lee MY, Lin PS. The sitto-stand movement in stroke patients and its correlation with falling. Arch Phys Med Rehabil 1998;79:1043—6. [8] Chu VW, Hornby TG, Schmit BD. Perception of lower extremity loads in stroke survivors. Clin Neurophysiol 2015;126:372—81. [9] Collins JJ, DeLuca CJ. Open loop and closed-loop control of posture: a random-walk analysis of center of pressure trajectories. Exp Brain Res 1993;95:308—18. [10] Davenport RJ, Dennis MS, Wellwood I, Warlow CP. Complications after acute stroke. Stroke 1996;27:415—20. [11] De Haart M, Geurts AC, Huidekoper SC, Fasotti L, van Limbeek J. Recovery of standing balance in postacute stroke patients: a rehabilitation cohort study. Arch Phys Med Rehabil 2004;85:886—95.
Please cite this article in press as: Tasseel-Ponche S, et al. Motor strategies of postural control after hemispheric stroke. Neurophysiologie Clinique/Clinical Neurophysiology (2015), http://dx.doi.org/10.1016/j.neucli.2015.09.003
+Model NEUCLI-2489; No. of Pages 7
ARTICLE IN PRESS
6
S. Tasseel-Ponche et al.
[12] De Peretti C, Grimaud O, Tuppin P, Chin F, Woimant F. Prévalence des AVC et de leurs séquelles et impact sur les activités de la vie quotidienne : apport des enquêtes déclaratives Handicap-santé-ménages et Handicap-santé-institution 2008—09. Bull Epidemiol Hebd (Paris) 2012:1. [13] De Sèze M, Wiart L, Bon-Saint-Côme A, Debelleix X, Joseph PA, Mazaux JM, et al. Rehabilitation of postural disturbances of hemiplegic patients by using trunk control retraining during exploratory exercises. Arch Phys Med Rehabil 2001;82:793—800. [14] Dean CM, Shepherd RB. Task-related training improves performance of seated reaching tasks after stroke. A randomized controlled trial. Stroke 1997;28:722—8. [15] Dettmann MA, Linder MT, Sepic SB. Relationships among walking performance, postural stability and functional assessments of the hemiplegic patient. Am J Phys Med 1987;66:77—90. [16] Di Fabio RP. Lower extremity antagonist muscle response following standing perturbation in subjects with cerebrovascular disease. Brain Res 1987;405:43—51. [17] Dickstein R, Hocherman S, Dannenbaum E, Pillar T. Responses of ankle musculature of healthy subjects and hemiplegic patients to sinusoidal anterior-posterior movements of the base of support. J Mot Behav 1989;21:99—112. [18] Diener HC, Bacher M, Guschlbauer B, Thomas C, Dichgans J. The coordination of posture and voluntary movement in patients with hemiparesis. J Neurol 1993;240:161—7. [19] Dietz V, Berger W. Interlimb coordination of posture in patients with spastic paresis. Brain 1984;107:965—78. [20] Eng JJ, Chu KS. Reliability and comparison of weight-bearing ability during standing tasks for individuals with chronic stroke. Arch Phys Med Rehabil 2002;83:1138—44. [21] Engardt M, Olsson E. Body weight-bearing while rising and sitting down in patients with stroke. Scand J Rehabil Med 1992;24:67—74. [22] Franchignoni FP, Tesio L, Ricupero C, Martino MT. Trunk control test as an early predictor of stroke rehabilitation outcome. Stroke 1997;28:1382—5. [23] Garland SJ, Stevenson TJ, Ivanova T. Postural responses to unilateral arm perturbation in young, elderly, and hemiplegic subjects. Arch Phys Med Rehabil 1997;78:1072—7. [24] Genthon N, Rougier P, Gissot AS, Froger J, Pélissier J, Perennou D. Contribution of each lower limb to upright standing in stroke patients. Stroke 2008;39:1793—9. [25] Geurts AC, de Haart M, van Nes IJ, Duysens J. A review of standing balance recovery from stroke. Gait Posture 2005;22:267—81. [26] Goldie PA, Matyas TA, Spencer KI, McGinley RB. Postural control in standing following stroke: test-retest reliability of some quantitative clinical tests. Phys Ther 1990;70: 234—43. [27] Goldie PA, Matyas TA, Evans OM, Galea M, Bach TM. Maximum voluntary weight-bearing by the affected and unaffected legs in standing following stroke. Clin Biomech (Bristol, Avon) 1996;11:333—42. [28] Hesse S, Schauer M, Petersen M, Jahnke M. Sit-to-stand manoeuvre in hemiparetic patients before and after a 4-week rehabilitation programme. Scand J Rehabil Med 1998;30:81—6. [29] Hocherman S, Dickstein R, Hirschbiene A, Pillar T. Postural responses of normal geriatric and hemiplegic patients to a continuing perturbation. Exp Neurol 1988;99:388—402. [30] Holt RR, Simpson D, Jenner JR, Kirker SGB, Wing AM. Ground reaction force after a sideways push as a measure of balance in recovery from stroke. Clin Rehabil 2000;14:88—95. [31] Horak FB, Nashner LM. Central programming of postural movements: adaptation to altered support-surface configurations. J Neurophysiol 1986;55:1369—81. [32] Horak FB, Esselman P, Anderson ME, Lynch MK. The effects of movement velocity, mass displaced, and task certainty on
[33] [34]
[35]
[36]
[37]
[38]
[39]
[40]
[41]
[42]
[43]
[44]
[45]
[46]
[47]
[48] [49]
[50] [51] [52]
[53]
[54]
associated postural adjustments made by normal and hemiplegic individuals. J Neurol Neurosurg Psychiatry 1984;47:1020—8. Karnath HO, Broetz D. Understanding and treating ‘‘pusher syndrome’’. Phys Ther 2003;83:1119—25. Karnath HO, Ferber S, Dichgans J. The origin of contraversive pushing: evidence for a second graviceptive system in humans. Neurology 2000;55:1298—304. Kirker SG, Simpson DS, Jenner JR, Wing AM. Stepping before standing: hip muscle function in stepping and standing balance after stroke. J Neurol Neurosurg Psychiatry 2000;68:458—64. Kirker SG, Jenner JR, Simpson DS, Wing AM. Changing patterns of postural hip muscle activity during recovery from stroke. Clin Rehabil 2000;14:618—26. Lamb SE, Ferrucci L, Volapto S, Fried LP, Guralnik JM. Study risk factors for falling in home-dwelling older women with stroke: the Women’s Health and Aging Study. Stroke 2003;34:494—501. Lee WA, Derning L, Sahgal V. Quantitative and clinical measures of static standing balance in hemiparetic and normal subjects. Phys Ther 1988;68:970—6. Maki BE, McIlroy WE. The role of limb movements in maintaining upright stance: the ‘‘change-in-support’’ strategy. Phys Ther 1997;77:488—507. Maki BE, Holliday PJ, Topper AK. A prospective study of postural balance and risk of falling in an ambulatory and independent elderly population. J Gerontol 1994;49:72—84. Mansfield A, Inness EL, Lakhani B, McIlroy WE. Determinants of limb preference for initiating compensatory stepping poststroke. Arch Phys Med Rehabil 2012;93:1179—84. Mansfield A, Danells CJ, Zettel JL, Black SE, McIlroy WE. Determinants and consequences for standing balance of spontaneous weight-bearing on the paretic side among individuals with chronic stroke. Gait Posture 2013;38:428—32. Marigold DS, Eng JJ. Altered timing of postural reflexes contributes to falling in persons with chronic stroke. Exp Brain Res 2006;171:459—68. Massion J, Ioffe M, Schmitz C, Viallet F, Gantcheva R. Acquisition of anticipatory postural adjustments in a bimanual load-lifting task: normal and pathological aspects. Exp Brain Res 1999;128:229—35. Massion J, Alexandrov A, Frolov A. Why and how are posture and movement coordinated? Prog Brain Res 2004;143: 13—27. McIlroy WE, Maki BE. Preferred placement of the feet during quiet stance: development of a standardized foot placement for balance testing. Clin Biomech 1997;12:66—70. Nardone A, Godi M, Grasso M, Guglielmetti S, Schieppati M. Stabilometry is a predictor of gait performance in chronic hemiparetic stroke patients. Gait Posture 2009;30:5—10. Nashner LM. Analysis of movement control in man using the movable platform. Adv Neurol 1983;39:607—19. Nashner LM, Shumway-Cook A, Marin O. Stance posture control in select groups of children with cerebral palsy: deficits in sensory organization and muscular coordination. Exp Brain Res 1983;49:393—409. Paillex R, So A. Changes in the standing posture of stroke patients during rehabilitation. Gait Posture 2005;21:403—9. Perennou D. Weight bearing asymmetry in standing hemiparetic patients. J Neurol Neurosurg Psychiatry 2005;76:621. Pérennou DA, Amblard B, Leblond C, Pélissier J. Biased postural vertical in humans with hemispheric cerebral lesions. Neurosci Lett 1998;252:75—8. 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;82:440—8. Pérennou DA, Amblard B, Laassel el M, Benaim C, Hérisson C, Pélissier J. Understanding the pusher behavior of some stroke
Please cite this article in press as: Tasseel-Ponche S, et al. Motor strategies of postural control after hemispheric stroke. Neurophysiologie Clinique/Clinical Neurophysiology (2015), http://dx.doi.org/10.1016/j.neucli.2015.09.003
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[55]
[56]
[57]
[58]
[59]
[60]
[61]
[62] [63]
[64]
patients with spatial deficits: a pilot study. Arch Phys Med Rehabil 2002;83:570—5. Pérennou DA, Mazibrada G, Chauvineau V, Greenwood R, Rothwell J, Gresty MA, et al. Lateropulsion, pushing and verticality perception in hemisphere stroke: a causal relationship? Brain 2008;131:2401—13. Persson CU, Hansson PO, Sunnerhagen KS. Clinical tests performed in acute stroke identify the risk of falling during the first year: postural stroke study in Gothenburg (POSTGOT). J Rehabil Med 2011;43:348—53. Rode G, Tiliket C, Boisson D. Predominance of postural imbalance in left hemiparetic patients. Scand J Rehabil Med 1997;29:11—6. Rode G, Tiliket C, Charlopain P, et al. Postural asymmetry reduction by vestibular caloric stimulation in left hemiparetic patients. Scand J Rehabil Med 1998;30:9—14. Roerdink M, De Haart M, Daffertshofer A, Donker SF, Geurts AC, Beek PJ. Dynamical structure of center-of-pressure trajectories in patients recovering from stroke. Exp Brain Res 2006;174:256—69. Roerdink M, Geurts AC, de Haart M, Beek PJ. On the relative contribution of the paretic leg to the control of posture after stroke. Neurorehabil Neural Repair 2009;23:267—74. Runge CF, Shupert CL, Horak FB, Zajac FE. Ankle and hip postural strategies defined by joint torques. Gait Posture 1999;10:161—70. Sackley CM. Falls, sway, and symmetry of weight-bearing after stroke. Int Disabil Stud 1991;13:1—4. Schmid AA, Van Puymbroeck M, Altenburger PA, Miller KK, Combs SA, Page SJ. Balance is associated with quality of life in chronic stroke. Top Stroke Rehabil 2013;20:340—6. Slijper H, Latash ML, Rao N, Aruin AS. Task-specific modulation of anticipatory postural adjustments in individuals with hemiparesis. Clin Neurophysiol 2002;113:642—55.
7 [65] Spinazzola L, Cubelli R, Della Sala S. Impairments of trunk movements following left or right hemisphere lesions: dissociation between apraxic errors and postural instability. Brain 2003;126:2656—66. [66] Tilikete C, Rode G, Nighoghossian N, Boisson D, Vighetto A. Otolith manifestations in Wallenberg syndrome. Rev Neurol 2001;157:198—208. [67] Turnbull GI, Charteris J, Wall JC. Deficiencies in standing weight shifts by ambulant hemiplegic subjects. Arch Phys Med Rehabil 1996;77:356—62. [68] Viallet F, Massion J, Massarino R, Khalil R. Coordination between posture and movement in a bimanual load lifting task: putative role of a medial frontal region including the supplementary area. Exp Brain Res 1992;88:674—84. [69] Wing AM, Goodrich S, Virji-Babul N, Jenner JR, Clapp S. Balance evaluation in hemiparetic stroke patients using lateral forces applied to the hip. Arch Phys Med Rehabil 1993;74: 292—9. [70] Winstein CJ, Gardner ER, McNeal DR, Barto PS, Nicholson DE. Standing balance training: effect on balance and locomotion in hemiparetic adults. Arch Phys Med Rehabil 1989;70: 755—62. [71] Yanohara R, Teranishi T, Tomita Y, Tanino G, Ueno Y, Sonoda S. Recovery process of standing postural control in hemiplegia after stroke. J Phys Ther Sci 2014;26: 1761—5. [72] Yelnik AP, Kassouha A, Bonan IV, Leman MC, Jacq C, Vicaut E, et al. Postural visual dependence after recent stroke: assessment by optokinetic stimulation. Gait Posture 2006;24: 262—9. [73] Yelnik AP, Le Breton F, Colle FM, Bonan IV, Hugeron C, Egal V, et al. Rehabilitation of balance after stroke with multisensorial training: a single-blind randomized controlled study. Neurorehabil Neural Repair 2008;22:468—76.
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Motor strategies of postural control after hemispheric stroke Stratégies motrices du contrôle postural après AVC hémisphérique S. Tasseel-Ponche a,∗, A.P. Yelnik b,c, I.V. Bonan d a
Service de médecine physique et de réadaptation, université Picardie-Jules-Verne, CHU d’Amiens, avenue René-Laënnec, Salouel, 80054 Amiens cedex 1, France b Service de médecine physique et de réadaptation, université Paris-Diderot, groupe hospitalier Saint-Louis-Lariboisière-F. Widal, AP—HP, 200, rue du Faubourg-Saint-Denis, 75010 Paris, France c COGNAC G (COGNition and Action Group), université Paris-Descartes, CNRS, UMR 8257, 45, rue des Saints-Pères, 75270 Paris cedex 06, France d Service de médecine physique et de réadaptation, université de Rennes 1, 2, rue Henri-Le-Guilloux, 35000 Rennes, France Received 5 September 2015; accepted 7 September 2015
KEYWORDS Stroke; Posture; Strategies; Balance; Standing; Rehabilitation; Adaptation
∗
Summary After stroke, the causes of balance disorders include motor disorders, sensory loss, perceptual deficits and altered spatial cognition. This review focuses on motor strategies for postural control after stroke. Weight-bearing asymmetry, smaller surface of stability, increased sway, body tilting and sometimes pushing syndrome are observed. Weakness and sensory impairments account only for some of these disturbances; altered postural reactions and anticipated postural adjustments as well as abnormal synergistic muscular activation play an important part. These disorders are often linked to cognitive impairments (visuospatial analysis, perception of verticality, use of sensory information, attention, etc.), which explain the preeminent disorders of postural control seen with right rather than left-hemisphere lesions. Most of the motor changes are due to an impaired central nervous system but some could be considered adaptive behaviors. These changes have consequences for rehabilitation and need further studies for building customized programs based on the motor comportment of a given patient. © 2015 Elsevier Masson SAS. All rights reserved.
Corresponding author. E-mail address: [email protected] (S. Tasseel-Ponche).
http://dx.doi.org/10.1016/j.neucli.2015.09.003 0987-7053/© 2015 Elsevier Masson SAS. All rights reserved.
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MOTS CLÉS AVC ; Posture ; Stratégies ; Équilibre ; Debout ; Adaptation ; Rééducation
Résumé Les troubles de la posture et de l’équilibre résultent de déficiences sensorimotrices, de troubles perceptifs sensoriels et/ou d’altération de la cognition spatiale. Cette revue de la littérature se focalise sur les stratégies motrices du contrôle postural après accident vasculaire cérébral (AVC). La diminution de la surface de la stabilité, l’asymétrie d’appui entre les deux membres inférieurs, les oscillations posturales et l’inclinaison posturale voire le « Pusher syndrome » peuvent être observés chez ces patients. Le déficit hémicorporel sensitivomoteur n’explique qu’en partie les troubles de la posture assise et debout. L’altération des stratégies posturales, des ajustements posturaux anticipés et les coactivations musculaires synergiques y participent aussi. De plus il existe des interactions entre ces stratégies motrices et les troubles de la cognition spatiale (négligence visuospatiale, bais de perception de la verticalité, préférences sensorielles, troubles attentionnels. . .). Les mécanismes des troubles posturaux prédominent chez les sujets avec lésion hémisphérique droite du fait d’une prédominance de celui-ci dans le contrôle spatial. La majorité des stratégies motrices posturales observées après un AVC sont secondaires à l’atteinte des réseaux neuronaux du système nerveux central mais certaines peuvent aussi être considérées comme des comportements adaptatifs. Comprendre les stratégies motrices d’un sujet donné est primordial pour construire des programmes de rééducation posturale personnalisés. © 2015 Elsevier Masson SAS. Tous droits réservés.
Introduction Postural control is the ability to control posture in order to maintain an upright stance during functional activities and to compensate for external and internal body perturbations to avoid falls. Impaired balance was found to be a predictor of falls in community-dwelling older women after stroke [37]. Balance and postural disorders are among the most prevalent consequences, affecting 50% of post-stroke patients in France [12]. They are responsible for medical and surgical complications due to falls, social isolation and impaired quality of life [10,63]. Rapid and optimal improvement of postural control in stroke patients is essential to ensure their independence, social participation and overall health. The mechanisms of post-stroke balance disorders are diverse [25,56]. This postural disturbance may involve motor weakness, asymmetrical muscular tone, sensory loss, perceptual deficits and altered spatial cognition with reference to the postural body scheme. However, compensation strategies to stabilize posture could be developed. After stroke, the postural control would be more sensory-driven rather than anticipatory [29] because the anticipatory mechanism involves many cerebral structures: cortical (supplementary motor area and premotor area), subcortical (central gray nuclei and thalamus) and subtentorial (vestibular nuclei and cerebellum) [45]. Different postural strategies could be controlled by the central nervous system (CNS) to coordinate muscle activity against destabilizing forces applied to the body (extrinsic destabilization) or with self-induced movements (intrinsic destabilization). This review focuses on studies of post-stroke motor strategies involved in the recovery of postural control during both quiet standing balance control and dynamic conditions.
Sitting posture Impaired sitting posture is by itself a major cause of dependency because trunk control is required for the control of
more complex activities such as voluntary movements of the upper limb or standing posture or gait [22]. After stroke, the automatic axial muscle tonus and voluntary strength of the trunk are bilaterally impaired, most prominently on the paretic side [3]. Besides the paresis, other components in trunk control may be impaired, depending on the side of the lesion: ‘‘postural instability’’ would be significantly more frequent among patients with right-hemisphere lesions, and ‘‘apraxic responses’’ would be predominant among those with left-hemisphere lesions [3,65]. Indeed, the voluntary trunk control involves cognitive functions such as visuospatial exploration and mental representation ability for postural adaptation and the construction of the postural body schema [57,13]. Hemineglect and bias of the subjective vertical are important causes of postural asymmetry and instability [57,58,52,34,54,4]. Contraversive pushing, called ‘‘Pusher syndrome,’’ is the most serious postural impairment [55]. It is a perceptual disorder observed with acute stroke, whereby patients lean towards the affected side and actively resist any attempt to correct this posture [33]. Pushing has been linked to biased verticality and hemispatial neglect, more common among patients with right — rather than left-hemisphere lesions [55].
Quiet standing balance control Quiet standing postural control requires maintaining the center of gravity (CoG) within limits of stability. Center of pressure (CoP) measures are commonly used to assess this control by measuring the body position and the amount of body sway. After stroke, stabilometry is used to assess a surface of stability, which is smaller than for healthy subjects, beyond which the CoG cannot move without exposing the hemiparetic patient to loss of balance [51]. Weight-bearing asymmetry (WBA) The quiet standing posture of hemiplegic patients after stroke is characterized by WBA, a shift in the mean position of the CoP toward the unaffected side and increased
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Motor strategies of postural control after hemispheric stroke body sway as compared with age-matched healthy people. WBA is very common, predominant with right-hemisphere lesions [58,51]. However, the shift toward the non-paretic lower limb is not systematic. Mansfield et al. studied the prevalence of stance asymmetry 1 year after stroke: 48% of patients were asymmetric, favoring the non-paretic lower limb; 12% favored the paretic lower limb; and 40% were symmetric [42]. Hence, the behavior favoring the paretic lower limb is unusual and could reflect a strategy learned during rehabilitation to favor the paretic lower limb or may represent a pre-planned strategy to permit a rapid compensatory step with the non-paretic limb in the event of instability. WBA diminishes considerably during the 4 first weeks after stroke. A substantial degree of WBA persists during the eighth week and increases during attention-demanding arithmetic tasks, such that weight-bearing symmetry can never become fully automated [11]. The paresis after stroke explains in part the coordination difficulties of each body segment with WBA. Patients with severe motor impairments of the paretic lower limb seem to use this strategy more systematically than do less severely impaired patients [60]. The CoP could shift towards the non-paretic side during standing to minimize instability due to unilateral lower limb impairment [60,59,24]. Sway is greater when loading the paretic than non-paretic lower limb during quiet standing [62]. Sensitivity impairment is another major cause of WBA, as we have observed in our daily clinical practice, although studies devoted to this issue are surprisingly few [60,8]. The abnormal CoP displacement under the paretic lower limb, recorded with a dual-force platform, reflects impaired stabilization control of the paretic lower limb. Patients seem to be constrained in developing an adaptive strategy with greater involvement of the non-paretic lower limb. However, the non-paretic lower limb alone seems unable to compensate for the postural impairment [24]. WBA has also been related to neglect and more generally spatial cognition disturbances [58,52,54,4,53]. Postural control is organized on the basis of internal models that closely deal with the body scheme. Distortions in the coordinates used to distribute the body weight over the two lower limbs during standing could be disrupted, especially with right-hemisphere lesions. The right hemisphere is indeed devoted to spatial processing and is the site of processing for multisensory integration. The right-hemisphere lesion that induces a pronounced disruption in the processing of spatial information is also likely to impair the internal representation of the body in space and, consequently, postural control [57]. A contralesional rotation in the representation of the longitudinal axis could also be involved in the WBA [1] as well as misrepresentation of the midsagittal plane [52,66]. The crucial role of the right hemisphere would thus account for the lateral CoP deviation in such patients [57,51]. The degree of WBA during quiet standing has been associated with the level of independent self-care and length of hospital stay [62]. WBA is strongly related to several gait variables such as gait velocity, cadence, and duration of a single support phase, as if the degree of asymmetry of weight distribution is maintained during gait [47]. However, WBA may not be the main target of rehabilitation programs aimed at restoring standing balance after stroke, especially in patients with the most motor impairment [60,24]. The
3 compensatory role of the non-paretic lower limb should be accepted and the balance rehabilitation program should focus on intensive destabilizing exercises, rather than the quality of the posture and movement during gait, specifically for the most-impaired patients [73]. More than asymmetry of the body weight, tilt and instability should be a concern. The same disorders with standing are seen with sitting and can disrupt balance, especially among pushers [55,33]. Bias of verticality and spatial cognition disorders are often associated with sensorimotor impairments that disrupt standing posture [4,55]. Body sway After stroke, the amplitude of body sway is increased, in particular in the frontal plane [11,50]. With body instability, significant improvement, particularly in the frontal plane, requires more time than with WBA [71]; the condition is negatively associated with gait velocity and is related to risk of falling [62]. In addition, postural sway can distinguish between fallers and non-fallers in community-dwelling older adults [40]. Nevertheless, an increase in sway for some patients could be, at least in part, a necessary comportment to increase sensory feedback [9,5,72].
Postural strategies for maintaining standing posture in dynamic conditions Deviations from a set position are regulated by postural adjustments relying on both feedback, with extrinsic perturbation, and a feedforward control mechanism when the movement can be anticipated for intrinsic perturbations. Intrinsic perturbations During self-initiated movements, internal perturbations must be counteracted automatically to maintain balance by anticipated postural adjustments. Weight-shifting ability. The ability to execute a selfgenerated weight shift within the base of support without adjusting the foot position is crucial, notably in the frontal plane, when rising from a chair, transferring, walking, turning or stair climbing. When leaning the body as far as possible in a specific direction, stroke patients have difficulties in all planes but mostly in the direction of the paretic lower limb [15,26,67]. Voluntary weight shifting to one limb while standing [27] or during dynamic tasks such as rising from a chair [21,28,7] is compromised after stroke. During voluntary displacements, patients use only part of their base of support [35]. Weight-shifting ability during different dynamic tasks is correlated [20]. Poor weight-bearing ability may result from an impaired concentric knee muscle component specific to the task of rising [20]. Interestingly, although subjects can shift more than half of their body weight onto the paretic limb during a voluntary weight shift in any direction, they spontaneously bear less than half of their body weight on the paretic limb during the static task of standing or the dynamic task of rising from a chair. The ability to transfer body weight laterally or forward onto the paretic lower limb while standing is indicative of walking performance [15]; this impaired ability contributes to falls after stroke [7]. Weight-bearing ability can be
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improved with rehabilitation [11], with positive impact on rising from a chair and bilateral standing symmetry [70,14]. Limits of stability (LoS). In standing posture, LoS are defined when the CoP displaces voluntarily to the outer limits of the base of support. Post-stroke patients have greater difficulty than control subjects in displacing the CoP in both the forward and backward directions [27]. However, in our experience, the limits of stability do not reflect the efficiency of balance control but rather the fear of falling and the mental representation relating to supposed balance performance [73]. This situation is especially true for post-stroke patients: besides the possible difficulty in understanding the task, the hip strategy post-stroke patients often use reduces the displacement of the CoP; moreover, neglect patients often show larger limits of stability despite a greater risk of falling. Anticipatory postural adjustments (APAs). APAs are muscular responses to stabilize posture before movement. Preparatory muscle activity serves to compensate for the disturbing forces due to displacements by sequential activations [32,6]. The failure to coordinate postural muscle adjustments may contribute to the instability of patients with hemiparesis [32,23]. After stroke, the ability to perform adequate APAs is related to good balance performance, assessed by the Berg Balance Scale [23], and the acquisition of APAs associated with a newly learned task is impaired [44]. When normal subjects raise their right arm, left paraspinal and right biceps femoris activity is usually initiated before right deltoid activity. In hemiparetic patients, the sequence of hip, back, and shoulder muscle activation is the same as in control subjects when the speed of arm movement is similar, but muscle activation is delayed and reduced, particularly on the paretic side [64]. Some patients raise their arm very slowly as compared with controls, then spatial and temporal muscle activation becomes more variable and the timing of postural muscle activity changes. Some muscles with normal early activity before rapid movement show no measurable activity during slower movement [32,23]. One explanation for this observation is that lesions of the CNS decrease APAs, especially for the paretic lower limb [32,6]. Hemiplegic patients avoid excessive use of the muscles in the paretic lower limb even when the task requires it [64]. Indeed, healthy subjects with postural instability show attenuated APAs. The reduced speed of self-initiated arm movements in hemiparetic patients as compared with controls could be a compensatory strategy to decrease intrinsic perturbations of posture [32,23]. Considering that APAs represent preprogrammed activity due to the central initiation of the motor command, the contralateral supplementary motor area is involved [68]. Chang et al. showed that a unique premotor cortex lesion impairs APAs of both the contralateral and ipsilateral lower limbs during stepping [6].
Extrinsic perturbation Investigation of feedback systems typically involves comparison of physiological or biomechanical responses to externally applied perturbations or manipulations of the sensory environment. To study feedback control, some dynamic platforms produce a rhythmic oscillatory
destabilization, and others produce a single unpredictable destabilization. Phasic disturbance. Hocherman et al. studied postural reactions to disturbances imposed by reciprocal movement of an oscillatory platform [29]. The posture of hemiplegic patients differed from the reactions of controls by longer tonic and periodic activation of the gastrocnemius or tibialis anterior muscles. With oscillatory movements of the platform, both muscles often showed co-contractions without synchronization [29,17]. The periodic muscular contractions in hemiplegic patients could be due to abnormal postural strategies such as fixation of the ankles rather than oscillatory contraction of ankle muscle groups [29] or spasticity. Postural reactions after perturbation. After stroke, patients poorly tolerate unexpected external perturbation in an upright position and during walking [38], in particular in the frontal plane toward the paretic side [30]. Platform translations are used to study postural reactions. They provoke a coordinated activation of ankles, hips and trunk muscles [48,49]. During rotational (toe up/down) and horizontal perturbations (fore and back) in the sagittal direction, two distinct muscle responses are observed: • an initial long-latency response (LLR) of the muscles lengthened by perturbation; • a subsequent antagonist response (AR) in the opposing muscles passively shortened by the movement stimulus [16]. The pattern observed is classically a coordinated muscle synergy, with distal to proximal activation and intralimb coupling. This efficient postural response maintains upright stability following a platform translation. Temporal level. After stroke, postural reflexes show delayed, temporally disrupted and weakened short-latency [16] as well as medium — and long — latency leg-muscle responses on the paretic side when reacting to movements of the support surface [29,16]. The same pattern is observed during simultaneous bilateral [16] and unilateral lower-limb perturbations during standing [19]. The delayed inter-limb coupling between the two lower limbs prevails in the distal portion of the paretic limb with the AR, which is shifted later in time as compared with the non-paretic extremity. The delayed paretic-muscle onset latencies combined with impaired modulation of ankle dorsiflexor postural reflexes may contribute to the instability and frequent falls observed after stroke [43]. Spatial level. The activation pattern of muscle could be altered in hemiplegic patients. The rapid motor-response pattern is not consistently graded or sequential [19]. Simultaneous activation of proximal and distal muscles during the initial response and the AR demonstrates a loss of fine motor coordination in both paretic and non-paretic lower extremities. Horak hypothesized that the coactivation was due to the integrity of the polysynaptic spinal reflexes dependent on the supraspinal control [32]. In spastic paresis, this control is impaired, firstly lacking inhibition of monosynaptic stretch reflexes followed by reduced facilitation of polysynaptic spinal reflexes [32,2]. This observation raises the question of the muscle co-contraction mechanism, which is explained in part by the spasticity but also by an ‘‘in mass’’ strategy (cf. below).
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Motor strategies of postural control after hemispheric stroke A lack of knee flexion was observed among faller patients during platform translation [43]. In contrast, the large knee flexion observed among non-fallers may have facilitated their recovery response. Thus, differences in the latency of postural reflexes and the resulting changes in kinematics among faller patients contributed to the large number of fall episodes in this group. During standing, hemiparetic patients fall more frequently when the trunk has a faster backward displacement at the end of the platform translation. Altered muscle reflexes result in a recoil of the trunk further behind the ankle axis [43]. Useful compensatory reaction?. Excessive support on the non-paretic lower limb. Excessive support on the non-paretic lower limb could stabilize posture in reaction to movements of the support surface. Coupling strategy of agonist and antagonist muscles. Coactivation of distal and proximal synergist muscles (intralimb coupling of triceps — quadriceps or gastrocnemius — hamstrings) is more frequent in the paretic lower limb of hemiplegic patients than controls [43]. The increased incidence of distal—proximal coactivation during the AR for within-limb synergy in vascular hemiplegic patients also parallels similar findings of synergistic coactivation in patients with cerebral palsy lesions [49]. Lower-limb synergistic coactivation could be considered a mechanism to increase postural stability because of the additional recruitment [18]. However, in response to forward platform translations, paretic and non-paretic intralimb coupling durations are longer for faller than non-faller patients [43]. The activation of the antagonist response (AR) is frequently activated earlier with respect to the initial long-latency response (LLR). This brief within-limb LLR-AR separation seen in both lower limbs of hemiplegic patients creates excessive stabilization of the lower extremities by contracting agonists and antagonists together. A cerebral lesion increases the likelihood of competing muscle contraction, which renders the lower limb rigid or excessively stable [49]. Hip strategy. A hip strategy, defined by a hip flexion in response to an external destabilization, can be observed [31,61]. After sideways-induced sway, the pattern of muscle activity is modified during standing to compensate for the hemiparesis [69]. Healthy adductors are recruited early and with greater amplitude than in normal controls. This hip strategy compensates for the weak and delayed response of the hemiparetic muscles [36]. Kirker et al. described 4 different hip muscular activations; patterns 1 and 2 could reveal compensatory adductor activity of the non-paretic lower limb and patterns 3 and 4 could reveal physiological recovery in response to standardized sideways perturbations. Stepping responses. A stepping response strategy is defined by the ability to make fast and multidirectional stepping responses to unexpected perturbations [39]. In the absence of external support to the trunk or the arms, the posture-control system may no longer be able to rely on reactive postural adjustments to keep the CoG within the limits of the base of support. Instead, the system may need to execute a stepping response to adjust the base of support to the movement of the CoG to prevent a fall [39,46]. In hemiparetic patients, the step would be executed
5 predominantly with the non-paretic limb [41]. However, the initiation of paretic hip muscles while taking a voluntary step is relatively preserved in patients with chronic stroke as compared to the same muscle activity during automatic equilibrium reactions of a compensatory stepping response [36].
Conclusion Post-stroke patients show many changes in motor strategies for postural control, mainly body weight asymmetry, delayed and reduced anticipatory postural adjustments, synergistic muscle coactivation and abnormal postural tilt. Most of the changes are due to an impaired CNS, but some could be considered adaptive comportments. The consequences for rehabilitation are important and the topic needs further study for developing customized programs based on an understanding of the motor comportment for a given subject. The important link between these disorders and cognitive impairments (visuospatial analysis, perception of verticality, use of sensory information, attention, etc.) deserves another specific review.
Disclosure of interest The authors declare that they have no competing interest.
References [1] Barra J, Chauvineau V, Ohlmann T, Gresty M, Perennou D. Perception of longitudinal body axis in patients with stroke: a pilot study. J Neurol Neurosurg Psychiatry 2007;78:43—8. [2] Berger W, Horstmann GA, Dietz V. Spastic paresis: impaired spinal reflexes and intact motor programs. J Neurol Neurosurg Psychiatry 1988;51:568—71. [3] Bohannon RW, Smith M, Larkin P. Relationship between independent sitting balance and side of hemiparesis. Phys Ther 1986;66:944—5. [4] Bonan IV, Guettard E, Leman MC, Colle FM, Yelnik AP. Subjective visual vertical perception relates to balance in acute stroke. Arch Phys Med Rehabil 2006;87:642—6. [5] Bottaro A, Casadio M, Morasso PG, Sanguineti V. Body sway during quiet standing: is it the residual chattering of an intermittent stabilization process? Hum Mov Sci 2005;24:588—615. [6] Chang WH, Tang PF, Wang YH, Lin KH, Chiu MJ, Chen SH. Role of the premotor cortex in leg selection and anticipatory postural adjustments associated with a rapid stepping task in patients with stroke. Gait Posture 2010;32:487—93. [7] Cheng PT, Liaw MY, Wong MK, Tang FT, Lee MY, Lin PS. The sitto-stand movement in stroke patients and its correlation with falling. Arch Phys Med Rehabil 1998;79:1043—6. [8] Chu VW, Hornby TG, Schmit BD. Perception of lower extremity loads in stroke survivors. Clin Neurophysiol 2015;126:372—81. [9] Collins JJ, DeLuca CJ. Open loop and closed-loop control of posture: a random-walk analysis of center of pressure trajectories. Exp Brain Res 1993;95:308—18. [10] Davenport RJ, Dennis MS, Wellwood I, Warlow CP. Complications after acute stroke. Stroke 1996;27:415—20. [11] De Haart M, Geurts AC, Huidekoper SC, Fasotti L, van Limbeek J. Recovery of standing balance in postacute stroke patients: a rehabilitation cohort study. Arch Phys Med Rehabil 2004;85:886—95.
Please cite this article in press as: Tasseel-Ponche S, et al. Motor strategies of postural control after hemispheric stroke. Neurophysiologie Clinique/Clinical Neurophysiology (2015), http://dx.doi.org/10.1016/j.neucli.2015.09.003
+Model NEUCLI-2489; No. of Pages 7
ARTICLE IN PRESS
6
S. Tasseel-Ponche et al.
[12] De Peretti C, Grimaud O, Tuppin P, Chin F, Woimant F. Prévalence des AVC et de leurs séquelles et impact sur les activités de la vie quotidienne : apport des enquêtes déclaratives Handicap-santé-ménages et Handicap-santé-institution 2008—09. Bull Epidemiol Hebd (Paris) 2012:1. [13] De Sèze M, Wiart L, Bon-Saint-Côme A, Debelleix X, Joseph PA, Mazaux JM, et al. Rehabilitation of postural disturbances of hemiplegic patients by using trunk control retraining during exploratory exercises. Arch Phys Med Rehabil 2001;82:793—800. [14] Dean CM, Shepherd RB. Task-related training improves performance of seated reaching tasks after stroke. A randomized controlled trial. Stroke 1997;28:722—8. [15] Dettmann MA, Linder MT, Sepic SB. Relationships among walking performance, postural stability and functional assessments of the hemiplegic patient. Am J Phys Med 1987;66:77—90. [16] Di Fabio RP. Lower extremity antagonist muscle response following standing perturbation in subjects with cerebrovascular disease. Brain Res 1987;405:43—51. [17] Dickstein R, Hocherman S, Dannenbaum E, Pillar T. Responses of ankle musculature of healthy subjects and hemiplegic patients to sinusoidal anterior-posterior movements of the base of support. J Mot Behav 1989;21:99—112. [18] Diener HC, Bacher M, Guschlbauer B, Thomas C, Dichgans J. The coordination of posture and voluntary movement in patients with hemiparesis. J Neurol 1993;240:161—7. [19] Dietz V, Berger W. Interlimb coordination of posture in patients with spastic paresis. Brain 1984;107:965—78. [20] Eng JJ, Chu KS. Reliability and comparison of weight-bearing ability during standing tasks for individuals with chronic stroke. Arch Phys Med Rehabil 2002;83:1138—44. [21] Engardt M, Olsson E. Body weight-bearing while rising and sitting down in patients with stroke. Scand J Rehabil Med 1992;24:67—74. [22] Franchignoni FP, Tesio L, Ricupero C, Martino MT. Trunk control test as an early predictor of stroke rehabilitation outcome. Stroke 1997;28:1382—5. [23] Garland SJ, Stevenson TJ, Ivanova T. Postural responses to unilateral arm perturbation in young, elderly, and hemiplegic subjects. Arch Phys Med Rehabil 1997;78:1072—7. [24] Genthon N, Rougier P, Gissot AS, Froger J, Pélissier J, Perennou D. Contribution of each lower limb to upright standing in stroke patients. Stroke 2008;39:1793—9. [25] Geurts AC, de Haart M, van Nes IJ, Duysens J. A review of standing balance recovery from stroke. Gait Posture 2005;22:267—81. [26] Goldie PA, Matyas TA, Spencer KI, McGinley RB. Postural control in standing following stroke: test-retest reliability of some quantitative clinical tests. Phys Ther 1990;70: 234—43. [27] Goldie PA, Matyas TA, Evans OM, Galea M, Bach TM. Maximum voluntary weight-bearing by the affected and unaffected legs in standing following stroke. Clin Biomech (Bristol, Avon) 1996;11:333—42. [28] Hesse S, Schauer M, Petersen M, Jahnke M. Sit-to-stand manoeuvre in hemiparetic patients before and after a 4-week rehabilitation programme. Scand J Rehabil Med 1998;30:81—6. [29] Hocherman S, Dickstein R, Hirschbiene A, Pillar T. Postural responses of normal geriatric and hemiplegic patients to a continuing perturbation. Exp Neurol 1988;99:388—402. [30] Holt RR, Simpson D, Jenner JR, Kirker SGB, Wing AM. Ground reaction force after a sideways push as a measure of balance in recovery from stroke. Clin Rehabil 2000;14:88—95. [31] Horak FB, Nashner LM. Central programming of postural movements: adaptation to altered support-surface configurations. J Neurophysiol 1986;55:1369—81. [32] Horak FB, Esselman P, Anderson ME, Lynch MK. The effects of movement velocity, mass displaced, and task certainty on
[33] [34]
[35]
[36]
[37]
[38]
[39]
[40]
[41]
[42]
[43]
[44]
[45]
[46]
[47]
[48] [49]
[50] [51] [52]
[53]
[54]
associated postural adjustments made by normal and hemiplegic individuals. J Neurol Neurosurg Psychiatry 1984;47:1020—8. Karnath HO, Broetz D. Understanding and treating ‘‘pusher syndrome’’. Phys Ther 2003;83:1119—25. Karnath HO, Ferber S, Dichgans J. The origin of contraversive pushing: evidence for a second graviceptive system in humans. Neurology 2000;55:1298—304. Kirker SG, Simpson DS, Jenner JR, Wing AM. Stepping before standing: hip muscle function in stepping and standing balance after stroke. J Neurol Neurosurg Psychiatry 2000;68:458—64. Kirker SG, Jenner JR, Simpson DS, Wing AM. Changing patterns of postural hip muscle activity during recovery from stroke. Clin Rehabil 2000;14:618—26. Lamb SE, Ferrucci L, Volapto S, Fried LP, Guralnik JM. Study risk factors for falling in home-dwelling older women with stroke: the Women’s Health and Aging Study. Stroke 2003;34:494—501. Lee WA, Derning L, Sahgal V. Quantitative and clinical measures of static standing balance in hemiparetic and normal subjects. Phys Ther 1988;68:970—6. Maki BE, McIlroy WE. The role of limb movements in maintaining upright stance: the ‘‘change-in-support’’ strategy. Phys Ther 1997;77:488—507. Maki BE, Holliday PJ, Topper AK. A prospective study of postural balance and risk of falling in an ambulatory and independent elderly population. J Gerontol 1994;49:72—84. Mansfield A, Inness EL, Lakhani B, McIlroy WE. Determinants of limb preference for initiating compensatory stepping poststroke. Arch Phys Med Rehabil 2012;93:1179—84. Mansfield A, Danells CJ, Zettel JL, Black SE, McIlroy WE. Determinants and consequences for standing balance of spontaneous weight-bearing on the paretic side among individuals with chronic stroke. Gait Posture 2013;38:428—32. Marigold DS, Eng JJ. Altered timing of postural reflexes contributes to falling in persons with chronic stroke. Exp Brain Res 2006;171:459—68. Massion J, Ioffe M, Schmitz C, Viallet F, Gantcheva R. Acquisition of anticipatory postural adjustments in a bimanual load-lifting task: normal and pathological aspects. Exp Brain Res 1999;128:229—35. Massion J, Alexandrov A, Frolov A. Why and how are posture and movement coordinated? Prog Brain Res 2004;143: 13—27. McIlroy WE, Maki BE. Preferred placement of the feet during quiet stance: development of a standardized foot placement for balance testing. Clin Biomech 1997;12:66—70. Nardone A, Godi M, Grasso M, Guglielmetti S, Schieppati M. Stabilometry is a predictor of gait performance in chronic hemiparetic stroke patients. Gait Posture 2009;30:5—10. Nashner LM. Analysis of movement control in man using the movable platform. Adv Neurol 1983;39:607—19. Nashner LM, Shumway-Cook A, Marin O. Stance posture control in select groups of children with cerebral palsy: deficits in sensory organization and muscular coordination. Exp Brain Res 1983;49:393—409. Paillex R, So A. Changes in the standing posture of stroke patients during rehabilitation. Gait Posture 2005;21:403—9. Perennou D. Weight bearing asymmetry in standing hemiparetic patients. J Neurol Neurosurg Psychiatry 2005;76:621. Pérennou DA, Amblard B, Leblond C, Pélissier J. Biased postural vertical in humans with hemispheric cerebral lesions. Neurosci Lett 1998;252:75—8. 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;82:440—8. Pérennou DA, Amblard B, Laassel el M, Benaim C, Hérisson C, Pélissier J. Understanding the pusher behavior of some stroke
Please cite this article in press as: Tasseel-Ponche S, et al. Motor strategies of postural control after hemispheric stroke. Neurophysiologie Clinique/Clinical Neurophysiology (2015), http://dx.doi.org/10.1016/j.neucli.2015.09.003
+Model NEUCLI-2489; No. of Pages 7
ARTICLE IN PRESS
Motor strategies of postural control after hemispheric stroke
[55]
[56]
[57]
[58]
[59]
[60]
[61]
[62] [63]
[64]
patients with spatial deficits: a pilot study. Arch Phys Med Rehabil 2002;83:570—5. Pérennou DA, Mazibrada G, Chauvineau V, Greenwood R, Rothwell J, Gresty MA, et al. Lateropulsion, pushing and verticality perception in hemisphere stroke: a causal relationship? Brain 2008;131:2401—13. Persson CU, Hansson PO, Sunnerhagen KS. Clinical tests performed in acute stroke identify the risk of falling during the first year: postural stroke study in Gothenburg (POSTGOT). J Rehabil Med 2011;43:348—53. Rode G, Tiliket C, Boisson D. Predominance of postural imbalance in left hemiparetic patients. Scand J Rehabil Med 1997;29:11—6. Rode G, Tiliket C, Charlopain P, et al. Postural asymmetry reduction by vestibular caloric stimulation in left hemiparetic patients. Scand J Rehabil Med 1998;30:9—14. Roerdink M, De Haart M, Daffertshofer A, Donker SF, Geurts AC, Beek PJ. Dynamical structure of center-of-pressure trajectories in patients recovering from stroke. Exp Brain Res 2006;174:256—69. Roerdink M, Geurts AC, de Haart M, Beek PJ. On the relative contribution of the paretic leg to the control of posture after stroke. Neurorehabil Neural Repair 2009;23:267—74. Runge CF, Shupert CL, Horak FB, Zajac FE. Ankle and hip postural strategies defined by joint torques. Gait Posture 1999;10:161—70. Sackley CM. Falls, sway, and symmetry of weight-bearing after stroke. Int Disabil Stud 1991;13:1—4. Schmid AA, Van Puymbroeck M, Altenburger PA, Miller KK, Combs SA, Page SJ. Balance is associated with quality of life in chronic stroke. Top Stroke Rehabil 2013;20:340—6. Slijper H, Latash ML, Rao N, Aruin AS. Task-specific modulation of anticipatory postural adjustments in individuals with hemiparesis. Clin Neurophysiol 2002;113:642—55.
7 [65] Spinazzola L, Cubelli R, Della Sala S. Impairments of trunk movements following left or right hemisphere lesions: dissociation between apraxic errors and postural instability. Brain 2003;126:2656—66. [66] Tilikete C, Rode G, Nighoghossian N, Boisson D, Vighetto A. Otolith manifestations in Wallenberg syndrome. Rev Neurol 2001;157:198—208. [67] Turnbull GI, Charteris J, Wall JC. Deficiencies in standing weight shifts by ambulant hemiplegic subjects. Arch Phys Med Rehabil 1996;77:356—62. [68] Viallet F, Massion J, Massarino R, Khalil R. Coordination between posture and movement in a bimanual load lifting task: putative role of a medial frontal region including the supplementary area. Exp Brain Res 1992;88:674—84. [69] Wing AM, Goodrich S, Virji-Babul N, Jenner JR, Clapp S. Balance evaluation in hemiparetic stroke patients using lateral forces applied to the hip. Arch Phys Med Rehabil 1993;74: 292—9. [70] Winstein CJ, Gardner ER, McNeal DR, Barto PS, Nicholson DE. Standing balance training: effect on balance and locomotion in hemiparetic adults. Arch Phys Med Rehabil 1989;70: 755—62. [71] Yanohara R, Teranishi T, Tomita Y, Tanino G, Ueno Y, Sonoda S. Recovery process of standing postural control in hemiplegia after stroke. J Phys Ther Sci 2014;26: 1761—5. [72] Yelnik AP, Kassouha A, Bonan IV, Leman MC, Jacq C, Vicaut E, et al. Postural visual dependence after recent stroke: assessment by optokinetic stimulation. Gait Posture 2006;24: 262—9. [73] Yelnik AP, Le Breton F, Colle FM, Bonan IV, Hugeron C, Egal V, et al. Rehabilitation of balance after stroke with multisensorial training: a single-blind randomized controlled study. Neurorehabil Neural Repair 2008;22:468—76.
Please cite this article in press as: Tasseel-Ponche S, et al. Motor strategies of postural control after hemispheric stroke. Neurophysiologie Clinique/Clinical Neurophysiology (2015), http://dx.doi.org/10.1016/j.neucli.2015.09.003