Management of postural sensory conflict and dynamic balance control in late-stage Parkinson's disease

Neuroscience 193 (2011) 363–369

MANAGEMENT OF POSTURAL SENSORY CONFLICT AND DYNAMIC BALANCE CONTROL IN LATE-STAGE PARKINSON’S DISEASE S. COLNAT-COULBOIS,a,b,c* G. C. GAUCHARD,a,b L. MAILLARD,d,e G. BARROCHE,d H. VESPIGNANI,d J. AUQUEc AND P. P. PERRINb,f

postural regulation involving more hip joint than ankle joint in patients with advanced PD than in controls. Difficulties in managing complex postural situations, such as sensory conflicting and dynamic situations might reflect an inadequate sensory organization suggesting impairment in central information processing. © 2011 Published by Elsevier Ltd on behalf of IBRO.

a INSERM U 954, Thematic group “Neurodegenerative Diseases, Neuroplasticity, Cognition”, Faculty of Medicine, Vandoeuvre-lès-Nancy, France b Nancy-University, Henri Poincaré University, Balance Control and Motor Performance, UFR STAPS, Villers-lès-Nancy, France

Key words: advanced Parkinson’s disease, static and dynamic postural control, sensory conflict, postural sensorimotor strategies.

c

Department of Neurosurgery, University Hospital of Nancy, Nancy, France d Department of Neurology, University Hospital of Nancy, Nancy, France

Standing postural control in man is a complex sensorymotor function requiring central processing of information from the visual, somatokinesthetic and vestibular systems, leading to a context-specific motor response. This response results in stabilization of anti-gravity activity and gaze and adjustment of static and dynamic postures (Massion and Woollacott, 1996). Amblard et al. (1985) suggested the existence of a dual postural control system, one dealing with postural orientation with respect to gravity and one dealing with postural stabilization (i.e. equilibrium). These two systems probably interact. The contributions of peripheral inputs of different modalities of balance control have been well documented (Massion and Woollacott, 1996; Bloem et al., 2001). During quiet stance, the contribution of visual and somesthetic inputs is important to perceive head and body sways (Bronstein et al., 1990; Fitzpatrick and McCloskey, 1994). However, the vestibular system, especially the otolithic organs, detects gravitational verticality, enabling the central nervous system to organize balance and posture according to the gravity reference frame and modulate postural tone (Massion and Woollacott, 1996; Bloem et al., 2001). During environmental or task condition change or sensory challenging situations, like those inducing motion sickness (Dai et al., 2011) or in microgravity (Viel et al., 2010), during sensory reweighting in the case of vestibular disorders and unilateral vestibular deafferentation (Parietti-Winkler et al., 2008, 2011) or during adolescence (Viel et al., 2009), a switch between the sensory information is weighted according to the resulting balance difficulties and the gain of the different afferent-postural loops is modified (Bronstein et al., 1990; Bloem et al., 2001). Thus, sensory information is complementary and partially redundant, providing fine-tuning of postural control, especially in complex balance situations such as during sensory conflicting situations (Massion and Woollacott, 1996). Parkinson’s disease (PD) is one of the most common neurodegenerative diseases and is characterized by motor symptoms such as akinesia, rigidity and tremor. Postural

e

CRAN, UMR 7039, CNRS, Nancy-University, France

f

Department of ENT, University Hospital of Nancy, Nancy, France

Abstract—Parkinson’s disease (PD) is known to affect postural control, especially in situations needing a change in balance strategy or when a concurrent task is simultaneously performed. However, few studies assessing postural control in patients with PD included homogeneous population in late stage of the disease. Thus, this study aimed to analyse postural control and strategies in a homogeneous population of patients with idiopathic advanced (late-stage) PD, and to determine the contribution of peripheral inputs in simple and more complex postural tasks, such as sensory conflicting and dynamic tasks. Twenty-four subjects with advanced PD (duration: median (M)ⴝ11.0 years, interquartile range (IQR)ⴝ4.3 years; Unified Parkinson’s Disease Rating Scale (UPDRS): M “on-dopa”ⴝ13.5, IQRⴝ7.8; UPDRS: M “off-dopa”ⴝ48.5, IQRⴝ16.8; Hoehn and Yahr stage IV in all patients) and 48 age-matched healthy controls underwent static (SPT) and dynamic posturographic (DPT) tests and a sensory organization test (SOT). In SPT, patients with PD showed reduced postural control precision with increased oscillations in both anterior–posterior and medial–lateral planes. In SOT, patients with PD displayed reduced postural performances especially in situations in which visual and vestibular cues became predominant to organize balance control, as was the ability to manage balance in situations for which visual or proprioceptive inputs are disrupted. In DPT, postural restabilization strategies were often inefficient to maintain equilibrium resulting in falls. Postural strategies were often precarious, *Correspondence to: S. Colnat-Coulbois, Département de Neurochirurgie, CHU de Nancy, Hôpital Central, 29 Avenue de Lattre de Tassigny, 54000 Nancy, France. Tel: ⫹33-383-85-15-79; fax: ⫹33-38385-26-12. E-mail address: [email protected] (S. Colnat-Coulbois). Abbreviations: BMI, body mass index; CoG, centre of gravity; CoP, centre of foot pressure; DPT, dynamic posturographic test; ES, equilibrium score; FFT, fast Fourier transformations; IQR, interquartile range; PD, Parkinson’s disease; RQ, Romberg’s quotient; RSOM, somesthetic ratio; RVEST, vestibular ratio; RVIS, visual ratio; SOT, sensory organisation test; SPT, static posturographic test; SRsup, sway-referenced support motion; SRsur, sway-referenced visual surround motion; SS, strategy score; UPDRS, Unified Parkinson’s Disease Rating Scale.

0306-4522/11 $ - see front matter © 2011 Published by Elsevier Ltd on behalf of IBRO. doi:10.1016/j.neuroscience.2011.04.043

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instability in association with motor disability increases associated morbidity and mortality, especially in late stage of the disease (Hoehn and Yahr Score IV and V) (Coelho et al., 2010). Several posturographic studies reported balance abnormalities in PD: Bronte-Stewart et al. (2002) described greater postural sway especially when somatosensory and visual inputs are disrupted. Vaugoyeau and Azulay (2010) demonstrated that patients with PD present major deficit of postural orientation that develop earlier than equilibrium deficit. Vaugoyeau et al. (2007) and King and Horak, (2008) found more instability in patients with PD than control subjects in response to lateral disequilibrium. This deficient postural control is worsened when patients have to change their postural strategies (Toole et al., 2000) or when they have to manage a concurrent task (Morris et al., 2000). Patients with PD use inadequate postural strategies leading to falls (Bloem et al., 2001). Peripheral inputs are considered to be intact but the central use of this neurosensory information seems to be inadequate (Pastor et al., 1993). Thus, a misinterpretation of visual inputs is observed in those patients (Bronstein et al., 1990). These data suggest the existence of conflict in central information processing that could be the result of misinterpretation or misintegration of correct peripheral inputs (Jacobs and Horak, 2006). Postural abnormalities in PD have been reported at every stages of the disease (Nallegowda et al., 2004; Blaszczyk et al., 2007; Vaugoyeau et al., 2007; Chastan et al., 2008; Termoz et al., 2008). However, many studies dealt with heterogeneous populations of patients with wide ranges of Hoehn and Yahr scores (Waterston et al., 1993; King and Horak, 2008; Kim et al., 2009). Within this context, the present study aimed to analyse the characteristics of postural control and strategies in a homogeneous population of PD patients displaying severe disability (Hoehn and Yahr Score⫽IV), in “on-dopa” state, that is in optimal motor state. We aimed to determine how peripheral inputs are used to manage complex postural tasks such as sensory conflicting and dynamic postural tasks in order to understand the mechanisms of falls and associated morbidity in these patients.

EXPERIMENTAL PROCEDURES Patients The present study was conducted in Nancy University Hospital (in North-Eastern France) and involved 24 subjects with late-stage PD and 48 healthy individuals (Table 1). No significant differences in age, height, weight and BMI were observed between PD and control groups. Median duration of the disease was 11.0 years, [interquartile range (IQR)⫽4.3 years]. Unified Parkinson’s Disease Rating Scale (UPDRS) score (part III) was used for clinical assessment of patients. All patients were in Hoehn-Yahr stage IV and therefore constituted a homogeneous population considering the severity of the disease. Median values of “on-dopa” and “off-dopa” motor score were respectively 13.5 (IQR⫽7.8) and 48.5 (IQR⫽16.8). Median daily dose of levodopa was 1000.0 mg (IQR⫽487.5 mg). The PD group underwent posturographic tests during their best “on-dopa” state to evaluate the performances in the optimal motor state, as close as possible to their daily living conditions. Patients

Table 1. Characteristics of patients with late-stage Parkinson’s disease (PD group) and of healthy individuals (control group). Intergroup comparisons have been performed with the Mann & Whitney test for the quantitative parameters (expressed in median associated with the interquartile range (IQR)), such as age, height, weight and body mass index (BMI⫽weight/height2), and with the Fisher’s exact test for gender parameter Intergroup Control group, PD group, comparison n⫽48 n⫽24 median (IQR)/n= median (IQR)/n= Age (years) Gender Women Men Height (m) Weight (kg) Body mass index (kg/m2)

60.0 (14.0)

62.0 (11.0)

z⫽⫺0.40, NS

10 14 1.69 (0.08) 69.0 (15.5) 24.9 (4.6)

20 28 1.66 (0.09) 68.5 (14.0) 24.4 (5.2)

Fisher’s exact P⬎0.999 z⫽⫺1.53, NS z⫽⫺0.32, NS z⫽⫺0.55, NS

NS, non significant.

were evaluated in the context of pre-surgical evaluation for deep brain stimulation. All controls were free from any central nervous system disease, and presented no orthopaedic disorders either of the trunk or the lower limbs that could affect postural performance.

Posturography General principles. The method used aimed at evaluating two modalities of postural regulation— quiet stance and during continuous support perturbation—and their related neurosensory organization (Massion and Woollacott, 1996). Thus, postural control during quiet stance was evaluated with and without sensory conflict by a static posturographic test (Toennies GmbH, Freiburg, Germany) and by a sensory organization test (EquiTest®, Neurocom, Clackamas, OR, USA); postural control during continuous support perturbation was evaluated by a dynamic posturographic test with slow sinusoidal oscillations of the support (Toennies). For each posturographic test, subjects were barefoot, the feet placed on footprints materialized on the platform (Toennies) or on marks to align medialis malleolus to horizontal line and lateral calcaneous to T line (EquiTest®), in an upright position in as stable manner as possible, breathing normally, arms at the side, and were instructed to look straight ahead. To protect against falls, an operator stood within touching distance of the subject and all wore a safety harness connected to the ceiling by two suspension straps in all the test conditions. Posturographic procedure was carried out in the Laboratory for the Analysis of Posture, Equilibrium and Movement (LAPEM) of the University Hospital of Nancy (Ministry of Health approval for research) and all subjects gave informed consent prior to the study. Static posturographic test. In SPT, successive centre of foot pressure (CoP) positions and displacements were recorded for 20 s, in eyes open and then in eyes closed conditions. Statokinesigrams represented measurement of the sway path travelled and the area covered by CoP displacements. Low sway path values, expressing low energy consumption and small CoP displacement area, expressing precision, are representative of good postural control. Eyes open and eyes closed data were used to determine Romberg’s quotients (RQ) (RQ sway path: eyes closed/ eyes open sway path ratio, RQ area: eyes closed/eyes open area ratio), which represent the contribution of visual information to balance control. Sways in the anterior–posterior and medial–lateral axes were determined by vectorial analysis of CoP displacements (Colnat-Coulbois et al., 2005; Gauchard et al., 2010).

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Table 2. Sensory organization test (EquiTest®, Neurocom®, Clackamas, OR, USA): determination of the six conditions and significance of sensory ratios Sensory organisation test Conditions Name Condition 1 (C1) Condition 2 (C2) Condition 3 (C3) Condition 4 (C4) Condition 5 (C5) Condition 6 (C6) Ratios Name Somatosensory (RSOM)

Situation Eyes open, fixed support Eyes closed, fixed support SR surround, fixed support Eyes open, SR support Eyes closed, SR support SR surround, SR support

Available cues Vision, vestibular, somatosensory Vestibular, somatosensory Vestibular, somatosensory Vision, vestibular Vestibular Vestibular

Pair C2/C1

Significance Question: Does sway increase when visual cues are removed? Low scores: Poor use of somatosensory references. Question: Does sway increase when somatosensory cues are removed? Low scores: Poor use of visual references. Question: Does sway increase when visual cues are removed and somatosensory cues are inaccurate? Low scores: Poor use of vestibular cues or vestibular cues unavailable. Question: Do inaccurate visual cues result in increased sway compared to no visual cues? Low scores:Reliance on visual cues even inaccurate. Question: Do inaccurate somatosensory cues result in increased sway compared to accurate somatosensory cues? Low scores: Poor compensation for disruptions in selected sensory inputs.

Visual (RVIS)

C4/C1

Vestibular (RVEST)

C5/C1

Visual preference (RPREF)

(C3⫹C6)/(C2⫹C5)

Altered proprioceptive information management (RPMAN)

(C4⫹C5⫹C6)/(C1⫹C2⫹C3)

Unavailable or altered cues — No vision Vision altered Somatosensory altered No vision, somatosensory altered Vision altered, somatosensory altered

SR, sway-referenced.

Sensory organization test. SOT evaluates the patient’s ability to make effective use of visual, vestibular and somatosensory inputs separately and to suppress sensory information that is inappropriate. To give inadequate information, somatosensory and visual cues are disrupted by using a technique commonly referred to as sway-referenced, which involves tilting the support surface and/or the visual surround to directly follow the anterior– posterior sways of the subject’s centre of gravity (Nashner and Peters, 1990). The subject’s task is to maintain an upright stance during three 20 s tests in six conditions that combine three visual conditions [eyes open, eyes closed and sway-referenced visual surround motion (SRsur)] with two platform conditions [stable support, sway-referenced support motion (SRsup)] as follows: eyes open/stable support (C1), eyes closed/stable support (C2), SRsur/stable support (C3), eyes open/SRsup (C4), eyes closed/ SRsup (C5), SRsur/SRsup (C6) (Table 2). The theoretical limit of stability is based on the individual’s height and size of the base of support. It represents an angle (8.5° anteriorly and 4.0° posteriorly) at which the person can lean in any direction before the centre of gravity would move beyond a point that allows him/her to remain upright (i.e., point of falling). The following formula was used to calculate the equilibrium score: [12.5°⫺((␪max⫺␪min)/ 12.5°)]⫻100, where ␪max indicates the greatest anterior–posterior CoG sway angle displayed by the subject, while ␪min indicates the lowest anterior–posterior CoG sway angle (Nashner and Peters, 1990). Equilibrium (ES) scores were calculated for every condition: the averaged ES of the three trials were C1ES in condition 1, C2ES in condition 2, C3ES in condition 3, C4ES in condition 4, C5ES in condition 5, and C6ES in condition 6. A composite equilibrium score (CES) was calculated by adding the average scores from conditions 1 and 2 and the ES from each trial of sensory conditions 3, 4, 5 and 6, and finally dividing that sum by the total number of trials, that would smooth the data across all conditions (Nashner and Peters, 1990). By using the individual scores for conditions 3, 4, 5 and 6, CES is effectively weighted to the more difficult conditions and characterizes the overall level of postural control performance, that is coupling both simple and

complex postural tasks (without and with sensory conflicts). Lower sways lead to a higher composite score, indicating a better balance control performance (a score of 100 represents no sway, while 0 indicates sway that exceeds the limit of stability, resulting in a fall). Each ES was adjusted on C1ES to identify the significance of each sensory system influencing postural control, the C2ES/C1ES ratio representing somatosensory contribution to postural control (RSOM), the C4ES/C1ES ratio the visual contribution (RVIS) and the C5ES/C1ES ratio the vestibular contribution (RVEST). The ability to rely on vision, even if inadequate, was evaluated by comparing the sway-referenced visual surround with the absence of vision [(C3ES⫹C6ES)/(C2ES⫹C5ES)], which conveys visual preference (RPREF). The ability to manage altered proprioceptive inputs (RPMAN) was evaluated by comparing all the sway-referenced platform conditions with all the fixed platform conditions [(C4ES⫹ C5ES⫹C6ES)/(C1ES⫹C2ES⫹C3ES)] (Table 2) (Black et al., 1995; Herdman et al., 1995; Gauchard et al., 2010; Parietti-Winkler et al., 2011). Moreover, the relative amounts of ankle movements (ankle strategy) and hip movements (hip strategy) that the individual used to maintain balance during each procedure were calculated. Exclusive use of ankle strategy to maintain equilibrium resulted in a score of 100. Exclusive use of hip strategy yielded a score close to 0. Strategy scores (SS) between these two extremes represented a combination of the two strategies. SS is computed from the maximum and minimum horizontal shear forces detected by the support platform (SHmax, SHmin) and referenced to a theoretical maximum shear force of 25 lbs and is calculated by: [(1⫺(SHmax⫺SHmin)/25)⫻100] (Nashner and Peters, 1990). C1SS represented the averaged strategy score of the three trials in condition 1, C2SS in condition 2, C3SS in condition 3, C4SS in condition 4, C5SS in condition 5, and C6SS in condition 6. A composite strategy score (CSS) was calculated by independently averaging the scores for conditions 1 and 2, then adding to the strategy scores from each trial of sensory conditions 3, 4, 5 and 6, and finally dividing that sum by the total number of trials (ColnatCoulbois et al., 2005; Gauchard et al., 2010).

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Dynamic posturographic test. In DPT, platform movement consisted of slow 4° amplitude sinusoidal anterior–posterior oscillations of the support at a frequency of 0.5 Hz for 20 s in eyes open and eyes closed conditions. CoP displacements were analyzed by comparing them with the sinusoidal waveform yielded by the movement of the platform and as fast Fourier transformations (FFT). When the participant succeeded to maintain his/her equilibrium during the test, FFT graphs were analysed by determining the frequencies and amplitudes of different peaks, and splitting them into two groups. In this differentiation, the presence of high frequency peaks, which mainly reflect upper limb movements, was not taken into account, as it was considered that they do not reflect the level of instability of the subject. Thus, posturographic recordings were split into two types: ●

●

Type 1 recordings were characterized by regular patterns at the same frequency as the stimulus, but in opposite phase with low or high amplitude. FFT analysis showed a major peak at 0.5 Hz, with other small peaks of no more than 75% of the amplitude of the major peak, indicating high stability of the participant during the test. This pattern corresponds to a bottom-up regulation model, with the body oscillating like an inverted pendulum, and is considered to be anticipatory. Type 2 recordings were characterized by irregular patterns, at a different frequency from that of the stimulus with high amplitude at the low frequencies. FFT analysis shows a major 0.5 Hz peak associated with peaks at lower frequencies reaching more than 75% of the amplitude of the major peak or a major peak occurring at frequency lower than 0.5 Hz, expressing the instability of the participant during the recording. This pattern corresponds to a top-down regulation model, and necessitates reactional adjustments.

In case of failure in maintaining equilibrium, that is by observing participants reaching for support or obviously leaning on the safety belt, a fall was defined (Colnat-Coulbois et al., 2005; Gauchard et al., 2010). Procedure. The same posturographic procedure was applied to all patients and controls, that is SPT eyes open, SPT eyes closed, DPT eyes open, DPT eyes closed and SOT C1 to C6. The whole testing lasted about 30 min, with rest breaks of about 2–3 min between SPT eyes closed and DPT eyes open and of 5 min between DPT eyes closed and SOT. According to a longer time to perform SOT (about 10 –15 min), rest breaks were proposed at the request of the participants.

Statistical analysis According to the lack of normality of data distribution for some posturographic parameters and to the low sample size in PD group, the SPT and SOT performances between PD and control groups were compared with a Mann–Whitney test, as well as age, height, weight and BMI parameters described in the Experimental procedures section. The ␹2 or Fisher’s exact tests were used to compare sensory-motor strategies during DPT and gender described in Experimental procedures section. Because of the high number of comparisons, a Holland-Copenhaver procedure, which is a modified Bonferroni adjustment, was used to avoid inflation of the overall type I error rate. The approach was to order the P-values from the smallest to the largest. If the number of comparisons was k, the smallest P-value was compared against an adjusted ␣: 1⫺(1⫺␣)(1/(k⫺1⫹1)). The next smallest P-value was compared against a new adjusted ␣: 1⫺(1⫺␣)(1/(k⫺2⫹1)), and so on until the largest P-value was compared against ␣ (i.e. 0.05). This method, which is less conservative than the usual Bonferroni adjustment, was applied to SPT (k⫽10), SOT (k⫽19) and DPT (k⫽2).

Fig. 1. Static tests (SPT)—Median results, associated with the interquartile range, of sway path (SP, cm/s), area (cm2/s), anterior-posterior (AP, cm/s) and lateral (Lat, cm/s) sways in the eyes open (A) and eyes closed (B) conditions in patients with Parkinson’s disease (PD group, white bars) and in controls (control group, grey bars). Statistical significance (after Holland-Copenhaver procedure): *** Pⱕ0.001.

RESULTS Patients with Parkinson’s disease presented postural control abnormalities in simple (SPT) and complex (SOT) static posturographic tests and dynamic posturographic test (DPT). In SPT (Fig. 1), balance abnormalities were characterized by significantly higher values in PD group both in eyes open and in eyes closed conditions for the sway path (eyes open: z⫽⫺6.20, P⬍0.001; eyes closed: z⫽⫺4.73, P⬍0.001) and area (eyes open: z⫽⫺5.14, P⬍0.001; eyes closed: z⫽⫺4.95, P⬍0.001) parameters as well as for anterior–posterior sway (eyes open: z⫽⫺4.39, P⬍0.001; eyes closed: z⫽⫺3.28, P⬍0.001) and medial–lateral sway (eyes open: z⫽⫺4.19, P⬍0.001; eyes closed: z⫽⫺4.05, P⬍0.001) parameters. On the other hand, no statistically significant difference was observed between the two groups for the RQ sway path and RQ area. In SOT (Fig. 2), balance abnormalities were characterized by lower equilibrium (Fig. 2A) and strategy (Fig. 2C) scores in PD group, statistically significant differences being observed for composite scores (CES: z⫽⫺5.93, P⬍0.001; CSS: z⫽⫺3.67, P⬍0.001), and for each equilibrium score (C1ES: z⫽⫺4.52, P⬍0.001; C2ES: z⫽⫺3.98, P⬍0.001; C3ES: z⫽⫺3.57, P⬍0.001; C4ES: z⫽⫺4.27, P⬍ 0.001; C5ES: z⫽⫺5.24, P⬍0.001; C6ES: z⫽⫺4.40, P⬍0.001) and strategy score (C1SS: z⫽⫺2.53, P⫽0.011; C2SS: z⫽⫺2.80, P⫽0.005; C4SS: z⫽⫺2.57, P⫽0.010; C6SS: z⫽⫺2.91, P⫽0.004). Concerning sensory analysis

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against 18.8% of the controls, and 25.0% a Type 2 (reactional) strategy against 70.8%.

DISCUSSION

Fig. 2. Sensory organization test (SOT)—Median results, associated with the interquartile range, of the equilibrium (A; ES) and strategy (C; SS) scores for the six conditions, the composite equilibrium and strategy scores, and of the different ratios (B; RSOM, RVIS, RVEST, RPREF and RPMAN) in patients with Parkinson’s disease (PD group, white bars) and in controls (control group, grey bars). Statistical significance (after Holland-Copenhaver procedure): * Pⱕ0.05; ** Pⱕ0.01; *** Pⱕ 0.001.

(Fig. 2B), the PD group had more difficulties to control balance sways in the more complex sensory conflicting situations, that is in which visual information is the main reliable cue (RVIS: z⫽⫺2.98, P⫽0.003), vestibular information was the only reliable cue (RVEST: z⫽⫺4.80, P⬍0.001), or proprioceptive information was systematically disrupted (RPMAN: z⫽⫺4.77, P⬍0.001). In DPT (Table 3), the two groups preferentially displayed a Type 1 (anticipatory) strategy in eyes open; however, one participant of the PD group presented a fall during the test. In eyes closed, the PD group had more difficulties to maintain balance on the platform (70.8% fallers) than controls (10.4% fallers). Moreover, with eyes closed, the postural strategies were reversed, only 4.2% of patients with PD being able to maintain a Type 1 strategy

This study reports that postural control in quiet stance and during continuous support perturbation is impaired in patients with late-stage PD. Static postural control is poorer and characterized by a higher area and an increased sway path both in the anterior–posterior and medial–lateral planes. Moreover, the ability to control balance in the more complex situations, especially when visual or proprioceptive inputs are disturbed, is less efficient in the PD group, indicating difficulties to control balance from erroneous information. Management of sensory conflicting situations is compromised in the PD group indicating difficulties to distinguish and select reliable information to ensure postural control. Besides, in most cases postural restabilization strategies are ineffective for maintaining equilibrium, leading to falls. For the few patients who were able to control dynamic balance, strategies used were often precarious, postural regulation involving the hip joint more than the ankle joint. Postural instability is responsible for a significant morbidity in the late stage of PD (Coelho et al., 2010). Conventionally, balance during quiet stance is supported by the use of an inverted pendulum model (Gage et al., 2004), and its regulation and adaptation to the environment is based on postural tone and on postural reflexes, which are generated by the vestibular, visual and somatosensory systems and involve higher levels of control (Massion and Woollacott, 1996). Nevertheless, somatosensory and visual inputs are sufficient to feed information for postural regulation during quiet stance, the sway-related accelerations being below the thresholds of vestibular organ perception (Fitzpatrick and McCloskey, 1994). This study shows that patients with advanced PD display deficient static postural control compared to controls, both for area and sway path with higher oscillations and anterior–posterior angular deviation. These results are consistent with those of Blaszczyk et al. (2007) and Rocchi et al. (2006) who demonstrated, in PD patients, an increase in sway path, lateral sway range and angular deviation from anterior–posterior sway. In more complex postural situations, that is in quiet stance situations with sensory conflicts and in dynamic situations, patients with late-stage PD show reduced postural abilities and higher risk of falling. In sensory conflicting situations, that is where a minimum of information is available or valid, a switch between sensory information is necessary to balance the gain of different afferent-postural loops that reflects accurate processing of central information. De Nunzio et al. (2007) demonstrated that PD patients exhibited a major delay in reconfiguring their balance strategy when sensory conditions change. In this study, patients with late-stage PD presented difficulties to generate an appropriate postural stabilization strategy, especially in situations where proprioceptive information was disruptive, resulting here in the use of unstable strategies that increased the likelihood of falling. These results were consistent with those of Toole et al.

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Table 3. Dynamic posturographic test (DPT): frequency distribution of the two types of sensorimotor strategies and of falls in eyes open and eyes closed conditions observed in the Parkinson’s disease (PD) and control groups DPT

Sensory-motor strategies

PD group n⫽24 n= (%)

Control group n⫽48 n= (%)

␹2-test ␹2-value (P)

Eyes open

Type Type Fall Type Type Fall

13 (54.2%) 10 (41.6%) 1 (4.2%) 1 (4.2%) 6 (25.0%) 17 (70.8%)

34 (70.8%) 14 (29.2%) 0 (0%) 9 (18.8%) 34 (70.8%) 5 (10.4%)

␹2df2⫽3.43 (NS)

Eyes closed

1 (anticipatory) 2 (reactional) 1 (anticipatory) 2 (reactional)

(2000) and Shivitz et al. (2006) who found poorer postural control in PD especially in situations where somatosensory information was impaired, reflecting difficulties to use visual or vestibular feedback. Similarly, Trenkwalder et al. (1995) showed that patients with PD had a higher dependence on visual inputs even when they conflicted with vestibular or somatosensory inputs. This overdependence on visual information is probably worsened by impaired visuo-spatial organization (Testa et al., 1993). Depending on the degree of deficiency in managing proprioceptive information, this study highlights that these postural motor perturbations are greater since sensory deficits are present due to impaired proprioceptive feedback during continuous support perturbation. In the same way, Vaugoyeau and Azulay (2010) demonstrated that PD patients presented postural orientation deficit that may be associated with proprioceptive integration deficits. They also suggested that the visuodependance observed in PD might represent an adaptive strategy to compensate for the proprioceptive deficit. These results should be considered in relation to those observed in DPT, which show that the PD group presented more falling events than the control group and used hip joints more to regulate balance. Traditionally, good performances in DPT are seen from the use of an anticipatory strategy, involving the ankle joint rather than the hip joint (Horak and Nashner, 1986; Gauchard et al., 2010). These results are consistent with those of Nallegowda et al. (2004) and Termoz et al. (2008) who showed that PD patients used less ankle strategy and more hip strategy for balance control. Postural abnormalities have been described at early stages of PD (Jacobs and Horak, 2006) and increased while the disease progressed. Thus, Chastan et al. (2008) showed that even when there is no clinical balance impairment, sway area increases in early PD. Early modifications of postural strategies have also been reported (Chastan et al., 2008; Nallegowda et al., 2004). Frenklach et al. (2009) demonstrated that postural sway and falls were correlated to the disease severity. Moreover, Valkovic et al. (2006) showed that the amplitude of postural reactions was significantly larger in advanced PD and that proprioceptive information was less used in advanced PD. Our results shows that in late-stage PD postural strategies are in most case ineffective to maintain equilibrium and avoid falls, especially in dynamic conditions and sensory conflicting conditions.

␹2df2⫽27.61 (P⬍0.001)

As peripheral inputs are intact in PD (Pastor et al., 1993), postural instability seems to result from abnormal central processing of this information, leading to inadequate postural response (Bronte-Stewart et al., 2002). Thus, Maurer et al. (2004) demonstrated that there is an abnormal resonance behavior of the postural central loop in PD. In a previous study, we showed that the addition of levodopa and bilateral chronic stimulation of the subthalamic nucleus in PD improved postural control both in static and dynamic conditions, therefore confirming the central origin of postural abnormalities in PD (Colnat-Coulbois et al., 2005). Recently, Karachi et al. (2010) demonstrated the involvement of the pedonculopontine nucleus (PPN) in the pathophysiology of postural disorders in PD: they established a correlation between falls and loss of cholinergic neurons in PPN in PD patients. Some features of our study should be considered. As PD patients underwent posturographic tests in their best on-dopa state, we could not assess the influence of dopaminergic medications on their performance. Recently, Wright et al. (2010) demonstrated that kinaesthetic sensitivity of axial musculature is impaired in PD, especially when using levodopa medication, that contributes to impairment of posture. In conclusion, patients with late-stage PD showed major impairment of postural control. Postural control precision is impaired and postural strategies are inadequate, leading to falls. Furthermore, their inability to manage complex postural situations, such as sensory conflicting and dynamic situations, might reflect an inadequate sensory organization suggesting impairment in central information processing. Future studies should focus on the influence of a rehabilitation program in which the PD patients would be exposed to sensorial conflict situations.

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(Accepted 16 April 2011) (Available online 27 May 2011)