Effect of chronic bilateral subthalamic nucleus (STN) stimulation on postural control in Parkinson's disease.

Postural instability is one of the most incapacitating factors in Parkinson's disease (PD). The underlying deficits and the effects of treatment are still not well understood. The aims of the present study were: (i) to identify abnormalities of postural control in PD patients during unperturbed stance and externally perturbed stance (anterior-posterior tilts of the support surface and of the visual scene); (ii) to assess the effects of L-dopa medication and subthalamic nucleus (STN) stimulation on posture control; and (iii) to characterize potential differential or additive effects of both treatments. Eight PD patients under chronic STN stimulation were investigated and compared with 10 normal controls. The assessment was performed in a crossover design (+/- STN stimulation, +/- L-dopa). During unperturbed stance, we recorded measures of spontaneous sway in terms of displacement, velocity and frequency of the centre of pressure (COP), lower body (LB) and upper body (UB) excursions. In addition, inter-segmental UB-LB coupling was investigated as a measure of axial stiffness. All these measures were abnormally large in patients OFF treatment. Under L-dopa treatment, the velocity, frequency and coupling measures were reduced, whereas sway amplitude increased. Very similar effects were obtained under STN stimulation, and these effects became more pronounced in the combined treatment condition. In these data, reduction of inter-segmental coupling correlated with increase in sway amplitude. The finding suggests that axial stiffness reduction under treatment revealed a treatment- resistant deficit in the sensorimotor postural control loop. However, these two effects did not correlate with the motor subscores of the unified Parkinson's disease rating scale (UPDRS), which indicates that they are of minor functional relevance for posture control. A frequency peak in the COP excursions at 0.7-1.1 Hz, which we take to indicate a resonance behaviour of the postural control loop, became reduced under therapy. The reduction of this peak did correlate with most improvements in the UPDRS under therapy. Support surface tilt revealed that an UB righting on the LB segment, which is present in normal controls, is missing in the patients. The postural responses to visual tilt were abnormally large in patients, independent of whether the support was stable or slightly moving, while the control subjects clearly profited from a stable support. This finding suggests that PD patients lack the ability of normal subjects to use sensory or cognitive information when suppressing the destabilizing effect of visual tilt. These abnormal tilt reactions of the patients were resistant to treatment with L-dopa, STN stimulation and a combination of the two. Overall, the effects of STN stimulation on posture control essentially paralleled those of L-dopa during both unperturbed and externally perturbed stance.

[1]  R. J. Helscher,et al.  Does deep brain stimulation of the nucleus ventralis intermedius affect postural control and locomotion in Parkinson's disease? , 1999, Movement disorders : official journal of the Movement Disorder Society.

[2]  B. Day,et al.  Effect of vision and stance width on human body motion when standing: implications for afferent control of lateral sway. , 1993, The Journal of physiology.

[3]  A. Benabid,et al.  Effect of subthalamic nucleus stimulation on levodopa-induced dyskinesia in Parkinson’s disease , 2000, Neurology.

[4]  M P Remler,et al.  Impaired scaling of long latency postural reflexes in patients with Parkinson's disease. , 1993, Electroencephalography and clinical neurophysiology.

[5]  D. O'Boyle,et al.  Proprioceptive regulation of voluntary ankle movements, demonstrated using muscle vibration, is impaired by Parkinson’s disease , 1999, Journal of neurology, neurosurgery, and psychiatry.

[6]  C Maurer,et al.  Visual object localisation in space. Interaction of retinal, eye position, vestibular and neck proprioceptive information. , 2001, Experimental brain research.

[7]  Robert J. Peterka,et al.  Postural control model interpretation of stabilogram diffusion analysis , 2000, Biological Cybernetics.

[8]  J. Turner Third Symposium on Parkinson's Disease , 1970 .

[9]  C. Marsden,et al.  The functions of the basal ganglia and the paradox of stereotaxic surgery in Parkinson's disease. , 1994, Brain : a journal of neurology.

[10]  R. Peterka Sensorimotor integration in human postural control. , 2002, Journal of neurophysiology.

[11]  N Accornero,et al.  Clinical multisegmental posturography: age-related changes in stance control. , 1997, Electroencephalography and clinical neurophysiology.

[12]  J. D. Hood,et al.  Visual control of balance in cerebellar and parkinsonian syndromes. , 1990, Brain : a journal of neurology.

[13]  M Hallett,et al.  Physiological mechanisms of rigidity in Parkinson's disease. , 1983, Journal of neurology, neurosurgery, and psychiatry.

[14]  J. Molinuevo,et al.  Levodopa withdrawal after bilateral subthalamic nucleus stimulation in advanced Parkinson disease. , 2000, Archives of neurology.

[15]  G A Horstmann,et al.  Posture in Parkinson's disease: Impairment of reflexes and programming , 1988, Annals of neurology.

[16]  L. T. Robertson,et al.  Assessments of Axial Motor Control during Deep Brain Stimulation in Parkinsonian Patients , 2001, Neurosurgery.

[17]  F. Horak,et al.  Effects of dopamine on postural control in parkinsonian subjects: scaling, set, and tone. , 1996, Journal of neurophysiology.

[18]  V. Dietz,et al.  Balance control in Parkinson's disease , 1993 .

[19]  R. Turner,et al.  Treatment of advanced Parkinson's disease by posterior GPi pallidotomy: 1‐year results of a pilot study , 1996, Annals of neurology.

[20]  A. Benabid,et al.  Electrical stimulation of the subthalamic nucleus in advanced Parkinson's disease. , 1998, The New England journal of medicine.

[21]  Claude Prablanc,et al.  Neural control of space coding and action production , 2003 .

[22]  A. Bronstein,et al.  Visually and posturally mediated tilt illusion in Parkinson's disease and in labyrinthine defective subjects , 1996, Neurology.

[23]  F. W. Cody,et al.  Proprioceptive control of wrist movements in Parkinson's disease. Reduced muscle vibration-induced errors. , 1997, Brain : a journal of neurology.

[24]  P. Perozzo,et al.  Deep brain stimulation of the subthalamic nucleus: Clinical effectiveness and safety , 2001, Neurology.

[25]  F. Horak,et al.  Postural inflexibility in parkinsonian subjects , 1992, Journal of the Neurological Sciences.

[26]  B L Day,et al.  Vestibular induced postural responses in Parkinson's disease. , 1993, Brain : a journal of neurology.

[27]  M. Ouaknine,et al.  Sensory strategies in human postural control before and after unilateral vestibular neurotomy , 1997, Experimental Brain Research.

[28]  C Maurer,et al.  Visual object localization through vestibular and neck inputs. 1: Localization with respect to space and relative to the head and trunk mid-sagittal planes. , 1997, Journal of vestibular research : equilibrium & orientation.

[29]  A L Benabid,et al.  Subthalamic nucleus or internal pallidal stimulation in young onset Parkinson's disease. , 1998, Brain : a journal of neurology.

[30]  J. Lakke Axial apraxia in Parkinson's disease , 1985, Journal of the Neurological Sciences.

[31]  E. Scholz,et al.  Increased shortening reaction in Parkinson's disease reflects a difficulty in modulating long loop reflexes , 1987, Movement disorders : official journal of the Movement Disorder Society.

[32]  C H Lücking,et al.  Effect of bilateral subthalamic nucleus stimulation on gait in Parkinson's disease. , 2001, Brain : a journal of neurology.

[33]  I. Hwang,et al.  Quantitative analysis of the velocity related pathophysiology of spasticity and rigidity in the elbow flexors , 2002, Journal of neurology, neurosurgery, and psychiatry.

[34]  Ian David Loram,et al.  Human balancing of an inverted pendulum: position control by small, ballistic‐like, throw and catch movements , 2002, The Journal of physiology.

[35]  C. Marsden The mysterious motor function of the basal ganglia , 1982, Neurology.

[36]  C Maurer,et al.  Vestibular, visual, and somatosensory contributions to human control of upright stance , 2000, Neuroscience Letters.

[37]  N. Paquet,et al.  Responses to Dynamic Head-and-Body Tilts are Enhanced in Parkinson's Disease , 1997, Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques.

[38]  David A. Winter,et al.  Human balance and posture control during standing and walking , 1995 .

[39]  J C Rothwell,et al.  The behaviour of the long-latency stretch reflex in patients with Parkinson's disease , 1983, Journal of neurology, neurosurgery, and psychiatry.

[40]  J. Nutt,et al.  Interactions between deep brain stimulation and levodopa in Parkinson’s disease , 2001, Neurology.

[41]  M. Hallett,et al.  Pathophysiology of bradykinesia in Parkinson's disease. , 2001, Brain : a journal of neurology.

[42]  T. Mergner,et al.  Visual object localisation in space , 2001, Experimental Brain Research.

[43]  M. Rizzone,et al.  Deep brain stimulation of the subthalamic nucleus in Parkinson's disease: effects of variation in stimulation parameters , 2001, Journal of neurology, neurosurgery, and psychiatry.

[44]  J Dichgans,et al.  Medium and long latency EMG responses in leg muscles: Parkinson's disease. , 1987, Journal of neurology, neurosurgery, and psychiatry.

[45]  B. R. Bloem,et al.  Are medium and long latency reflexes a screening tool for early Parkinson's disease? , 1992, Journal of the Neurological Sciences.

[46]  M. Aminoff,et al.  Sensory perception in Parkinson disease. , 1997, Archives of neurology.

[47]  M Hallett,et al.  Physiology of Basal Ganglia Disorders: An Overview , 1993, Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques.

[48]  M. Rogers,et al.  Postural adjustments preceding rapid arm movements in parkinsonian subjects , 1987, Neuroscience Letters.

[49]  Thomas Rosemeier,et al.  Interaction of vestibular, somatosensory and visual signals for postural control and motion perception under terrestrial and microgravity conditions—a conceptual model , 1998, Brain Research Reviews.

[50]  Y. Agid,et al.  Axial parkinsonian symptoms can be improved: the role of levodopa and bilateral subthalamic stimulation , 2000, Journal of neurology, neurosurgery, and psychiatry.

[51]  C D Marsden,et al.  Problems with long-term levodopa therapy for Parkinson's disease. , 1994, Clinical neuropharmacology.

[52]  R. Lee,et al.  Evidence for abnormal long-loop reflexes in rigid Parkinsonian patients , 1975, Brain Research.

[53]  A. Lang,et al.  Double-blind evaluation of subthalamic nucleus deep brain stimulation in advanced Parkinson's disease , 1998, Neurology.

[54]  M. Hoehn,et al.  Parkinsonism , 1967, Neurology.

[55]  Z. Schwab,et al.  Projection technique for evaluating surgery in Parkinson’s disease , 1969 .

[56]  M. Borutta,et al.  A defect of kinesthesia in Parkinson's disease , 1995, Movement disorders : official journal of the Movement Disorder Society.

[57]  A. Benabid,et al.  Response to levodopa in parkinsonian patients with bilateral subthalamic nucleus stimulation. , 2002, Brain : a journal of neurology.

[58]  C Kennard,et al.  Influence of sensory manipulation on postural control in Parkinson's disease. , 1993, Journal of neurology, neurosurgery, and psychiatry.

[59]  S Corna,et al.  Subjective perception of body sway , 1999, Journal of neurology, neurosurgery, and psychiatry.

[60]  R. Walker,et al.  Incidence and prediction of falls in Parkinson's disease: a prospective multidisciplinary study , 2002, Journal of neurology, neurosurgery, and psychiatry.

[61]  M. Rizzone,et al.  Deep brain stimulation of the subthalamic nucleus: selection of patients and clinical results , 2001, Neurological Sciences.

[62]  C Maurer,et al.  A multisensory posture control model of human upright stance. , 2003, Progress in brain research.

[63]  J. Burgunder,et al.  Long-term pallidal deep brain stimulation in patients with advanced Parkinson disease: 1-year follow-up study. , 2002, Journal of neurosurgery.

[64]  F. Horak,et al.  Effects of deep brain stimulation and levodopa on postural sway in Parkinson's disease , 2002, Journal of neurology, neurosurgery, and psychiatry.

[65]  V Sturm,et al.  Bilateral high‐frequency stimulation of the internal globus pallidus in advanced Parkinson's disease , 1998, Annals of neurology.

[66]  J. Rothwell,et al.  The impact of deep brain stimulation on executive function in Parkinson's disease. , 2000, Brain : a journal of neurology.

[67]  S. Rapcsak,et al.  Falling and postural deficits due to acute unilateral basal ganglia lesions. , 1989, Archives of neurology.

[68]  G. E. Alexander,et al.  Functional architecture of basal ganglia circuits: neural substrates of parallel processing , 1990, Trends in Neurosciences.

[69]  C. Lücking,et al.  Contractile properties of lower leg muscles are normal in Parkinson's disease. , 1991, Journal of neurology, neurosurgery, and psychiatry.

[70]  L. Nashner,et al.  Postural instability in idiopathic Parkinson's disease: the role of medication and unilateral pallidotomy. , 2002, Brain : a journal of neurology.

[71]  J. Masdeu,et al.  Thalamic astasia: Inability to stand after unilateral thalamic lesions , 1988, Annals of neurology.

[72]  M. Schieppati,et al.  Free and supported stance in Parkinson's disease. The effect of posture and 'postural set' on leg muscle responses to perturbation, and its relation to the severity of the disease. , 1991, Brain : a journal of neurology.

[73]  F. Horak,et al.  Levodopa Reduces Muscle Tone and Lower Extremity Tremor in Parkinson’s Disease , 1995, Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques.

[74]  A Straube,et al.  Visual stabilization of posture. Physiological stimulus characteristics and clinical aspects. , 1984, Brain : a journal of neurology.

[75]  J K Krauss,et al.  Postural control in Parkinson's disease after unilateral posteroventral pallidotomy. , 2000, Brain : a journal of neurology.