Deep brain stimulation suppresses pallidal low frequency activity in patients with phasic dystonic movements.

Deep brain stimulation of the globus pallidus internus alleviates involuntary movements in patients with dystonia. However, the mechanism is still not entirely understood. One hypothesis is that deep brain stimulation suppresses abnormally enhanced synchronized oscillatory activity within the motor cortico-basal ganglia network. Here, we explore deep brain stimulation-induced modulation of pathological low frequency (4-12 Hz) pallidal activity that has been described in local field potential recordings in patients with dystonia. Therefore, local field potentials were recorded from 16 hemispheres in 12 patients undergoing deep brain stimulation for severe dystonia using a specially designed amplifier allowing simultaneous high frequency stimulation at therapeutic parameter settings and local field potential recordings. For coherence analysis electroencephalographic activity (EEG) over motor areas and electromyographic activity (EMG) from affected neck muscles were recorded before and immediately after cessation of high frequency stimulation. High frequency stimulation led to a significant reduction of mean power in the 4-12 Hz band by 24.8 ± 7.0% in patients with predominantly phasic dystonia. A significant decrease of coherence between cortical EEG and pallidal local field potential activity in the 4-12 Hz range was revealed for the time period of 30 s after switching off high frequency stimulation. Coherence between EMG activity and pallidal activity was mainly found in patients with phasic dystonic movements where it was suppressed after high frequency stimulation. Our findings suggest that high frequency stimulation may suppress pathologically enhanced low frequency activity in patients with phasic dystonia. These dystonic features are the quickest to respond to high frequency stimulation and may thus directly relate to modulation of pathological basal ganglia activity, whereas improvement in tonic features may depend on long-term plastic changes within the motor network.

[1]  J. Winn,et al.  Brain , 1878, The Lancet.

[2]  J. Penney,et al.  The functional anatomy of basal ganglia disorders , 1989, Trends in Neurosciences.

[3]  M. Delong,et al.  Primate models of movement disorders of basal ganglia origin , 1990, Trends in Neurosciences.

[4]  P. V. van Harten,et al.  [Tardive dystonia]. , 1992, Nederlands tijdschrift voor geneeskunde.

[5]  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.

[6]  A M Amjad,et al.  A framework for the analysis of mixed time series/point process data--theory and application to the study of physiological tremor, single motor unit discharges and electromyograms. , 1995, Progress in biophysics and molecular biology.

[7]  M. Hallett,et al.  The pathophysiology of primary dystonia. , 1998, Brain : a journal of neurology.

[8]  Klaus Mewes,et al.  Neuronal activity in the basal ganglia in patients with generalized dystonia and hemiballismus , 1999, Annals of neurology.

[9]  J. Burgunder,et al.  Bilateral stimulation of globus pallidus internus for treatment of cervical dystonia , 1999, The Lancet.

[10]  J. Marsden,et al.  Frequency analysis of EMG activity in patients with idiopathic torticollis. , 2000, Brain : a journal of neurology.

[11]  S. Hemm,et al.  Treatment of DYT1-generalised dystonia by stimulation of the internal globus pallidus , 2000, The Lancet.

[12]  K. Bhatia,et al.  Descending control of muscles in patients with cervical dystonia , 2002, Movement disorders : official journal of the Movement Disorder Society.

[13]  Joachim K. Krauss,et al.  Deep Brain Stimulation for Dystonia in Adults , 2003, Stereotactic and Functional Neurosurgery.

[14]  J. Volkmann,et al.  Deep brain stimulation for dystonia: Patient selection and evaluation , 2002, Movement disorders : official journal of the Movement Disorder Society.

[15]  R. Miall,et al.  Involvement of the medial pallidum in focal myoclonic dystonia: A clinical and neurophysiological case study , 2002, Movement disorders : official journal of the Movement Disorder Society.

[16]  J. Jankovic,et al.  Basal Ganglia Neuronal Discharge in Primary and Secondary Dystonia in Patients Undergoing Pallidotomy , 2003, Neurosurgery.

[17]  A. Oliviero,et al.  Patterning of globus pallidus local field potentials differs between Parkinson's disease and dystonia. , 2003, Brain : a journal of neurology.

[18]  A. Kupsch,et al.  Modulation of motor cortex excitability by pallidal stimulation in patients with severe dystonia , 2003, Neurology.

[19]  C. Vaughan,et al.  Rectification and non-linear pre-processing of EMG signals for cortico-muscular analysis , 2003, Journal of Neuroscience Methods.

[20]  P. Brown.  Oscillatory nature of human basal ganglia activity: Relationship to the pathophysiology of Parkinson's disease , 2003, Movement disorders : official journal of the Movement Disorder Society.

[21]  J F Stein,et al.  Post‐operative progress of dystonia patients following globus pallidus internus deep brain stimulation , 2003, European journal of neurology.

[22]  Hagai Bergman,et al.  Oscillatory activity in the basal ganglia--relationship to normal physiology and pathophysiology. , 2004, Brain : a journal of neurology.

[23]  John Yianni,et al.  Deep Brain Stimulation for Dystonia , 2004, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[24]  Antonio Oliviero,et al.  Effects of stimulation of the subthalamic area on oscillatory pallidal activity in Parkinson's disease , 2004, Experimental Neurology.

[25]  Ron Alterman,et al.  Deep brain stimulation for dystonia , 2004, Expert review of medical devices.

[26]  J. Dostrovsky,et al.  Neuronal Oscillations in the Basal Ganglia and Movement Disorders: Evidence from Whole Animal and Human Recordings , 2004, The Journal of Neuroscience.

[27]  S. Hemm,et al.  Electrical stimulation of the globus pallidus internus in patients with primary generalized dystonia: long-term results. , 2004, Journal of neurosurgery.

[28]  Andrew J Lees,et al.  Patterns of EMG–EMG coherence in limb dystonia , 2004, Movement disorders : official journal of the Movement Disorder Society.

[29]  A. Priori,et al.  Rhythm-specific pharmacological modulation of subthalamic activity in Parkinson's disease , 2004, Experimental Neurology.

[30]  Tipu Z. Aziz,et al.  Extracting burst and tonic components from surface electromyograms in dystonia using adaptive wavelet shrinkage , 2004, Journal of Neuroscience Methods.

[31]  Peter Brown,et al.  Basal ganglia local field potential activity: Character and functional significance in the human , 2005, Clinical Neurophysiology.

[32]  Tardive dystonia , 2005, Current treatment options in neurology.

[33]  Houeto Jean-Luc.  [Parkinson's disease]. , 2022, La Revue du praticien.

[34]  P. Ferroli,et al.  Long-term high-frequency bilateral pallidal stimulation for neuroleptic-induced tardive dystonia. Report of two cases. , 2005, Journal of neurosurgery.

[35]  G. Deuschl,et al.  Treatment of severe tardive dystonia with pallidal deep brain stimulation , 2005, Neurology.

[36]  A. Destée,et al.  Bilateral deep-brain stimulation of the globus pallidus in primary generalized dystonia. , 2005, The New England journal of medicine.

[37]  Tipu Z. Aziz,et al.  A dominant bursting electromyograph pattern in dystonic conditions predicts an early response to pallidal stimulation , 2006, Journal of Clinical Neuroscience.

[38]  J. Krauss,et al.  Patterns of reoccurrence of segmental dystonia after discontinuation of deep brain stimulation , 2006, Journal of Neurology, Neurosurgery & Psychiatry.

[39]  P. Mulder,et al.  Long-term aesthetic results of frontoorbital correction for frontal plagiocephaly. , 2006, Journal of neurosurgery.

[40]  Paul Alan Cox,et al.  BMAA selectively injures motor neurons via AMPA/kainate receptor activation , 2006, Experimental Neurology.

[41]  J A Obeso,et al.  Slow oscillatory activity and levodopa-induced dyskinesias in Parkinson's disease. , 2006, Brain : a journal of neurology.

[42]  P. Brown,et al.  Oscillatory pallidal local field potential activity correlates with involuntary EMG in dystonia , 2006, Neurology.

[43]  G. Deuschl,et al.  Pallidal deep-brain stimulation in primary generalized or segmental dystonia. , 2006, The New England journal of medicine.

[44]  Pablo Mir,et al.  Abnormalities in motor cortical plasticity differentiate manifesting and nonmanifesting DYT1 carriers , 2006, Movement disorders : official journal of the Movement Disorder Society.

[45]  J. Stein,et al.  Different mechanisms may generate sustained hypertonic and rhythmic bursting muscle activity in idiopathic dystonia , 2006, Experimental Neurology.

[46]  J. Rothwell,et al.  Changes in blink reflex excitability after globus pallidus internus stimulation for dystonia , 2006, Movement disorders : official journal of the Movement Disorder Society.

[47]  P. Brown,et al.  Neuronal activity in globus pallidus interna can be synchronized to local field potential activity over 3–12 Hz in patients with dystonia , 2006, Experimental Neurology.

[48]  Mandy Miller Koop,et al.  Intra-operative STN DBS attenuates the prominent beta rhythm in the STN in Parkinson's disease , 2006, Experimental Neurology.

[49]  Shouyan Wang,et al.  Use of surface electromyography to assess and select patients with idiopathic dystonia for bilateral pallidal stimulation. , 2006, Journal of neurosurgery.

[50]  P. Brown,et al.  Reduction in subthalamic 8–35 Hz oscillatory activity correlates with clinical improvement in Parkinson's disease , 2006, The European journal of neuroscience.

[51]  Tatiana Witjas,et al.  Bilateral deep brain stimulation of the globus pallidus to treat tardive dyskinesia. , 2007, Archives of general psychiatry.

[52]  L. Bour,et al.  Local field potentials and oscillatory activity of the internal globus pallidus in myoclonus–dystonia , 2007, Movement disorders : official journal of the Movement Disorder Society.

[53]  H. Bergman,et al.  Pathological synchronization in Parkinson's disease: networks, models and treatments , 2007, Trends in Neurosciences.

[54]  S. Hassin-Baer,et al.  Deep brain stimulation of the internal globus pallidus for refractory tardive dystonia. , 2007, Parkinsonism & related disorders.

[55]  P. Starr,et al.  Pallidal deep brain stimulation in patients with cranial–cervical dystonia (Meige syndrome) , 2007, Movement disorders : official journal of the Movement Disorder Society.

[56]  Robert Chen,et al.  Changes in cortical and pallidal oscillatory activity during the execution of a sensory trick in patients with cervical dystonia , 2007, Experimental Neurology.

[57]  J. Dostrovsky,et al.  Long-term outcome of bilateral pallidal deep brain stimulation for primary cervical dystonia , 2007, Neurology.

[58]  K. Dujardin,et al.  Bilateral, pallidal, deep-brain stimulation in primary generalised dystonia: a prospective 3 year follow-up study , 2007, The Lancet Neurology.

[59]  M. Eliasziw,et al.  The Canadian multicentre study of deep brain stimulation for cervical dystonia. , 2007, Brain : a journal of neurology.

[60]  Peter Brown,et al.  Paradoxes of functional neurosurgery: Clues from basal ganglia recordings , 2008, Movement disorders : official journal of the Movement Disorder Society.

[61]  Tipu Aziz,et al.  Movement‐related synchronization of gamma activity is lateralized in patients with dystonia , 2008, The European journal of neuroscience.

[62]  Andrea A. Kühn,et al.  High-Frequency Stimulation of the Subthalamic Nucleus Suppresses Oscillatory β Activity in Patients with Parkinson's Disease in Parallel with Improvement in Motor Performance , 2008, The Journal of Neuroscience.

[63]  F. Cogiamanian,et al.  Subthalamic local field potential oscillations during ongoing deep brain stimulation in Parkinson's disease , 2008, Brain Research Bulletin.

[64]  J. Stein,et al.  The sensory and motor representation of synchronized oscillations in the globus pallidus in patients with primary dystonia. , 2008, Brain : a journal of neurology.

[65]  N. Murase,et al.  Bilateral deep brain stimulation of the globus pallidus internus in tardive dystonia , 2008, Movement disorders : official journal of the Movement Disorder Society.

[66]  A. Engel,et al.  Is the synchronization between pallidal and muscle activity in primary dystonia due to peripheral afferance or a motor drive? , 2008, Brain : a journal of neurology.

[67]  J. Obeso,et al.  Efficacy and safety of pallidal stimulation in primary dystonia: results of the Spanish multicentric study , 2009, Journal of Neurology, Neurosurgery & Psychiatry.

[68]  Andrea A. Kühn,et al.  Pathological synchronisation in the subthalamic nucleus of patients with Parkinson's disease relates to both bradykinesia and rigidity , 2009, Experimental Neurology.

[69]  D. Gruber,et al.  Long-term effects of pallidal deep brain stimulation in tardive dystonia , 2009, Neurology.

[70]  Nicola J. Ray,et al.  The role of the subthalamic nucleus in response inhibition: Evidence from deep brain stimulation for Parkinson's disease , 2009, Neuropsychologia.

[71]  M. Vidailhet,et al.  Pathophysiology of dystonia , 2009, Current opinion in neurology.

[72]  P. Starr,et al.  Induction of Bradykinesia with Pallidal Deep Brain Stimulation in Patients with Cranial-Cervical Dystonia , 2009, Stereotactic and Functional Neurosurgery.

[73]  A. Kupsch,et al.  Automated Optimization of Subcortical Cerebral MR Imaging−Atlas Coregistration for Improved Postoperative Electrode Localization in Deep Brain Stimulation , 2009, American Journal of Neuroradiology.

[74]  Philip J. Hahn,et al.  Network perspectives on the mechanisms of deep brain stimulation , 2010, Neurobiology of Disease.

[75]  M. Hariz,et al.  Which patients with dystonia benefit from deep brain stimulation? A metaregression of individual patient outcomes , 2010, Journal of Neurology, Neurosurgery & Psychiatry.

[76]  T. Gasserc,et al.  EFNS guidelines on diagnosis and treatment of primary dystonias , 2010 .

[77]  P. Brown,et al.  Deep brain stimulation can suppress pathological synchronisation in parkinsonian patients , 2010, Journal of Neurology, Neurosurgery & Psychiatry.

[78]  J. Burgunder,et al.  Factors predicting protracted improvement after pallidal DBS for primary dystonia: the role of age and disease duration , 2011, Journal of Neurology.

[79]  Matthew D. Johnson,et al.  Mechanisms and targets of deep brain stimulation in movement disorders , 2008, Neurotherapeutics.

[80]  D. Grabli,et al.  Les nouvelles approches des dystonies (clinique, génétique et hypothèses physio-pathologiques) , 2011 .

[81]  J. Rothwell,et al.  Shaping reversibility? Long-term deep brain stimulation in dystonia: the relationship between effects on electrophysiology and clinical symptoms. , 2011, Brain : a journal of neurology.

[82]  P. Starr,et al.  Treatment of dystonia with deep brain stimulation , 2008, Neurotherapeutics.

[83]  [New approaches in dystonia (clinical features, genetic issues and pathophysiology]. , 2011, Bulletin de l'Academie nationale de medecine.

[84]  J. Rothwell,et al.  Deep brain stimulation effects in dystonia: Time course of electrophysiological changes in early treatment , 2011, Movement disorders : official journal of the Movement Disorder Society.

[85]  P. Starr,et al.  Deep brain stimulation in children: experience and technical pearls. , 2011, Journal of neurosurgery. Pediatrics.

[86]  Jerrold L. Vitek,et al.  External pallidal stimulation improves parkinsonian motor signs and modulates neuronal activity throughout the basal ganglia thalamic network , 2012, Experimental Neurology.

[87]  J. Dostrovsky,et al.  Oscillatory activity in the globus pallidus internus: Comparison between Parkinson’s disease and dystonia , 2012, Clinical Neurophysiology.

[88]  Günther Deuschl,et al.  Pallidal deep brain stimulation in patients with primary generalised or segmental dystonia: 5-year follow-up of a randomised trial , 2012, The Lancet Neurology.

[89]  Alexander L Green,et al.  Subthalamic nucleus activity optimizes maximal effort motor responses in Parkinson's disease. , 2012, Brain : a journal of neurology.

[90]  Wolf-Julian Neumann,et al.  Enhanced low‐frequency oscillatory activity of the subthalamic nucleus in a patient with dystonia , 2012, Movement disorders : official journal of the Movement Disorder Society.

[91]  Peter Brown,et al.  Scaling of Movement Is Related to Pallidal γ Oscillations in Patients with Dystonia , 2012, The Journal of Neuroscience.

[92]  V. Visser-Vandewalle,et al.  Efficacy and safety of deep brain stimulation in patients with medication-induced tardive dyskinesia and/or dystonia: a systematic review. , 2012, The Journal of clinical psychiatry.

[93]  P. Starr,et al.  Shorter disease duration correlates with improved long-term deep brain stimulation outcomes in young-onset DYT1 dystonia. , 2012, Neurosurgery.

[94]  J. Obeso,et al.  Impairment of brain vessels may contribute to mortality in patients with Parkinson's disease , 2012, Movement disorders : official journal of the Movement Disorder Society.

[95]  Interhemispheric difference of pallidal local field potential activity in cervical dystonia , 2013, Journal of Neurology, Neurosurgery & Psychiatry.

[96]  P. Brown,et al.  Adaptive Deep Brain Stimulation In Advanced Parkinson Disease , 2013, Annals of neurology.

[97]  K. Bhatia,et al.  Primary and secondary dystonic syndromes: an update , 2013, Current opinion in neurology.

[98]  K. Ashkan,et al.  Proportion of life lived with dystonia inversely correlates with response to pallidal deep brain stimulation in both primary and secondary childhood dystonia , 2013, Developmental medicine and child neurology.

[99]  R. Alterman,et al.  Deep brain stimulation in DYT1 dystonia: a 10-year experience. , 2013, Neurosurgery.

[100]  M. Hallett,et al.  Emerging concepts in the physiological basis of dystonia , 2013, Movement disorders : official journal of the Movement Disorder Society.

[101]  M. Hellmich,et al.  Effects of deep brain stimulation in dyskinetic cerebral palsy: A meta‐analysis , 2013, Movement disorders : official journal of the Movement Disorder Society.

[102]  A. Lozano,et al.  Bilateral pallidal stimulation in cervical dystonia: blinded evidence of benefit beyond 5 years. , 2013, Brain : a journal of neurology.

[103]  P. Brown,et al.  Different patterns of local field potentials from limbic DBS targets in patients with major depressive and obsessive compulsive disorder , 2014, Molecular Psychiatry.

[104]  A. Engel,et al.  Asymmetric pallidal neuronal activity in patients with cervical dystonia , 2014, Front. Syst. Neurosci..

[105]  G. Deuschl,et al.  Pallidal neurostimulation in patients with medication-refractory cervical dystonia: a randomised, sham-controlled trial , 2014, The Lancet Neurology.