Subthalamic nucleus stimulation and dysarthria in Parkinson's disease: a PET study.

In Parkinson's disease, functional imaging studies during limb motor tasks reveal cerebral activation abnormalities that can be reversed by subthalamic nucleus (STN) stimulation. The effect of STN stimulation on parkinsonian dysarthria has not, however, been investigated using PET. The aim of the present study was to evaluate the effect of STN stimulation on regional cerebral blood flow (rCBF) during speech production and silent articulation in patients with Parkinson's disease. Ten Parkinson's disease patients surgically implanted bilaterally in the STN and with significant improvement of their dysarthria induced by STN stimulation were included. Ten healthy control subjects also participated in this study. Control subjects performed six sessions of [15O]H2O-PET scanning corresponding to three duplicated conditions externally cued by an auditory signal. The conditions were: (i) rest; (ii) production of a short, simple sentence; and (iii) silent articulation of the same sentence. Parkinson's disease patients carried out the six PET sessions twice, i.e., in the ON and OFF STN stimulation states. PET data analysis was performed using statistical parametric mapping (SPM99). In control subjects, speech production (SP) compared with rest was associated with increased rCBF bilaterally in the primary motor cortex (M1) corresponding to the orofacial somatotopy, the supplementary motor area (SMA), the associative auditory cortex and the cerebellar hemispheres. Silent articulation (SA) compared with rest induced a bilateral rCBF increase restricted to the orofacial M1 and cerebellar hemispheres. In Parkinson's disease patients in the OFF stimulation condition, during both SP and SA there was a lack of activation in the right orofacial M1 and in the cerebellum, abnormal increased rCBF in the right superior premotor cortex, and overactivation of the SMA. There was also an abnormal, increased rCBF in the dorsolateral prefrontal cortex (DLPFC) only during SP and increased rCBF in the left insula only during SA. In Parkinson's disease patients ON stimulation, for both SP and SA the activation pattern appeared similar to that in control subjects. In conclusion, our results suggest that parkinsonian dysarthria is associated with altered recruitment of the main motor cerebral regions (orofacial M1, cerebellum), and increased involvement of the premotor and prefrontal cortices (DLPFC, SMA, superior premotor cortex). These abnormal activations are different from those reported during hand motor tasks. They could be a compensatory mechanism, but might also arise directly as part of the pathophysiology of Parkinson's disease. STN stimulation tends to reverse these abnormal activations, which is consistent with the observed improvement of Parkinson's disease dysarthria.

[1]  W Fernandez,et al.  Impaired activation of the supplementary motor area in Parkinson's disease is reversed when akinesia is treated with apomorphine , 1992, Annals of neurology.

[2]  R J Wise,et al.  Cerebral areas associated with motor control of speech in humans. , 1997, Journal of applied physiology.

[3]  M. Hariz,et al.  Ventroposterolateral pallidotomy can abolish all parkinsonian symptoms. , 1992, Stereotactic and functional neurosurgery.

[4]  A. Benabid,et al.  Effect on parkinsonian signs and symptoms of bilateral subthalamic nucleus stimulation , 1995, The Lancet.

[5]  Wolfgang Grodd,et al.  Reorganization of Speech Production at the Motor Cortex and Cerebellum following Capsular Infarction: a Follow-up Functional Magnetic Resonance Imaging Study , 2002, Neurocase.

[6]  P. Strick,et al.  Motor areas of the medial wall: a review of their location and functional activation. , 1996, Cerebral cortex.

[7]  O. Creutzfeldt,et al.  Neuronal activity in the human lateral temporal lobe , 1989, Experimental Brain Research.

[8]  A. Cools,et al.  Evidence for lateral premotor and parietal overactivity in Parkinson's disease during sequential and bimanual movements. A PET study. , 1998, Brain : a journal of neurology.

[9]  S. Fahn.  Unified Parkinson's Disease Rating Scale , 1987 .

[10]  M. Hallett,et al.  A PET study of sequential finger movements of varying length in patients with Parkinson's disease. , 1999, Brain : a journal of neurology.

[11]  D Le Bihan,et al.  Postoperative speech disorder after medial frontal surgery , 2003, Neurology.

[12]  A. Marchal,et al.  Speech production and speech modelling , 1990 .

[13]  W. Penfield.  The Cerebral Cortex of Man , 1950 .

[14]  S. Bookheimer,et al.  Activation of language cortex with automatic speech tasks , 2000, Neurology.

[15]  Iwona Stepniewska,et al.  Pallidal and cerebellar afferents to pre‐supplementary motor area thalamocortical neurons in the owl monkey: A multiple labeling study , 2000, The Journal of comparative neurology.

[16]  Richard S. J. Frackowiak,et al.  Changes in cerebral activity pattern due to subthalamic nucleus or internal pallidum stimulation in Parkinson's disease , 1997, Annals of neurology.

[17]  G. McCarthy,et al.  Functional organization of human supplementary motor cortex studied by electrical stimulation , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  S. Countryman,et al.  Intensive voice treatment (LSVT®) for patients with Parkinson's disease: a 2 year follow up , 2001 .

[19]  Sylvain Houle,et al.  Functional neuroimaging of cerebellar activation during single word reading and verb generation in stuttering and nonstuttering adults , 2001, Neuroscience Letters.

[20]  W. Gibb,et al.  The relevance of the Lewy body to the pathogenesis of idiopathic Parkinson's disease. , 1988, Journal of neurology, neurosurgery, and psychiatry.

[21]  A. Benabid,et al.  Bilateral subthalamic stimulation effects on oral force control in Parkinson's disease , 2003, Journal of Neurology.

[22]  F. Mauguière,et al.  The role of the insular cortex in temporal lobe epilepsy , 2000, Annals of neurology.

[23]  A. Lang,et al.  An investigation of the effects of subthalamic nucleus stimulation on acoustic measures of voice , 2000, Movement disorders : official journal of the Movement Disorder Society.

[24]  J. Villemure,et al.  How do parkinsonian signs return after discontinuation of subthalamic DBS? , 2003, Neurology.

[25]  F. Chollet,et al.  The ipsilateral cerebellar hemisphere is overactive during hand movements in akinetic parkinsonian patients. , 1997, Brain : a journal of neurology.

[26]  H. Klawans.  Individual manifestations of Parkinson's disease after ten or more years of levodopa , 1986, Movement disorders : official journal of the Movement Disorder Society.

[27]  O. Creutzfeldt,et al.  Neuronal activity in the human lateral temporal lobe , 2004, Experimental Brain Research.

[28]  Kamil Ugurbil,et al.  A functional magnetic resonance imaging study of the role of left posterior superior temporal gyrus in speech production: implications for the explanation of conduction aphasia , 2000, Neuroscience Letters.

[29]  Colin Humphries,et al.  Role of left posterior superior temporal gyrus in phonological processing for speech perception and production , 2001, Cogn. Sci..

[30]  M. Schwaiger,et al.  Event-related functional magnetic resonance imaging in Parkinson's disease before and after levodopa. , 2001, Brain : a journal of neurology.

[31]  E. Miller,et al.  The Prefrontal Cortex Complex Neural Properties for Complex Behavior , 1999, Neuron.

[32]  A. Stracciari,et al.  Development of palilalia after stereotaxic thalamotomy in Parkinson's disease. , 1993, European neurology.

[33]  M Wiesendanger,et al.  Cerebellothalamocortical and pallidothalamocortical projections to the primary and supplementary motor cortical areas: A multiple tracing study in macaque monkeys , 1994, The Journal of comparative neurology.

[34]  D J Brooks,et al.  Impaired activation of frontal areas during movement in Parkinson's disease: a PET study. , 1993, Advances in neurology.

[35]  Rajesh Pahwa,et al.  Stroke , 1987, Neurology.

[36]  V. Walsh,et al.  TMS Produces Two Dissociable Types of Speech Disruption , 2001, NeuroImage.

[37]  A. Benabid,et al.  Effect of stimulation of the subthalamic nucleus on oral control of patients with parkinsonism , 1999, Journal of neurology, neurosurgery, and psychiatry.

[38]  P. Goldman-Rakic,et al.  Prefrontal connections of medial motor areas in the rhesus monkey , 1993, The Journal of comparative neurology.

[39]  Y. Samson,et al.  Movement‐ and task‐related activations of motor cortical areas: A positron emission tomographic study , 1994, Annals of neurology.

[40]  Richard S. J. Frackowiak,et al.  Impaired mesial frontal and putamen activation in Parkinson's disease: A positron emission tomography study , 1992, Annals of neurology.

[41]  I. Daum,et al.  Kinematic analysis of articulatory movements in central motor disorders , 1997, Movement disorders : official journal of the Movement Disorder Society.

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

[43]  C. Tamminga.  Images in neuroscience , 1998 .

[44]  F. Chollet,et al.  Cortical motor reorganization in akinetic patients with Parkinson's disease: a functional MRI study. , 2000, Brain : a journal of neurology.

[45]  C. Marsden,et al.  Recent Developments in Parkinson's Disease , 1986 .

[46]  Peter Ford Dominey,et al.  Effects of subthalamic nucleus stimulation on actual and imagined movement in Parkinson's disease : a PET study , 2002, Journal of Neurology.

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

[48]  Karl J. Friston,et al.  Role of the human rostral supplementary motor area and the basal ganglia in motor sequence control: investigations with H2 15O PET. , 1998, Journal of neurophysiology.

[49]  G. Johannsson,et al.  Growth Hormone Deficiency: Strategies and Indications to Continue Growth Hormone Therapy in Transition from Adolescence to Adult Life , 2003, Hormone Research in Paediatrics.

[50]  J. Abbs,et al.  Force transducers for the evaluation of labial, lingual, and mandibular motor impairments. , 1983, Journal of speech and hearing research.

[51]  N. Dronkers.  A new brain region for coordinating speech articulation , 1996, Nature.

[52]  L. Raming,et al.  Voice treatment for patients with Parkinson desease: Development of an approach and preliminary efficacy data , 1994 .

[53]  R.N.Dej.,et al.  The Cerebral Cortex of Man , 1951, Neurology.

[54]  D. Darby,et al.  Identification of brain region for coordinating speech articulation , 1997, The Lancet.

[55]  W. Grodd,et al.  Does the cerebellum contribute to cognitive aspects of speech production? A functional magnetic resonance imaging (fMRI) study in humans , 1998, Neuroscience Letters.

[56]  R. Ingham,et al.  A PET study of the neural systems of stuttering , 1996, Nature.

[57]  W. Friedman,et al.  Changes in vocal intensity in Parkinson's disease following pallidotomy surgery. , 2000, Journal of voice : official journal of the Voice Foundation.

[58]  Serge Pinto,et al.  Effect of bilateral stimulation of the subthalamic nucleus on parkinsonian dysarthria , 2003, Brain and Language.

[59]  F. Darley,et al.  Diagnosis of Motor Speech Disorders , 1975 .

[60]  A W Downie,et al.  Parkinson's disease: disability, review, and management. , 1986, British medical journal.

[61]  Michèle Gentil,et al.  Organization of the Articulatory System: Peripheral Mechanisms and Central Coordination , 1990 .

[62]  C. Ludlow,et al.  Manual of Nerve Conduction Velocity and Clinical Neurophysiology, 3rd Ed. , 1994, Neurology.

[63]  Karl J. Friston,et al.  Hearing and saying. The functional neuro-anatomy of auditory word processing. , 1996, Brain : a journal of neurology.

[64]  H H Holcomb,et al.  Images in neuroscience. Progressive dysarthria: structural and brain correlations. , 1996, The American journal of psychiatry.

[65]  R. Ingham,et al.  Hypophonia in Parkinson’s disease: Neural correlates of voice treatment revealed by PET , 2003 .

[66]  S. Fahn.  Members of the UPDRS Development Committee. Unified Parkinson's Disease Rating Scale , 1987 .

[67]  Peter Ford Dominey,et al.  Overactivation of primary motor cortex is asymmetrical in hemiparkinsonian patients , 2000, Neuroreport.

[68]  A. Benabid,et al.  Effect of Bilateral Stimulation of the Subthalamic Nucleus on Parkinsonian Voice , 2001, Brain and Language.

[69]  M Lotze,et al.  The representation of articulation in the primary sensorimotor cortex , 2000, Neuroreport.

[70]  Karl J. Friston,et al.  Cortical areas and the selection of movement: a study with positron emission tomography , 1991, Experimental Brain Research.

[71]  D. Guehl,et al.  High-frequency stimulation of the globus pallidus internalis in Parkinson's disease: a study of seven cases. , 1997, Journal of neurosurgery.

[72]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[73]  C Büchel,et al.  Brain regions involved in articulation , 1999, The Lancet.

[74]  P. MacNeilage,et al.  Motor mechanisms in speech ontogeny: phylogenetic, neurobiological and linguistic implications , 2001, Current Opinion in Neurobiology.

[75]  P. Pollak,et al.  Effects of levodopa on finger and orofacial movements in Parkinson's disease , 1998, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[76]  R. M. Murray,et al.  Functional anatomy of inner speech and auditory verbal imagery , 1995, Schizophrenia Research.

[77]  H. Tachibana,et al.  Cerebral blood flow in pure dysarthria: role of frontal cortical hypoperfusion. , 1999, Stroke.

[78]  Jun Tanji,et al.  The relationship between MI and SMA afferents and cerebellar and pallidal efferents in the macaque monkey , 2002, Somatosensory & motor research.

[79]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[80]  B Conrad,et al.  A positron emission tomographic study of subthalamic nucleus stimulation in Parkinson disease: enhanced movement-related activity of motor-association cortex and decreased motor cortex resting activity. , 1999, Archives of neurology.

[81]  H. Rusinek,et al.  Functional magnetic resonance imaging of human brain activity in a verbal fluency task , 1998, Journal of neurology, neurosurgery, and psychiatry.

[82]  T. Robbins,et al.  Planning and spatial working memory following frontal lobe lesions in man , 1990, Neuropsychologia.

[83]  P. T. Fox,et al.  Positron emission tomographic studies of the cortical anatomy of single-word processing , 1988, Nature.