The STN beta-band profile in Parkinson's disease is stationary and shows prolonged attenuation after deep brain stimulation

Producing accurate movements may rely on the functional independence of sensorimotor circuits within basal ganglia nuclei. In parkinsonism there is abnormal synchrony of electrical activity within these circuits that results in a loss of independence across motor channels. Local field potential (LFP) recordings reflect the summation of local electrical fields and an increase in LFP power reflects increased synchrony in local neuronal networks. We recorded LFPs from the subthalamic nucleus (STN) deep brain stimulation (DBS) lead in the operating room in 22 cases from 16 subjects with Parkinson's disease (PD) who were off medication. There was elevated LFP power at beta frequencies (13-35 Hz) at rest. The LFP spectral profile was consistent across several periods of rest that were separated by movement and/or DBS, and appeared to be a relatively stationary phenomenon. The spectral profile and frequencies of the beta-band peak(s) varied among subjects but were similar between the right and left STNs within certain individuals. These results suggest that the LFP spectrum at rest may characterize a "signature" rhythm for an individual with PD. Beta-band power was attenuated after intra-operative STN DBS (p<0.05). The attenuation lasted for 10 s after short periods (30 s) and for up to 50 s after longer periods (5 min) of DBS. The finding that longer periods of DBS attenuated beta power for a longer time suggests that there may be long-acting functional changes to networks in the STN in PD after chronic DBS.

[1]  J. Fermaglich Electric Fields of the Brain: The Neurophysics of EEG , 1982 .

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

[3]  A. Kondacs,et al.  Long-term intra-individual variability of the background EEG in normals , 1999, Clinical Neurophysiology.

[4]  P. Brown,et al.  Event-related beta desynchronization in human subthalamic nucleus correlates with motor performance. , 2004, Brain : a journal of neurology.

[5]  Mandy Miller Koop,et al.  Improvement in a quantitative measure of bradykinesia after microelectrode recording in patients with Parkinson's disease during deep brain stimulation surgery , 2006, Movement disorders : official journal of the Movement Disorder Society.

[6]  G. Heit,et al.  Regular Article Intra-operative STN DBS attenuates the prominent beta rhythm in the STN in Parkinson's disease , 2006 .

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

[8]  A. Benabid,et al.  Effect of high-frequency stimulation of the subthalamic nucleus on the neuronal activities of the substantia nigra pars reticulata and ventrolateral nucleus of the thalamus in the rat , 2000, Neuroscience.

[9]  J. Marsden,et al.  Intermuscular coherence in Parkinson's disease: effects of subthalamic nucleus stimulation , 2001, Neuroreport.

[10]  J. Dostrovsky,et al.  Effects of apomorphine on subthalamic nucleus and globus pallidus internus neurons in patients with Parkinson's disease. , 2001, Journal of neurophysiology.

[11]  Janey Prodoehl,et al.  Effects of deep brain stimulation and medication on bradykinesia and muscle activation in Parkinson's disease. , 2003, Brain : a journal of neurology.

[12]  M R DeLong,et al.  The primate subthalamic nucleus. III. Changes in motor behavior and neuronal activity in the internal pallidum induced by subthalamic inactivation in the MPTP model of parkinsonism. , 1994, Journal of neurophysiology.

[13]  P. Brown,et al.  Dopamine depletion increases the power and coherence of β‐oscillations in the cerebral cortex and subthalamic nucleus of the awake rat , 2005, The European journal of neuroscience.

[14]  J. Mink THE BASAL GANGLIA: FOCUSED SELECTION AND INHIBITION OF COMPETING MOTOR PROGRAMS , 1996, Progress in Neurobiology.

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

[16]  A. Priori,et al.  Movement-related modulation of neural activity in human basal ganglia and its L-DOPA dependency: recordings from deep brain stimulation electrodes in patients with Parkinson's disease , 2002, Neurological Sciences.

[17]  E. Vaadia,et al.  Physiological aspects of information processing in the basal ganglia of normal and parkinsonian primates , 1998, Trends in Neurosciences.

[18]  Vladimir Litvak,et al.  Excessive synchronization of basal ganglia neurons at 20 Hz slows movement in Parkinson's disease , 2007, Experimental Neurology.

[19]  E. Vaadia,et al.  Firing Patterns and Correlations of Spontaneous Discharge of Pallidal Neurons in the Normal and the Tremulous 1-Methyl-4-Phenyl-1,2,3,6-Tetrahydropyridine Vervet Model of Parkinsonism , 2000, The Journal of Neuroscience.

[20]  H. Bergman,et al.  Information processing, dimensionality reduction and reinforcement learning in the basal ganglia , 2003, Progress in Neurobiology.

[21]  L. Tremblay,et al.  Responses of pallidal neurons to striatal stimulation in intact waking monkeys , 1989, Brain Research.

[22]  P. Brown,et al.  Different functional loops between cerebral cortex and the subthalmic area in Parkinson's disease. , 2006, Cerebral cortex.

[23]  P. Strick,et al.  Multiple output channels in the basal ganglia. , 1993, Science.

[24]  H. Bergman,et al.  Neurons in the globus pallidus do not show correlated activity in the normal monkey, but phase-locked oscillations appear in the MPTP model of parkinsonism. , 1995, Journal of neurophysiology.

[25]  J. Dostrovsky,et al.  Synchronized Neuronal Discharge in the Basal Ganglia of Parkinsonian Patients Is Limited to Oscillatory Activity , 2002, The Journal of Neuroscience.

[26]  M. Delong,et al.  Functional and pathophysiological models of the basal ganglia , 1996, Current Opinion in Neurobiology.

[27]  Shlomo Elias,et al.  Complex Locking Rather Than Complete Cessation of Neuronal Activity in the Globus Pallidus of a 1-Methyl-4-Phenyl-1,2,3,6-Tetrahydropyridine-Treated Primate in Response to Pallidal Microstimulation , 2004, The Journal of Neuroscience.

[28]  C. Hammond,et al.  High-frequency stimulation produces a transient blockade of voltage-gated currents in subthalamic neurons. , 2001, Journal of neurophysiology.

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

[30]  A. Priori,et al.  Subthalamic oscillatory activities at beta or higher frequency do not change after high-frequency DBS in Parkinson's disease , 2006, Brain Research Bulletin.

[31]  L. Defebvre,et al.  Intermuscular coherence in Parkinson's disease: relationship to bradykinesia , 2001, Neuroreport.

[32]  A. Oliviero,et al.  Movement-related changes in synchronization in the human basal ganglia. , 2002, Brain : a journal of neurology.

[33]  M Abeles,et al.  Activity of Pallidal and Striatal Tonically Active Neurons Is Correlated in MPTP-Treated Monkeys But Not in Normal Monkeys , 2001, The Journal of Neuroscience.

[34]  Peter Brown,et al.  Effects of low-frequency stimulation of the subthalamic nucleus on movement in Parkinson's disease , 2007, Experimental Neurology.

[35]  G. Heit,et al.  Bilateral subthalamic nucleus deep brain stimulation improves certain aspects of postural control in Parkinson's disease, whereas medication does not , 2006, Movement disorders : official journal of the Movement Disorder Society.

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

[37]  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.

[38]  H. Bergman,et al.  The primate subthalamic nucleus. II. Neuronal activity in the MPTP model of parkinsonism. , 1994, Journal of neurophysiology.

[39]  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.

[40]  T. Hastie,et al.  Quantitative measurements of alternating finger tapping in Parkinson's disease correlate with UPDRS motor disability and reveal the improvement in fine motor control from medication and deep brain stimulation , 2005, Movement disorders : official journal of the Movement Disorder Society.

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

[42]  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.

[43]  A. Priori,et al.  Low-frequency subthalamic oscillations increase after deep brain stimulation in Parkinson's disease , 2006, Brain Research Bulletin.

[44]  J. Dostrovsky,et al.  Dependence of subthalamic nucleus oscillations on movement and dopamine in Parkinson's disease. , 2002, Brain : a journal of neurology.

[45]  D. Vaillancourt,et al.  Effects of deep brain stimulation and medication on strength, bradykinesia, and electromyographic patterns of the ankle joint in Parkinson's disease , 2006, Movement disorders : official journal of the Movement Disorder Society.

[46]  T. Sejnowski,et al.  Correlated neuronal activity and the flow of neural information , 2001, Nature Reviews Neuroscience.

[47]  A. Graybiel,et al.  Synchronous, Focally Modulated β-Band Oscillations Characterize Local Field Potential Activity in the Striatum of Awake Behaving Monkeys , 2003, The Journal of Neuroscience.