Low-beta cortico-pallidal coherence decreases during movement and correlates with overall reaction time

Abstract Beta band oscillations (13–30 Hz) are a hallmark of cortical and subcortical structures that are part of the motor system. In addition to local population activity, oscillations also provide a means for synchronization of activity between regions. Here we examined the role of beta band coherence between the internal globus pallidus (GPi) and (motor) cortex during a simple reaction time task performed by nine patients with idiopathic dystonia. We recorded local field potentials from deep brain stimulation (DBS) electrodes implanted in bilateral GPi in combination with simultaneous whole‐head magneto‐encephalography (MEG). Patients responded to visually presented go or stop‐signal cues by pressing a button with left or right hand. Although coherence between signals from DBS electrodes and MEG sensors was observed throughout the entire beta band, a significant movement‐related decrease prevailed in lower beta frequencies (˜13–21 Hz). In addition, patients’ absolute coherence values in this frequency range significantly correlated with their median reaction time during the task (r = 0.89, p = 0.003). These findings corroborate the recent idea of two functionally distinct frequency ranges within the beta band, as well as the anti‐kinetic character of beta oscillations. HighlightsSimultaneous internal pallidum LFP and MEG recordings in dystonia patients.Cortico‐pallidal coherence was found throughout the beta frequency range.Predominantly low‐beta coherence (13–21 Hz) decreased with movement.Overall level of coherence was indicative of subject's median reaction time.No correlations were found between beta coherence measures and clinical scores.

[1]  David Garcia-Garcia,et al.  High beta activity in the subthalamic nucleus and freezing of gait in Parkinson's disease , 2014, Neurobiology of Disease.

[2]  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.

[3]  Peter Brown,et al.  Modulation of beta oscillations in the subthalamic area during motor imagery in Parkinson's disease. , 2006, Brain : a journal of neurology.

[4]  Peter Brown,et al.  Bilateral Functional Connectivity of the Basal Ganglia in Patients with Parkinson’s Disease and Its Modulation by Dopaminergic Treatment , 2013, PloS one.

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

[6]  Y. Benjamini,et al.  THE CONTROL OF THE FALSE DISCOVERY RATE IN MULTIPLE TESTING UNDER DEPENDENCY , 2001 .

[7]  Daniel M. Corcos,et al.  Subthalamic nucleus and internal globus pallidus scale with the rate of change of force production in humans , 2004, NeuroImage.

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

[9]  J. Artieda,et al.  Changes in subthalamic activity during movement observation in Parkinson’s disease: Is the mirror system mirrored in the basal ganglia? , 2010, Clinical Neurophysiology.

[10]  J. Ushiba,et al.  Prolonged reaction time during episodes of elevated β-band corticomuscular coupling and associated oscillatory muscle activity. , 2013, Journal of applied physiology.

[11]  S Fahn,et al.  Tolcapone , 1998, Neurology.

[12]  Peter Brown,et al.  Dopaminergic therapy promotes lateralized motor activity in the subthalamic area in Parkinson's disease. , 2007, Brain : a journal of neurology.

[13]  K. Bötzel,et al.  Globus pallidus internus oscillatory activity is related to movement speed , 2013, The European journal of neuroscience.

[14]  X.L. Chen,et al.  Deep Brain Stimulation , 2013, Interventional Neurology.

[15]  Ana L. N. Fred,et al.  Unveiling the Biometric Potential of Finger-Based ECG Signals , 2011, Comput. Intell. Neurosci..

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

[17]  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.

[18]  Clement Hamani,et al.  Movement related potentials and oscillatory activities in the human internal globus pallidus during voluntary movements , 2011, Journal of Neurology, Neurosurgery & Psychiatry.

[19]  Hong Yu,et al.  Role of individual basal ganglia nuclei in force amplitude generation. , 2007, Journal of neurophysiology.

[20]  Peter Redgrave,et al.  Basal Ganglia , 2020, Encyclopedia of Autism Spectrum Disorders.

[21]  A. Daffertshofer,et al.  A role of beta oscillatory synchrony in biasing response competition? , 2009, Cerebral cortex.

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

[23]  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.

[24]  Jerrold L Vitek,et al.  Toward a network model of dystonia , 2012, Annals of the New York Academy of Sciences.

[25]  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.

[26]  G. Schneider,et al.  Cortico-pallidal oscillatory connectivity in patients with dystonia. , 2015, Brain : a journal of neurology.

[27]  Jean-Michel Deniau,et al.  High Frequency Stimulation of the Subthalamic Nucleus , 2005 .

[28]  Matthew C. Keller,et al.  Increased sensitivity in neuroimaging analyses using robust regression , 2005, NeuroImage.

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

[30]  Peter Brown,et al.  Boosting Cortical Activity at Beta-Band Frequencies Slows Movement in Humans , 2009, Current Biology.

[31]  Andrea A. Kühn,et al.  Thalamic gamma oscillations correlate with reaction time in a Go/noGo task in patients with essential tremor , 2013, NeuroImage.

[32]  John-Stuart Brittain,et al.  Oscillations and the basal ganglia: Motor control and beyond , 2014, NeuroImage.

[33]  Tipu Z. Aziz,et al.  The role of the subthalamic nucleus in response inhibition: Evidence from local field potential recordings in the human subthalamic nucleus , 2012, NeuroImage.

[34]  J. Dostrovsky,et al.  Beta oscillatory activity in the subthalamic nucleus and its relation to dopaminergic response in Parkinson's disease. , 2006, Journal of neurophysiology.

[35]  Karl J. Friston,et al.  Movement-Related Changes in Local and Long-Range Synchronization in Parkinson's Disease Revealed by Simultaneous Magnetoencephalography and Intracranial Recordings , 2012, The Journal of Neuroscience.

[36]  Paul L. Furlong,et al.  Oscillatory Beta Activity Mediates Neuroplastic Effects of Motor Cortex Stimulation in Humans , 2013, The Journal of Neuroscience.

[37]  Guillermo Paradiso,et al.  Involvement of human thalamus in the preparation of self-paced movement. , 2004, Brain : a journal of neurology.

[38]  Robert Oostenveld,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2010, Comput. Intell. Neurosci..

[39]  A. Engel,et al.  Beta-band oscillations—signalling the status quo? , 2010, Current Opinion in Neurobiology.

[40]  G. Deuschl,et al.  Subthalamic nucleus deep brain stimulation: Summary and meta‐analysis of outcomes , 2006, Movement disorders : official journal of the Movement Disorder Society.

[41]  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.

[42]  Markus Butz,et al.  Distinct oscillatory STN-cortical loops revealed by simultaneous MEG and local field potential recordings in patients with Parkinson's disease , 2011, NeuroImage.

[43]  Karl J. Friston,et al.  Resting oscillatory cortico-subthalamic connectivity in patients with Parkinson's disease. , 2011, Brain : a journal of neurology.

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

[45]  Andreas Daffertshofer,et al.  Neural synchrony within the motor system: what have we learned so far? , 2012, Front. Hum. Neurosci..

[46]  P. Brown,et al.  Deep brain stimulation suppresses pallidal low frequency activity in patients with phasic dystonic movements. , 2014, Brain : a journal of neurology.

[47]  Vladimir Litvak,et al.  Deep brain stimulation modulates synchrony within spatially and spectrally distinct resting state networks in Parkinson’s disease , 2016, Brain : a journal of neurology.

[48]  Vladimir Litvak,et al.  Anticipatory changes in beta synchrony in the human corticospinal system and associated improvements in task performance , 2007, The European journal of neuroscience.

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

[50]  J A Obeso,et al.  Movement‐related changes in oscillatory activity in the human subthalamic nucleus: ipsilateral vs. contralateral movements , 2005, The European journal of neuroscience.

[51]  Tipu Z. Aziz,et al.  Subthalamic nucleus phase–amplitude coupling correlates with motor impairment in Parkinson’s disease , 2016, Clinical Neurophysiology.

[52]  Georgios A. Keliris,et al.  Introduction to Research Topic – Binocular Rivalry: A Gateway to Studying Consciousness , 2012, Front. Hum. Neurosci..

[53]  Karl J. Friston,et al.  EEG and MEG Data Analysis in SPM8 , 2011, Comput. Intell. Neurosci..

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

[55]  Hong Yu,et al.  Role of the basal ganglia and frontal cortex in selecting and producing internally guided force pulses , 2007, NeuroImage.

[56]  Tipu Z. Aziz,et al.  Driving Oscillatory Activity in the Human Cortex Enhances Motor Performance , 2012, Current Biology.

[57]  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.

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

[59]  Andrea A. Kühn,et al.  Beta-band amplitude oscillations in the human internal globus pallidus support the encoding of sequence boundaries during initial sensorimotor sequence learning , 2014, NeuroImage.

[60]  B. Mittelman,et al.  On control. , 1979, Dental management.

[61]  Peter Brown,et al.  Existing Motor State Is Favored at the Expense of New Movement during 13-35 Hz Oscillatory Synchrony in the Human Corticospinal System , 2005, The Journal of Neuroscience.

[62]  Markus Butz,et al.  Differential modulation of STN-cortical and cortico-muscular coherence by movement and levodopa in Parkinson's disease , 2013, NeuroImage.

[63]  G. Curio,et al.  Task‐related differential dynamics of EEG alpha‐ and beta‐band synchronization in cortico‐basal motor structures , 2007, The European journal of neuroscience.

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

[65]  S Fahn,et al.  Concept and classification of dystonia. , 1988, Advances in neurology.

[66]  A. Oliviero,et al.  Dopamine Dependency of Oscillations between Subthalamic Nucleus and Pallidum in Parkinson's Disease , 2001, The Journal of Neuroscience.

[67]  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.

[68]  K. Amirdelfan,et al.  High-Frequency Stimulation , 2018 .

[69]  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.

[70]  Yan Zhang,et al.  Prestimulus Cortical Activity is Correlated with Speed of Visuomotor Processing , 2008, Journal of Cognitive Neuroscience.

[71]  Peter Brown,et al.  Subthalamic synchronized oscillatory activity correlates with motor impairment in patients with Parkinson's disease , 2016, Movement disorders : official journal of the Movement Disorder Society.

[72]  M. Popovic,et al.  Time-course of coherence in the human basal ganglia during voluntary movements , 2016, Scientific Reports.

[73]  Peter Brown,et al.  Patterns of Bidirectional Communication between Cortex and Basal Ganglia during Movement in Patients with Parkinson Disease , 2008, The Journal of Neuroscience.