Human Motor Cortical Activity Is Selectively Phase-Entrained on Underlying Rhythms

The functional significance of electrical rhythms in the mammalian brain remains uncertain. In the motor cortex, the 12–20 Hz beta rhythm is known to transiently decrease in amplitude during movement, and to be altered in many motor diseases. Here we show that the activity of neuronal populations is phase-coupled with the beta rhythm on rapid timescales, and describe how the strength of this relation changes with movement. To investigate the relationship of the beta rhythm to neuronal dynamics, we measured local cortical activity using arrays of subdural electrocorticographic (ECoG) electrodes in human patients performing simple movement tasks. In addition to rhythmic brain processes, ECoG potentials also reveal a spectrally broadband motif that reflects the aggregate neural population activity beneath each electrode. During movement, the amplitude of this broadband motif follows the dynamics of individual fingers, with somatotopically specific responses for different fingers at different sites on the pre-central gyrus. The 12–20 Hz beta rhythm, in contrast, is widespread as well as spatially coherent within sulcal boundaries and decreases in amplitude across the pre- and post-central gyri in a diffuse manner that is not finger-specific. We find that the amplitude of this broadband motif is entrained on the phase of the beta rhythm, as well as rhythms at other frequencies, in peri-central cortex during fixation. During finger movement, the beta phase-entrainment is diminished or eliminated. We suggest that the beta rhythm may be more than a resting rhythm, and that this entrainment may reflect a suppressive mechanism for actively gating motor function.

[1]  E. Fetz,et al.  Coherent 25- to 35-Hz oscillations in the sensorimotor cortex of awake behaving monkeys. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[2]  R. Lesser,et al.  Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. I. Alpha and beta event-related desynchronization. , 1998, Brain : a journal of neurology.

[3]  Jaimie M. Henderson,et al.  Bilateral symmetry and coherence of subthalamic nuclei beta band activity in Parkinson's disease , 2010, Experimental Neurology.

[4]  Karl J. Friston,et al.  Unified segmentation , 2005, NeuroImage.

[5]  Guy Marchal,et al.  Multimodality image registration by maximization of mutual information , 1997, IEEE Transactions on Medical Imaging.

[6]  W. Pennya,et al.  Testing for nested oscillation , 2008 .

[7]  B. Kaada,et al.  Electrical activity of the brain. , 1953, Annual review of physiology.

[8]  Yehezkel Ben-Ari,et al.  Rapid cortical oscillations and early motor activity in premature human neonate. , 2007, Cerebral cortex.

[9]  Bradley Greger,et al.  Decoding spoken words using local field potentials recorded from the cortical surface , 2010, Journal of neural engineering.

[10]  Peter Brown,et al.  Parkinsonian Beta Oscillations in the External Globus Pallidus and Their Relationship with Subthalamic Nucleus Activity , 2008, The Journal of Neuroscience.

[11]  Kai J Miller,et al.  Reorganization of large-scale physiology in hand motor cortex following hemispheric stroke , 2011, Neurology.

[12]  N. Ramsey,et al.  Neurophysiologic correlates of fMRI in human motor cortex , 2012, Human brain mapping.

[13]  Rui M. Costa,et al.  Rapid Alterations in Corticostriatal Ensemble Coordination during Acute Dopamine-Dependent Motor Dysfunction , 2006, Neuron.

[14]  P. Starr,et al.  Oscillations in sensorimotor cortex in movement disorders: an electrocorticography study. , 2012, Brain : a journal of neurology.

[15]  N. Ramsey,et al.  Phase Navigator Correction in 3D fMRI Improves Detection of Brain Activation: Quantitative Assessment with a Graded Motor Activation Procedure , 1998, NeuroImage.

[16]  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.

[17]  Brendan Z. Allison,et al.  Brain-Computer Interfaces , 2010 .

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

[19]  Guy Marchal,et al.  Multi-modality image registration by maximization of mutual information , 1996, Proceedings of the Workshop on Mathematical Methods in Biomedical Image Analysis.

[20]  G. A. Woonton,et al.  EFFECTS OF ESERINE, ACETYLCHOLINE AND ATROPINE ON THE ELECTROCORTICOGRAM , 1940 .

[21]  I. Stanford,et al.  Pharmacologically induced and stimulus evoked rhythmic neuronal oscillatory activity in the primary motor cortex in vitro , 2008, Neuroscience.

[22]  E. Fetz,et al.  Decoupling the Cortical Power Spectrum Reveals Real-Time Representation of Individual Finger Movements in Humans , 2009, The Journal of Neuroscience.

[23]  Rajesh P. N. Rao,et al.  Brain surface electrode co-registration using MRI and x-ray , 2010, 2010 Annual International Conference of the IEEE Engineering in Medicine and Biology.

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

[25]  Andrea A. Kühn,et al.  Increased beta activity in dystonia patients after drug-induced dopamine deficiency , 2008, Experimental Neurology.

[26]  Mikko Pohja,et al.  On the human sensorimotor-cortex beta rhythm: Sources and modeling , 2005, NeuroImage.

[27]  Abbas F. Sadikot,et al.  The neural response to transcranial magnetic stimulation of the human motor cortex. II. Thalamocortical contributions , 2006, Experimental Brain Research.

[28]  Nick F. Ramsey,et al.  Automated electrocorticographic electrode localization on individually rendered brain surfaces , 2010, Journal of Neuroscience Methods.

[29]  J. Bouyer,et al.  Ventral mesencephalic tegmentum (VMT) controls electrocortical beta rhythms and associated attentive behaviour in the cat , 1982, Behavioural Brain Research.

[30]  Jeffrey G. Ojemann,et al.  Power-Law Scaling in the Brain Surface Electric Potential , 2009, PLoS Comput. Biol..

[31]  C. Calautti,et al.  Dynamics of Motor Network Overactivation After Striatocapsular Stroke: A Longitudinal PET Study Using a Fixed-Performance Paradigm , 2001, Stroke.

[32]  M. Schieber Constraints on somatotopic organization in the primary motor cortex. , 2001, Journal of neurophysiology.

[33]  Rajesh P. N. Rao,et al.  Cortical activity during motor execution, motor imagery, and imagery-based online feedback , 2010, Proceedings of the National Academy of Sciences.

[34]  W. Penfield,et al.  Electrocorticograms in man: Effect of voluntary movement upon the electrical activity of the precentral gyrus , 2005, Archiv für Psychiatrie und Nervenkrankheiten.

[35]  G. Ojemann,et al.  Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. , 1989, Journal of neurosurgery.

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

[37]  Boaz Porat,et al.  A course in digital signal processing , 1996 .

[38]  Moritz Grosse-Wentrup,et al.  Critical issues in state-of-the-art brain–computer interface signal processing , 2011, Journal of neural engineering.

[39]  Natalia Petridou,et al.  Dissociation between Neuronal Activity in Sensorimotor Cortex and Hand Movement Revealed as a Function of Movement Rate , 2012, The Journal of Neuroscience.

[40]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[41]  S. Howard Bartley,et al.  THE RESPONSE OF THE SENSORIMOTOR CORTEX TO STIMULATION OF A PERIPHERAL NERVE , 1937 .

[42]  G. Pfurtscheller,et al.  Post-movement beta synchronization. A correlate of an idling motor area? , 1996, Electroencephalography and clinical neurophysiology.

[43]  F. Varela,et al.  Measuring phase synchrony in brain signals , 1999, Human brain mapping.

[44]  Gert Pfurtscheller,et al.  EEG event-related desynchronization (ERD) and synchronization (ERS) , 1997 .

[45]  M. Ghilardi,et al.  Functional networks in motor sequence learning: Abnormal topographies in Parkinson's disease , 2001, Human brain mapping.

[46]  Adrián Ponce-Alvarez,et al.  Context-related frequency modulations of macaque motor cortical LFP beta oscillations. , 2012, Cerebral cortex.

[47]  W. Singer,et al.  Interhemispheric synchronization of oscillatory neuronal responses in cat visual cortex , 1991, Science.

[48]  P. Pahapill,et al.  Deep brain stimulation for Parkinson's disease dissociates mood and motor circuits: A functional MRI case study , 2003, Movement disorders : official journal of the Movement Disorder Society.

[49]  M. Greicius,et al.  Default-mode network activity distinguishes Alzheimer's disease from healthy aging: Evidence from functional MRI , 2004, Proc. Natl. Acad. Sci. USA.

[50]  G. Glover,et al.  Resting-State Functional Connectivity in Major Depression: Abnormally Increased Contributions from Subgenual Cingulate Cortex and Thalamus , 2007, Biological Psychiatry.

[51]  W. Liao,et al.  Impaired attention network in temporal lobe epilepsy: A resting FMRI study , 2009, Neuroscience Letters.

[52]  Adriano B. L. Tort,et al.  Sharp edge artifacts and spurious coupling in EEG frequency comodulation measures , 2008, Journal of Neuroscience Methods.

[53]  Michelle M. McCarthy,et al.  Striatal origin of the pathologic beta oscillations in Parkinson's disease , 2011, Proceedings of the National Academy of Sciences.

[54]  Erno J. Hermans,et al.  Enhanced sensitivity with fast three‐dimensional blood‐oxygen‐level‐dependent functional MRI: comparison of SENSE–PRESTO and 2D‐EPI at 3 T , 2008, NMR in biomedicine.

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

[56]  K. Miller,et al.  A Simple, Spectral-Change Based, Electrocorticographic Brain–Computer Interface , 2009 .

[57]  G. Shepherd The Synaptic Organization of the Brain , 1979 .

[58]  N. Hatsopoulos,et al.  Periodicity and Evoked Responses in Motor Cortex , 2010, The Journal of Neuroscience.

[59]  Heiko J Luhmann,et al.  Carbachol-induced network oscillations in the intact cerebral cortex of the newborn rat. , 2003, Cerebral cortex.

[60]  Jeremy R. Manning,et al.  Broadband Shifts in Local Field Potential Power Spectra Are Correlated with Single-Neuron Spiking in Humans , 2009, The Journal of Neuroscience.

[61]  H. L. Andrews,et al.  BRAIN POTENTIALS AND VOLUNTARY MUSCLE ACTIVITY IN MAN , 1938 .

[62]  Rajesh P. N. Rao,et al.  Dynamic Modulation of Local Population Activity by Rhythm Phase in Human Occipital Cortex During a Visual Search Task , 2010, Front. Hum. Neurosci..

[63]  O. Jensen,et al.  Gamma Power Is Phase-Locked to Posterior Alpha Activity , 2008, PloS one.

[64]  W PENFIELD,et al.  Mechanisms of voluntary movement. , 1954, Brain : a journal of neurology.

[65]  J. A. Bates,et al.  Electrical activity of the cortex accompanying movement , 1951, The Journal of physiology.

[66]  M. Berger,et al.  High Gamma Power Is Phase-Locked to Theta Oscillations in Human Neocortex , 2006, Science.

[67]  A. Grossmann,et al.  Cycle-octave and related transforms in seismic signal analysis , 1984 .

[68]  N. Birbaumer,et al.  BCI2000: a general-purpose brain-computer interface (BCI) system , 2004, IEEE Transactions on Biomedical Engineering.

[69]  E. Fetz,et al.  Synchronization of neurons during local field potential oscillations in sensorimotor cortex of awake monkeys. , 1996, Journal of neurophysiology.

[70]  M. Greicius Resting-state functional connectivity in neuropsychiatric disorders , 2008, Current opinion in neurology.

[71]  J. Maunsell,et al.  Different Origins of Gamma Rhythm and High-Gamma Activity in Macaque Visual Cortex , 2011, PLoS biology.

[72]  Michael T. Jurkiewicz,et al.  Post-movement beta rebound is generated in motor cortex: Evidence from neuromagnetic recordings , 2006, NeuroImage.

[73]  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.

[74]  M. Schieber,et al.  How somatotopic is the motor cortex hand area? , 1993, Science.

[75]  Rajesh P. N. Rao,et al.  Spectral Changes in Cortical Surface Potentials during Motor Movement , 2007, The Journal of Neuroscience.

[76]  A Eusebio,et al.  Suppression of beta oscillations in the subthalamic nucleus following cortical stimulation in humans , 2008, The European journal of neuroscience.

[77]  K. Miller Broadband Spectral Change: Evidence for a Macroscale Correlate of Population Firing Rate? , 2010, The Journal of Neuroscience.

[78]  G A Ojemann,et al.  Models of the brain organization for higher integrative functions derived with electrical stimulation techniques. , 1982, Human neurobiology.

[79]  Jianing Yu,et al.  Top-down laminar organization of the excitatory network in motor cortex , 2008, Nature Neuroscience.