Frequency-specific modulation of connectivity in the ipsilateral sensorimotor cortex by different forms of movement initiation

Abstract A consistent finding in motor EEG research is a bilateral attenuation of oscillatory activity over sensorimotor regions close to the onset of an upcoming unilateral hand movement. In contrast, little is known about how movement initiation affects oscillatory activity, especially in the hemisphere ipsilateral to the moving hand. We here investigated the neural mechanisms modulating oscillatory activity in the ipsilateral motor cortex prior to movement onset under the control of two different initiating networks, namely, Self‐initiated and Visually‐cued actions. During motor preparation, a contralateral preponderance of power over sensorimotor cortex (SM) was observed in &agr; and &bgr; bands during Visually‐cued movements, whereas power changes were more bilateral during Self‐initiated movements. Coherence between ipsilateral SM (iSM) and contralateral SM (cSM) in the &agr;‐band was significantly increased compared to the respective baseline values, independent of the context of movement initiation. However, this context‐independent cSM‐iSM coherence modulated the power changes in iSM in a context‐dependent manner, that is, a stronger cSM‐iSM coherence correlated with a larger decrease in high‐&bgr; power over iSM in the Self‐initiated condition, in contrast to a smaller decrease in &agr; power in the Visually‐cued condition. In addition, the context‐dependent coherence between SMA and iSM in the &agr;‐band and &dgr;‐&THgr;‐band for the Self‐initiated and Visually‐cued condition, respectively, exhibited a similar context‐dependent modulation for power changes. Our findings suggest that the initiation of regional oscillations over iSM reflects changes in the information flow with the contralateral sensorimotor and premotor areas dependent upon the context of movement initiation. Importantly, the interaction between regional oscillations and network‐like oscillatory couplings indicates different frequency‐specific inhibitory mechanisms that modulate the activity in the ipsilateral sensorimotor cortex dependent upon how the movement is initiated.

[1]  A. E. Schulman,et al.  Functional coupling and regional activation of human cortical motor areas during simple, internally paced and externally paced finger movements. , 1998, Brain : a journal of neurology.

[2]  C. Tenke,et al.  Principal components analysis of Laplacian waveforms as a generic method for identifying ERP generator patterns: II. Adequacy of low-density estimates , 2006, Clinical Neurophysiology.

[3]  I. Toni,et al.  Distinct roles for alpha- and beta-band oscillations during mental simulation of goal-directed actions. , 2014, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  R. Passingham,et al.  Neural correlates of visuomotor associations. Spatial rules compared with arbitrary rules. , 2001, Experimental brain research.

[5]  W. Prinz,et al.  Neural and behavioral correlates of intentional actions , 2011, Neuropsychologia.

[6]  M. Hallett,et al.  Involvement of the ipsilateral motor cortex in finger movements of different complexities , 1997, Annals of neurology.

[7]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[8]  Gabriel Curio,et al.  Event-related desynchronization of sensorimotor EEG rhythms in hemiparetic patients with acute stroke , 2011, Neuroscience Letters.

[9]  F. Perrin,et al.  Spherical splines for scalp potential and current density mapping. , 1989, Electroencephalography and clinical neurophysiology.

[10]  G. Pfurtscheller Functional Topography During Sensorimotor Activation Studied with Event‐Related Desynchronization Mapping , 1989, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[11]  G. Pfurtscheller,et al.  Calculation of event-related coherence—A new method to study short-lasting coupling between brain areas , 2005, Brain Topography.

[12]  P. Brown,et al.  New insights into the relationship between dopamine, beta oscillations and motor function , 2011, Trends in Neurosciences.

[13]  Wim L. C. Rutten,et al.  Temporal evolution of event-related desynchronization in acute stroke: A pilot study , 2014, Clinical Neurophysiology.

[14]  A Daffertshofer,et al.  Differential modulations of ipsilateral and contralateral beta (de)synchronization during unimanual force production , 2012, The European journal of neuroscience.

[15]  Andreas Keil,et al.  Relation of Accelerometer and EMG Recordings for the Measurement of Upper , 1999 .

[16]  Alireza Gharabaghi,et al.  Lateralized alpha-band cortical networks regulate volitional modulation of beta-band sensorimotor oscillations , 2014, NeuroImage.

[17]  M. Hallett,et al.  Asymmetric spatiotemporal patterns of event-related desynchronization preceding voluntary sequential finger movements: a high-resolution EEG study , 2005, Clinical Neurophysiology.

[18]  Simon B. Eickhoff,et al.  Dynamic intra- and interhemispheric interactions during unilateral and bilateral hand movements assessed with fMRI and DCM , 2008, NeuroImage.

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

[20]  H. Steinmetz,et al.  Craniocerebral topography within the international 10-20 system. , 1989, Electroencephalography and clinical neurophysiology.

[21]  Clemens Brunner,et al.  Mu rhythm (de)synchronization and EEG single-trial classification of different motor imagery tasks , 2006, NeuroImage.

[22]  M. Hallett,et al.  Task-related coherence and task-related spectral power changes during sequential finger movements. , 1998, Electroencephalography and clinical neurophysiology.

[23]  W. Klimesch,et al.  EEG alpha oscillations: The inhibition–timing hypothesis , 2007, Brain Research Reviews.

[24]  Gloria Menegaz,et al.  Brain Network Connectivity and Topological Analysis During Voluntary Arm Movements , 2016, Clinical EEG and neuroscience.

[25]  L. Cohen,et al.  Influence of interhemispheric interactions on motor function in chronic stroke , 2004, Annals of neurology.

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

[27]  L. Cohen,et al.  Disrupting the ipsilateral motor cortex interferes with training of a complex motor task in older adults. , 2014, Cerebral cortex.

[28]  G. Fink,et al.  Dopaminergic modulation of motor network dynamics in Parkinson’s disease , 2015, Brain : a journal of neurology.

[29]  Jaimie M. Henderson,et al.  The STN beta-band profile in Parkinson's disease is stationary and shows prolonged attenuation after deep brain stimulation , 2009, Experimental Neurology.

[30]  M. Brass,et al.  Top-down modulation of brain activity underlying intentional action and its relationship with awareness of intention: an ERP/Laplacian analysis , 2013, Experimental Brain Research.

[31]  Nick S. Ward,et al.  Beta oscillations reflect changes in motor cortex inhibition in healthy ageing , 2014, NeuroImage.

[32]  Michael X. Cohen,et al.  Midfrontal conflict-related theta-band power reflects neural oscillations that predict behavior. , 2013, Journal of neurophysiology.

[33]  D. Eagleman The Where and When of Intention , 2004, Science.

[34]  William D. Penny,et al.  Age-related changes in causal interactions between cortical motor regions during hand grip , 2012, NeuroImage.

[35]  Sukhvinder S. Obhi,et al.  Internally generated and externally triggered actions are physically distinct and independently controlled , 2004, Experimental Brain Research.

[36]  Alvaro Pascual-Leone,et al.  Ipsilateral motor cortex activation on functional magnetic resonance imaging during unilateral hand movements is related to interhemispheric interactions , 2003, NeuroImage.

[37]  S. Baker Oscillatory interactions between sensorimotor cortex and the periphery , 2007, Current Opinion in Neurobiology.

[38]  M. Desmurget,et al.  A parietal-premotor network for movement intention and motor awareness , 2009, Trends in Cognitive Sciences.

[39]  S. Makeig Auditory event-related dynamics of the EEG spectrum and effects of exposure to tones. , 1993, Electroencephalography and clinical neurophysiology.

[40]  N. Ward,et al.  Age-dependent changes in the neural correlates of force modulation: An fMRI study , 2008, Neurobiology of Aging.

[41]  F. Zappasodi,et al.  Local and remote effects of transcranial direct current stimulation on the electrical activity of the motor cortical network , 2014, Human brain mapping.

[42]  A. Mognon,et al.  ADJUST: An automatic EEG artifact detector based on the joint use of spatial and temporal features. , 2011, Psychophysiology.

[43]  M. Hallett,et al.  Hemispheric asymmetry of ipsilateral motor cortex activation during unimanual motor tasks: further evidence for motor dominance , 2001, Clinical Neurophysiology.

[44]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[45]  D. Wolpert,et al.  Rhythm generation in monkey motor cortex explored using pyramidal tract stimulation , 2002, The Journal of physiology.

[46]  Christian Gerloff,et al.  Ipsilateral cortical activation during finger sequences of increasing complexity: representation of movement difficulty or memory load? , 2003, Clinical Neurophysiology.

[47]  R. Verleger,et al.  Control of hand movements after striatocapsular stroke: high-resolution temporal analysis of the function of ipsilateral activation , 2003, Clinical Neurophysiology.

[48]  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.

[49]  Michele Tinazzi,et al.  Modulation of ipsilateral motor cortex in man during unimanual finger movements of different complexities , 1998, Neuroscience Letters.

[50]  J. Fell,et al.  Phase/amplitude reset and theta–gamma interaction in the human medial temporal lobe during a continuous word recognition memory task , 2005, Hippocampus.

[51]  P. Haggard Human volition: towards a neuroscience of will , 2008, Nature Reviews Neuroscience.

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

[53]  Leonardo G. Cohen,et al.  Mechanisms Underlying Functional Changes in the Primary Motor Cortex Ipsilateral to an Active Hand , 2008, The Journal of Neuroscience.

[54]  B Saltzberg,et al.  Electrophysiological measures of regional neural interactive coupling. Linear and non-linear dependence relationships among multiple channel electroencephalographic recordings. , 1986, International journal of bio-medical computing.

[55]  Asymmetric Spatiotemporal Patterns of Reduction Waves in the Belousov-Zhabotinsky Reaction. , 2001 .

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

[57]  S. Rossi,et al.  Involvement of the human dorsal premotor cortex in unimanual motor control: an interference approach using transcranial magnetic stimulation , 2004, Neuroscience Letters.

[58]  G. Aschersleben,et al.  Intention-based and stimulus-based mechanisms in action selection , 2005, Experimental Brain Research.

[59]  P. Derambure,et al.  Event-related variations in the activity of EEG-rhythms. Application to the physiology and the pathology of movements. , 2002, Epileptic disorders.

[60]  Daniel M. Alschuler,et al.  Current Source Density Measures of Electroencephalographic Alpha Predict Antidepressant Treatment Response , 2011, Biological Psychiatry.

[61]  P. Brown Abnormal oscillatory synchronisation in the motor system leads to impaired movement , 2007, Current Opinion in Neurobiology.

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

[63]  Wolfgang Prinz,et al.  The role of the preSMA and the rostral cingulate zone in internally selected actions , 2007, NeuroImage.

[64]  Andrew C. N. Chen,et al.  Anticipation of somatosensory and motor events increases centro-parietal functional coupling: An EEG coherence study , 2006, Clinical Neurophysiology.

[65]  G. Fink,et al.  Differential effects of dopaminergic medication on basic motor performance and executive functions in Parkinson's disease , 2012, Neuropsychologia.

[66]  G. Fink,et al.  Cortical connectivity after subcortical stroke assessed with functional magnetic resonance imaging , 2008, Annals of neurology.

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

[68]  Michael X Cohen,et al.  Analyzing Neural Time Series Data: Theory and Practice , 2014 .

[69]  Eran Dayan,et al.  Alpha and Beta Band Event-Related Desynchronization Reflects Kinematic Regularities , 2015, The Journal of Neuroscience.

[70]  C. Marsden,et al.  Self-initiated versus externally triggered movements. I. An investigation using measurement of regional cerebral blood flow with PET and movement-related potentials in normal and Parkinson's disease subjects. , 1995, Brain : a journal of neurology.

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

[72]  G. Pfurtscheller Central beta rhythm during sensorimotor activities in man. , 1981, Electroencephalography and clinical neurophysiology.

[73]  C. Gerloff,et al.  The control of complex finger movements by directional information flow between mesial frontocentral areas and the primary motor cortex , 2014, The European journal of neuroscience.

[74]  Victor M. Yakovenko,et al.  Temporal Evolution , 2005, Encyclopedia of Database Systems.

[75]  P. Rossini,et al.  Motor cortical disinhibition in the unaffected hemisphere after unilateral cortical stroke. , 2002, Brain : a journal of neurology.

[76]  Jen-Chuen Hsieh,et al.  Loss of interhemispheric inhibition on the ipsilateral primary sensorimotor cortex in patients with brachial plexus injury: fMRI study , 2002, Annals of neurology.

[77]  Wolfgang Prinz,et al.  Two Modes of Sensorimotor Integration in Intention-Based and Stimulus-Based Actions , 2007, Quarterly journal of experimental psychology.

[78]  M. Hirata,et al.  Ipsilateral Motor-Related Hyperactivity in Patients With Cerebral Occlusive Vascular Disease , 2008, Stroke.

[79]  Silvia Daun-Gruhn,et al.  Movement-related phase locking in the delta–theta frequency band , 2016, NeuroImage.

[80]  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.

[81]  John G. Oakeshott,et al.  Bridging the Synaptic Gap: Neuroligins and Neurexin I in Apis mellifera , 2008, PloS one.

[82]  G. Fink,et al.  Reorganization of cerebral networks after stroke: new insights from neuroimaging with connectivity approaches , 2011, Brain : a journal of neurology.

[83]  A. von Stein,et al.  Different frequencies for different scales of cortical integration: from local gamma to long range alpha/theta synchronization. , 2000, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[84]  M. Frank,et al.  Frontal theta as a mechanism for cognitive control , 2014, Trends in Cognitive Sciences.

[85]  F. L. D. Silva,et al.  Event-related EEG/MEG synchronization and desynchronization: basic principles , 1999, Clinical Neurophysiology.

[86]  M. Hallett,et al.  Event-related coherence and event-related desynchronization/synchronization in the 10 Hz and 20 Hz EEG during self-paced movements. , 1997, Electroencephalography and clinical neurophysiology.