Beta-Band Activity during Motor Planning Reflects Response Uncertainty

It has been known for many years that the power of beta-band oscillatory activity in motor-related brain regions decreases during the preparation and execution of voluntary movements. However, it is not clear yet whether the amplitude of this desynchronization is modulated by any parameter of the motor task. Here, we examined whether the degree of uncertainty about the upcoming movement direction modulated beta-band desynchronization during motor preparation. To this end, we recorded whole-head neuromagnetic signals while human subjects performed an instructed-delay reaching task with one, two, or three possible target directions. We found that the reduction of power of beta-band activity (16–28 Hz) during motor preparation was scaled relative to directional uncertainty. Furthermore, we show that the change of beta-band power correlates with the change of latency of response associated with response uncertainty. Finally, we show that the main source of beta-band desynchronization was located in the peri-Rolandic region. The results establish directional uncertainty as an important determinant of beta-band power during motor preparation and indicate that neural activity in the sensorimotor cortex during motor preparation covaries with directional uncertainty.

[1]  G. W. Milligan,et al.  An examination of procedures for determining the number of clusters in a data set , 1985 .

[2]  G. Pfurtscheller,et al.  Patterns of cortical activation during planning of voluntary movement. , 1989, Electroencephalography and clinical neurophysiology.

[3]  J. Donoghue,et al.  Oscillations in local field potentials of the primate motor cortex during voluntary movement. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[4]  André Hardy,et al.  An examination of procedures for determining the number of clusters in a data set , 1994 .

[5]  William A. MacKay,et al.  Field potential oscillatory bursts in parietal cortex before and during reach , 1995, Brain Research.

[6]  W. Sommer,et al.  Partial advance information and response preparation: inferences from the lateralized readiness potential. , 1996, Journal of experimental psychology. General.

[7]  G. Pfurtscheller,et al.  Event-related desynchronisation of central beta-rhythms during brisk and slow self-paced finger movements of dominant and nondominant hand. , 1996, Brain research. Cognitive brain research.

[8]  E. Fetz,et al.  Oscillatory activity in sensorimotor cortex of awake monkeys: synchronization of local field potentials and relation to behavior. , 1996, Journal of neurophysiology.

[9]  Michele A. Basso,et al.  Modulation of neuronal activity by target uncertainty , 1997, Nature.

[10]  V. Jousmäki,et al.  Involvement of Primary Motor Cortex in Motor Imagery: A Neuromagnetic Study , 1997, NeuroImage.

[11]  G. Pfurtscheller,et al.  Motor imagery activates primary sensorimotor area in humans , 1997, Neuroscience Letters.

[12]  M. A. Basso,et al.  Modulation of Neuronal Activity in Superior Colliculus by Changes in Target Probability , 1998, The Journal of Neuroscience.

[13]  J. Donoghue,et al.  Neural discharge and local field potential oscillations in primate motor cortex during voluntary movements. , 1998, Journal of neurophysiology.

[14]  D. Munoz,et al.  Saccadic Probability Influences Motor Preparation Signals and Time to Saccadic Initiation , 1998, The Journal of Neuroscience.

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

[16]  C. Marsden,et al.  Bradykinesia and impairment of EEG desynchronization in Parkinson's disease , 1999, Movement disorders : official journal of the Movement Disorder Society.

[17]  M. Hallett,et al.  Force level modulates human cortical oscillatory activities , 1999, Neuroscience Letters.

[18]  John Fox,et al.  Linear Mixed Models , 1999 .

[19]  M. Steriade Corticothalamic resonance, states of vigilance and mentation , 2000, Neuroscience.

[20]  P. Derambure,et al.  Brief and sustained movements: differences in event-related (de)synchronization (ERD/ERS) patterns , 2000, Clinical Neurophysiology.

[21]  J L Lancaster,et al.  Automated Talairach Atlas labels for functional brain mapping , 2000, Human brain mapping.

[22]  Andrew Rutherford,et al.  Introducing Anova and Ancova: A Glm Approach , 2000 .

[23]  R C Littell,et al.  Mixed Models: Modelling Covariance Structure in the Analysis of Repeated Measures Data , 2005 .

[24]  A. Schnitzler,et al.  Dynamic imaging of coherent sources: Studying neural interactions in the human brain. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[25]  P. Robinson,et al.  Prediction of electroencephalographic spectra from neurophysiology. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[26]  N. Birbaumer,et al.  Event-related beta desynchronization indicates timing of response selection in a delayed-response paradigm in humans , 2001, Neuroscience Letters.

[27]  W. Schultz Getting Formal with Dopamine and Reward , 2002, Neuron.

[28]  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.

[29]  Alberto Labarga,et al.  Alpha and beta oscillatory changes during stimulus-induced movement paradigms: effect of stimulus predictability , 2003, Neuroreport.

[30]  G. Pellizzer,et al.  Motor planning: effect of directional uncertainty with discrete spatial cues , 2003, Experimental Brain Research.

[31]  E. Fetz,et al.  Oscillatory activity in forelimb muscles of behaving monkeys evoked by microstimulation in the cerebellar nuclei , 2004, Neuroscience Letters.

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

[33]  O. Bock,et al.  Motor control prior to movement onset: preparatory mechanisms for pointing at visual targets , 2004, Experimental Brain Research.

[34]  J. Bolam Faculty Opinions recommendation of Synchronous, focally modulated beta-band oscillations characterize local field potential activity in the striatum of awake behaving monkeys. , 2004 .

[35]  S. Bressler,et al.  Beta oscillations in a large-scale sensorimotor cortical network: directional influences revealed by Granger causality. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[36]  Rolf Ulrich,et al.  Preparing for Action: Inferences from CNV and LRP , 2004 .

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

[38]  Giuseppe Pellizzer,et al.  Time-dependent effects of discrete spatial cues on the planning of directed movements , 2006, Experimental Brain Research.

[39]  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.

[40]  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.

[41]  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.

[42]  Lewis Bott,et al.  Modulations in the degree of synchronization during ongoing oscillatory activity in the human brain , 2005, The European journal of neuroscience.

[43]  P. Brown,et al.  Levodopa‐induced modulation of subthalamic beta oscillations during self‐paced movements in patients with Parkinson's disease , 2005, The European journal of neuroscience.

[44]  Charles E. Heckler,et al.  Applied Multivariate Statistical Analysis , 2005, Technometrics.

[45]  Ritske de Jong,et al.  Movement-related EEG indices of preparation in task switching and motor control , 2006, Brain Research.

[46]  Kestutis Kveraga,et al.  Directional Uncertainty in Visually Guided Pointing , 2006, Perceptual and motor skills.

[47]  John J. Foxe,et al.  Oscillatory beta activity predicts response speed during a multisensory audiovisual reaction time task: a high-density electrical mapping study. , 2005, Cerebral cortex.

[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]  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.

[50]  Alexander Kraskov,et al.  Selectivity for Grasp in Local Field Potential and Single Neuron Activity Recorded Simultaneously from M1 and F5 in the Awake Macaque Monkey , 2008, The Journal of Neuroscience.

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

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

[53]  S. Bressler,et al.  Response preparation and inhibition: The role of the cortical sensorimotor beta rhythm , 2008, Neuroscience.

[54]  C. Braun,et al.  Hand Movement Direction Decoded from MEG and EEG , 2008, The Journal of Neuroscience.

[55]  Timothy E. J. Behrens,et al.  Choice, uncertainty and value in prefrontal and cingulate cortex , 2008, Nature Neuroscience.

[56]  Colin Camerer,et al.  Explicit neural signals reflecting reward uncertainty , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[57]  P. Manganotti,et al.  EEG and fMRI Coregistration to Investigate the Cortical Oscillatory Activities During Finger Movement , 2008, Brain Topography.

[58]  M. Shadlen,et al.  Decision-making with multiple alternatives , 2008, Nature Neuroscience.

[59]  G. Edelman,et al.  Large-scale model of mammalian thalamocortical systems , 2008, Proceedings of the National Academy of Sciences.

[60]  Kianoush Nazarpour,et al.  Simultaneous preparation of multiple potential movements: opposing effects of spatial proximity mediated by premotor and parietal cortex. , 2009, Journal of neurophysiology.

[61]  Loredana Zollo,et al.  Brain activity preceding a 2D manual catching task , 2009, NeuroImage.

[62]  Geert Molenberghs,et al.  Linear Mixed Models , 2011, International Encyclopedia of Statistical Science.