Distinct α- and β-band rhythms over rat somatosensory cortex with similar properties as in humans.

We demonstrate distinct α- (7-14 Hz) and β-band (15-30 Hz) rhythms in rat somatosensory cortex in vivo using epidural electrocorticography recordings. Moreover, we show in rats that a genuine β-rhythm coexists alongside β-activity that reflects the second harmonic of the arch-shaped somatosensory α-rhythm. This demonstration of a genuine somatosensory β-rhythm depends on a novel quantification of neuronal oscillations that is based on their rhythmic nature: lagged coherence. Using lagged coherence, we provide two lines of evidence that this somatosensory β-rhythm is distinct from the second harmonic of the arch-shaped α-rhythm. The first is based on the rhythms' spatial properties: the α- and β-rhythms are demonstrated to have significantly different topographies. The second is based on the rhythms' temporal properties: the lagged phase-phase coupling between the α- and β-rhythms is demonstrated to be significantly less than would be expected if both reflected a single underlying nonsinusoidal rhythm. Finally, we demonstrate that 1) the lagged coherence spectrum is consistent between signals from rat and human somatosensory cortex; and 2) a tactile stimulus has the same effect on the somatosensory α- and β-rhythms in both rats and humans, namely suppressing them. Thus we not only provide evidence for the existence of genuine α- and β-rhythms in rat somatosensory cortex, but also for their homology to the primate sensorimotor α- and β-rhythms.

[1]  Eric Maris,et al.  Identifying neuronal oscillations using rhythmicity , 2015, NeuroImage.

[2]  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.

[3]  Eric Maris,et al.  Anticipation increases tactile stimulus processing in the ipsilateral primary somatosensory cortex. , 2014, Cerebral cortex.

[4]  Joachim Lange,et al.  Beta oscillations and their functional role in movement perception , 2014 .

[5]  Eric Maris,et al.  Attentional modulations of somatosensory alpha, beta and gamma oscillations dissociate between anticipation and stimulus processing , 2014, NeuroImage.

[6]  Anne M. M. Fransen,et al.  Sensory and cognitive neurophysiology in rats, Part 1: Controlled tactile stimulation and micro-ECoG recordings in freely moving animals , 2014, Journal of Neuroscience Methods.

[7]  Anne M. M. Fransen,et al.  Sensory and cognitive neurophysiology in rats. Part 2: Validation and demonstration , 2014, Journal of Neuroscience Methods.

[8]  J. Gross Analytical methods and experimental approaches for electrophysiological studies of brain oscillations , 2014, Journal of Neuroscience Methods.

[9]  Miles A. Whittington,et al.  Neurosystems: brain rhythms and cognitive processing , 2013, The European journal of neuroscience.

[10]  N. Logothetis,et al.  Scaling Brain Size, Keeping Timing: Evolutionary Preservation of Brain Rhythms , 2013, Neuron.

[11]  A. Riehle,et al.  The ups and downs of beta oscillations in sensorimotor cortex , 2013, Experimental Neurology.

[12]  D. Cheyne MEG studies of sensorimotor rhythms: A review , 2013, Experimental Neurology.

[13]  E. Fetz Volitional Control of Cortical Oscillations and Synchrony , 2013, Neuron.

[14]  M. Wacker,et al.  Time-frequency Techniques in Biomedical Signal Analysis , 2013, Methods of Information in Medicine.

[15]  E. Maris,et al.  Beyond establishing involvement: quantifying the contribution of anticipatory α- and β-band suppression to perceptual improvement with attention. , 2012, Journal of neurophysiology.

[16]  Eric Maris,et al.  Attentional Cues Affect Accuracy and Reaction Time via Different Cognitive and Neural Processes , 2012, The Journal of Neuroscience.

[17]  D. Cheyne,et al.  Intended actions and unexpected outcomes: automatic and controlled processing in a rapid motor task , 2012, Front. Hum. Neurosci..

[18]  Daniel K. Leventhal,et al.  Basal Ganglia Beta Oscillations Accompany Cue Utilization , 2012, Neuron.

[19]  M. Ding,et al.  Attentional modulation of the somatosensory mu rhythm , 2011, Neuroscience.

[20]  A. Sobolewski,et al.  The 5–12Hz oscillations in the barrel cortex of awake rats – Sustained attention during behavioral idling? , 2011, Clinical Neurophysiology.

[21]  E. Maris,et al.  Orienting Attention to an Upcoming Tactile Event Involves a Spatially and Temporally Specific Modulation of Sensorimotor Alpha- and Beta-Band Oscillations , 2011, The Journal of Neuroscience.

[22]  R. Turner,et al.  Bursts and oscillations as independent properties of neural activity in the parkinsonian globus pallidus internus , 2011, Neurobiology of Disease.

[23]  Marieke K. van Vugt,et al.  Spatially distributed patterns of oscillatory coupling between high-frequency amplitudes and low-frequency phases in human iEEG , 2011, NeuroImage.

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

[25]  Ole Jensen,et al.  Tactile expectation modulates pre-stimulus β-band oscillations in human sensorimotor cortex , 2010, NeuroImage.

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

[27]  Dominique L. Pritchett,et al.  Quantitative analysis and biophysically realistic neural modeling of the MEG mu rhythm: rhythmogenesis and modulation of sensory-evoked responses. , 2009, Journal of neurophysiology.

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

[29]  Michael A. DiSano,et al.  Intracranial EEG Reveals a Time- and Frequency-Specific Role for the Right Inferior Frontal Gyrus and Primary Motor Cortex in Stopping Initiated Responses , 2009, The Journal of Neuroscience.

[30]  M. Breakspear,et al.  Bistability and Non-Gaussian Fluctuations in Spontaneous Cortical Activity , 2009, The Journal of Neuroscience.

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

[32]  Roger D. Traub,et al.  Rhythm Generation through Period Concatenation in Rat Somatosensory Cortex , 2008, PLoS Comput. Biol..

[33]  M. Heil,et al.  Expertise in dance modulates alpha/beta event‐related desynchronization during action observation , 2008, The European journal of neuroscience.

[34]  Robert Oostenveld,et al.  Motor-cortical beta oscillations are modulated by correctness of observed action , 2008, NeuroImage.

[35]  Stuart N Baker,et al.  Cells in somatosensory areas show synchrony with beta oscillations in monkey motor cortex , 2007, The European journal of neuroscience.

[36]  S. Baker,et al.  Network oscillations and intrinsic spiking rhythmicity do not covary in monkey sensorimotor areas , 2007, The Journal of physiology.

[37]  Miles A Whittington,et al.  A beta2-frequency (20–30 Hz) oscillation in nonsynaptic networks of somatosensory cortex , 2006, Proceedings of the National Academy of Sciences.

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

[39]  William Gaetz,et al.  Localization of sensorimotor cortical rhythms induced by tactile stimulation using spatially filtered MEG , 2006, NeuroImage.

[40]  R. Oostenveld,et al.  Tactile Spatial Attention Enhances Gamma-Band Activity in Somatosensory Cortex and Reduces Low-Frequency Activity in Parieto-Occipital Areas , 2006, The Journal of Neuroscience.

[41]  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.

[42]  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.

[43]  A. Bruns Fourier-, Hilbert- and wavelet-based signal analysis: are they really different approaches? , 2004, Journal of Neuroscience Methods.

[44]  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.

[45]  Fabrice Labeau,et al.  Discrete Time Signal Processing , 2004 .

[46]  Miguel A L Nicolelis,et al.  Behavioral detection of tactile stimuli during 7–12 Hz cortical oscillations in awake rats , 2003, Nature Neuroscience.

[47]  P. Derambure,et al.  Basic mechanisms of central rhythms reactivity to preparation and execution of a voluntary movement: a stereoelectroencephalographic study , 2003, Clinical Neurophysiology.

[48]  Febo Cincotti,et al.  Human Cortical Electroencephalography (EEG) Rhythms during the Observation of Simple Aimless Movements: A High-Resolution EEG Study , 2002, NeuroImage.

[49]  A. Oliviero,et al.  Dopamine-dependent changes in the functional connectivity between basal ganglia and cerebral cortex in humans. , 2002, Brain : a journal of neurology.

[50]  Andrea Brovelli,et al.  Medium-Range Oscillatory Network and the 20-Hz Sensorimotor Induced Potential , 2002, NeuroImage.

[51]  H. Berendse,et al.  Motor perseveration is an early sign of Parkinson’s disease , 2001, Neurology.

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

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

[54]  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.

[55]  G Pfurtscheller,et al.  Event-related beta synchronization after wrist, finger and thumb movement. , 1998, Electroencephalography and clinical neurophysiology.

[56]  A. Aertsen,et al.  Spike synchronization and rate modulation differentially involved in motor cortical function. , 1997, Science.

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

[58]  R. Hari,et al.  Cortical control of human motoneuron firing during isometric contraction. , 1997, Journal of neurophysiology.

[59]  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.

[60]  E. Olivier,et al.  Coherent oscillations in monkey motor cortex and hand muscle EMG show task‐dependent modulation , 1997, The Journal of physiology.

[61]  G. Pfurtscheller,et al.  On the existence of different types of central beta rhythms below 30 Hz. , 1997, Electroencephalography and clinical neurophysiology.

[62]  R. Hari,et al.  Human cortical oscillations: a neuromagnetic view through the skull , 1997, Trends in Neurosciences.

[63]  J. Vitek,et al.  Burst and oscillation as disparate neuronal properties , 1996, Journal of Neuroscience Methods.

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

[65]  R. Hari,et al.  Functional Segregation of Movement-Related Rhythmic Activity in the Human Brain , 1995, NeuroImage.

[66]  M. Nicolelis,et al.  Sensorimotor encoding by synchronous neural ensemble activity at multiple levels of the somatosensory system. , 1995, Science.

[67]  R. Hari,et al.  Spatiotemporal characteristics of sensorimotor neuromagnetic rhythms related to thumb movement , 1994, Neuroscience.

[68]  J. R. Rosenberg,et al.  The Fourier approach to the identification of functional coupling between neuronal spike trains. , 1989, Progress in biophysics and molecular biology.

[69]  Paul L. Nunez,et al.  A Study of Origins of the Time Dependencies of Scalp EEG: I - Theoretical Basis , 1981, IEEE Transactions on Biomedical Engineering.

[70]  Paul L. Nunez,et al.  A Study of Origins of the Time Dependencies of Scalp EEG: II-Experimental Support of Theory , 1981, IEEE Transactions on Biomedical Engineering.

[71]  Barry R. Komisaruk,et al.  Synchrony among rhythmical facial tremor, neocortical ‘ALPHA’ waves, and thalamic non-sensory neuronal bursts in intact awake rats , 1980, Brain Research.

[72]  M. Montaron,et al.  Relations entre l'attention et le rythme mu chez le chat et le singe* , 1979 .

[73]  B. Kaplan Morphological evidence that feline SMR and human Mu are analogous rhythms , 1979, Brain Research Bulletin.

[74]  J. Bouyer,et al.  Fast somato-parietal rhythms during combined focal attention and immobility in baboon and squirrel monkey. , 1979, Electroencephalography and clinical neurophysiology.

[75]  J. Bouyer,et al.  [Relationship between attention and mu rhythms in the cat and the monkey (author's transl)]. , 1979, Revue d'electroencephalographie et de neurophysiologie clinique.

[76]  Vanderwolf Ch,et al.  Neocortical and hippocampal activation in relation to behavior: Effects of atropine, eserine, phenothiazines, and amphetamine. , 1975 .

[77]  C. H. Vanderwolf Neocortical and hippocampal activation relation to behavior: effects of atropine, eserine, phenothiazines, and amphetamine. , 1975, Journal of comparative and physiological psychology.

[78]  M. R. Novick,et al.  Statistical Theories of Mental Test Scores. , 1971 .

[79]  H GASTAUT,et al.  [Study of a little electroencephalographic activity: rolandic arched rhythm]. , 1952, Marseille medical.

[80]  H. L. Andrews,et al.  ELECTRO-ENCEPHALOGRAPHY: III. NORMAL DIFFERENTIATION OF OCCIPITAL AND PRECENTRAL REGIONS IN MAN , 1938 .