Repetitive tactile stimulation changes resting-state functional connectivity—implications for treatment of sensorimotor decline

Neurological disorders and physiological aging can lead to a decline of perceptual abilities. In contrast to the conventional therapeutic approach that comprises intensive training and practicing, passive repetitive sensory stimulation (RSS) has recently gained increasing attention as an alternative to countervail the sensory decline by improving perceptual abilities without the need of active participation. A particularly effective type of high-frequency RSS, utilizing Hebbian learning principles, improves perceptual acuity as well as sensorimotor functions and has been successfully applied to treat chronic stroke patients and elderly subjects. High-frequency RSS has been shown to induce plastic changes of somatosensory cortex such as representational map reorganization, but its impact on the brain's ongoing network activity and resting-state functional connectivity has not been investigated so far. Here, we applied high-frequency RSS in healthy human subjects and analyzed resting state Electroencephalography (EEG) functional connectivity patterns before and after RSS by means of imaginary coherency (ImCoh), a frequency-specific connectivity measure which is known to reduce over-estimation biases due to volume conduction and common reference. Thirty minutes of passive high-frequency RSS lead to significant ImCoh-changes of the resting state mu-rhythm in the individual upper alpha frequency band within distributed sensory and motor cortical areas. These stimulation induced distributed functional connectivity changes likely underlie the previously observed improvement in sensorimotor integration.

[1]  M. Hallett,et al.  The non-motor syndrome of primary dystonia: clinical and pathophysiological implications. , 2012, Brain : a journal of neurology.

[2]  H. Dinse.  Choosing to improve or to impair , 2012, Clinical Neurophysiology.

[3]  S. Nagarajan,et al.  Clinical Symptoms and Alpha Band Resting-State Functional Connectivity Imaging in Patients With Schizophrenia: Implications for Novel Approaches to Treatment , 2011, Biological Psychiatry.

[4]  L Trahms,et al.  Characterization of motor and somatosensory function for stroke patients. , 2011, Physiological measurement.

[5]  Karel Svoboda,et al.  Long-Range Neuronal Circuits Underlying the Interaction between Sensory and Motor Cortex , 2011, Neuron.

[6]  D. J. McFarland,et al.  Trained modulation of sensorimotor rhythms can affect reaction time , 2011, Clinical Neurophysiology.

[7]  M. Alegre,et al.  Ketamine-Induced Oscillations in the Motor Circuit of the Rat Basal Ganglia , 2011, PloS one.

[8]  A. Villringer,et al.  How Ongoing Neuronal Oscillations Account for Evoked fMRI Variability , 2011, The Journal of Neuroscience.

[9]  Hubert R. Dinse,et al.  Improvement and Impairment of Visually Guided Behavior through LTP- and LTD-like Exposure-Based Visual Learning , 2011, Current Biology.

[10]  Anthony Randal McIntosh,et al.  Partial Least Squares (PLS) methods for neuroimaging: A tutorial and review , 2011, NeuroImage.

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

[12]  James A. Roberts,et al.  Biophysical Mechanisms of Multistability in Resting-State Cortical Rhythms , 2011, The Journal of Neuroscience.

[13]  Ernesto Pereda,et al.  Assessment of electroencephalographic functional connectivity in term and preterm neonates , 2011, Clinical Neurophysiology.

[14]  A. Kleinschmidt,et al.  Modulation of Visually Evoked Cortical fMRI Responses by Phase of Ongoing Occipital Alpha Oscillations , 2011, The Journal of Neuroscience.

[15]  Michael Breakspear,et al.  Exploiting the potential of three dimensional spatial wavelet analysis to explore nesting of temporal oscillations and spatial variance in simultaneous EEG-fMRI data. , 2011, Progress in biophysics and molecular biology.

[16]  Heidi E Kirsch,et al.  Resting functional connectivity in patients with brain tumors in eloquent areas , 2011, Annals of neurology.

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

[18]  Michael W. Cole,et al.  Prefrontal Dynamics Underlying Rapid Instructed Task Learning Reverse with Practice , 2010, The Journal of Neuroscience.

[19]  Dominique L. Pritchett,et al.  Cued Spatial Attention Drives Functionally Relevant Modulation of the Mu Rhythm in Primary Somatosensory Cortex , 2010, The Journal of Neuroscience.

[20]  A. Kleinschmidt,et al.  Intrinsic Connectivity Networks, Alpha Oscillations, and Tonic Alertness: A Simultaneous Electroencephalography/Functional Magnetic Resonance Imaging Study , 2010, The Journal of Neuroscience.

[21]  O. Jensen,et al.  Shaping Functional Architecture by Oscillatory Alpha Activity: Gating by Inhibition , 2010, Front. Hum. Neurosci..

[22]  C. Petersen,et al.  Long‐range connectivity of mouse primary somatosensory barrel cortex , 2010, The European journal of neuroscience.

[23]  Hubert R. Dinse,et al.  Repetitive Electric Stimulation Elicits Enduring Improvement of Sensorimotor Performance in Seniors , 2010, Neural plasticity.

[24]  Brendan Z. Allison,et al.  The Hybrid BCI , 2010, Frontiers in Neuroscience.

[25]  S. Nagarajan,et al.  Cognitive Impairments in Schizophrenia as Assessed Through Activation and Connectivity Measures of Magnetoencephalography (MEG) Data , 2009, Front. Hum. Neurosci..

[26]  Tobias Kalisch,et al.  Effects of repetitive electrical stimulation to treat sensory loss in persons poststroke. , 2009, Archives of physical medicine and rehabilitation.

[27]  Stefan Haufe,et al.  Now You'll Feel It, Now You Won't: EEG Rhythms Predict the Effectiveness of Perceptual Masking , 2009, Journal of Cognitive Neuroscience.

[28]  Bin He,et al.  Cortical imaging of sensorimotor rhythms for BCI applications , 2009, 2009 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[29]  Gabriel Curio,et al.  Ultrahigh-frequency EEG during fMRI: Pushing the limits of imaging-artifact correction , 2009, NeuroImage.

[30]  Arno Villringer,et al.  Oscillatory brain states interact with late cognitive components of the somatosensory evoked potential , 2009, Journal of Neuroscience Methods.

[31]  Petra Ritter,et al.  Detecting alpha rhythm phase reset by phase sorting: Caveats to consider , 2009, NeuroImage.

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

[33]  Patrick Ragert,et al.  Impaired tactile acuity in old age is accompanied by enlarged hand representations in somatosensory cortex. , 2009, Cerebral cortex.

[34]  Jacques Felblinger,et al.  Automated cortical projection of EEG sensors: Anatomical correlation via the international 10–10 system , 2009, NeuroImage.

[35]  A. Villringer,et al.  Rolandic alpha and beta EEG rhythms' strengths are inversely related to fMRI‐BOLD signal in primary somatosensory and motor cortex , 2009, Human brain mapping.

[36]  M. Hallett,et al.  Disordered plasticity in the primary somatosensory cortex in focal hand dystonia. , 2009, Brain : a journal of neurology.

[37]  Martin Tegenthoff,et al.  Improvement of sensorimotor functions in old age by passive sensory stimulation , 2008, Clinical interventions in aging.

[38]  Gabriel Curio,et al.  High-frequency (600 Hz) population spikes in human EEG delineate thalamic and cortical fMRI activation sites , 2008, NeuroImage.

[39]  D. Kleinfeld,et al.  'Where' and 'what' in the whisker sensorimotor system , 2008, Nature Reviews Neuroscience.

[40]  M. Berger,et al.  Mapping functional connectivity in patients with brain lesions , 2008, Annals of neurology.

[41]  Arno Villringer,et al.  Influence of ongoing alpha rhythm on the visual evoked potential , 2008, NeuroImage.

[42]  Klaus-Robert Müller,et al.  Machine learning for real-time single-trial EEG-analysis: From brain–computer interfacing to mental state monitoring , 2008, Journal of Neuroscience Methods.

[43]  Patrick Ragert,et al.  Contribution of transcranial magnetic stimulation to the understanding of cortical mechanisms involved in motor control , 2008, The Journal of physiology.

[44]  K. Furie,et al.  Heart disease and stroke statistics--2007 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. , 2008, Circulation.

[45]  Patrick Ragert,et al.  Differential effects of tactile high- and low-frequency stimulation on tactile discrimination in human subjects , 2008, BMC Neuroscience.

[46]  Patrick Ragert,et al.  Sustained increase of somatosensory cortex excitability by tactile coactivation studied by paired median nerve stimulation in humans correlates with perceptual gain , 2007, The Journal of physiology.

[47]  Simon Hanslmayr,et al.  Prestimulus oscillations predict visual perception performance between and within subjects , 2007, NeuroImage.

[48]  Klaus-Robert Müller,et al.  The non-invasive Berlin Brain–Computer Interface: Fast acquisition of effective performance in untrained subjects , 2007, NeuroImage.

[49]  Andreas Daffertshofer,et al.  Multivariate time–frequency analysis of electromagnetic brain activity during bimanual motor learning , 2007, NeuroImage.

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

[51]  L. Cohen,et al.  Effects of somatosensory stimulation on motor function in chronic cortico-subcortical strokes , 2007, Journal of Neurology.

[52]  Patrick Ragert,et al.  Tactile coactivation resets age‐related decline of human tactile discrimination , 2006, Annals of neurology.

[53]  Lumy Sawaki,et al.  Effects of Somatosensory Stimulation on Use-Dependent Plasticity in Chronic Stroke , 2006, Stroke.

[54]  Gert Pfurtscheller,et al.  The cortical activation model (CAM). , 2006, Progress in brain research.

[55]  W. Klimesch,et al.  Upper alpha ERD and absolute power: their meaning for memory performance. , 2006, Progress in brain research.

[56]  Patrick Ragert,et al.  Improvement of Tactile Discrimination Performance and Enlargement of Cortical Somatosensory Maps after 5 Hz rTMS , 2005, PLoS biology.

[57]  P. Brown,et al.  Cortico-cortical coupling in Parkinson's disease and its modulation by therapy. , 2005, Brain : a journal of neurology.

[58]  R. Enoka,et al.  Practice reduces motor unit discharge variability in a hand muscle and improves manual dexterity in old adults. , 2005, Journal of applied physiology.

[59]  Kuno Kirschfeld,et al.  The physical basis of alpha waves in the electroencephalogram and the origin of the “Berger effect” , 2005, Biological Cybernetics.

[60]  K. Linkenkaer-Hansen,et al.  Prestimulus Oscillations Enhance Psychophysical Performance in Humans , 2004, The Journal of Neuroscience.

[61]  M. Hallett,et al.  Identifying true brain interaction from EEG data using the imaginary part of coherency , 2004, Clinical Neurophysiology.

[62]  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.

[63]  Patrick Ragert,et al.  Sustained increase of somatosensory cortex excitability by 5 Hz repetitive transcranial magnetic stimulation studied by paired median nerve stimulation in humans , 2004, Neuroscience Letters.

[64]  H. Dinse,et al.  Functional Imaging of Perceptual Learning in Human Primary and Secondary Somatosensory Cortex , 2003, Neuron.

[65]  H. Dinse,et al.  Pharmacological Modulation of Perceptual Learning and Associated Cortical Reorganization , 2003, Science.

[66]  A. Fiaschi,et al.  Role of the somatosensory system in primary dystonia , 2003, Movement disorders : official journal of the Movement Disorder Society.

[67]  Leonid Kopylev,et al.  Age‐dependent changes in the ability to encode a novel elementary motor memory , 2003, Annals of neurology.

[68]  C. Gerloff,et al.  Enhancing cognitive performance with repetitive transcranial magnetic stimulation at human individual alpha frequency , 2003, The European journal of neuroscience.

[69]  Wolfgang Klimesch,et al.  EEG alpha power and intelligence , 2002 .

[70]  T. Sejnowski,et al.  Dynamic Brain Sources of Visual Evoked Responses , 2002, Science.

[71]  L. Cohen,et al.  Increase in hand muscle strength of stroke patients after somatosensory stimulation , 2002, Annals of neurology.

[72]  J. Rothwell,et al.  Transcranial magnetic stimulation: new insights into representational cortical plasticity , 2002, Experimental Brain Research.

[73]  H. Dinse,et al.  Shifts in cortical representations predict human discrimination improvement , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[74]  W. Klimesch,et al.  The role of theta and alpha oscillations for language comprehension in the human electroencephalogram , 2001, Neuroscience Letters.

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

[76]  P. Nunez,et al.  Spatial‐temporal structures of human alpha rhythms: Theory, microcurrent sources, multiscale measurements, and global binding of local networks , 2001, Human brain mapping.

[77]  G. Pfurtscheller,et al.  Functional dissociation of lower and upper frequency mu rhythms in relation to voluntary limb movement , 2000, Clinical Neurophysiology.

[78]  B. Godde,et al.  Tactile Coactivation-Induced Changes in Spatial Discrimination Performance , 2000, The Journal of Neuroscience.

[79]  M. Granat,et al.  Electrical stimulation of wrist extensors in poststroke hemiplegia. , 1999, Stroke.

[80]  H. Feys,et al.  Effect of a therapeutic intervention for the hemiplegic upper limb in the acute phase after stroke: a single-blind, randomized, controlled multicenter trial. , 1998, Stroke.

[81]  M Doppelmayr,et al.  Brain oscillations and human memory: EEG correlates in the upper alpha and theta band , 1997, Neuroscience Letters.

[82]  M. R. DeLong,et al.  Tactile spatial acuity and roughness discrimination: Impairments due to aging and Parkinson's disease , 1997, Neurology.

[83]  W. Klimesch.  Memory processes, brain oscillations and EEG synchronization. , 1996, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[84]  J. V. Haxby,et al.  Spatial Pattern Analysis of Functional Brain Images Using Partial Least Squares , 1996, NeuroImage.

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

[86]  Terrence J. Sejnowski,et al.  An Information-Maximization Approach to Blind Separation and Blind Deconvolution , 1995, Neural Computation.

[87]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[88]  W. Klimesch,et al.  Episodic and semantic memory: an analysis in the EEG theta and alpha band. , 1994, Electroencephalography and clinical neurophysiology.

[89]  R. Hari,et al.  Characterization of spontaneous MEG rhythms in healthy adults. , 1994, Electroencephalography and clinical neurophysiology.

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

[91]  L. Carey,et al.  Sensory loss in stroke patients: effective training of tactile and proprioceptive discrimination. , 1993, Archives of physical medicine and rehabilitation.

[92]  G. Pfurtscheller.  Event-related synchronization (ERS): an electrophysiological correlate of cortical areas at rest. , 1992, Electroencephalography and clinical neurophysiology.

[93]  W. Koller,et al.  Sensory symptoms in Parkinson's disease , 1984, Neurology.

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

[95]  J. W. Kuhlman,et al.  Functional topography of the human mu rhythm. , 1978, Electroencephalography and clinical neurophysiology.

[96]  H. Gastaut.  [Electrocorticographic study of the reactivity of rolandic rhythm]. , 1952, Revue neurologique.