Attention modulates beta oscillations during prolonged tactile stimulation

The inter‐play between changes in beta‐band (14–30‐Hz) cortical rhythms and attention during somatosensation informs us about where and when relevant processes occur in the brain. As such, we investigated the effects of attention on somatosensory evoked and induced responses using vibrotactile stimulation and magnetoencephalographic recording. Subjects received trains of vibration at 23 Hz to the right index finger while watching a movie and ignoring the somatosensory stimuli or paying attention to the stimuli to detect a change in the duration of the stimulus. The amplitude of the evoked 23‐Hz steady‐state response in the contralateral primary somatosensory cortex (SI) was enhanced by attention and the underlying dipole source was located 2 mm more medially, indicating top‐down recruitment of additional neuronal populations for the functionally relevant stimulus. Attentional modulation of the somatosensory evoked response indicates facilitation of early processing of the tactile stimulus. Beta‐band activity increased after vibration offset in the contralateral primary motor cortex (MI) [event‐related synchronization (ERS)] and this increase was larger for attended than ignored stimuli. Beta‐band activity decreased in the ipsilateral SI prior to stimulus offset [event‐related desynchronization (ERD)] for attended stimuli only. Whereas attention modulation of the evoked response was confined to the contralateral SI, event‐related changes of beta‐band activity involved contralateral SI–MI and inter‐hemispheric SI–SI connections. Modulation of neural activity in such a large sensorimotor network indicates a role for beta activity in higher‐order processing.

[1]  Simon J Graham,et al.  Activation in SI and SII: the influence of vibrotactile amplitude during passive and task-relevant stimulation. , 2004, Brain research. Cognitive brain research.

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

[3]  D. S. Barth,et al.  Neuromagnetic investigation of somatotopy of human hand somatosensory cortex , 2004, Experimental Brain Research.

[4]  Larry E. Roberts,et al.  Functional Organization of Primary Somatosensory Cortex Depends on the Focus of Attention , 2002, NeuroImage.

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

[6]  Robert Galambos,et al.  A Comparison of Certain Gamma Band (40-HZ) Brain Rhythms in Cat and Man , 1992 .

[7]  T. Bullock,et al.  Induced Rhythms in the Brain , 1992, Brain Dynamics.

[8]  Shozo Tobimatsu,et al.  Steady-state vibration somatosensory evoked potentials: physiological characteristics and tuning function , 1999, Clinical Neurophysiology.

[9]  Fred Tam,et al.  Magnetoencephalographic study of vibrotactile evoked transient and steady-state responses in human somatosensory cortex , 2006, NeuroImage.

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

[11]  T. Picton,et al.  The effect of attention on the auditory steady-state response. , 2004, Neurology & clinical neurophysiology : NCN.

[12]  L. Deecke,et al.  Somatotopy of human hand somatosensory cortex as studied in scalp EEG. , 1993, Electroencephalography and clinical neurophysiology.

[13]  P. Derambure,et al.  Relationship between event-related beta synchronization and afferent inputs: Analysis of finger movement and peripheral nerve stimulations , 2006, Clinical Neurophysiology.

[14]  F. Varela,et al.  Neuromagnetic imaging of cortical oscillations accompanying tactile stimulation. , 2003, Brain research. Cognitive brain research.

[15]  F. L. D. Silva,et al.  Beta rebound after different types of motor imagery in man , 2005, Neuroscience Letters.

[16]  Norihiko Fujita,et al.  Movement-Related Desynchronization of the Cerebral Cortex Studied with Spatially Filtered Magnetoencephalography , 2000, NeuroImage.

[17]  R. Johansson,et al.  Tactile sensibility in the human hand: relative and absolute densities of four types of mechanoreceptive units in glabrous skin. , 1979, The Journal of physiology.

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

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

[20]  A Z Snyder,et al.  Steady-state vibration evoked potentials: descriptions of technique and characterization of responses. , 1992, Electroencephalography and clinical neurophysiology.

[21]  Matthias M. Müller,et al.  Selective spatial attention to left or right hand flutter sensation modulates the steady-state somatosensory evoked potential. , 2004, Brain research. Cognitive brain research.

[22]  T. Lagerlund,et al.  Spatial filtering of multichannel electroencephalographic recordings through principal component analysis by singular value decomposition. , 1997, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[23]  Matthias M. Müller,et al.  Sustained spatial attention to vibration is mediated in primary somatosensory cortex , 2007, NeuroImage.

[24]  Alfons Schnitzler,et al.  Rapid mapping of finger representations in human primary somatosensory cortex applying neuromagnetic steady-state responses , 2002, Neuroreport.

[25]  R. Ivry,et al.  Ipsilateral motor cortex activity during unimanual hand movements relates to task complexity. , 2005, Journal of neurophysiology.

[26]  C Pantev,et al.  Stimulus induced desynchronization of human auditory 40-Hz steady-state responses. , 2005, Journal of neurophysiology.

[27]  R Hari,et al.  Magnetic evoked fields of the human brain: basic principles and applications. , 1990, Electroencephalography and clinical neurophysiology. Supplement.

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

[29]  R. Hari,et al.  Functional Organization of the Human First and Second Somatosensory Cortices: a Neuromagnetic Study , 1993, The European journal of neuroscience.

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

[31]  G. Sperling,et al.  Attentional modulation of SSVEP power depends on the network tagged by the flicker frequency. , 2006, Cerebral cortex.

[32]  H. Heinze,et al.  Reproducibility and Stability of Neuromagnetic Source Imaging in Primary Somatosensory Cortex , 2004, Brain Topography.

[33]  Marcia Grabowecky,et al.  Attention induces synchronization-based response gain in steady-state visual evoked potentials , 2007, Nature Neuroscience.

[34]  Se Robinson,et al.  Functional neuroimaging by Synthetic Aperture Magnetometry (SAM) , 1999 .

[35]  F. Castellanos,et al.  MEG event-related desynchronization and synchronization deficits during basic somatosensory processing in individuals with ADHD , 2008, Behavioral and Brain Functions.

[36]  S. Kuriki,et al.  Principal component elimination method for the improvement of S/N in evoked neuromagnetic field measurements , 1999, IEEE Transactions on Biomedical Engineering.

[37]  H. Flor,et al.  Reproducibility and Stability of Neuroelectric Source Imaging in Primary Somatosensory Cortex , 2004, Brain Topography.

[38]  F E Bloom,et al.  Noninvasive somatosensory homunculus mapping in humans by using a large-array biomagnetometer. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[39]  H Johansen-Berg,et al.  The physiology and psychology of selective attention to touch. , 2000, Frontiers in bioscience : a journal and virtual library.

[40]  Gabriel Curio,et al.  Spatial attention related SEP amplitude modulations covary with BOLD signal in S1--a simultaneous EEG--fMRI study. , 2008, Cerebral cortex.

[41]  TACTILE AND AUDITORY STIMULI REPEATED AT HIGH RATES (30–50 PER SEC) PRODUCE SIMILAR EVENT RELATED POTENTIALS * , 1980, Annals of the New York Academy of Sciences.

[42]  Sandra E. Black,et al.  Task-Relevant Modulation of Contralateral and Ipsilateral Primary Somatosensory Cortex and the Role of a Prefrontal-Cortical Sensory Gating System , 2002, NeuroImage.

[43]  O. Bertrand,et al.  Effects of Selective Attention on the Electrophysiological Representation of Concurrent Sounds in the Human Auditory Cortex , 2007, The Journal of Neuroscience.

[44]  Debra F. McLaughlin,et al.  Evoked potentials as indices of adaptation in the somatosensory system in humans: A review and prospectus , 1993, Brain Research Reviews.