Synchronization of beta and gamma oscillations in the somatosensory evoked neuromagnetic steady-state response

The sensory evoked neuromagnetic response consists of superimposition of an immediately stimulus-driven component and induced changes in the autonomous brain activity, each having distinct functional relevance. Commonly, the strength of phase locking in neural activities has been used to differentiate the different responses. The steady-state response is a strong oscillatory neural activity, which is evoked with rhythmic stimulation, and provides an effective tool to investigate oscillatory brain networks. In this case, both the sensory response and intrinsic activity, representing higher order processes, are highly synchronized to the stimulus. In this study we hypothesized that temporal dynamics of oscillatory activities would characterize the differences between the two types of activities and that beta and gamma oscillations are differently involved in this distinction. We used magnetoencephalography (MEG) for studying how ongoing steady-state responses elicited by a 20-Hz vibro-tactile stimulus to the right index finger were affected by a concurrent isolated touch stimulus to the same hand ring finger. SI source activity showed oscillations at multiples of 20 Hz with characteristic differences in the beta band and the gamma band. The response amplitudes were largest at 20 Hz (beta) and significantly reduced at 40 Hz and 60 Hz (gamma), although synchronization strength, indicated by inter-trial coherence (ITC), did not substantially differ between 20 Hz and 40 Hz. Moreover, the beta oscillations showed a fast onset, whereas the amplitude of gamma oscillations increased slowly and reached the steady state 400 ms after onset of the vibration stimulus. Most importantly, the pulse stimuli interacted only with gamma oscillations in a way that gamma oscillations decreased immediately after the concurrent stimulus onset and recovered slowly, resembling the initial slope. Such time course of gamma oscillations is similar to our previous observations in the auditory system. The time constant is in line with the time required for conscious perception of the sensory stimulus. Based on the observed different spectro-temporal dynamics, we propose that while beta activities likely relate to independent representation of the sensory input, gamma oscillation likely relates to binding of sensory information for higher order processing.

[1]  D. Cheyne,et al.  Cortical dynamics of selective attention to somatosensory events , 2010, NeuroImage.

[2]  R. Kakigi,et al.  1914 Effects of tactile interference stimulation on somatosensory evoked magnetic fields , 1996, Neuroscience Research.

[3]  T. Picton,et al.  Human auditory steady-state responses: Respuestas auditivas de estado estable en humanos , 2003, International journal of audiology.

[4]  W. Singer,et al.  Visuomotor integration is associated with zero time-lag synchronization among cortical areas , 1997, Nature.

[5]  Guido Conti,et al.  Generation of human auditory steady-state responses , 1998 .

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

[7]  R. Llinás,et al.  Of dreaming and wakefulness , 1991, Neuroscience.

[8]  Christo Pantev,et al.  Auditory steady-state responses reveal amplitude modulation gap detection thresholds. , 2004, The Journal of the Acoustical Society of America.

[9]  C. Escera,et al.  The role of the dopamine transporter DAT1 genotype on the neural correlates of cognitive flexibility , 2010, The European journal of neuroscience.

[10]  N. E. Crone,et al.  Computationally efficient approaches to calculating significant ERD/ERS changes in the time–frequency plane , 2005, Journal of Neuroscience Methods.

[11]  W. Sannita Stimulus-specific oscillatory responses of the brain: a time/frequency-related coding process , 2000, Clinical Neurophysiology.

[12]  S. Makeig,et al.  A 40-Hz auditory potential recorded from the human scalp. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[13]  Mark Tommerdahl,et al.  Dynamic representations of the somatosensory cortex , 2010, Neuroscience & Biobehavioral Reviews.

[14]  Alan C. Evans,et al.  Enhancement of MR Images Using Registration for Signal Averaging , 1998, Journal of Computer Assisted Tomography.

[15]  G. Ermentrout,et al.  Gamma rhythms and beta rhythms have different synchronization properties. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[16]  Jürgen Kurths,et al.  Detection of n:m Phase Locking from Noisy Data: Application to Magnetoencephalography , 1998 .

[17]  R. Ilmoniemi,et al.  Temporal window of integration of auditory information in the human brain. , 1998, Psychophysiology.

[18]  M. Breakspear,et al.  Multi-frequency phase locking in human somatosensory cortex. , 2011, Progress in biophysics and molecular biology.

[19]  R Näätänen,et al.  Temporal constraints of auditory event synthesis: evidence from ERPs , 1998, Neuroreport.

[20]  Jonathan Z. Simon,et al.  Fully complex magnetoencephalography , 2005, Journal of Neuroscience Methods.

[21]  E. Adrian,et al.  The electrical activity of the mammalian olfactory bulb. , 1950, Electroencephalography and clinical neurophysiology.

[22]  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.

[23]  Saskia Haegens,et al.  Somatosensory Anticipatory Alpha Activity Increases to Suppress Distracting Input , 2012, Journal of Cognitive Neuroscience.

[24]  B. Ross,et al.  Precise mapping of the somatotopic hand area using neuromagnetic steady-state responses , 2012, Brain Research.

[25]  G. Buzsáki,et al.  Neuronal Oscillations in Cortical Networks , 2004, Science.

[26]  W. Singer,et al.  Dynamic predictions: Oscillations and synchrony in top–down processing , 2001, Nature Reviews Neuroscience.

[27]  G. Pfurtscheller,et al.  ERD/ERS patterns reflecting sensorimotor activation and deactivation. , 2006, Progress in brain research.

[28]  D. Pollen Brain stimulation and conscious experience , 2004, Consciousness and Cognition.

[29]  D. Regan Some characteristics of average steady-state and transient responses evoked by modulated light. , 1966, Electroencephalography and clinical neurophysiology.

[30]  G J Vachtsevanos,et al.  Gamma coherence and conscious perception , 2002, Neurology.

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

[32]  M. Scherg,et al.  Deconvolution of 40 Hz steady-state fields reveals two overlapping source activities of the human auditory cortex , 1999, Clinical Neurophysiology.

[33]  Timothy Bardouille,et al.  MEG imaging of sensorimotor areas using inter-trial coherence in vibrotactile steady-state responses , 2008, NeuroImage.

[34]  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.

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

[36]  C. Herrmann Human EEG responses to 1–100 Hz flicker: resonance phenomena in visual cortex and their potential correlation to cognitive phenomena , 2001, Experimental Brain Research.

[37]  A. Cichocki,et al.  Steady-state visually evoked potentials: Focus on essential paradigms and future perspectives , 2010, Progress in Neurobiology.

[38]  W. Freeman,et al.  Harmonic Oscillation as Model for Cortical Excitability Changes with Attention in Cats , 1961, Science.

[39]  R. Llinás,et al.  In vitro neurons in mammalian cortical layer 4 exhibit intrinsic oscillatory activity in the 10- to 50-Hz frequency range. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[40]  C M Michel,et al.  Intracerebral dipole source localization for FFT power maps. , 1990, Electroencephalography and clinical neurophysiology.

[41]  W. Freeman,et al.  Aperiodic phase re‐setting in scalp EEG of beta–gamma oscillations by state transitions at alpha–theta rates , 2003, Human brain mapping.

[42]  Y. Yarom,et al.  Resonance, oscillation and the intrinsic frequency preferences of neurons , 2000, Trends in Neurosciences.

[43]  Y Okada,et al.  An automatic identification and removal method for eye-blink artifacts in event-related magnetoencephalographic measurements , 2007, Physiological measurement.

[44]  Maurizio Maurizi,et al.  Generation of human auditory steady-state responses (SSRs). II: Addition of responses to individual stimuli , 1995, Hearing Research.

[45]  V. Hömberg,et al.  Influence of stimulus repetition rate on cortical somatosensory potentials evoked by median nerve stimulation: Implications for generation mechanisms , 1991, Journal of the Neurological Sciences.

[46]  C Pantev,et al.  A high-precision magnetoencephalographic study of human auditory steady-state responses to amplitude-modulated tones. , 2000, The Journal of the Acoustical Society of America.

[47]  R. Näätänen,et al.  Gabor filters: an informative way for analysing event-related brain activity , 1995, Journal of Neuroscience Methods.

[48]  T W Picton,et al.  Potentials evoked by the sinusoidal modulation of the amplitude or frequency of a tone. , 1987, The Journal of the Acoustical Society of America.

[49]  O. Bertrand,et al.  Oscillatory gamma activity in humans and its role in object representation , 1999, Trends in Cognitive Sciences.

[50]  B. Ross A novel type of auditory responses: temporal dynamics of 40-Hz steady-state responses induced by changes in sound localization. , 2008, Journal of neurophysiology.

[51]  B. Ross,et al.  Interference in dichotic listening: the effect of contralateral noise on oscillatory brain networks , 2012, The European journal of neuroscience.

[52]  B LIBET,et al.  PRODUCTION OF THRESHOLD LEVELS OF CONSCIOUS SENSATION BY ELECTRICAL STIMULATION OF HUMAN SOMATOSENSORY CORTEX. , 1964, Journal of neurophysiology.

[53]  D Regan,et al.  A high frequency mechanism which underlies visual evoked potentials. , 1968, Electroencephalography and clinical neurophysiology.

[54]  W. Singer,et al.  The gamma cycle , 2007, Trends in Neurosciences.

[55]  Alessandro Presacco,et al.  Auditory steady-state responses to 40-Hz click trains: Relationship to middle latency, gamma band and beta band responses studied with deconvolution , 2010, Clinical Neurophysiology.

[56]  Yasuhiko Saito,et al.  Reciprocal modulation of somatosensory evoked N20m primary response and high-frequency oscillations by interference stimulation , 1999, Clinical Neurophysiology.

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

[58]  Terence W. Picton,et al.  Temporal integration in the human auditory cortex as represented by the development of the steady-state magnetic field , 2002, Hearing Research.

[59]  B. Ross,et al.  Attention modulates beta oscillations during prolonged tactile stimulation , 2010, The European journal of neuroscience.

[60]  T. Picton,et al.  Physiological detection of interaural phase differences. , 2007, The Journal of the Acoustical Society of America.

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