Sensorimotor synchronization: neurophysiological markers of the asynchrony in a finger-tapping task

Sensorimotor synchronization (SMS) is a form of referential behavior in which an action is coordinated with a predictable external stimulus. The neural bases of the synchronization ability remain unknown, even in the simpler, paradigmatic task of finger tapping to a metronome. In this task the subject is instructed to tap in synchrony with a periodic sequence of brief tones, and the time difference between each response and the corresponding stimulus tone (asynchrony) is recorded. We make a step towards the identification of the neurophysiological markers of SMS by recording high-density EEG event-related potentials and the concurrent behavioral response-stimulus asynchronies during an isochronous paced finger-tapping task. Using principal component analysis, we found an asymmetry between the traces for advanced and delayed responses to the stimulus, in accordance with previous behavioral observations from perturbation studies. We also found that the amplitude of the second component encodes the higher-level percept of asynchrony 100 ms after the current stimulus. Furthermore, its amplitude predicts the asynchrony of the next step, past 300 ms from the previous stimulus, independently of the period length. Moreover, the neurophysiological processing of synchronization errors is performed within a fixed-duration interval after the stimulus. Our results suggest that the correction of a large asynchrony in a periodic task and the recovery of synchrony after a perturbation could be driven by similar neural processes.

[1]  T. Zanto,et al.  Neural correlates of rhythmic expectancy , 2006 .

[2]  Jirí Mates,et al.  A model of synchronization of motor acts to a stimulus sequence , 2004, Biological Cybernetics.

[3]  Bruno H Repp,et al.  Rate Limits in Sensorimotor Synchronization With Auditory and Visual Sequences: The Synchronization Threshold and the Benefits and Costs of Interval Subdivision , 2003, Journal of motor behavior.

[4]  David G. Stork,et al.  Pattern Classification (2nd ed.) , 1999 .

[5]  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.

[6]  D. Hary,et al.  Synchronizing human movement with an external clock source , 1987, Biological Cybernetics.

[7]  Bruno H Repp,et al.  Phase correction in sensorimotor synchronization: nonlinearities in voluntary and involuntary responses to perturbations. , 2002, Human movement science.

[8]  Wolfgang Prinz,et al.  Cortical activations associated with auditorily paced finger tapping , 2003, Neuroreport.

[9]  Wolfgang Prinz,et al.  Neuromagnetic Correlates of Sensorimotor Synchronization , 2000, Journal of Cognitive Neuroscience.

[10]  G. Aschersleben.  Temporal Control of Movements in Sensorimotor Synchronization , 2002, Brain and Cognition.

[11]  J B Poline,et al.  Cerebral mechanisms of word masking and unconscious repetition priming , 2001, Nature Neuroscience.

[12]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[13]  Jeff Pressing,et al.  Spectral properties of human cognition and skill , 1997, Biological Cybernetics.

[14]  L. Jäncke,et al.  Cortical activations during paced finger-tapping applying visual and auditory pacing stimuli. , 2000, Brain research. Cognitive brain research.

[15]  D. Childers,et al.  Distribution of ocular dominance and effect of image clarity , 1973 .

[16]  E. Large,et al.  The dynamics of attending: How people track time-varying events. , 1999 .

[17]  A. Kristofferson,et al.  Response delays and the timing of discrete motor responses , 1973 .

[18]  M. Peters.  The relationship between variability of intertap intervals and interval duration , 1989 .

[19]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[20]  B. Repp.  Sensorimotor synchronization: A review of the tapping literature , 2005, Psychonomic bulletin & review.

[21]  P Praamstra,et al.  Neurophysiological correlates of error correction in sensorimotor-synchronization , 2003, NeuroImage.

[22]  Michael D. Hunter,et al.  The Role of the Cerebellum in Sub- and Supraliminal Error Correction during Sensorimotor Synchronization: Evidence from fMRI and TMS , 2011, Journal of Cognitive Neuroscience.

[23]  Wolfgang Prinz,et al.  The role of the primary somatosensory cortex in an auditorily paced finger tapping task , 2004, Experimental Brain Research.

[24]  M. Sigman,et al.  Brain Mechanisms of Serial and Parallel Processing during Dual-Task Performance , 2008, The Journal of Neuroscience.

[25]  P. A. Lewis,et al.  Brain activity correlates differentially with increasing temporal complexity of rhythms during initialisation, synchronisation, and continuation phases of paced finger tapping , 2004, Neuropsychologia.

[26]  Bruno H. Repp,et al.  Tapping in Synchrony With a Perturbed Metronome: The Phase Correction Response to Small and Large Phase Shifts as a Function of Tempo , 2011, Journal of motor behavior.

[27]  Mingzhou Ding,et al.  Origins of Timing Errors in Human Sensorimotor Coordination , 2001, Journal of motor behavior.

[28]  Joachim Gross,et al.  Evidence for Anticipatory Motor Control within a Cerebello-Diencephalic-Parietal Network , 2008, Journal of Cognitive Neuroscience.

[29]  Sabine Weiss,et al.  Multivariate tests for the evaluation of high-dimensional EEG data , 2004, Journal of Neuroscience Methods.

[30]  B. Repp,et al.  Sensorimotor synchronization: A review of recent research (2006–2012) , 2013, Psychonomic Bulletin & Review.

[31]  Dirk Vorberg,et al.  Keeping Synchrony While Tempo Changes: Accelerando and Ritardando , 2005 .

[32]  A. Kristofferson,et al.  The timing of interresponse intervals , 1973 .

[33]  J A Michon,et al.  A dynamic model of timing behavior. , 1967, Acta psychologica.

[34]  Jirí Mates,et al.  A model of synchronization of motor acts to a stimulus sequence , 2004, Biological Cybernetics.

[35]  Tzyy-Ping Jung,et al.  Independent Component Analysis of Electroencephalographic Data , 1995, NIPS.

[36]  Thomas F Münte,et al.  Time Course of Error Detection and Correction in Humans: Neurophysiological Evidence , 2002, The Journal of Neuroscience.

[37]  A. Mognon,et al.  ADJUST: An automatic EEG artifact detector based on the joint use of spatial and temporal features. , 2011, Psychophysiology.

[38]  Enzo Tagliazucchi,et al.  Small perturbations in a finger-tapping task reveal inherent nonlinearities of the underlying error correction mechanism. , 2013, Human movement science.

[39]  Bruno H. Repp,et al.  Auditory dominance in temporal processing: new evidence from synchronization with simultaneous visual and auditory sequences. , 2002, Journal of experimental psychology. Human perception and performance.

[40]  Peter E. Keller,et al.  The time course of phase correction: a kinematic investigation of motor adjustment to timing perturbations during sensorimotor synchronization. , 2014, Journal of experimental psychology. Human perception and performance.

[41]  Marco Molinari,et al.  The cerebellum and neural networks for rhythmic sensorimotor synchronization in the human brain , 2008, The Cerebellum.

[42]  Kurt Wiesenfeld,et al.  Neural correlates of the complexity of rhythmic finger tapping , 2003, NeuroImage.

[43]  Mahmood R. Azimi-Sadjadi,et al.  Rhythmic finger tapping to cosine-wave modulated metronome sequences: Evidence of subliminal entrainment , 1998 .

[44]  Hugo Merchant,et al.  Measuring time with different neural chronometers during a synchronization-continuation task , 2011, Proceedings of the National Academy of Sciences.

[45]  Mariano Sigman,et al.  Fixation-related potentials in visual search: a combined EEG and eye tracking study. , 2012, Journal of vision.

[46]  Dirk Vorberg,et al.  Linear phase-correction in synchronization: predictions, parameter estimation, and simulations , 2002 .