Neural Control of Rhythmic Sequences

Abstract: We investigated whether the temporal structure of movement sequences can be represented and learned independently of their ordinal structure, and whether some brain regions are particularly important for temporal sequence performance. Using a learning transfer design, we found evidence for independent temporal representations: learning a spatiotemporal sequence facilitated learning its temporal and ordinal structure alone; learning a temporal and an ordinal structure facilitated learning of a sequence where the two were coupled. Second, learning of temporal structures was found during reproduction of sequential stimuli with random ordinal structure, suggesting independent mechanisms for temporal learning. We then used functional magnetic resonance imaging to investigate the neural control of sequences during well‐learned performance. The temporal and ordinal structures of the sequences were varied in a 2 × 2 factorial design. A dissociation was found between brain regions involved in ordinal and temporal control, the latter mainly involving the presupplementary motor area, the inferior frontal gyrus and precentral sulcus, and the superior temporal gyri. Finally, in a second fMRI experiment, well‐learned temporal sequences were performed with the left or right index fingers, or using rhythmic speech. The overlap in brain activity during performance with the different effectors included a similar set of brain regions as that found in the first fMRI experiment: the supplementary motor area (SMA), the superior temporal gyrus, and the inferior frontal cortex. We thus suggest that this set of regions is important for abstract, movement‐independent, temporal sequence control. This organization may be important for increased flexibility in voluntarily timed motor tasks.

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

[2]  R. Turner,et al.  Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

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

[4]  Hans Forssberg,et al.  Dissociating brain regions controlling the temporal and ordinal structure of learned movement sequences , 2004, The European journal of neuroscience.

[5]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[6]  L. Shaffer 26 Analysing Piano Performance: A Study of Concert Pianists , 1980 .

[7]  D. Lee Learning of spatial and temporal patterns in sequential hand movements. , 2000, Brain research. Cognitive brain research.

[8]  Katsuyuki Sakai,et al.  Learning of sequences of finger movements and timing: frontal lobe and action-oriented representation. , 2002, Journal of neurophysiology.

[9]  H. Forssberg,et al.  Neural networks for the coordination of the hands in time. , 2003, Journal of neurophysiology.

[10]  J. Tanji,et al.  The role of premotor cortex and the supplementary motor area in the temporal control of movement in man. , 1993, Brain : a journal of neurology.

[11]  M. Nissen,et al.  Attentional requirements of learning: Evidence from performance measures , 1987, Cognitive Psychology.

[12]  Guido Nolte,et al.  Shared Brain Areas But Not Functional Connections Controlling Movement Timing and Order , 2005, The Journal of Neuroscience.

[13]  D. V. von Cramon,et al.  Interval and ordinal properties of sequences are associated with distinct premotor areas. , 2001, Cerebral cortex.

[14]  Fredrik Ullén,et al.  Independent processing of the temporal and ordinal structure of movement sequences. , 2003, Journal of neurophysiology.

[15]  Fredrik Ullén,et al.  Dissociation between melodic and rhythmic processing during piano performance from musical scores , 2006, NeuroImage.

[16]  Alan C. Evans,et al.  Cerebellar Contributions to Motor Timing: A PET Study of Auditory and Visual Rhythm Reproduction , 1998, Journal of Cognitive Neuroscience.

[17]  N. Logothetis The neural basis of the blood-oxygen-level-dependent functional magnetic resonance imaging signal. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[18]  Jesper Andersson,et al.  Valid conjunction inference with the minimum statistic , 2005, NeuroImage.

[19]  Fred L. Steinberg,et al.  Functional MRI reveals the existence of modality and coordination-dependent timing networks , 2005, NeuroImage.

[20]  Robert J Zatorre,et al.  Tapping in Synchrony to Auditory Rhythms , 2005, Annals of the New York Academy of Sciences.

[21]  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.

[22]  G. Stelmach,et al.  Tutorials in Motor Behavior , 1980 .

[23]  Fred L. Steinberg,et al.  Brain networks underlying human timing behavior are influenced by prior context. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[24]  Richard B Ivry,et al.  Concurrent learning of temporal and spatial sequences. , 2002, Journal of experimental psychology. Learning, memory, and cognition.

[25]  F. Vidal,et al.  Activation of the supplementary motor area and of attentional networks during temporal processing , 2002, Experimental Brain Research.

[26]  O Hikosaka,et al.  Neural Representation of a Rhythm Depends on Its Interval Ratio , 1999, The Journal of Neuroscience.

[27]  R. E. Passingham,et al.  Changes in the Human Brain during Rhythm Learning , 2001, Journal of Cognitive Neuroscience.

[28]  M. Mon-Williams,et al.  Motor Control and Learning , 2006 .

[29]  Ravi S. Menon,et al.  Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[30]  J. Doyon,et al.  Dynamic Cortical and Subcortical Networks in Learning and Delayed Recall of Timed Motor Sequences , 2002, The Journal of Neuroscience.

[31]  P. Viviani,et al.  32 Space-Time Invariance in Learned Motor Skills , 1980 .