Spatiotemporal reorganization of electrical activity in the human brain associated with a timing transition

Abstract We used a 61-channel electrode array to investigate the spatiotemporal dynamics of electroencephalographic (EEG) activity related to behavioral transitions in rhythmic sensorimotor coordination. Subjects were instructed to maintain a 1:1 relationship between repeated right index finger flexion and a series of periodically delivered tones (metronome) in a syncopated (anti-phase) fashion. Systematic increases in stimulus presentation rate are known to induce a spontaneous switch in behavior from syncopation to synchronization (in-phase coordination). We show that this transition is accompanied by a large-scale reorganization of cortical activity manifested in the spatial distributions of EEG power at the coordination frequency. Significant decreases in power were observed at electrode locations over left central and anterior parietal areas, most likely reflecting reduced activation of left primary sensorimotor cortex. A second condition in which subjects were instructed to synchronize with the metronome controlled for the effects of movement frequency, since synchronization is known to remain stable across a wide range of frequencies. Different, smaller spatial differences were observed between topographic patterns associated with synchronization at low versus high stimulus rates. Our results demonstrate qualitative changes in the spatial dynamics of human brain electrical activity associated with a transition in the timing of sensorimotor coordination and suggest that maintenance of a more difficult anti-phase timing relation is associated with greater activation of primary sensorimotor areas.

[1]  R. Kirk Experimental Design: Procedures for the Behavioral Sciences , 1970 .

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

[3]  K. Steinmüller HAKEN, H.: Synergetics. An Introduction. Springer‐Verlag, Berlin‐Heidelberg‐New York 1977. XII, 325 S., 125 Abb., DM 72.—. , 1978 .

[4]  R. Hari,et al.  Interstimulus interval dependence of the auditory vertex response and its magnetic counterpart: implications for their neural generation. , 1982, Electroencephalography and clinical neurophysiology.

[5]  J. Kelso Phase transitions and critical behavior in human bimanual coordination. , 1984, The American journal of physiology.

[6]  R. Shaw,et al.  Persistence and Change : Proceedings of the First International Conference on Event Perception , 1985 .

[7]  M A Arbib,et al.  Schemas for the temporal organization of behaviour. , 1985, Human neurobiology.

[8]  J. Kelso,et al.  Dynamics governs switching among patterns of coordination in biological movement , 1988 .

[9]  S. Keele,et al.  Timing Functions of The Cerebellum , 1989, Journal of Cognitive Neuroscience.

[10]  J. Kelso,et al.  Intentional switching between patterns of bimanual coordination depends on the intrinsic dynamics of the patterns. , 1990, Journal of motor behavior.

[11]  R. H. Wimmers,et al.  Phase transitions in rhythmic tracking movements: A case of unilateral coupling , 1992 .

[12]  H. Haken,et al.  PHASE TRANSITIONS IN THE HUMAN BRAIN: SPATIAL MODE DYNAMICS , 1992 .

[13]  A. Fuchs,et al.  A phase transition in human brain and behavior , 1992 .

[14]  M. Honda,et al.  Both primary motor cortex and supplementary motor area play an important role in complex finger movement. , 1993, Brain : a journal of neurology.

[15]  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.

[16]  H Shibasaki,et al.  Enhanced negative slope of cortical potentials before sequential as compared with simultaneous extensions of two fingers. , 1993, Electroencephalography and clinical neurophysiology.

[17]  P A Bandettini,et al.  Effects of stimulus rate on signal response during functional magnetic resonance imaging of auditory cortex. , 1994, Brain research. Cognitive brain research.

[18]  J. Kelso,et al.  The informational character of self-organized coordination dynamics , 1994 .

[19]  J. Kelso,et al.  Phase transitions in spatiotemporal patterns of brain activity and behavior , 1995 .

[20]  Pierre-Alain Joseph,et al.  Movement disturbances following frontal lobe lesions: qualitative analysis of gesture and motor programming , 1995 .

[21]  B. Gulyás,et al.  Cortical representation of self‐paced finger movement , 1996, Neuroreport.

[22]  M. Hallett,et al.  Complexity affects regional cerebral blood flow change during sequential finger movements , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  P A Bandettini,et al.  Relationship between Finger Movement Rate and Functional Magnetic Resonance Signal Change in Human Primary Motor Cortex , 1996, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[24]  M Hallett,et al.  Stimulation over the human supplementary motor area interferes with the organization of future elements in complex motor sequences. , 1997, Brain : a journal of neurology.

[25]  R. Passingham,et al.  The effect of movement frequency on cerebral activation: a positron emission tomography study , 1997, Journal of the Neurological Sciences.

[26]  M. Hallett,et al.  Involvement of the ipsilateral motor cortex in finger movements of different complexities , 1997, Annals of neurology.

[27]  J. Binder,et al.  Distributed Neural Systems Underlying the Timing of Movements , 1997, The Journal of Neuroscience.

[28]  M. Hallett,et al.  Frequency-Dependent Changes of Regional Cerebral Blood Flow during Finger Movements: Functional MRI Compared to PET , 1997, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[29]  Deborah L. Harrington,et al.  Sequencing and timing operations of the basal ganglia. , 1998 .

[30]  M. Hallett,et al.  The functional neuroanatomy of simple and complex sequential finger movements: a PET study. , 1998, Brain : a journal of neurology.

[31]  D. Rosenbaum,et al.  Timing of behavior : neural, psychological, and computational perspectives , 1998 .

[32]  Karl J. Friston,et al.  Role of the human rostral supplementary motor area and the basal ganglia in motor sequence control: investigations with H2 15O PET. , 1998, Journal of neurophysiology.

[33]  A. E. Schulman,et al.  Functional coupling and regional activation of human cortical motor areas during simple, internally paced and externally paced finger movements. , 1998, Brain : a journal of neurology.

[34]  Pier-Giorgio Zanone,et al.  Attentional load associated with performing and stabilizing preferred bimanual patterns , 1999 .

[35]  J. Kelso,et al.  Action-Perception as a Pattern Formation Process , 2018, Attention and Performance XIII.