Transient increases of synchronized neural activity during movement preparation: influence of cognitive constraints

The ability to prepare movement is an essential requirement for the control of goal-directed actions. It allows us to respond in an adaptable and swift manner to environmental conditions. In the present study, we manipulate cognitive context, by means of response probability, to modify the degree of movement preparation in a delayed cueing task performed with the right hand, and evaluate the neural dynamics (EEG coherence) and behavioural output (reaction time). Task-related coherence was stronger over the contralateral hemisphere. In particular, coherence between the left sensorimotor area and frontal (C3-F3, C3-FC3) and parietal (C3-P3) regions was increased during right-hand movement preparation as compared to rest in the alpha frequency band (8–12 Hz). Reducing response probability diminished the degree of functional coupling between C3-F3 and C3-FC3, and was associated with a prolonged reaction time. These findings suggest an association between neural dynamics and behavioural performance and emphasize that response predictability biases information processing in goal-oriented behaviour.

[1]  G. Pfurtscheller,et al.  Do changes in coherence always reflect changes in functional coupling? , 1998, Electroencephalography and clinical neurophysiology.

[2]  K. Zilles,et al.  Differential Involvement of Parietal and Precentral Regions in Movement Preparation and Motor Intention , 2002, The Journal of Neuroscience.

[3]  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.

[4]  P. Nunez.  Toward a quantitative description of large-scale neocortical dynamic function and EEG , 2000, Behavioral and Brain Sciences.

[5]  T. Braver,et al.  Sensitivity of prefrontal cortex to changes in target probability: A functional MRI study , 2001, Human brain mapping.

[6]  柴田 忠彦.  The synchronization between brain areas under motor inhibition process in humans estimated by event-related EEG coherence , 1999 .

[7]  Jorge Bosch-Bayard,et al.  Wisconsin card sorting test synchronizes the prefrontal, temporal and posterior association cortex in different frequency ranges and extensions , 2002, Human brain mapping.

[8]  P. Matthews,et al.  Neurophysiological approaches to higher brain functions E. V. Evarts, Y. Shinoda and S. P. Wise. Wiley and Sons, New York (1984). 198 pp., cloth £40.90 , 1986, Neuroscience.

[9]  R. C. Oldfield.  THE ASSESSMENT AND ANALYSIS OF HANDEDNESS , 1971 .

[10]  H. Steinmetz,et al.  Craniocerebral topography within the international 10-20 system. , 1989, Electroencephalography and clinical neurophysiology.

[11]  R. Homan,et al.  Cerebral location of international 10-20 system electrode placement. , 1987, Electroencephalography and clinical neurophysiology.

[12]  S. Bressler.  Large-scale cortical networks and cognition , 1995, Brain Research Reviews.

[13]  T. Mima,et al.  Increased Synchronization of Cortical Oscillatory Activities between Human Supplementary Motor and Primary Sensorimotor Areas during Voluntary Movements , 2001, The Journal of Neuroscience.

[14]  P. Brown,et al.  The importance of the dominant hemisphere in the organization of bimanual movements , 2003, Human brain mapping.

[15]  R A Andersen,et al.  Multimodal integration for the representation of space in the posterior parietal cortex. , 1997, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

[17]  M. Hallett,et al.  Cerebral structures participating in motor preparation in humans: a positron emission tomography study. , 1996, Journal of neurophysiology.

[18]  R. Thatcher,et al.  Tomographic Electroencephalography/Magnetoencephalography , 1995, Journal of neuroimaging : official journal of the American Society of Neuroimaging.

[19]  E. Miller,et al.  The prefontral cortex and cognitive control , 2000, Nature Reviews Neuroscience.

[20]  P. König,et al.  Top-down processing mediated by interareal synchronization. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[21]  G. Pfurtscheller,et al.  Event-related synchronization (ERS) in the alpha band--an electrophysiological correlate of cortical idling: a review. , 1996, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[22]  W Singer,et al.  Coherence as an organizing principle of cortical functions. , 1994, International review of neurobiology.

[23]  C. Schreiner,et al.  Low-frequency oscillations of visual, auditory and somatosensory cortical neurons evoked by sensory stimulation. , 1997, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[24]  G Yan,et al.  The temporal and spatial features of event-related EEG spectral changes in 4 mental conditions. , 1998, Electroencephalography and clinical neurophysiology.

[25]  J. Fuster.  Frontal lobes , 1993, Current Opinion in Neurobiology.

[26]  Apostolos P Georgopoulos,et al.  Neural aspects of cognitive motor control , 2000, Current Opinion in Neurobiology.

[27]  A S Gevins,et al.  Human neuroelectric patterns predict performance accuracy. , 1987, Science.

[28]  W Singer,et al.  Consciousness and the structure of neuronal representations. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[29]  E. Miller,et al.  THE PREFRONTAL CORTEX AND COGNITIVE CONTROL , 2000 .

[30]  K Friston,et al.  Signal-, set- and movement-related activity in the human brain: an event-related fMRI study. , 1999, Cerebral cortex.

[31]  Konrad P. Körding,et al.  Integrating Top-Down and Bottom-Up Sensory Processing by Somato-Dendritic Interactions , 2004, Journal of Computational Neuroscience.

[32]  W. Klimesch,et al.  Alpha frequency, reaction time, and the speed of processing information. , 1996, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[33]  W. Singer.  Synchronization of cortical activity and its putative role in information processing and learning. , 1993, Annual review of physiology.

[34]  R. Passingham,et al.  Signal-, set-, and movement-related activity in the human premotor cortex , 1998, Neuropsychologia.

[35]  J. Fuster,et al.  From perception to action: temporal integrative functions of prefrontal and parietal neurons. , 1999, Cerebral cortex.

[36]  E. Basar,et al.  Are cognitive processes manifested in event-related gamma, alpha, theta and delta oscillations in the EEG? , 1999, Neuroscience Letters.

[37]  Carlos M. Gómez,et al.  Alpha EEG coherence in different brain states: an electrophysiological index of the arousal level in human subjects , 1999, Neuroscience Letters.

[38]  S. Bressler,et al.  Synchronized activity in prefrontal cortex during anticipation of visuomotor processing , 2002, Neuroreport.

[39]  L. Goldstein.  The frontal lobes and voluntary action , 1996 .

[40]  W. Ray,et al.  EEG alpha activity reflects attentional demands, and beta activity reflects emotional and cognitive processes. , 1985, Science.

[41]  W. Klimesch.  Memory processes, brain oscillations and EEG synchronization. , 1996, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[42]  I..  THE ATTENTION SYSTEM OF THE HUMAN BRAIN , 2002 .

[43]  W. Klimesch.  EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis , 1999, Brain Research Reviews.

[44]  W Singer,et al.  Visual feature integration and the temporal correlation hypothesis. , 1995, Annual review of neuroscience.

[45]  Ravi S. Menon,et al.  Human fMRI evidence for the neural correlates of preparatory set , 2002, Nature Neuroscience.