The supplementary motor area in motor and perceptual time processing: fMRI studies

The neural bases of timing mechanisms in the second-to-minute range are currently investigated using multidisciplinary approaches. This paper documents the involvement of the supplementary motor area (SMA) in the encoding of target durations by reporting convergent fMRI data from motor and perceptual timing tasks. Event-related fMRI was used in two temporal procedures, involving (1) the production of an accurate interval as compared to an accurate force, and (2) a dual-task of time and colour discrimination with parametric manipulation of the level of attention attributed to each parameter. The first study revealed greater activation of the SMA proper in skilful control of time compared to force. The second showed that increasing attentional allocation to time increased activity in a cortico-striatal network including the pre-SMA (in contrast with the occipital cortex for increasing attention to colour). Further, the SMA proper was sensitive to the attentional modulation cued prior to the time processing period. Taken together, these data and related literature suggest that the SMA plays a key role in time processing as part of the striato-cortical pathway previously identified by animal studies, human neuropsychology and neuroimaging.

[1]  D. Cheyne,et al.  Supplementary motor area activation while tapping bimanually different rhythms in musicians , 2004, Experimental Brain Research.

[2]  Mingxiong Huang,et al.  Neural representation of interval encoding and decision making. , 2004, Brain research. Cognitive brain research.

[3]  L. Jäncke,et al.  Cortical activations in primary and secondary motor areas for complex bimanual movements in professional pianists. , 2000, Brain research. Cognitive brain research.

[4]  R. Miall,et al.  Distinct systems for automatic and cognitively controlled time measurement: evidence from neuroimaging , 2003, Current Opinion in Neurobiology.

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

[6]  R. Miall,et al.  Brain activation patterns during measurement of sub- and supra-second intervals , 2003, Neuropsychologia.

[7]  P. Strick,et al.  Motor areas of the medial wall: a review of their location and functional activation. , 1996, Cerebral cortex.

[8]  J Sergent,et al.  Distributed neural network underlying musical sight-reading and keyboard performance. , 1992, Science.

[9]  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.

[10]  Katya Rubia,et al.  A right hemispheric frontocerebellar network for time discrimination of several hundreds of milliseconds , 2003, NeuroImage.

[11]  J. A. S. Kelso,et al.  Practice-dependent modulation of neural activity during human sensorimotor coordination: a functional Magnetic Resonance Imaging study , 2002, Neuroscience Letters.

[12]  Franck Vidal,et al.  Timing functions of the supplementary motor area: an event-related fMRI study. , 2004, Brain research. Cognitive brain research.

[13]  F. Vidal,et al.  Functional Anatomy of the Attentional Modulation of Time Estimation , 2004, Science.

[14]  Karl J. Friston,et al.  A direct demonstration of functional specialization in human visual cortex , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  W. Meck.  Neuropharmacology of timing and time perception. , 1996, Brain research. Cognitive brain research.

[16]  F. Vidal,et al.  Event-Related Potentials as Indices of Time Processing: A Review , 2004 .

[17]  F. Macar,et al.  Effects of attention manipulation on judgments of duration and of intensity in the visual modality , 1997, Memory & cognition.

[18]  Scott W. Brown.  Attentional resources in timing: Interference effects in concurrent temporal and nontemporal working memory tasks , 1997, Perception & psychophysics.

[19]  Andrew Simmons,et al.  Prefrontal involvement in temporal bridging and timing movement , 1998, Neuropsychologia.

[20]  Wolfgang Grodd,et al.  Discrimination of temporal information at the cerebellum: functional magnetic resonance imaging of nonverbal auditory memory , 2004, NeuroImage.

[21]  Fred L. Steinberg,et al.  Cortical and subcortical networks underlying syncopated and synchronized coordination revealed using fMRI , 2002 .

[22]  Ewart A. C. Thomas,et al.  Cognitive processing and time perception , 1975 .

[23]  Stephen M. Rao,et al.  The evolution of brain activation during temporal processing , 2001, Nature Neuroscience.

[24]  F. Macar,et al.  Controlled attention sharing influences time estimation , 1994, Memory & cognition.

[25]  M. Bianciardi,et al.  Visually cued motor synchronization: modulation of fMRI activation patterns by baseline condition , 2004, Neuroscience Letters.

[26]  Dan Zakay,et al.  Chapter 10 Subjective Time and Attentional Resource Allocation: An Integrated Model of Time Estimation , 1989 .

[27]  R. Turner,et al.  Event-Related fMRI: Characterizing Differential Responses , 1998, NeuroImage.

[28]  R. Passingham,et al.  Relation between cerebral activity and force in the motor areas of the human brain. , 1995, Journal of neurophysiology.

[29]  Masaya Hirashima,et al.  Selective activation and deactivation of the human brain structures between speeded and precisely timed tapping responses to identical visual stimulus: an fMRI study , 2004, NeuroImage.

[30]  Stephen M. Rao,et al.  Neural basis for impaired time reproduction in Parkinson's disease: An fMRI study , 2003, Journal of the International Neuropsychological Society.

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

[32]  Hans Forssberg,et al.  Human brain activity in the control of fine static precision grip forces: an fMRI study , 2001, The European journal of neuroscience.

[33]  C. Gallistel,et al.  Toward a neurobiology of temporal cognition: advances and challenges , 1997, Current Opinion in Neurobiology.

[34]  Jordan Grafman,et al.  Distributed neural systems for temporal production: A functional MRI study , 2003, Brain Research Bulletin.

[35]  Hermann Ackermann,et al.  Cerebellar Contributions to the Perception of Temporal Cues within the Speech and Nonspeech Domain , 1999, Brain and Language.

[36]  P. Cavanagh,et al.  Retinotopy and color sensitivity in human visual cortical area V8 , 1998, Nature Neuroscience.

[37]  D. Harrington,et al.  Neural Underpinnings of Temporal Processing: Α Review of Focal Lesion, Pharmacological, and Functional Imaging Research , 1999, Reviews in the neurosciences.

[38]  J. Tanji.  The supplementary motor area in the cerebral cortex , 1994, Neuroscience Research.

[39]  R. Kawashima,et al.  Human cerebellum plays an important role in memory-timed finger movement: an fMRI study. , 2000, Journal of neurophysiology.

[40]  R. Ivry,et al.  The neural representation of time , 2004, Current Opinion in Neurobiology.

[41]  Karl J. Friston,et al.  Event-related fMRI , 1997 .

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

[43]  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.

[44]  Warren H Meck,et al.  Frontal-striatal circuitry activated by human peak-interval timing in the supra-seconds range. , 2004, Brain research. Cognitive brain research.

[45]  Jeffrey R Binder,et al.  Neural systems supporting timing and chronometric counting: an FMRI study. , 2004, Brain research. Cognitive brain research.

[46]  G. Meinhardt,et al.  Attentional control in learning to discriminate bars and gratings , 2002, Experimental Brain Research.

[47]  J. Coull.  fMRI studies of temporal attention: allocating attention within, or towards, time. , 2004, Brain research. Cognitive brain research.