Activation of the supplementary motor area and of attentional networks during temporal processing

Abstract. This paper first provides a survey of the expanding brain imaging literature in the field of time processing, showing that particular task features (discrete vs rhythmic, perceptual vs motor) do not significantly affect the basic pattern of activation observed. Next, positron emission tomography (PET) data obtained in a timing task (temporal reproduction) with two distinct duration ranges (2.2–3.2 and 9–13 s) are reported. The stimuli consisted of vibrations applied to the subject's right middle finger. When the vibration ended, the subject estimated an interval identical to its length before pressing a response button. The control task used cued responses with comparable intervals and stimuli. The pattern of activation obtained in the timing task as compared to control mainly included areas having attentional functions (the right dorsolateral prefrontal, inferior parietal, and anterior cingulate cortices), and the supplementary motor area (SMA). No significant difference was seen as a function of the duration range. It is argued, firstly, that involvement of the attentional areas derives from specific relations between attention and the temporal accumulator, as described by dominant timing models; and, secondly, that the SMA, or more probably one of its subregions, subserves time processing.

[1]  Gerald Westheimer,et al.  Discrimination of short time intervals by the human observer , 1999, Experimental Brain Research.

[2]  The neuropsychology of human temporal information processing , 1993 .

[3]  M. Jüptner,et al.  Localization of a cerebellar timing process using PET , 1995, Neurology.

[4]  A. Nobre,et al.  Where and When to Pay Attention: The Neural Systems for Directing Attention to Spatial Locations and to Time Intervals as Revealed by Both PET and fMRI , 1998, The Journal of Neuroscience.

[5]  R. Kawashima,et al.  A positron emission tomography study of self-paced finger movements at different frequencies , 1999, Neuroscience.

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

[7]  R Ivry,et al.  Cerebellar Involvement in the Explicit Representation of Temporal Information a , 1993, Annals of the New York Academy of Sciences.

[8]  J. Gibbon,et al.  Timing and time perception. , 1984, Annals of the New York Academy of Sciences.

[9]  Françoise Macar,et al.  Prefrontal slow potential in temporal compared to nontemporal tasks. , 1996 .

[10]  H. Lejeune Switching or gating? The attentional challenge in cognitive models of psychological time , 1998, Behavioural Processes.

[11]  Jordan Grafman,et al.  Perceptual timing in cerebellar degeneration , 1996, Neuropsychologia.

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

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

[14]  Françoise Macar,et al.  Relation Between Level of Prefrontal Activity and Subject's Performance , 1999 .

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

[16]  M. Pinsk,et al.  Functional Localization of a “Time Keeper” Function Separate from Attentional Resources and Task Strategy , 2000, NeuroImage.

[17]  M. Himmelbach,et al.  A parametric analysis of the `rate effect' in the sensorimotor cortex: a functional magnetic resonance imaging analysis in human subjects , 1998, Neuroscience Letters.

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

[19]  Franck Vidal,et al.  The supplementary motor area in motor and sensory timing: evidence from slow brain potential changes , 1999, Experimental Brain Research.

[20]  R. Knight,et al.  Cortical Networks Underlying Mechanisms of Time Perception , 1998, The Journal of Neuroscience.

[21]  J. Mazziotta,et al.  Brain Activation Induced by Estimation of Duration: A PET Study , 1996, NeuroImage.

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

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

[24]  A. Ferrandez,et al.  ERPs and PET analysis of time perception: Spatial and temporal brain mapping during visual discrimination tasks , 2000, Human brain mapping.

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

[26]  Karl J. Friston Imaging cognitive anatomy , 1997, Trends in Cognitive Sciences.

[27]  M. Raichle,et al.  Localization of a human system for sustained attention by positron emission tomography , 1991, Nature.

[28]  J. Gibbon,et al.  Coupled Temporal Memories in Parkinson's Disease: A Dopamine-Related Dysfunction , 1998, Journal of Cognitive Neuroscience.

[29]  G. Rizzolatti,et al.  The organization of the cortical motor system: new concepts. , 1998, Electroencephalography and clinical neurophysiology.

[30]  Doreen Kimura,et al.  Neuromotor mechanisms in human communication , 1993 .

[31]  T. Rammsayer,et al.  Impaired temporal discrimination in Parkinson's disease: temporal processing of brief durations as an indicator of degeneration of dopaminergic neurons in the basal ganglia. , 1997, The International journal of neuroscience.

[32]  Nancy Byl,et al.  Practice-Related Improvements in Somatosensory Interval Discrimination Are Temporally Specific But Generalize across Skin Location, Hemisphere, and Modality , 1998, The Journal of Neuroscience.

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

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

[35]  Karl J. Friston,et al.  Human Brain Function , 1997 .

[36]  J. Jonides,et al.  Storage and executive processes in the frontal lobes. , 1999, Science.

[37]  P. Roland,et al.  Bilateral activation of fronto-parietal networks by incrementing demand in a working memory task. , 1997, Cerebral cortex.

[38]  M. Posner,et al.  The attention system of the human brain. , 1990, Annual review of neuroscience.

[39]  U. Jürgens,et al.  The efferent and afferent connections of the supplementary motor area , 1984, Brain Research.

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

[41]  D. Harrington,et al.  Temporal processing in the basal ganglia. , 1998, Neuropsychology.

[42]  Franck Vidal,et al.  Programming the duration of a motor sequence: role of the primary and supplementary motor areas in man , 2004, Experimental Brain Research.

[43]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[44]  A. Friederici,et al.  Time Perception and Motor Timing: A Common Cortical and Subcortical Basis Revealed by fMRI , 2000, NeuroImage.

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

[46]  F. Binkofski,et al.  Cerebral correlates of working memory for temporal information , 2000, NeuroReport.

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

[48]  K. Leibovic Information Processing in The Nervous System , 1969, Springer Berlin Heidelberg.

[49]  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.

[50]  Karl J. Friston,et al.  Willed action and the prefrontal cortex in man: a study with PET , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[51]  J A Obeso,et al.  The anatomical basis of somaesthetic temporal discrimination in humans. , 1991, Journal of neurology, neurosurgery, and psychiatry.

[52]  R M Church,et al.  Scalar Timing in Memory , 1984, Annals of the New York Academy of Sciences.

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

[54]  J A Obeso,et al.  Temporal discrimination is abnormal in Parkinson's disease. , 1992, Brain : a journal of neurology.

[55]  R M Church,et al.  Properties of the Internal Clock a , 1984, Annals of the New York Academy of Sciences.

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

[57]  D. Brooks,et al.  Motor sequence learning: a study with positron emission tomography , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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