Selective activation and deactivation of the human brain structures between speeded and precisely timed tapping responses to identical visual stimulus: an fMRI study

We investigated the difference between brain activities in speeded and precisely timed responses to identical visual stimulus using fMRI. Stimulus used was a row of seven light-emitting diodes (LEDs) lightened up one after another with constant speed within a trial but with various speeds between trials. Subjects were asked to execute finger-thumb tapping with the right hand in response to the onset of the first LED light in the reaction time (RT) task and in anticipation of the onset of the last (i.e., seventh) LED light in the timing task. In control condition, they were asked to passively view the stimulus without motor response. Results showed that various movement-related areas including contralateral cingulate motor cortex were commonly activated for both tasks relative to the control condition, suggesting these structures are involved in general perception and response execution rather than specific function for speeded or precisely timed responses. In the RT task, the presupplementary motor area extending to the cingulate sulcus was activated more strongly than in the timing task probably to focus attention to the onset of the first LED light unpredictably presented after random foreperiods. The lateral occipital area extending to the temporo-parieto-occipital junction was activated more strongly in the timing task than in the RT task; the same area was deactivated in the RT task relative to the control condition. Auditory-related areas were also deactivated in the both tasks. This inter- and intramodal task-specific modification including deactivation underscores significance of the context for perception and action and can have an important role in dexterous or skilled performance.

[1]  Skyler Dean,et al.  Mind's Eye , 1973 .

[2]  D. Heeger,et al.  Task-related modulation of visual cortex. , 2000, Journal of neurophysiology.

[3]  Richard S. J. Frackowiak,et al.  Area V5 of the human brain: evidence from a combined study using positron emission tomography and magnetic resonance imaging. , 1993, Cerebral cortex.

[4]  S. P. Wise,et al.  Premotor cortex of rhesus monkeys: set-related activity during two conditional motor tasks , 2004, Experimental Brain Research.

[5]  J Tanji,et al.  Role for cells in the presupplementary motor area in updating motor plans. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[6]  M. Corbetta,et al.  Selective and divided attention during visual discriminations of shape, color, and speed: functional anatomy by positron emission tomography , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  J. Hennig,et al.  The Processing of First- and Second-Order Motion in Human Visual Cortex Assessed by Functional Magnetic Resonance Imaging (fMRI) , 1998, The Journal of Neuroscience.

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

[9]  N. A. Bernstein Dexterity and Its Development , 1996 .

[10]  M Corbetta,et al.  Attentional modulation of neural processing of shape, color, and velocity in humans. , 1990, Science.

[11]  R. Duncan Luce,et al.  Response Times: Their Role in Inferring Elementary Mental Organization , 1986 .

[12]  J. Tanji,et al.  Anticipatory activity of motor cortex neurons in relation to direction of an intended movement. , 1976, Journal of neurophysiology.

[13]  L. Jäncke,et al.  Tapping movements according to regular and irregular visual timing signals investigated with fMRI , 2000, Neuroreport.

[14]  D. V. Cramon,et al.  Subprocesses of Performance Monitoring: A Dissociation of Error Processing and Response Competition Revealed by Event-Related fMRI and ERPs , 2001, NeuroImage.

[15]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[16]  T. Paus Location and function of the human frontal eye-field: A selective review , 1996, Neuropsychologia.

[17]  Jun Tanji,et al.  New concepts of the supplementary motor area , 1996, Current Opinion in Neurobiology.

[18]  W. Meck,et al.  Neuropsychological mechanisms of interval timing behavior. , 2000, BioEssays : news and reviews in molecular, cellular and developmental biology.

[19]  K. Zilles,et al.  Functions and structures of the motor cortices in humans , 1996, Current Opinion in Neurobiology.

[20]  G. Orban,et al.  Attention to Speed of Motion, Speed Discrimination, and Task Difficulty: An fMRI Study , 2000, NeuroImage.

[21]  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 .

[22]  D. Levy,et al.  Differences in cerebral activation during smooth pursuit and saccadic eye movements using positron-emission tomography , 1998, Biological Psychiatry.

[23]  K. Sasaki,et al.  Cortical field potentials preceding visually initiated hand movements and cerebellar actions in the monkey , 2004, Experimental Brain Research.

[24]  J V Haxby,et al.  Dissociation of saccade-related and pursuit-related activation in human frontal eye fields as revealed by fMRI. , 1997, Journal of neurophysiology.

[25]  Dan Milea,et al.  Intraoperative frontal eye field stimulation elicits ocular deviation and saccade suppression , 2002, Neuroreport.

[26]  R B Ivry,et al.  Dissociable contributions of the prefrontal and neocerebellar cortex to time perception. , 1998, Brain research. Cognitive brain research.

[27]  R. Kawashima,et al.  Selective Visual and Auditory Attention Toward Utterances—A PET Study , 1999, NeuroImage.

[28]  Pascal Boyer,et al.  How the brain perceives causality: an event-related fMRI study , 2001, Neuroreport.

[29]  S. Keele,et al.  Dissociation of the lateral and medial cerebellum in movement timing and movement execution , 2004, Experimental Brain Research.

[30]  W. Eddy,et al.  Pursuit and saccadic eye movement subregions in human frontal eye field: a high-resolution fMRI investigation. , 2002, Cerebral cortex.

[31]  G. Krüger,et al.  MRI of Functional Deactivation: Temporal and Spatial Characteristics of Oxygenation-Sensitive Responses in Human Visual Cortex , 1999, NeuroImage.

[32]  O. Hikosaka,et al.  What and When: Parallel and Convergent Processing in Motor Control , 2000, The Journal of Neuroscience.

[33]  C. Koch,et al.  Brain Areas Specific for Attentional Load in a Motion-Tracking Task , 2001, Journal of Cognitive Neuroscience.

[34]  G. Mangun,et al.  The neural mechanisms of top-down attentional control , 2000, Nature Neuroscience.

[35]  R Kawashima,et al.  Positron-emission tomography studies of cross-modality inhibition in selective attentional tasks: closing the "mind's eye". , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[36]  Leslie G. Ungerleider,et al.  Sustained Activity in the Medial Wall during Working Memory Delays , 1998, The Journal of Neuroscience.

[37]  E V Evarts,et al.  Reaction time in Parkinson's disease. , 1981, Brain : a journal of neurology.

[38]  C H Shea,et al.  Effects of extended practice and movement time on motor control of a coincident timing task. , 1980, Research quarterly for exercise and sport.

[39]  Patrick Dupont,et al.  Human brain activity related to speed discrimination tasks , 1998, Experimental Brain Research.

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

[41]  J C Mazziotta,et al.  Tomographic mapping of human cerebral metabolism: Sensory deprivation , 1982, Annals of neurology.

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

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

[44]  Timothy D. Lee,et al.  Motor Control and Learning: A Behavioral Emphasis , 1982 .

[45]  E. DeYoe,et al.  Mapping striate and extrastriate visual areas in human cerebral cortex. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[46]  John H. R. Maunsell,et al.  Visual processing in monkey extrastriate cortex. , 1987, Annual review of neuroscience.

[47]  P. Cavanagh,et al.  Cortical fMRI activation produced by attentive tracking of moving targets. , 1998, Journal of neurophysiology.

[48]  John H. R. Maunsell,et al.  Attentional modulation of visual motion processing in cortical areas MT and MST , 1996, Nature.

[49]  G. Orban,et al.  Motion-responsive regions of the human brain , 1999, Experimental Brain Research.

[50]  J R Tresilian,et al.  Analysis of recent empirical challenges to an account of interceptive timing , 1999, Perception & psychophysics.

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

[52]  C. N. Guy,et al.  The parallel visual motion inputs into areas V1 and V5 of human cerebral cortex. , 1995, Brain : a journal of neurology.

[53]  Alan C. Evans,et al.  Role of the human anterior cingulate cortex in the control of oculomotor, manual, and speech responses: a positron emission tomography study. , 1993, Journal of neurophysiology.

[54]  James R. Tresilian,et al.  Perceptual and motor processes in interceptive timing , 1994 .

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

[56]  K. Kudo,et al.  Functional modification of agonist-antagonist electromyographic activity for rapid movement inhibition , 1998, Experimental Brain Research.

[57]  K. Wessel,et al.  Somatotopic motor representation in the human anterior cerebellum. A high-resolution functional MRI study. , 1996, Brain : a journal of neurology.

[58]  R. Turner,et al.  Functional magnetic resonance imaging of the human brain: data acquisition and analysis , 1998, Experimental Brain Research.

[59]  Umberto Castiello,et al.  Posterior parietal cortex control of reach‐to‐grasp movements in humans , 2002, The European journal of neuroscience.

[60]  Richard S. J. Frackowiak,et al.  Cortical control of saccades and fixation in man. A PET study. , 1994, Brain : a journal of neurology.

[61]  Y. Yen,et al.  Deactivation of Sensory-Specific Cortex by Cross-Modal Stimuli , 2002, Journal of Cognitive Neuroscience.

[62]  M. Mintun,et al.  Positron emission tomography study of voluntary saccadic eye movements and spatial working memory. , 1996, Journal of neurophysiology.

[63]  P. Beitel,et al.  Stimulus Velocity and Movement Distance as Determiners of Movement Velocity and Coincident Timing Accuracy , 1982, Human factors.

[64]  K. Meador,et al.  Functional MRI cerebral activation and deactivation during finger movement , 2000, Neurology.

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

[66]  D. Heeger,et al.  Spatial attention affects brain activity in human primary visual cortex. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[67]  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.

[68]  Karl J. Friston,et al.  A direct quantitative relationship between the functional properties of human and macaque V5 , 2000, Nature Neuroscience.

[69]  A. Dale,et al.  Visual motion aftereffect in human cortical area MT revealed by functional magnetic resonance imaging , 1995, Nature.

[70]  G. Orban,et al.  The kinetic occipital region in human visual cortex. , 1997, Cerebral cortex.

[71]  R. Kawashima,et al.  Changes in regional cerebral blood flow during self-paced arm and finger movements. A PET study , 1996, Brain Research.

[72]  O. Hikosaka,et al.  Activation of human presupplementary motor area in learning of sequential procedures: a functional MRI study. , 1996, Journal of neurophysiology.

[73]  J Tanji,et al.  Changing directions of forthcoming arm movements: neuronal activity in the presupplementary and supplementary motor area of monkey cerebral cortex. , 1996, Journal of neurophysiology.

[74]  E. DeYoe,et al.  Graded effects of spatial and featural attention on human area MT and associated motion processing areas. , 1997, Journal of neurophysiology.

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

[76]  T. Paus Primate anterior cingulate cortex: Where motor control, drive and cognition interface , 2001, Nature Reviews Neuroscience.

[77]  S. Kornblum,et al.  Isolation of Specific Interference Processing in the Stroop Task: PET Activation Studies , 1997, NeuroImage.

[78]  K. Zilles,et al.  Fast reaction to different sensory modalities activates common fields in the motor areas, but the anterior cingulate cortex is involved in the speed of reaction. , 2000, Journal of neurophysiology.

[79]  Dae-Shik Kim,et al.  Origin of Negative Blood Oxygenation Level—Dependent fMRI Signals , 2002, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[80]  G A Orban,et al.  Attention-dependent suppression of metabolic activity in the early stages of the macaque visual system. , 2000, Cerebral cortex.

[81]  V M Haughton,et al.  Cortical activation response to acoustic echo planar scanner noise. , 1998, Journal of computer assisted tomography.

[82]  Cortical field potential associated with hand movement on warning-imperative visual stimulus and cerebellum in the monkey , 1990, Brain Research.

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

[84]  G. Orban,et al.  The kinetic occipital (KO) region in man: an fMRI study. , 1997, Cerebral cortex.

[85]  L. Deecke,et al.  The Preparation and Execution of Self-Initiated and Externally-Triggered Movement: A Study of Event-Related fMRI , 2002, NeuroImage.