Contribution of the pre-SMA to the production of words and non-speech oral motor gestures, as revealed by repetitive transcranial magnetic stimulation (rTMS)

An emerging theoretical perspective, largely based on neuroimaging studies, suggests that the pre-SMA is involved in planning cognitive aspects of motor behavior and language, such as linguistic and non-linguistic response selection. Neuroimaging studies, however, cannot indicate whether a brain region is equally important to all tasks in which it is activated. In the present study, we tested the hypothesis that the pre-SMA is an important component of response selection, using an interference technique. High frequency repetitive TMS (10 Hz) was used to interfere with the functioning of the pre-SMA during tasks requiring selection of words and oral gestures under different selection modes (forced, volitional) and attention levels (high attention, low attention). Results show that TMS applied to the pre-SMA interferes selectively with the volitional selection condition, resulting in longer RTs. The low- and high-attention forced selection conditions were unaffected by TMS, demonstrating that the pre-SMA is sensitive to selection mode but not attentional demands. TMS similarly affected the volitional selection of words and oral gestures, reflecting the response-independent nature of the pre-SMA contribution to response selection. The implications of these results are discussed.

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

[2]  Sarah E. Donohue,et al.  Neural Correlates of Preparation for Action Selection as a Function of Specific Task Demands , 2008, Journal of Cognitive Neuroscience.

[3]  H. Rusinek,et al.  Functional magnetic resonance imaging of human brain activity in a verbal fluency task , 1998, Journal of neurology, neurosurgery, and psychiatry.

[4]  P. Kelly,et al.  Incidence and Clinical Evolution of Postoperative Deficits after Volumetric Stereotactic Resection of Glial Neoplasms Involving the Supplementary Motor Area , 2003, Neurosurgery.

[5]  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.

[6]  Christopher Barry,et al.  Naming the Snodgrass and Vanderwart Pictures: Effects of Age of Acquisition, Frequency, and Name Agreement , 1997 .

[7]  M. Jahanshahi,et al.  The left dorsolateral prefrontal cortex and random generation of responses: studies with transcranial magnetic stimulation , 1998, Neuropsychologia.

[8]  Eraldo Paulesu,et al.  Preserved functional competence of perilesional areas in drug-resistant epilepsy with lesion in supplementary motor cortex: fMRI and neuropsychological observations , 2003, NeuroImage.

[9]  A. Braun,et al.  Comparison of continuous overt speech fMRI using BOLD and arterial spin labeling , 2005, Human brain mapping.

[10]  Ralph-Axel Müller,et al.  Effects of generation mode in fMRI adaptations of semantic fluency: Paced production and overt speech , 2007, Neuropsychologia.

[11]  Andrew W. Ellis,et al.  ROLES OF WORD FREQUENCY AND AGE OF ACQUISITION IN WORD NAMING AND LEXICAL DECISION , 1995 .

[12]  Satrajit S. Ghosh,et al.  Neural modeling and imaging of the cortical interactions underlying syllable production , 2006, Brain and Language.

[13]  Michael J Brammer,et al.  Functional magnetic resonance imaging of verbal fluency and confrontation naming using compressed image acquisition to permit overt responses , 2003, Human brain mapping.

[14]  G. Rizzolatti,et al.  Multiple representations of body movements in mesial area 6 and the adjacent cingulate cortex: An intracortical microstimulation study in the macaque monkey , 1991, The Journal of comparative neurology.

[15]  A. Braun,et al.  The neural organization of discourse: an H2 15O-PET study of narrative production in English and American sign language. , 2001, Brain : a journal of neurology.

[16]  James K. Nelson,et al.  Selection requirements during verb generation: differential recruitment in older and younger adults , 2004, NeuroImage.

[17]  R. Poldrack,et al.  Common neural substrates for inhibition of spoken and manual responses. , 2008, Cerebral cortex.

[18]  M. Inase,et al.  Corticostriatal and corticosubthalamic input zones from the presupplementary motor area in the macaque monkey: comparison with the input zones from the supplementary motor area , 1999, Brain Research.

[19]  John L. Bradshaw,et al.  Articulatory interference and the mown-down heterophone effect , 1974 .

[20]  Jan Derrfuss,et al.  Cognitive control in the posterior frontolateral cortex: evidence from common activations in task coordination, interference control, and working memory , 2004, NeuroImage.

[21]  G. Rizzolatti,et al.  Corticocortical connections of area F3 (SMA‐proper) and area F6 (pre‐SMA) in the macaque monkey , 1993, The Journal of comparative neurology.

[22]  P. Goldman-Rakic,et al.  Prefrontal connections of medial motor areas in the rhesus monkey , 1993, The Journal of comparative neurology.

[23]  Laurent Capelle,et al.  Somatotopy of the Supplementary Motor Area: Evidence from Correlation of the Extent of Surgical Resection with the Clinical Patterns of Deficit , 2002, Neurosurgery.

[24]  Fritz Schick,et al.  Whole-body MRI at high field: technical limits and clinical potential , 2005, European Radiology.

[25]  D. V. von Cramon,et al.  Comparative magnetic resonance imaging at 1.5 and 3 Tesla for the evaluation of traumatic microbleeds. , 2007, Journal of neurotrauma.

[26]  Vincent L. Gracco,et al.  Contribution of the frontal lobe to externally and internally specified verbal responses: fMRI evidence , 2006, NeuroImage.

[27]  M. Erb,et al.  Overt sentence production in event-related fMRI , 2005, Neuropsychologia.

[28]  M. Mendez,et al.  Aphemia-like syndrome from a right supplementary motor area lesion , 2004, Clinical Neurology and Neurosurgery.

[29]  E. Gibson,et al.  Utilization of spelling patterns by deaf and hearing subjects , 1971 .

[30]  E. Phelps,et al.  "Willed action": a functional MRI study of the human prefrontal cortex during a sensorimotor task. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[31]  R. Solomon,et al.  Visual duration threshold as a function of word-probability. , 1951, Journal of experimental psychology.

[32]  A. Aschoff,et al.  Enhancing gray-to-white matter contrast in 3T T1 spin-echo brain scans by optimizing flip angle. , 2005, AJNR. American journal of neuroradiology.

[33]  Bruce D. McCandliss,et al.  Response Anticipation and Response Conflict: An Event-Related Potential and Functional Magnetic Resonance Imaging Study , 2007, The Journal of Neuroscience.

[34]  Clifford R Jack,et al.  Functional heterogeneity of the supplementary motor area. , 2005, AJNR. American journal of neuroradiology.

[35]  Manuel Carreiras,et al.  Brain Activation for Lexical Decision and Reading Aloud: Two Sides of the Same Coin? , 2007, Journal of Cognitive Neuroscience.

[36]  E. Wassermann Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation, June 5-7, 1996. , 1998, Electroencephalography and clinical neurophysiology.

[37]  M. Rushworth,et al.  Organization of action sequences and the role of the pre-SMA. , 2004, Journal of neurophysiology.

[38]  H. C Lau,et al.  Willed action and attention to the selection of action , 2004, NeuroImage.

[39]  Wolfgang Prinz,et al.  The role of the preSMA and the rostral cingulate zone in internally selected actions , 2007, NeuroImage.

[40]  Kevin Murphy,et al.  Speech production: Wernicke, Broca and beyond. , 2002, Brain : a journal of neurology.

[41]  Parashkev Nachev,et al.  Volition and Conflict in Human Medial Frontal Cortex , 2005, Current Biology.

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

[43]  S. Bookheimer,et al.  Activation of language cortex with automatic speech tasks , 2000, Neurology.

[44]  Ivanei E. Bramati,et al.  The cerebral correlates of set-shifting: an fMRI study of the trail making test. , 2002, Arquivos de neuro-psiquiatria.

[45]  P. Strick,et al.  Supplementary Motor Area and Presupplementary Motor Area: Targets of Basal Ganglia and Cerebellar Output , 2007, The Journal of Neuroscience.

[46]  J. Schramm,et al.  Functional results after resective procedures involving the supplementary motor area. , 1996, Journal of neurosurgery.

[47]  M. Erb,et al.  fMRI reveals two distinct cerebral networks subserving speech motor control , 2005, Neurology.

[48]  G Rizzolatti,et al.  Parcellation of human mesial area 6: cytoarchitectonic evidence for three separate areas , 1998, The European journal of neuroscience.

[49]  Ming-Chyi Pai,et al.  Supplementary motor area aphasia: a case report , 1999, Clinical Neurology and Neurosurgery.

[50]  Wilhelm Eisner,et al.  Surgical Resection of Grade II Astrocytomas in the Superior Frontal Gyrus , 2002, Neurosurgery.

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

[52]  W PENFIELD,et al.  The supplementary motor area of the cerebral cortex; a clinical and experimental study. , 1951, A.M.A. archives of neurology and psychiatry.

[53]  E Kanal,et al.  A comparison between magnetic resonance imaging and computed tomography for stereotactic coordinate determination. , 1992, Neurosurgery.

[54]  G. Rizzolatti,et al.  Architecture of superior and mesial area 6 and the adjacent cingulate cortex in the macaque monkey , 1991, The Journal of comparative neurology.

[55]  A. Elster Clinical advantages of 3.0 T MRI over 1.5 T , 2009 .

[56]  P. Strick,et al.  Frontal lobe inputs to primate motor cortex: evidence for four somatotopically organized ‘premotor’ areas , 1979, Brain Research.

[57]  M. Coles,et al.  On the programming and reprogramming of actions. , 2007, Cerebral cortex.

[58]  K. Forster,et al.  Lexical Access and Naming Time. , 1973 .

[59]  Guy Marchal,et al.  FMRI Studies of the Supplementary Motor Area and the Premotor Cortex , 1997, NeuroImage.

[60]  Alvaro Pascual-Leone,et al.  Transcranial magnetic stimulation: a neurochromometrics of mind. , 2003 .

[61]  Gary W. Thickbroom,et al.  Differential activation of frontal lobe areas by lexical and semantic language tasks: A functional magnetic resonance imaging study , 2006, Journal of Clinical Neuroscience.

[62]  R. E. Passingham,et al.  Interference with Performance of a Response Selection Task that has no Working Memory Component: An rTMS Comparison of the Dorsolateral Prefrontal and Medial Frontal Cortex , 2001, Journal of Cognitive Neuroscience.

[63]  J. B. Preston,et al.  Interconnections between the prefrontal cortex and the premotor areas in the frontal lobe , 1994, The Journal of comparative neurology.

[64]  James L. Herrick,et al.  Cortical innervation of the facial nucleus in the non-human primate: a new interpretation of the effects of stroke and related subtotal brain trauma on the muscles of facial expression. , 2001, Brain : a journal of neurology.

[65]  Emmanuel Mellet,et al.  Picture naming without Broca's and Wernicke's area , 2000, Neuroreport.

[66]  Giuseppe Luppino,et al.  Thalamic input to mesial and superior area 6 in the macaque monkey , 1996, The Journal of comparative neurology.

[67]  P. Rossini,et al.  Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. , 1994, Electroencephalography and clinical neurophysiology.

[68]  H. Chainay,et al.  Motor and language deficits before and after surgical resection of mesial frontal tumour , 2009, Clinical Neurology and Neurosurgery.

[69]  L. Cohen,et al.  The role of the supplementary motor area (SMA) in word production , 2006, Brain Research.

[70]  Catriona M. Morrison,et al.  Real age-of-acquisition effects in lexical retrieval. , 1998, Journal of experimental psychology. Learning, memory, and cognition.

[71]  Vincent L. Gracco,et al.  On the selection of words and oral motor responses: Evidence of a response-independent fronto-parietal network , 2010, Cortex.

[72]  Jonathan D. Cohen,et al.  Conflict monitoring versus selection-for-action in anterior cingulate cortex , 1999, Nature.

[73]  A. Braun,et al.  Temporal dissociation of early lexical access and articulation using a delayed naming task--an FMRI study. , 2006, Cerebral cortex.

[74]  Christopher Barry,et al.  Age-of-acquisition and frequency effects in speeded word naming , 1999, Cognition.

[75]  Hakwan C. Lau,et al.  Dissociating response selection and conflict in the medial frontal surface , 2006, NeuroImage.

[76]  D. Poeppel,et al.  The cortical organization of speech processing , 2007, Nature Reviews Neuroscience.

[77]  Pascale Tremblay,et al.  Clinical implications of cross-system interactions. , 2006, Seminars in speech and language.

[78]  Randy L. Buckner,et al.  An Event-Related fMRI Study of Overt and Covert Word Stem Completion , 2001, NeuroImage.

[79]  G. Goldberg Supplementary motor area structure and function: Review and hypotheses , 1985, Behavioral and Brain Sciences.

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

[81]  Don L. Scarborough,et al.  Frequency and Repetition Effects in Lexical Memory. , 1977 .

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

[83]  N Palomero-Gallagher,et al.  Receptor autoradiographic mapping of the mesial motor and premotor cortex of the macaque monkey , 1998, The Journal of comparative neurology.

[84]  W. Levelt,et al.  The spatial and temporal signatures of word production components , 2004, Cognition.

[85]  A. Mechelli,et al.  Effect of word and syllable frequency on activation during lexical decision and reading aloud , 2006, Human brain mapping.

[86]  S. Gerhand,et al.  Word frequency effects in oral reading are not merely age-of-acquisition effects in disguise. , 1998 .

[87]  S. Petersen,et al.  Effects of Lexicality, Frequency, and Spelling-to-Sound Consistency on the Functional Anatomy of Reading , 1999, Neuron.

[88]  E. Auerbach,et al.  Relative Shift in Activity from Medial to Lateral Frontal Cortex During Internally Versus Externally Guided Word Generation , 2001, Journal of Cognitive Neuroscience.

[89]  Jun Tanji,et al.  Prefrontal cortical cells projecting to the supplementary eye field and presupplementary motor area in the monkey , 2005, Neuroscience Research.

[90]  Harry Levin,et al.  Basic studies on reading , 1970 .

[91]  R. Chris Miall,et al.  Differentiation between external and internal cuing: An fMRI study comparing tracing with drawing , 2007, NeuroImage.

[92]  G. Rizzolatti,et al.  The Organization of the Frontal Motor Cortex. , 2000, News in physiological sciences : an international journal of physiology produced jointly by the International Union of Physiological Sciences and the American Physiological Society.

[93]  RP Dum,et al.  The origin of corticospinal projections from the premotor areas in the frontal lobe , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[94]  Catriona M. Morrison,et al.  Real age of acquisition effects in word naming and lexical decision. , 2000, British journal of psychology.

[95]  K. A. Hadland,et al.  Role of the human medial frontal cortex in task switching: a combined fMRI and TMS study. , 2002, Journal of neurophysiology.