Subsecond Changes in Top–Down Control Exerted by Human Medial Frontal Cortex during Conflict and Action Selection: A Combined Transcranial Magnetic Stimulation–Electroencephalography Study

Action selection requires choosing one of all the possible conflicting action plans that are available. There is currently a debate as to whether the dorsal medial frontal cortex (dMFC) merely detects or actively resolves response conflict. We used combined on-line transcranial magnetic stimulation and electroencephalographic recording (TMS–EEG) to test whether human dMFC plays a critical causal role in conflict resolution, and whether the mechanism for such a function is via interactions with primary motor cortex. In an Eriksen flanker task, subjects discriminated the direction of the centermost arrow in an array of five, responding with the left or right hand. The lateralized readiness potential (LRP), a measure of relative levels of activity in left and right motor cortices, was also recorded. Reaction times and error rates were higher on incongruent than congruent trials, and incongruent trials produced a positive LRP deflection reflecting initial partial activation of the incorrect response. On one-half of trials, repetitive TMS was applied to left dMFC starting 100 ms before visual stimulus onset and ending 100 ms afterward. TMS disrupted performance by selectively increasing error rates on contralateral (right hand) incongruent trials. TMS also only modulated the LRP on incongruent trials, causing an increased positive deflection (associated with preparation of the incorrect response) starting 180 ms after visual stimulus onset. TMS of a control site did not interfere with behavior or motor cortical activity. dMFC has a direct causal role in resolving conflict during action selection, and the mechanism involves the top–down modulation of primary motor cortical activity.

[1]  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.

[2]  M Hallett,et al.  Topographic mapping of the human motor cortex with magnetic stimulation: factors affecting accuracy and reproducibility. , 1992, Electroencephalography and clinical neurophysiology.

[3]  C. Eriksen,et al.  Effects of noise letters upon the identification of a target letter in a nonsearch task , 1974 .

[4]  R. Passingham,et al.  Attention to Intention , 2004, Science.

[5]  M. Brass,et al.  Internally generated and directly cued task sets: an investigation with fMRI , 2005, Neuropsychologia.

[6]  C. Eriksen,et al.  Pre- and poststimulus activation of response channels: a psychophysiological analysis. , 1988, Journal of experimental psychology. Human perception and performance.

[7]  Christopher L. Asplund,et al.  Isolation of a Central Bottleneck of Information Processing with Time-Resolved fMRI , 2006, Neuron.

[8]  M. Walton,et al.  Action sets and decisions in the medial frontal cortex , 2004, Trends in Cognitive Sciences.

[9]  M. Rushworth,et al.  A primer of magnetic stimulation as a tool for neuropsychology. , 1999, Neuropsychologia.

[10]  R. Passingham,et al.  Active maintenance in prefrontal area 46 creates distractor-resistant memory , 2002, Nature Neuroscience.

[11]  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.

[12]  RP Dum,et al.  Topographic organization of corticospinal projections from the frontal lobe: motor areas on the lateral surface of the hemisphere , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  John C. Rothwell,et al.  Time Course of Functional Connectivity between Dorsal Premotor and Contralateral Motor Cortex during Movement Selection , 2006, The Journal of Neuroscience.

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

[15]  E. Crone,et al.  Brain Regions Mediating Flexible Rule Use during Development , 2006, The Journal of Neuroscience.

[16]  Michael G. H. Coles,et al.  Mental chronometry and the study of human information processing. , 1995 .

[17]  H. Kornhuber,et al.  [CHANGES IN THE BRAIN POTENTIAL IN VOLUNTARY MOVEMENTS AND PASSIVE MOVEMENTS IN MAN: READINESS POTENTIAL AND REAFFERENT POTENTIALS]. , 1965, Pflugers Archiv fur die gesamte Physiologie des Menschen und der Tiere.

[18]  Anna C Nobre,et al.  FEF TMS affects visual cortical activity. , 2006, Cerebral cortex.

[19]  Carter Wendelken,et al.  Neurocognitive development of the ability to manipulate information in working memory. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[20]  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.

[21]  Jun Tanji,et al.  Distribution of eye- and arm-movement-related neuronal activity in the SEF and in the SMA and Pre-SMA of monkeys. , 2002, Journal of neurophysiology.

[22]  M. Brass,et al.  The role of the frontal cortex in task preparation. , 2002, Cerebral cortex.

[23]  J. Schall,et al.  Executive control of countermanding saccades by the supplementary eye field , 2006, Nature Neuroscience.

[24]  Martin Eimer,et al.  Cortico-cortical interactions in spatial attention: A combined ERP/TMS study. , 2006, Journal of neurophysiology.

[25]  Kae Nakamura,et al.  Neuronal activity in medial frontal cortex during learning of sequential procedures. , 1998, Journal of neurophysiology.

[26]  R. Passingham,et al.  The functions of the medial premotor cortex , 2004, Experimental Brain Research.

[27]  R. Poldrack,et al.  Cortical and Subcortical Contributions to Stop Signal Response Inhibition: Role of the Subthalamic Nucleus , 2006, The Journal of Neuroscience.

[28]  RP Dum,et al.  Topographic organization of corticospinal projections from the frontal lobe: motor areas on the medial surface of the hemisphere , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  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.

[30]  O. Hikosaka,et al.  Switching from automatic to controlled action by monkey medial frontal cortex , 2007, Nature Neuroscience.

[31]  Karl J. Friston,et al.  Cortical areas and the selection of movement: a study with positron emission tomography , 1991, Experimental Brain Research.

[32]  M. Coles Modern mind-brain reading: psychophysiology, physiology, and cognition. , 1989, Psychophysiology.

[33]  C. Liston,et al.  Anterior Cingulate and Posterior Parietal Cortices Are Sensitive to Dissociable Forms of Conflict in a Task-Switching Paradigm , 2006, Neuron.

[34]  Geraint Rees,et al.  Self-control during response conflict by human supplementary eye field , 2003, Nature Neuroscience.

[35]  E. Miller,et al.  Neural circuits subserving the retrieval and maintenance of abstract rules. , 2003, Journal of neurophysiology.

[36]  H. Vaughan,et al.  Cortical potentials associated with voluntary movements in the monkey , 1975, Brain Research.

[37]  H. Kornhuber,et al.  Hirnpotentialänderungen bei Willkürbewegungen und passiven Bewegungen des Menschen: Bereitschaftspotential und reafferente Potentiale , 1965, Pflüger's Archiv für die gesamte Physiologie des Menschen und der Tiere.

[38]  M. Ridding,et al.  Rapid rate transcranial magnetic stimulation--a safety study. , 1997, Electroencephalography and clinical neurophysiology.

[39]  Alan Cowey,et al.  Transcranial magnetic stimulation and cognitive neuroscience , 2000, Nature Reviews Neuroscience.

[40]  J C Rothwell,et al.  Effect of transcranial magnetic stimulation over the cerebellum on the excitability of human motor cortex. , 1996, Electroencephalography and clinical neurophysiology.

[41]  C. Brunia Movement and stimulus preceding negativity , 1988, Biological Psychology.

[42]  C. A. Marzi,et al.  Transcranial magnetic stimulation selectively impairs interhemispheric transfer of visuo-motor information in humans , 1998, Experimental Brain Research.

[43]  Juha Silvanto,et al.  Stimulation of the human frontal eye fields modulates sensitivity of extrastriate visual cortex. , 2006, Journal of neurophysiology.

[44]  E. Crone,et al.  Neural evidence for dissociable components of task-switching. , 2006, Cerebral cortex.

[45]  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.

[46]  Kristina M. Visscher,et al.  A Core System for the Implementation of Task Sets , 2006, Neuron.

[47]  Matthew F. S. Rushworth,et al.  Attention systems and the organization of the human parietal cortex , 2001, NeuroImage.

[48]  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.

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

[50]  A. Riehle,et al.  Neuronal activity and information processing in motor control: From stages to continuous flow , 1988, Biological Psychology.

[51]  Xiaofeng Lu,et al.  Organization of Multisynaptic Inputs from Prefrontal Cortex to Primary Motor Cortex as Revealed by Retrograde Transneuronal Transport of Rabies Virus , 2005, The Journal of Neuroscience.

[52]  Jeremy R. Reynolds,et al.  Neural Mechanisms of Transient and Sustained Cognitive Control during Task Switching , 2003, Neuron.

[53]  M. Brass,et al.  Neural Circuitry Underlying Rule Use in Humans and Nonhuman Primates , 2005, The Journal of Neuroscience.

[54]  R. Passingham,et al.  Prefrontal interactions reflect future task operations , 2003, Nature Neuroscience.

[55]  Jonathan D. Cohen,et al.  Conflict monitoring and anterior cingulate cortex: an update , 2004, Trends in Cognitive Sciences.