Dissociable mechanisms of cognitive control in prefrontal and premotor cortex.

Intelligent behavior depends on the ability to suppress inappropriate actions and resolve interference between competing responses. Recent clinical and neuroimaging evidence has demonstrated the involvement of prefrontal, parietal, and premotor areas during behaviors that emphasize conflict and inhibition. It remains unclear, however, whether discrete subregions within this network are crucial for overseeing more specific inhibitory demands. Here we probed the functional specialization of human prefrontal cortex by combining repetitive transcranial magnetic stimulation (rTMS) with integrated behavioral measures of response inhibition (stop-signal task) and response competition (flanker task). Participants undertook a combined stop-signal/flanker task after rTMS of the inferior frontal gyrus (IFG) or dorsal premotor cortex (dPM) in each hemisphere. Stimulation of the right IFG impaired stop-signal inhibition under conditions of heightened response competition but did not influence the ability to suppress a competing response. In contrast, stimulation of the right dPM facilitated execution but had no effect on inhibition. Neither of these results was observed during rTMS of corresponding left-hemisphere regions. Overall, our findings are consistent with existing evidence that the right IFG is crucial for inhibitory control. The observed double dissociation of neurodisruptive effects between the right IFG and right dPM further implies that response inhibition and execution rely on distinct neural processes despite activating a common cortical network.

[1]  Jason B. Mattingley,et al.  Distance-adjusted motor threshold for transcranial magnetic stimulation , 2007, Clinical Neurophysiology.

[2]  M. Rushworth,et al.  Functionally Specific Reorganization in Human Premotor Cortex , 2007, Neuron.

[3]  Benjamin A. Parris,et al.  The role of the ventrolateral frontal cortex in inhibitory oculomotor control. , 2007, Brain : a journal of neurology.

[4]  Timothy Edward John Behrens,et al.  Triangulating a Cognitive Control Network Using Diffusion-Weighted Magnetic Resonance Imaging (MRI) and Functional MRI , 2007, The Journal of Neuroscience.

[5]  T. Shallice,et al.  Effects of focal frontal lesions on response inhibition. , 2006, Cerebral cortex.

[6]  Donald T. Stuss,et al.  Inhibitory Control is Slowed in Patients with Right Superior Medial Frontal Damage , 2006, Journal of Cognitive Neuroscience.

[7]  R. Deichmann,et al.  Concurrent TMS-fMRI and Psychophysics Reveal Frontal Influences on Human Retinotopic Visual Cortex , 2006, Current Biology.

[8]  J. Jonides,et al.  Brain mechanisms of proactive interference in working memory , 2006, Neuroscience.

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

[10]  Jason B. Mattingley,et al.  Executive “Brake Failure” following Deactivation of Human Frontal Lobe , 2006, Journal of Cognitive Neuroscience.

[11]  Tracy R. Henderson,et al.  Simple metric for scaling motor threshold based on scalp-cortex distance: application to studies using transcranial magnetic stimulation. , 2005, Journal of neurophysiology.

[12]  D. Boussaoud,et al.  Callosal connections of dorsal versus ventral premotor areas in the macaque monkey: a multiple retrograde tracing study , 2005, BMC Neuroscience.

[13]  W. Notebaert,et al.  Effects of stimulus-stimulus compatibility and stimulus-response compatibility on response inhibition. , 2005, Acta psychologica.

[14]  J. Mattingley,et al.  Neurodisruption of selective attention: insights and implications , 2005, Trends in Cognitive Sciences.

[15]  L. Jancke,et al.  The role of the right dorsal premotor cortex in visuomotor learning: a transcranial magnetic stimulation study , 2005, Neuroreport.

[16]  Hartwig R. Siebner,et al.  BOLD MRI responses to repetitive TMS over human dorsal premotor cortex , 2005, NeuroImage.

[17]  Tor D. Wager,et al.  Common and unique components of response inhibition revealed by fMRI , 2005, NeuroImage.

[18]  Lisa Koski,et al.  Exploring the contributions of premotor and parietal cortex to spatial compatibility using image-guided TMS , 2005, NeuroImage.

[19]  M. Bellgrove,et al.  The functional neuroanatomical correlates of response variability: evidence from a response inhibition task , 2004, Neuropsychologia.

[20]  Jason B. Mattingley,et al.  Modality-Specific Control of Strategic Spatial Attention in Parietal Cortex , 2004, Neuron.

[21]  J. Rothwell,et al.  Interhemispheric interaction between human dorsal premotor and contralateral primary motor cortex , 2004, The Journal of physiology.

[22]  K. R. Ridderinkhof,et al.  Neurocognitive mechanisms of cognitive control: The role of prefrontal cortex in action selection, response inhibition, performance monitoring, and reward-based learning , 2004, Brain and Cognition.

[23]  H. Karnath,et al.  Using human brain lesions to infer function: a relic from a past era in the fMRI age? , 2004, Nature Reviews Neuroscience.

[24]  Kevin Murphy,et al.  Beyond common resources: the cortical basis for resolving task interference , 2004, NeuroImage.

[25]  Michael E. Goldberg,et al.  Prefrontal Neurons Coding Suppression of Specific Saccades , 2004, Neuron.

[26]  S. Yamaguchi,et al.  Neural Correlates for the Suppression of Habitual Behavior: A Functional MRI Study , 2004, Journal of Cognitive Neuroscience.

[27]  A. Vandierendonck,et al.  The interaction between stop signal inhibition and distractor interference in the flanker and Stroop task. , 2004, Acta psychologica.

[28]  T. Robbins,et al.  Inhibition and the right inferior frontal cortex , 2004, Trends in Cognitive Sciences.

[29]  P. Brown,et al.  Event-related beta desynchronization in human subthalamic nucleus correlates with motor performance. , 2004, Brain : a journal of neurology.

[30]  R. Benecke,et al.  Inhibitory actions of motor cortex following unilateral brain lesions as studied by magnetic brain stimulation , 2004, Experimental Brain Research.

[31]  John D. E. Gabrieli,et al.  Material-dependent and material-independent selection processes in the frontal and parietal lobes: an event-related fMRI investigation of response competition , 2003, Neuropsychologia.

[32]  Tomás Paus,et al.  Transcranial Magnetic Stimulation of the Human Frontal Eye ®eld Facilitates Visual Awareness , 2022 .

[33]  M. D’Esposito,et al.  Neural Evidence for Representation-Specific Response Selection , 2003, Journal of Cognitive Neuroscience.

[34]  N. Kanwisher,et al.  Common Neural Substrates for Response Selection across Modalities and Mapping Paradigms , 2003, Journal of Cognitive Neuroscience.

[35]  R. Caminiti,et al.  Callosal connections of dorso‐lateral premotor cortex , 2003, The European journal of neuroscience.

[36]  G. Logan,et al.  Inhibitory attentional control in patients with frontal lobe damage , 2003, Brain and Cognition.

[37]  Sharon Morein-Zamir,et al.  The Effect of Methylphenidate on Three Forms of Response Inhibition in Boys with AD/HD , 2003, Journal of abnormal child psychology.

[38]  T. Robbins,et al.  Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans , 2003, Nature Neuroscience.

[39]  Eliot Hazeltine,et al.  Dissociable Contributions of Prefrontal and Parietal Cortices to Response Selection , 2002, NeuroImage.

[40]  A. Nambu,et al.  Functional significance of the cortico–subthalamo–pallidal ‘hyperdirect’ pathway , 2002, Neuroscience Research.

[41]  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.

[42]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[43]  J. Rothwell,et al.  Functional Connectivity of Human Premotor and Motor Cortex Explored with Repetitive Transcranial Magnetic Stimulation , 2002, The Journal of Neuroscience.

[44]  J. Rothwell,et al.  Transcranial magnetic stimulation: new insights into representational cortical plasticity , 2002, Experimental Brain Research.

[45]  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.

[46]  J. Rothwell,et al.  Decreased corticospinal excitability after subthreshold 1 Hz rTMS over lateral premotor cortex , 2001, NeuroImage.

[47]  G. Glover,et al.  Error‐related brain activation during a Go/NoGo response inhibition task , 2001, Human brain mapping.

[48]  E. Bullmore,et al.  Mapping Motor Inhibition: Conjunctive Brain Activations across Different Versions of Go/No-Go and Stop Tasks , 2001, NeuroImage.

[49]  R. Poldrack,et al.  Neural Activation During Response Competition , 2000, Journal of Cognitive Neuroscience.

[50]  J. Duncan,et al.  Common regions of the human frontal lobe recruited by diverse cognitive demands , 2000, Trends in Neurosciences.

[51]  C. Rorden,et al.  Stereotaxic display of brain lesions. , 2000, Behavioural neurology.

[52]  A. Schnitzler,et al.  Magnetic stimulation of the dorsal premotor cortex modulates the Simon effect. , 1999, Neuroreport.

[53]  E. Stein,et al.  Right hemispheric dominance of inhibitory control: an event-related functional MRI study. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[54]  Y. Miyashita,et al.  Common inhibitory mechanism in human inferior prefrontal cortex revealed by event-related functional MRI. , 1999, Brain : a journal of neurology.

[55]  K. R. Ridderinkhof,et al.  A study of adaptive behavior: effects of age and irrelevant information on the ability to inhibit one's actions , 1999 .

[56]  R. Passingham,et al.  Temporary interference in human lateral premotor cortex suggests dominance for the selection of movements. A study using transcranial magnetic stimulation. , 1998, Brain : a journal of neurology.

[57]  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.

[58]  Masahiko Inase,et al.  Corticosubthalamic input zones from forelimb representations of the dorsal and ventral divisions of the premotor cortex in the macaque monkey: comparison with the input zones from the primary motor cortex and the supplementary motor area , 1997, Neuroscience Letters.

[59]  M. Hallett,et al.  Depression of motor cortex excitability by low‐frequency transcranial magnetic stimulation , 1997, Neurology.

[60]  Paul B. Johnson,et al.  Premotor and parietal cortex: corticocortical connectivity and combinatorial computations. , 1997, Annual review of neuroscience.

[61]  K. R. Ridderinkhof,et al.  Limits on the application of additive factors logic: Violations of stage robustness suggest a dual-process architecture to explain flanker effects on target processing , 1995 .

[62]  David L. Strayer,et al.  Aging and inhibition: beyond a unitary view of inhibitory processing in attention. , 1994, Psychology and aging.

[63]  R. Passingham,et al.  Premotor cortex and the conditions for movement in monkeys (Macaca fascicularis) , 1985, Behavioural Brain Research.

[64]  G. Logan On the ability to inhibit thought and action , 1984 .

[65]  B. Bergum,et al.  Attention and performance IX , 1982 .