Intracranial EEG Reveals a Time- and Frequency-Specific Role for the Right Inferior Frontal Gyrus and Primary Motor Cortex in Stopping Initiated Responses

Swann, Nicole C.; Tandon, Nitin; Canolty, Ryan T.; Ellmore, Timothy M.; McEvoy, Linda K.; Dreyer, Stephen; Disano, Michael A.; Aron, Adam R.

doi:10.1523/jneurosci.3359-09.2009

Cited by 410 publications

(417 citation statements)

References 61 publications

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“…The current results support this claim. At 175 ms, the timing of rIFG's effect in the current experiments is reminiscent of the timing of changes in synchrony recorded in this area during action inhibition (8). Despite the evidence that rIFG induces inhibition at a physiological level when cognitive control is needed, it should also be emphasized that the part of rIFG we investigated here (SI Text Section 1) exerted an excitatory influence on M1 corticospinal activity during routine action selection on "stay" trials.…”

Section: Discussionmentioning

confidence: 63%

“…The rIFG has a preeminent role in a network for action inhibition because it inhibits M1 corticospinal activity during action reprogramming 175 ms after a visual cue, indicating that a change in action is needed (SI Text Section 2). It has previously been suggested that rIFG might exert its influence over other brain areas by inhibiting physiological activity (8), but this has been difficult to test empirically. The current results support this claim.…”

Section: Discussionmentioning

confidence: 99%

“…For example, at a cognitive level, the rIFG has been suggested to be involved in the inhibition of an incorrect motor program (2,7). However, whether this cognitive inhibition is also reflected at a physiological level remains subject to investigation (8). Moreover, how each individual node of the cortical network exerts its influence and interacts with other nodes is unknown.…”

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confidence: 99%

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Cortical and subcortical interactions during action reprogramming and their related white matter pathways

Neubert

Mars

Buch

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

239

266

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The right inferior frontal gyrus (rIFG) and the presupplementary motor area (pre-SMA) have been identified with cognitive controlthe top-down influence on other brain areas when nonroutine behavior is required. It has been argued that they "inhibit" habitual motor responses when environmental changes mean a different response should be made. However, whether such "inhibition" can be equated with inhibitory physiological interactions has been unclear, as has the areas' relationship with each other and the anatomical routes by which they influence movement execution. Paired-pulse transcranial magnetic stimulation (ppTMS) was applied over rIFG and primary motor cortex (M1) or over pre-SMA and M1 to measure their interactions, at a subsecond scale, during either inhibition and reprogramming of actions or during routine action selection. Distinct patterns of functional interaction between pre-SMA and M1 and between rIFG and M1 were found that were specific to action reprogramming trials; at a physiological level, direct influences of pre-SMA and rIFG on M1 were predominantly facilitatory and inhibitory, respectively. In a subsequent experiment, it was shown that the rIFG's inhibitory influence was dependent on pre-SMA. A third experiment showed that pre-SMA and rIFG influenced M1 at two time scales. By regressing white matter fractional anisotropy from diffusion-weighted magnetic resonance images against TMSmeasured functional connectivity, it was shown that short-latency (6 ms) and longer latency (12 ms) influences were mediated by cortico-cortical and subcortical pathways, respectively, with the latter passing close to the subthalamic nucleus.W e humans can engage in a complex repertoire of behaviors geared toward often far-removed goals. We have to override reflexive and habitual reactions to orchestrate behavior in accordance with our intentions. The mechanisms that allow us to act in this way are commonly referred to as "cognitive control processes," and their functions include controlling, and often preventing, lower level or more automatic sensory, memory, and motor operations (1). In the control of action, a network involving the presupplementary motor area (pre-SMA) and right inferior frontal gyrus (rIFG) has been commonly identified as crucial for the adaptation of actions to changes in the environment (2-10), a process we refer to as "action reprogramming" (6). The precise contributions of these regions, however, remain unknown. For example, at a cognitive level, the rIFG has been suggested to be involved in the inhibition of an incorrect motor program (2, 7). However, whether this cognitive inhibition is also reflected at a physiological level remains subject to investigation (8). Moreover, how each individual node of the cortical network exerts its influence and interacts with other nodes is unknown. Some authors have argued that interactions among cortical regions during action reprogramming occurs via direct cortical routes (11, 12), whereas others have argued for the involvement of subcortical routes,...

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Section: Discussionmentioning

confidence: 63%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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Cortical and subcortical interactions during action reprogramming and their related white matter pathways

Neubert

Mars

Buch

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

239

266

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“…In this multimodal study, a frontocentral increase of beta power starting at about 400-500 ms after an erroneous response showed a positive correlation with PES on the next correct trial. Importantly, this beta oscillatory component (13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28)(29)(30) has been linked to motor inhibition (Whittington et al, 2000;Alegre et al, 2004;Kramer et al, 2009;Swann et al, 2009;Walsh et al, 2010). Our results might be compatible with these findings, since the increase of excitability of the ipsilateral motor cortex at 450 ms occurred roughly at the same time as the betaoscillatory component associated to PES (see Danielmeier and Ullsperger, 2011 for a discussion).…”

Section: Discussionmentioning

confidence: 99%

Tracking post-error adaptation in the motor system by transcranial magnetic stimulation

et al. 2013

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Abstract-The commission of an error triggers cognitive control processes dedicated to error correction and prevention. Post-error adjustments leading to response slowing following an error (''post-error slowing''; PES) might be driven by changes in excitability of the motor regions and the corticospinal tract (CST). The time-course of such excitability modulations of the CST leading to PES is largely unknown. To track these presumed excitability changes after an error, single pulse transcranial magnetic stimulation (TMS) was applied to the motor cortex ipsilateral to the responding hand, while participants were performing an Eriksen flanker task. A robotic arm with a movement compensation system was used to maintain the TMS coil in the correct position during the experiment. Magnetic pulses were delivered over the primary motor cortex ipsilateral to the active hand at different intervals (150, 300, 450 ms) after correct and erroneous responses, and the motor-evoked potentials (MEP) of the first dorsal interosseous muscle (FDI) contralateral to the stimulated hemisphere were recorded. MEP amplitude was increased 450 ms after the error. Two additional experiments showed that this increase was neither associated to the correction of the erroneous responses nor to the characteristics of the motor command. To the extent to which the excitability of the motor cortex ipsi-and contralateral to the response hand are inversely related, these results suggest a decrease in the excitability of the active motor cortex after an erroneous response. This modulation of the activity of the CST serves to prevent further premature and erroneous responses. At a more general level, the study shows the power of the TMS technique for the exploration of the temporal evolution of post-error adjustments within the motor system. Ó

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“…This hyperdirect pathway assumes projections of the frontal cortex (pre-SMA, inferior frontal gyrus and anterior cingular cortices) onto the subthalamic nucleus (Haynes & Haber, 2013). This hypothesis is attractive, but it is currently only supported by a few intracerebral electrophysiological recordings in humans-during the stop signal task (SST)-showing that beta (15e35 Hz) oscillations of local field potentials (LFP) increased during stopping in the inferior frontal gyrus (Jha et al, 2015;Swann et al, 2009;Wessel, Conner, Aron, & Tandon, 2013) and in the STN at latencies that precede the time needed to cancel movements (stop signal reaction time, SSRT). Indirect evidence also comes from reports that showed that STN lesions cause ballistic and involuntary movement in non-human primates and humans (Crossman, Sambrook, & Jackson, 1984;Nishioka, Taguchi, Nanri, & Ikeda, 2008) as well as inaccurate and premature responding in reaction time tasks performed by rats (Baunez, Nieoullon, & Amalric, 1995;Eagle et al, 2008) and humans (Obeso et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Response inhibition rapidly increases single-neuron responses in the subthalamic nucleus of patients with Parkinson's disease

Bénis

David

Piallat

et al. 2016

Cortex

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ElectrophysiologyStop-signal task a b s t r a c tThe subthalamic nucleus (STN) plays a critical role during action inhibition, perhaps by acting like a fast brake on the motor system when inappropriate responses have to be rapidly suppressed. However, the mechanisms involving the STN during motor inhibition are still unclear, particularly because of a relative lack of single-cell responses reported in this structure in humans. In this study, we used extracellular microelectrode recordings during deep brain stimulation surgery in patients with Parkinson's disease (PD) to study STN neurophysiological correlates of inhibitory control during a stop signal task. We found two neuronal subpopulations responding either during motor execution (GO units) or during motor inhibition (STOP units). GO units fired selectively before patients' motor responses whereas STOP units fired selectively when patients successfully withheld their move at a latency preceding the duration of the inhibition process. These results provide electrophysiological evidence for the hypothesized role of the STN in current models of response inhibition.© 2016 Published by Elsevier Ltd. IntroductionNeuroimaging studies have shown that response-stopping processes activate a frontal-subcortical network (Aron, 2006;Chikazoe et al., 2009;Li, Yan, Sinha, & Lee, 2008). The dynamics of this network has been conceptualized in several computational models of response inhibition (Frank, 2006;Ratcliff & Frank, 2012;Wiecki & Frank, 2013) Available online at www.sciencedirect.com ScienceDirectJournal homepage: www.elsevier.com/locate/cortex c o r t e x 8 4 ( 2 0 1 6 ) 1 1 1 e1 2 3http://dx

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Intracranial EEG Reveals a Time- and Frequency-Specific Role for the Right Inferior Frontal Gyrus and Primary Motor Cortex in Stopping Initiated Responses

Cited by 410 publications

References 61 publications

Cortical and subcortical interactions during action reprogramming and their related white matter pathways

Cortical and subcortical interactions during action reprogramming and their related white matter pathways

Tracking post-error adaptation in the motor system by transcranial magnetic stimulation

Response inhibition rapidly increases single-neuron responses in the subthalamic nucleus of patients with Parkinson's disease

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