A Network Centered on Ventral Premotor Cortex Exerts Both Facilitatory and Inhibitory Control over Primary Motor Cortex during Action Reprogramming

Buch, Ethan R.; Mars, Rogier B.; Boorman, Erie D.; Rushworth, Matthew F. S.

doi:10.1523/jneurosci.4882-09.2010

Cited by 142 publications

(174 citation statements)

References 29 publications

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“…However, the IPLs of 6 or 8 ms used in previous ppTMS studies made it unlikely that the effects were mediated by such a route (12,23). To investigate this issue further, the present experiment assessed pre-SMA/M1 and rIFG/M1 interactions using a range of IPLs and looked for correlations between TMS effect sizes and white matter integrity.…”

Section: Discussionmentioning

confidence: 97%

“…The intensity of the preceding conditioning pulse was set at 110% of the resting motor threshold (RMT, defined as the minimum stimulator output required to elicit a 50-μV MEP in 5 of 10 trials) of the left FDI muscle (right M1), and the IPL was 8 ms (23,24). Several studies have used similar interhemispheric TMS coil configuration and conditioning and test pulse intensities, because the size of the head precludes placing two TMS coils over frontal and M1 areas in the same hemisphere in some participants and an interhemispheric configuration produces similar results, albeit with a slightly higher intensity conditioning pulse, to an intrahemispheric configuration (16,23). We hypothesized that the preceding conditioning pulse would change the MEP amplitude elicited by the test pulse, depending on the type of the trial (switch vs. stay trial) and the time after center cue color onset (75, 125, or 175 ms) (Fig.…”

Section: Methodsmentioning

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

270

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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: 97%

Section: Methodsmentioning

confidence: 99%

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

270

View full text Add to dashboard Cite

show abstract

“…This effect depends on cognitive state. When the PMv-M1 pathway is endogenously activated during grasping, an excitatory effect is observed (Davare et al, 2009;Buch et al, 2010). Projections from premotor cortex to M1 are glutamatergic, but while some synapse directly onto corticospinal neurons, many synapse onto GABAergic interneurons within M1 .…”

Section: Introductionmentioning

confidence: 99%

Noninvasive Associative Plasticity Induction in a Corticocortical Pathway of the Human Brain

Buch¹,

Johnen²,

Nelissen³

et al. 2011

J. Neurosci.

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121

187

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Coincident pairing of presynaptic and postsynaptic activity selectively strengthens synaptic connections, a key mechanism underlying cortical plasticity. Using paired associative transcranial magnetic stimulation (TMS), we demonstrate selective potentiation of physiological connectivity between two human brain regions, ventral premotor cortex (PMv) and primary motor cortex (M1) after repeated paired-pulse TMS of PMv and M1. The effect was anatomically specific: paired stimulation of the presupplementary motor area and M1 did not induce changes in PMv-M1 pathway connectivity. The effect was dependent on stimulation order: repeated stimulation of PMv before M1 led to strengthening of the PMv-M1 pathway, while repeated stimulation of M1 before PMv diminished the strength of the PMv-M1 pathway. The expression of the change in the pathway depended on the cognitive state of the subject at the time of testing: when the subject was tested at rest, paired PMv-M1 stimulation led to an increased inhibitory influence of PMv over M1, but when the subject was tested while engaged in a visuomotor task, PMv-M1 stimulation led to an increased facilitatory influence of PMv over M1. Plasticity evolved rapidly, lasted for at least 1 h, and began to reverse 3 h after intervention.

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“…For example, neuroimaging and transcranial magnetic stimulation (TMS) studies have shown that mid-dorsolateral and ventrolateral prefrontal areas (Bunge, 2004;Duncan & Owen, 2000) and the presupplementary motor area (pre-SMA; Buch, Mars, Boorman, & Rushworth, 2010) are activated by tasks that require the selection and inhibition of responses. For instance, Verbruggen, Aron, Stevens, and Chambers (2010) demonstrated that TMS of the right inferior frontal gyrus (IFG) impaired performance on both a stop-signal task and a dual task, suggesting that this region supports both response selection and inhibition processes.…”

mentioning

confidence: 99%

On the relationship between response selection and response inhibition: An individual differences approach

Bender

Filmer

Garner

et al. 2016

Atten Percept Psychophys

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The abilities to select appropriate responses and suppress unwanted actions are key executive functions that enable flexible and goal-directed behavior. However, to date it has been unclear whether these two cognitive operations tap a common action control resource or reflect two distinct processes. In the present study, we used an individual differences approach to examine the underlying relationships across seven paradigms that varied in their response selection and response inhibition requirements: stop-signal, go-no-go, Stroop, flanker, single-response selection, psychological refractory period, and attentional blink tasks. A confirmatory factor analysis suggested that response inhibition and response selection are separable, with stop-signal and go-no-go task performance being related to response inhibition, and performance in the psychological refractory period, Stroop, single-response selection, and attentional blink tasks being related to response selection. These findings provide evidence in support of the hypothesis that response selection and response inhibition reflect two distinct cognitive operations.

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A Network Centered on Ventral Premotor Cortex Exerts Both Facilitatory and Inhibitory Control over Primary Motor Cortex during Action Reprogramming

Cited by 142 publications

References 29 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

Noninvasive Associative Plasticity Induction in a Corticocortical Pathway of the Human Brain

On the relationship between response selection and response inhibition: An individual differences approach

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