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

Abstract

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,...

Posterior Medial Frontal Cortex Activity Predicts Post-Error Adaptations in Task-Related Visual and Motor Areas

“…Whereas previous evidence for a relationship between pMFC activity and PES (Gehring et al, 1993;Garavan et al, 2002;Kerns et al, 2004;Debener et al, 2005;di Pellegrino et al, 2007) did not speak to the specific role of the motor system in this adjustment, our finding of reduced post-error motor activity is in line with recent evidence (Marco-Pallares et al, 2008;King et al, 2010) suggesting motor inhibition as a mechanism underlying PES. Consistent with this, transcranial magnetic stimulation (TMS) studies have recently demonstrated that the pre-SMA can modulate M1 activity in conflicting situations and thus influence corticospinal excitability (Mars et al, 2009;Neubert et al, 2010). This corroborates our result showing that pMFC activity predicts the strengths of motor activity following errors, i.e., stronger pMFC activity leads to less motor activity in the post-error trial.…”

State-Dependent and Timing-Dependent Bidirectional Associative Plasticity in the Human SMA-M1 Network

“…3B). Recent paired-coil TMS studies demonstrated effective connectivity between pre-SMA and M1 via corticocortical and cortical-subcortical routes (Mars et al, 2009;Neubert et al, 2010), but these effects were specifically dependent on motor tasks requiring action reprogramming and for this reason are not at variance with the present results obtained at rest.…”

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

“…Additionally, little is known about potential role of other areas of the frontal lobe that might be involved in these post-error adjustments. Neubert et al (2010) reported evidences of the contribution of the inferior frontal gyrus as well as other non-primary areas of the motor system such the pre-supplementary motor area (pre-SMA) and the premotor cortex of the ipsilateral hemisphere in task switching and motor inhibition that might be also be implicated in the modulation of the excitability of the corticospinal system. Furthermore, other areas outside the frontal lobe, such as the intra-parietal sulcus implicated in sensory visual feedback and integration (Gre´a et al, 2002;Wolynski et al, 2009), might project to the DLPFC in the frontal lobe and ultimately to premotor and motor systems.…”