Journal Article

Roles for the pre-supplementary motor area and the right inferior frontal gyrus in stopping action: Electrophysiological responses and functional and structural connectivity

Tandon, Nitin, Swann, Nicole C., Claffey, Michael P., George, Jobi S., Pieters, Thomas A., Aron, Adam R., Cai, Weidong, Conner, Christopher R.

2012

Overview

Both the pre-supplementary motor area (preSMA) and the right inferior frontal gyrus (rIFG) are important for stopping action outright. These regions are also engaged when preparing to stop. We aimed to elucidate the roles of these regions by harnessing the high spatio-temporal resolution of electrocorticography (ECoG), and by using a task that engages both preparing to stop and stopping outright. First, we validated the task using fMRI in 16 healthy control participants to confirm that both the preSMA and the rIFG were active. Next, we studied a rare patient with intracranial grid coverage of both these regions, using macrostimulation, diffusion tractography, cortico-cortical evoked potentials (CCEPs) and task-based ECoG. Macrostimulation of the preSMA induced behavioral motor arrest. Diffusion tractography revealed a structural connection between the preSMA and rIFG. CCEP analysis showed that stimulation of the preSMA evoked strong local field potentials within 30ms in rIFG. During the task, when preparing to stop, there was increased high gamma amplitude (~70–250Hz) in both regions, with preSMA preceding rIFG by ~750ms. For outright stopping there was also a high gamma amplitude increase in both regions, again with preSMA preceding rIFG. Further, at the time of stopping, there was an increase in beta band activity (~16Hz) in both regions, with significantly stronger inter-regional coherence for successful vs. unsuccessful stop trials. The results complement earlier reports of a structural/functional action control network between the preSMA and rIFG. They go further by revealing between-region timing differences in the high gamma band when preparing to stop and stopping outright. They also reveal strong between-region coherence in the beta band when stopping is successful. Implications for theories of action control are discussed. ► We used fMRI in healthy adults and multiple methods in a single epilepsy patient. ► We studied the presupplementary motor area and right inferior frontal gyrus. ► The preSMA and rIFG are structurally and functionally connected. ► Gamma activity in preSMA occurs before rIFG in anticipation of action control. ► Beta-band coherence between preSMA and rIFG occurs during action control.

• Publisher: Elsevier Inc,Elsevier Limited
• Subject: Adolescent / Adult / Algorithms / Beta frequency band / Beta Rhythm - physiology / Cognitive control / Cues / Data Interpretation, Statistical / Diffusion Tensor Imaging / Electric Stimulation / Electrocorticography / Electrodes / Electrodes, Implanted / Electroencephalography / Epilepsy - psychology / Epilepsy - surgery / Evoked Potentials - physiology / Female / Frontal Lobe - physiology / Functional MRI / Gamma frequency band / Humans / Image Processing, Computer-Assisted / Inhibitory control / Magnetic Resonance Imaging / Male / Motor Cortex - physiology / Neural Pathways - physiology / Oxygen - blood / Photic Stimulation / Psychomotor Performance - physiology / Reaction Time - physiology / Stop signal task / Young Adult