Abstract
SummaryA fully adapted behavior requires maximum efficiency to inhibit processes in the motor domain [1]. Although a number of cortical and subcortical brain regions have been implicated, converging evidence suggests that activation of right inferior frontal gyrus (r-IFG) and right presupplementary motor area (r-preSMA) is crucial for successful response inhibition [2, 3]. However, it is still unknown how these prefrontal areas convey the necessary signal to the primary motor cortex (M1), the cortical site where the final motor plan eventually has to be inhibited or executed. On the basis of the widely accepted view that brain oscillations are fundamental for communication between neuronal network elements [4–6], one would predict that the transmission of these inhibitory signals within the prefrontal-central networks (i.e., r-IFG/M1 and/or r-preSMA/M1) is realized in rapid, periodic bursts coinciding with oscillatory brain activity at a distinct frequency. However, the dynamics of corticocortical effective connectivity has never been directly tested on such timescales. By using double-coil transcranial magnetic stimulation (TMS) and electroencephalography (EEG) [7, 8], we assessed instantaneous prefrontal-to-motor cortex connectivity in a Go/NoGo paradigm as a function of delay from (Go/NoGo) cue onset. In NoGo trials only, the effects of a conditioning prefrontal TMS pulse on motor cortex excitability cycled at beta frequency, coinciding with a frontocentral beta signature in EEG. This establishes, for the first time, a tight link between effective cortical connectivity and related cortical oscillatory activity, leading to the conclusion that endogenous (top-down) inhibitory motor signals are transmitted in beta bursts in large-scale cortical networks for inhibitory motor control.
Highlights
Area/left primary motor cortex (r-preSMA/l-M1) connections was tested in healthy volunteers by double-coil transcranial magnetic stimulation (TMS) during the early response period of a simple visually cued Go/NoGo task (Figures 1A and 1B)
We administered a conditioning stimulus (CS) over one of these right prefrontal areas followed by a test stimulus (TS) over left M1, always using a fixed CS-TS interstimulus interval of 6 ms [9, 10] (Figure 1A), but varying the delays of paired CS-TS TMS administration from the onset of the imperative (Go/NoGo) movement cue to probe for fluctuations of effective connectivity in these prefrontal/M1 networks over time (Figure 1B) during the execution of a Go/NoGo task [11]
We used motor-evoked potentials (MEPs) recorded from the first dorsal interosseus muscle of the right hand as dependent measure to verify the causal influence of conditioning pulses applied over either right inferior frontal gyrus (r-IFG) or r-preSMA
Summary
A fully adapted behavior requires maximum efficiency to inhibit processes in the motor domain [1]. A number of cortical and subcortical brain regions have been implicated, converging evidence suggests that activation of right inferior frontal gyrus (r-IFG) and right presupplementary motor area (r-preSMA) is crucial for successful response inhibition [2, 3] It is still unknown how these prefrontal areas convey the necessary signal to the primary motor cortex (M1), the cortical site where the final motor plan eventually has to be inhibited or executed. In NoGo trials only, the effects of a conditioning prefrontal TMS pulse on motor cortex excitability cycled at beta frequency, coinciding with a frontocentral beta signature in EEG This establishes, for the first time, a tight link between effective cortical connectivity and related cortical oscillatory activity, leading to the conclusion that endogenous (top-down) inhibitory motor signals are transmitted in beta bursts in large-scale cortical networks for inhibitory motor control
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