Spontaneous pre-stimulus fluctuations in the activity of right fronto-parietal areas influence inhibitory control performance

Camille F Chavan,Michael Mouthon,Aurelie L Manuel,Lucas Spierer

doi:10.3389/fnhum.2013.00238

Camille F Chavan, Michael Mouthon + Show 2 more

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https://doi.org/10.3389/fnhum.2013.00238

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Abstract

Inhibitory control refers to the ability to suppress planned or ongoing cognitive or motor processes. Electrophysiological indices of inhibitory control failure have been found to manifest even before the presentation of the stimuli triggering the inhibition, suggesting that pre-stimulus brain-states modulate inhibition performance. However, previous electrophysiological investigations on the state-dependency of inhibitory control were based on averaged event-related potentials (ERPs), a method eliminating the variability in the ongoing brain activity not time-locked to the event of interest. These studies thus left unresolved whether spontaneous variations in the brain-state immediately preceding unpredictable inhibition-triggering stimuli also influence inhibitory control performance. To address this question, we applied single-trial EEG topographic analyses on the time interval immediately preceding NoGo stimuli in conditions where the responses to NoGo trials were correctly inhibited [correct rejection (CR)] vs. committed [false alarms (FAs)] during an auditory spatial Go/NoGo task. We found a specific configuration of the EEG voltage field manifesting more frequently before correctly inhibited responses to NoGo stimuli than before FAs. There was no evidence for an EEG topography occurring more frequently before FAs than before CR. The visualization of distributed electrical source estimations of the EEG topography preceding successful response inhibition suggested that it resulted from the activity of a right fronto-parietal brain network. Our results suggest that the fluctuations in the ongoing brain activity immediately preceding stimulus presentation contribute to the behavioral outcomes during an inhibitory control task. Our results further suggest that the state-dependency of sensory-cognitive processing might not only concern perceptual processes, but also high-order, top-down inhibitory control mechanisms.

Highlights

Inhibitory control, the ability to suppress planned or ongoing cognitive or motor processes is necessary to ensure flexible and adapted goal-directed behavior in ever-changing environments (Aron, 2007; Dillon and Pizzagalli, 2007)
Converging functional neuroimaging, transcranial magnetic stimulation and lesion data indicate that inhibitory control relies on a cortico-subcortical network involving the right inferior frontal gyrus, the presupplementary motor area (SMA) and the basal ganglia (Garavan et al, 1999; Aron et al, 2003; Chambers et al, 2009; Majid et al, 2012), and manifesting at latencies of 150–400 ms after the onset of the stimuli associated with the inhibition goals (Kaiser et al, 2006; Smith and Douglas, 2011)
Criaud et al (2012) further demonstrated that proactive mechanisms persist once established at the beginning of each trial, suggesting that proactive inhibition has a transient effect and modifies the general response mode of the participants. These findings suggest that inhibitory control performance does not solely depend on how participants manage the conflict induced by the stimulus and on the state of the task-monitoring and control systems before the trial

Summary

Introduction

Inhibitory control, the ability to suppress planned or ongoing cognitive or motor processes is necessary to ensure flexible and adapted goal-directed behavior in ever-changing environments (Aron, 2007; Dillon and Pizzagalli, 2007). Britz and Michel (2010) extended these results by showing that dorsolateral prefrontal cortices were engaged differentially during the 100 ms preceding the stimulus onset in error vs correct trials during a classical color stroop task. These collective results suggest that errors are foreshadowed by a disruption of prefrontal task monitoring systems before the actual need for inhibitory control (see Eichele et al, 2010; Masaki et al, 2012; Steinhauser et al, 2012)

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