Abstract
The goal of the present study was to shed light on the respective contributions of three important action monitoring brain regions (i.e. cingulate cortex, insula, and orbitofrontal cortex) during the conscious detection of response errors. To this end, fourteen healthy adults performed a speeded Go/Nogo task comprising Nogo trials of varying levels of difficulty, designed to elicit aware and unaware errors. Error awareness was indicated by participants with a second key press after the target key press. Meanwhile, electromyogram (EMG) from the response hand was recorded in addition to high-density scalp electroencephalogram (EEG). In the EMG-locked grand averages, aware errors clearly elicited an error-related negativity (ERN) reflecting error detection, and a later error positivity (Pe) reflecting conscious error awareness. However, no Pe was recorded after unaware errors or hits. These results are in line with previous studies suggesting that error awareness is associated with generation of the Pe. Source localisation results confirmed that the posterior cingulate motor area was the main generator of the ERN. However, inverse solution results also point to the involvement of the left posterior insula during the time interval of the Pe, and hence error awareness. Moreover, consecutive to this insular activity, the right orbitofrontal cortex (OFC) was activated in response to aware and unaware errors but not in response to hits, consistent with the implication of this area in the evaluation of the value of an error. These results reveal a precise sequence of activations in these three non-overlapping brain regions following error commission, enabling a progressive differentiation between aware and unaware errors as a function of time elapsed, thanks to the involvement first of interoceptive or proprioceptive processes (left insula), later leading to the detection of a breach in the prepotent response mode (right OFC).
Highlights
Successful task performance entails action monitoring and online adjustment of behaviour
Because we previously found across several studies that a posterior portion of the cingulate cortex was the main source of the error-related negativity (ERN) generated in response to errors using a similar speeded Go/Nogo task [37,38,39,40], we predicted that the generators of the ERN would mainly concern a similar posterior cingulate region, as compared with more anterior dorsal Anterior Cingulate Cortex (dACC) activations found for errors in previous brain-imaging studies [13,58]
An increase in the level of fearfulness of the stimuli corresponded with a linear increase in the subjective ratings of fear level (M: 50% = 9.11, SD = 7.98, M: 75% = 14.91, SD = 6.33, M: 100% = 21.74, SD = 3.07; F(3,11) = 79.62, p,.001), demonstrating that the participants were able to tell apart the level of fear expressed by the stimuli, in agreement with the intensity of fearfulness shown in these blends after morphing
Summary
Successful task performance entails action monitoring and online adjustment of behaviour. In the averaged potential time-locked to the onset of response errors a negativegoing peak is observed at around 0 to 100 ms post-response with a fronto-central scalp distribution, the so-called error-related negativity (ERN) [2] or error negativity (Ne) [3]. The dorsal Anterior Cingulate Cortex (dACC) has been identified as the main neural generator of the ERN [5,13,14,15] This medial frontal structure consisting of a cognitive and an emotional division [16,17] receives dopamine input from the basal ganglia that have an evaluative function and assist in action selection by allocating attention to behaviourally salient events [18]. Several ERP studies have corroborated this assumption and a functional dissociation between the ERN and Pe component during error monitoring [7,19,20,21,22], the underlying brain networks (and their respective temporal properties) supporting this remarkable ability have not been clarified so far
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