Cascade of neural events leading from error commission to subsequent awareness revealed using EEG source imaging

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).

Figure 1. Trial presentation.

The example shows a cue followed by a Nogo stimulus. In the event of an error, a period of 1500 ms is allowed for subsequent error verification.

Figure 2. Subjective ratings.

Results of the control behavioural study show that participants were on average less certain of errors in the difficult than in the intermediate condition. Interestingly, ratings in the difficult condition suggest a bias towards the (right-end) error side, as if participants somehow “felt” they had committed an error in this condition. Importantly, participants were also quite certain of their correct responses on Go trials. Horizontal bars represent the S.E.M.

Figure 3. EMG-locked grand averages and global field power.

(A) The EMG-locked grand averages displaying the mean amplitude at FCz for aware errors (red), unaware errors (blue), and hits (green) as a function of time. (B) The global field power for aware errors revealed 3 peaks corresponding with the timing of the ERN, Pe, and a later peak around the time of error verification (at roughly 100, 300, and 670 ms). Corresponding horizontal voltage topographic maps are presented (C). For the Pe, the topography of the early (310 ms) and late phase (330 ms) are shown.

Figure 4. sLORETA sources in the PCMA, insula and OFC.

(A) The sLORETA source reconstruction in bin 1 (94–114 ms; ERN/CRN time-interval) showing the PCMA ROI (B) bin 2 (312–332 ms; Pe time-interval) depicting activation of the insular cortex, and (C) displaying the OFC activation in bin 3 (660–680 ms). Corresponding graphs depict the mean amplitude in each of the four seeds per ROI for hits (green), unaware errors (blue), and aware errors (red), vertical bars corresponding to the S.E.M. * indicates a p<.05 statistical difference; **p<.01. lPCMA  =  left posterior cingulate motor area (x = −15, y = −25, z = 45), rPCMA  =  right posterior cingulate motor area (x = 15, y = −25, z = 45), l.antIns  =  left anterior insula (x = −35, y = −10, z = 15), r.antIns  =  right anterior insula (x = 35, y = −10, z = 15), l.postIns  =  left posterior insula (x = −30, y = −25, z = 15), r.postIns  =  right posterior insula (x = 30, y = −25, z = 15), lOFC1  =  left orbitofrontal cortex (x = −25, y = 35, z = −25), rOFC1  =  right orbitofrontal cortex (x = 25, y = 35, z = −25), lOFC2 (x = −20, y = 35, z = −25), and rOFC2 (x = 20, y = 35, z = −25).

Figure 5. Time-course of activation.

Mean amplitude (mV) is shown for aware (solid lines) and unaware (dotted lines) errors, separately for each of the three main ROIs. (A) left PCMA; (B) left posterior insula, and (C) right OFC. Note the increase in amplitude difference between aware and unaware errors from PCMA to insula to OFC.