# Action Monitoring and Medial Frontal Cortex: Leading Role of Supplementary Motor Area

Francesca Bonini, Borís Burle, Catherine Liégeois-Chauvel, Jean Régis,

Patrick Chauvel, Franck Vidal

► To cite this version:

Francesca Bonini, Borís Burle, Catherine Liégeois-Chauvel, Jean Régis, Patrick Chauvel, et al.. Action Monitoring and Medial Frontal Cortex: Leading Role of Supplementary Motor Area. Science, 2014, 343 (6173), pp.888-891. 10.1126/science.1247412. hal-01384045

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# Action Monitoring and Medial Frontal Cortex: Leading Role of Supplementary Motor Area

Francesca Bonini,<fnref n="1" />,²,³,⁴* Boris Burle,<fnref n="1" />,³ Catherine Liégeois-Chauvel,<fnref n="1" />,² Jean Régis,<fnref n="1" />,²,⁴ Patrick Chauvel,<fnref n="1" />,²,⁴ Franck Vidal<fnref n="1" />,³

The capacity to evaluate the outcomes of our actions is fundamental for adapting and optimizing behavior and depends on an action-monitoring system that assesses ongoing actions and detects errors. The neuronal network underlying this executive function, classically attributed to the rostral cingulate zone, is poorly characterized in humans, owing to the limited number of direct neurophysiological data. Using intracerebral recordings, we show that the leading role is played by the supplementary motor area (SMA), which rapidly evaluates successful and erroneous actions. The rostral part of medial prefrontal cortex, driven by the SMA, was activated later and exclusively in the case of errors. This suggests a hierarchical organization of the different frontal regions involved in implementation of action monitoring and error processing.

I imagine a tennis player when serving. If the ball lands out, the subsequent serve is more likely to succeed. The required behavioral adjustments are subordinated to an error identification

process. Even during a successful first serve, the player may have tossed the ball too high, requiring a prompt adjustment of serving action. Such remedial actions rely on the existence of an

action monitoring system in charge of evaluating ongoing activities to adjust them and improve subsequent actions.

Studies in monkeys and humans have demonstrated the critical role of the medial frontal cortex (MFC) in such an evaluative process (1, 3). A particular subregion within the MFC, the rostral cingulate zone (RCZ) (4), is often considered the crucial node in this control network (1).

We investigated the anatomical substrate of action monitoring in humans in more detail using intracerebral electroencephalography (iEEG). Five subjects (5), undergoing presurgical evaluation of their epilepsy with iEEG, performed a Simon task (6). In this conflict task, different classes of behaviorally relevant responses can be distinguished by means of electromyography (EMG):

<footnote n="1">¹Aix Marseille Université, 13385, Marseille, France. ²INSERM, Institut de Neurosciences des Systèmes UMR 1106, 13385, Marseille, France. ³CNRS, Laboratoire de Neurosciences Cognitives, UMR 7291, 13331, Marseille, France. ⁴APHM (Assistance Publique Hôpitaux de Marseille), Pôle de Neurosciences Cliniques, Timone Hospital, 13005, Marseille, France.</footnote>

<footnote>*Corresponding author. E mail: francesca.bonini@univ amu.fr</footnote>
correct responses, overt errors, and covert errors (7) (Fig. 1 and supplementary materials). If we consider our initial analogy of the tennis player, overt errors represent a missed serve, whereas covert errors [often termed partial errors (8)] represent the ongoing serve's successful adjustment.

Local field potentials (LFPs) were recorded from 562 contacts on 42 electrodes positioned predominantly in the frontal cortex (Fig. 2 and table S1). LFPs were averaged time locked to subjects' responses (as recorded by the EMG of the

responding muscle; see Fig. 1B), so as to evaluate action monitoring activity (behavioral results are presented in the supplementary materials and fig. S1).

Error evoked LFPs were observed exclusive ly in the medial part of the frontal lobe. One set of electrodes clustered caudally, whereas other elec trodes were more dispersed rostrally (Fig. 2, col ored dots, and table S2).

In the caudal cluster, all subjects presented a sharp LFP, peaking between 100 and 190 ms af

ter EMG activation. The largest LFPs occurred after overt errors; smaller LFPs appeared after covert errors; and even smaller, but clearly still present, LFPs occurred after correct responses (Fig. 2 and table S3). This pattern replicates pre vious scalp EEG data (9, 11). Inspection of in dividual electrode placement showed that none of these active electrodes were positioned with in the RCZ, but all were clearly located within the SMA namely, above the calloso marginal fissure and immediately posterior to the vertical commissure anterior (VCA) boundary (Fig. 2).

Although intracerebral electrodes are sensitive to current within only a small volume of cerebral tissue, it is possible that the recorded activity may have been volume conducted from a remote gen erator outside the SMA. However, supplemen tary results (note S2 and figs. S2 and S3) exclude this possibility.

Other electrodes disclosing performance sensitive activity were located more rostrally, in the medial prefrontal region namely, in pregenual anterior cingulate cortex (pACC; i.e., in the an terior division of the RCZ) in patient 3 and in orbito medial prefrontal cortex (OMPFC) in pa tients 3 and 5 (Fig. 3, B and D, and table S2). The activation profile of those more rostral electrodes differed from that of the caudal cluster in three ways (Fig. 3, A and C, fig. S8, and table S3): (i) The prefrontal activity was delayed and had a longer duration, with a caudo rostral latency gradient; (ii) it was specific to errors (overt and covert); and (iii) it was more widespread than the activity within the SMA, as demonstrated by recordings from electrodes' lateral contacts.

<figure><img src="image_2.png" /><figcaption>**Fig. 1.** Experimental procedure. (A) The Simon task is a between-hand choice reaction time task that induces errors: Subjects had to respond with a left or right thumb key-press as a function of the color of a target stimulus. The target could be presented on the same side as the response to be given (congruent trials), or on the opposite side (incongruent trials). (B) Covert errors (often called partial errors) are characterized by a small subthreshold EMG burst on the incorrect side preceding the correct response.</figcaption></figure>

**Fig. 2.** Overview of EMG-locked LFPs and of all recording sites in the medial wall. A total of 562 contacts from 42 electrodes were included in the analysis, 34 of which were implanted up against the medial wall. The anatomical location of these 34 electrodes' internal contacts, converted into normalized MNI (Montreal Neurological Institute) brain space to allow comparison across subjects, is shown on a three-dimensional MNI standard brain in its medial aspect. The two red vertical bars represent the VCA (vertical commissure anterior) line and the VCP (vertical commissure posterior) line. A cluster of performance-sensitive electrodes (colored dots) is located in the SMA (caudal cluster, behind the VCA line), while other electrodes are more widespread in the rostral part of the medial prefrontal cortex (electrodes anterior to VCA). For each participant, averaged EMG-locked LFPs recorded from the SMA are displayed: The largest LFP occurs after overt errors (blue); a smaller LFP appears after covert errors (red); and an even smaller LFP occurs after correct responses (black). Colored bands represent between-trials confidence intervals set to 0.05. For each subject, an individual MRI and computed tomography (CT) fusion is provided, showing, in coronal view, the trajectory of the performance-sensitive electrode. All these electrodes were clearly located above the calloso-marginal fissure and behind the VCA line (that is, in the SMA).

<figure><img src="image_3.png" /></figure>
We further investigated the relation between rostral and caudal activity using trial by trial analysis (fig. S4 and note S3). Single trial LFPs recorded in the SMA and in the medial prefrontal regions were significantly and positively correlated both in terms of latencies [p 0.8, P < 0.01 between SMA and pACC on patient 3, and p 0.35, P < 0.05 between SMA and OMPFC on patient 5 (12)] and, less strongly, amplitudes (p 0.63, P < 0.01 and p 0.28, P < 0.1, for patient 3 and 5 respectively; fig. S5). Medial prefrontal activity appeared to be contingent upon activity in the SMA because it was always preceded by SMA activity, and importantly, it was never present when SMA activity was absent. By contrast, SMA activity can and occasionally did occur without the subsequent prefrontal activity. This suggests a strong connection and potential hierarchy between these two regions in error processing. Such a connection is not necessarily direct and might be mediated by a third structure.

To further describe the functional importance of the SMA activity, we focused on covert errors. These trials are a prototypical case of efficient on going action control because the incorrect action is interrupted and corrected (by the opposite “corrective” response). We therefore searched for a functional link between SMA activity and error correction (fig. S6 and note S4).

We correlated the latencies of LFPs and EMG activity in three patients for whom covert error LFPs were detectable in the SMA on a trial by trial basis. The offset of EMG bursts linked to incorrect responses, representing response interruption, strongly correlated with the peak of the SMA LFP (p 0.63 P < 0.01), whereas the onset of EMG bursts linked to corrective responses strongly correlated with the end of the SMA LFP (p 0.7, P < 0.01) (fig. S7 and note S4).

In covert errors, SMA activity began with the first incorrect muscular activation, culminated when this incorrect action was inhibited, decreased, and finally extinguished when the subsequent corrective response was issued. This correlation, consistent with previous scalp EEG data (13), suggests that the SMA intervenes in action monitoring by emitting a performance modulated “default” signal that possibly acts as an alert or a warning signal. Each time a behaviorally relevant response is produced, this default signal is emitted. For correct responses, it is rapidly subdued, giving rise to a small LFP. For covert errors, the warning signal keeps rising but begins to decrease once the incorrect action is inhibited and terminates with the activation of the corrective response. A slightly later suppression and correction would result in a prolonged alarm; that is, a longer and larger LFP. For overt errors, this alarm reaches its highest level, corresponding to the highest LFP’s amplitude. We thus hypothesize that this alarm, when crossing a given threshold, hints at the need to enhance cognitive control.

This study shows that action monitoring is largely carried out by the SMA. This is consistent with limited data reported in humans (11, 14 18)

and in monkeys (19, 20). However, much of the current literature indicates that human primate and nonprimate RCZ is sensitive to action outcome (14, 15, 17, 18, 21 25).

Even though the precise role of the RCZ vis à vis the SMA should be further evaluated with more extensive sampling, our data allow discussion of the apparent inconsistency in the literature from a new perspective. Functional magnetic resonance imaging (fMRI) data (contrasting errors minus correct responses) mainly show RCZ activity (1). By comparison, we showed a caudo rostral latency gradient in medial frontal areas. On this basis one may expect RCZ to be active only for erroneous action, shortly after SMA, but the extent to which RCZ activity depends on SMA remains an open question. However, our results suggest a schema of how this cognitive control function operates, and of its underlying cortical network. We propose that this network, encompassing caudal and rostral parts of the MFC, is hierarchically organized to implement action control: medial prefrontal cortex, including the anterior RCZ, is engaged in the case of

erroneous actions and thus, as usually assumed, is implicated in error processing following a caudo rostral gradient. The role of the most rostral activities remains to be elucidated, but it could be related to the estimated (negative) value of errors (26). However, this process seems to be embedded in an action monitoring process, which is carried out by the SMA. The SMA is therefore a core node in performance monitoring, whose function consists of continuously assessing on going actions and, in the case of errors only, recruiting the medial prefrontal cortex.

Action monitoring and error processing are thus two crucial stages of executive control in humans, allowing for efficient behavioral adjustment and optimization of performance. The involvement of the SMA in action monitoring appears functionally grounded, because the SMA is widely considered to be implicated in movement initiation and inhibition (27), response selection, and motor planning (28). The present study reveals a new function for SMA: the early evaluation of the outcome of actions that it has contributed to initiating.

<figure><img src="image_4.png" /><figcaption>**Fig. 3.** Medial prefrontal LFPs evoked by erroneous activations. (A) Averaged LFPs evoked by overt errors peaking at 260 ms in pACC (top) and at 295 ms in OMPFC (bottom) in subject 3. (B) Individual reconstruction of subject 3's prefrontal electrodes based on an MRI-CT fusion scan in axial and sagittal view (note also the overlying electrode placed in the SMA). (C) Averaged LFPs peaking at 355 ms evoked by covert and overt errors in subject 5. (D) Individual reconstruction of subject 5's prefrontal electrode based on an MRI-CT fusion scan in axial and sagittal view.</figcaption></figure>
References and Notes

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5. A sixth subject was not included (see note S1).

6. J. R. Simon, in *Stimulus Response Compatibility: An Integrated Perspective* (R. W. Proctor, T. G. Reeve, Eds. (North Holland, Amsterdam, 1990), pp. 31 86.

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11. C. Roger, C. G. Bénar, F. Vidal, T. Hasbroucq, B. Burle, *Neuroimage* **51**, 391 403 (2010).

12. Although the averaged activity in OMPFC in patient 3 was larger than activity in pACC, its signal/noise ratio was too low to reliably detect single trial activity on a sufficient number of trials for analysis.

13. B. Burle, C. Roger, S. Allain, F. Vidal, T. Hasbroucq, *J. Cogn. Neurosci.* **20**, 1637 1655 (2008).

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**Acknowledgments:** We thank P. Marquis for technical help in acquiring intracerebral recordings; D. Schön for critical discussion and reading the manuscript; and R. Hewett, M. Woodman, and J. Coull for English revision. B.B. was supported by the European Research Council under the European Community's Seventh Framework Program (FP7/2007 2013 Grant Agreement no. 241077). F.B. was supported by the Ecole Doctorale Science de la Vie et de la Santé, Aix Marseille Université. F.V. and B.B. designed the study. F.B. administered the Simon task and obtained intracerebral recordings. J.R. performed the surgical procedure and provided coordinates of intracerebral electrodes. F.B. analyzed data. B.B. and F.B. performed statistical analysis. F.V., B.B., F.B., P.C., and C.L. C. interpreted data and discussed results. F.B. and F.V. wrote the manuscript. All authors commented on and edited the manuscript. The authors declare no conflict of interest.
Supplementary Materials for

**Action Monitoring and Medial Frontal Cortex: Leading Role of
Supplementary Motor Area**

Francesca Bonini,* Boris Burle, Catherine Liégeois-Chauvel, Jean Régis, Patrick
Chauvel, Franck Vidal

*Corresponding author. E-mail: francesca.bonini@univ-amu.fr

**This PDF file includes:**

Materials and Methods

Supplementary Text

Figs. S1 to S8

Tables S1 to S3

References
# SUPPLEMENTARY MATERIAL

1) Material and Methods

2) Table S1, S2, S3

3) Behavioral Results

4) Note S1, S2, S3, S4

5) Figures S1, S2, S3, S4, S5, S6, S7, S8

## Material and Methods

Five human subjects (3 females, 2 males, mean age 23 ± 7.3) undergoing presurgical evaluation of drug-resistant epilepsy participated in this study because their implantation included electrodes in the medial frontal cortex. They all gave their informed consent prior to their participation. This study was approved by the Institutional Review Board of the French Institute of Health.

Intracerebral multiple contacts electrodes (10 to 15 contacts, length: 2 mm, diameter: 0.8 mm, 1.5 mm apart) were implanted using a stereotactic method (29). The precise anatomical position of electrode contacts was determined on individual MRIs through the superposition of anatomical MRI and computed tomography scan showing electrodes and based on anatomical landmarks as defined in the literature (30). The coordinates of active electrodes were converted from individual Talairach space to normalized Talairach space to allow comparison of electrode positions (see Table S2). Normalized MNI coordinates were obtained in order to visualize all patients' electrodes on a Montreal Neurological Institute (MNI) template (Fig. 2).

Patients were seated in a Faraday cage and stimuli were presented on a display monitor placed 70 cm from patient's eyes with an angular size of 1.26°. Patients had to respond with a right or left thumb keypress as fast as possible as a function of the color (red or green) of a target stimulus (Fig. 1). Stimulus could appear in a left or right location which was, however, irrelevant to the task. A trial began with a white fixation cross in the centre of the screen followed 500 msec later by the target stimulus. Participants had to respond within 1000 msec. If they did not respond, the stimulus disappeared and the white fixation cross of the next trial appeared on the screen. Every block contained 64 trials and every
patient performed a training block plus 8 to 11 experimental blocks. Three patients had to respond to a green stimulus by pressing the right key, whilst two patients performed the opposite stimulus-response mapping (i.e. responded to a red stimulus by pressing the right key).

IEEG signals and EMG activity (recorded from *flexor pollicis brevis* of each hand by paired surface electrodes) were acquired with a sampling frequency of 1000 Hz and an acquisition band-pass filter between 0.1 and 200 Hz.

EEG and EMG signals were processed off-line. EMG traces were inspected visually, and the onset and offset of EMG activity were marked manually. Visual inspection is thought to be the most accurate technique, as opposed to automated algorithms (31). Event-related LFPs were averaged time-locked to EMG onset for three categories of trials: correct trials; overt error trials; and covert error trials. Covert error trials were defined by the presence of an incorrect EMG burst without any mechanical response, followed by the correct EMG burst and the correct mechanical response. Statistics were performed on individual subject data by calculating the between-trials confidence intervals with probability set to 0.05. Differences between conditions were considered significant when their confidence interval did not overlap.
<table><thead><tr><th>Subject</th><th>Sex</th><th>Age</th><th>Hand laterality</th><th>SEEG side</th><th>Epileptogenic zone</th><th>Electrodes</th><th>N°overt and covert errors*</th></tr></thead><tbody><tr><td>1</td><td>F</td><td>32</td><td>R</td><td>L</td><td>Rolandic</td><td>SC', SA', CC', PM', L', LI'</td><td>28/99</td></tr><tr><td>2</td><td>M</td><td>17</td><td>L</td><td>L</td><td>Temporal</td><td>SA', SA', LP', CR', OF', PA', OT', GLP', GPH', TP'</td><td>0/33</td></tr><tr><td>3</td><td>F</td><td>22</td><td>L</td><td>L</td><td>Not defined</td><td>SA', L', OF', CR', OR', A', GPH', TB', TP'</td><td>27/46</td></tr><tr><td>4</td><td>F</td><td>15</td><td>R</td><td>R</td><td>Insular</td><td>SA, PM, LP, CP, I, OR', H, OP, OF, FT, CCZ, A</td><td>16/80</td></tr><tr><td>5</td><td>M</td><td>29</td><td>L</td><td>R/L</td><td>Right Pre-frontal</td><td>SA, SA', PM, PM', CCZ', R, FP, OR, TP, OF'</td><td>75/29</td></tr></tbody></table>

**Table S1. General characteristics of subjects and of electrode implantation.** Forty seven depth multicontact electrodes were recorded across all patients, 22 of which were located within the frontal lobe, with a total of 628 contacts (42/47 electrodes and 562/628 contacts were included in the analysis as they were located in healthy cerebral tissue). SA: SMA, PM: pre-SMA, OF: Insula/frontal operculum, A: Amygdala, CR: anterior division of the RCZ, OR: orbito-medial prefrontal cortex, CC: posterior division of the RCZ, CCZ: caudal cingulate zone, R: rostral inferior frontal gyrus, FP: frontal pole, TP: temporal pole, GPH: para-hyppocampal gyrus, TB: temporo-basal region, LP: para-central lobulus, PA: superior parietal lobulus, OP: parietal operculum, H: Heschl's gyrus, CU: Cuneus, FCA: anterior calcarine fissure, C: hippocampus's tail, CP: posterior cingulate gyrus, FT: pars triangularis of inferior frontal gyrus, GLP: posterior lingual gyrus, OT: fusiform gyrus, L: lesion, LI: lesion. Electrodes followed by the apostrophe are located in left hemisphere. *Here we report the number of errors/partial errors committed. The number of errors and partial errors actually analyzed were sometimes lower because of rejection of segments with artifacts (cfr main text for number of analyzed segments containing errors).
<table><caption>**Table S2. Electrophysiological data.** Normalized Talairach coordinates for those electrode contacts exhibiting an LFP. SMA: Supplementary motor area; pACC: pre-genual anterior cingulate cortex; OMPFC: orbito-medial prefrontal cortex</caption><thead><tr><th rowspan="2">Subject</th><th rowspan="2">Anatomical location</th><th colspan="3">Talairach coordinates</th></tr><tr><th>x</th><th>y</th><th>z</th></tr></thead><tbody><tr><td>1</td><td>SMA</td><td>-11.1</td><td>-21.6</td><td>43.4</td></tr><tr><td>2</td><td>SMA</td><td>-9.2</td><td>-16.7</td><td>53.3</td></tr><tr><td></td><td>SMA (rostral part)</td><td>-7</td><td>-2.4</td><td>43.2</td></tr><tr><td>3</td><td>SMA</td><td>-9.3</td><td>-2.1</td><td>50.2</td></tr><tr><td></td><td>pACC</td><td>-7.5</td><td>41.4</td><td>-4.8</td></tr><tr><td></td><td>OMPFC</td><td>-24.2</td><td>18.2</td><td>-9.6</td></tr><tr><td>4</td><td>SMA</td><td>4.7</td><td>-8.2</td><td>48.6</td></tr><tr><td>5</td><td>SMA</td><td>-12.7</td><td>-9</td><td>48.6</td></tr><tr><td></td><td>OMPFC</td><td>3.9</td><td>29.8</td><td>-12.5</td></tr></tbody></table>

<table><caption>**Table S3. Latency and amplitude of averaged LFP for each trial type for each subject**</caption><thead><tr><th>Subject</th><th>Latency (ms)<br>Amplitude (µV)<br>of SMA LFP for<br>correct<br>responses</th><th>Latency (ms)<br>Amplitude (µV)<br>of SMA LFP for<br>correct errors</th><th>Latency (ms)<br>Amplitude (µV)<br>of SMA LFP for<br>correct errors</th><th>Latency (ms)<br>Amplitude (µV)<br>of MPFC LFP for<br>correct errors</th><th>Latency (ms)<br>Amplitude (µV)<br>of MPFC LFP for<br>correct errors</th></tr></thead><tbody><tr><td>1</td><td>85 ms<br>35 µV</td><td>73 ms<br>51 µV</td><td>100 ms<br>125 µV</td><td></td><td></td></tr><tr><td>2</td><td>70 ms<br>28 µV</td><td>100 ms<br>158 µV</td><td></td><td></td><td></td></tr><tr><td>3</td><td>120 ms<br>25 µV</td><td>105 ms<br>50 µV</td><td>135 ms<br>130 µV</td><td>260 ms (pACC)<br>295 ms (OMPFC)<br>48 µV (pACC)<br>77µV (OMPFC)</td><td></td></tr><tr><td>4</td><td>170 ms<br>26 µV</td><td>150 ms<br>31 µV</td><td>190 ms<br>55 µV</td><td></td><td></td></tr><tr><td>5</td><td>125 ms<br>20 µV</td><td>82 ms<br>50 µV</td><td>125 ms<br>70 µV</td><td>110 ms<br>70 µV</td><td>355 ms<br>56 µV</td></tr></tbody></table>
## Behavioral results

Behavioral data show a typical pattern with higher error rates on incongruent trials (8%) and lower on congruent trials (4.9%). Similarly, the covert error rate was 6.9% on congruent trials and 12.1% on incongruent trials. Correspondingly in all subjects, despite the small population, the correct trials RT was significantly longer for incongruent (492 ms) than for congruent conditions (463 ms) (unilateral Wilcoxon test, *T* =: *p* = 0.028), that is, the congruency effect was present in all subjects.

A RT distribution analysis was carried out using the “Vincent averaging technique” (32). To perform these analyses, we binned the RT distribution in ten classes of equal size (same number of trials). We computed the mean RT and the percentage of correct responses for each class in each condition (congruent and incongruent). Means of each class were then averaged across subjects. This analysis revealed a large drop in performance for fast responses in incongruent conditions (Fig. S1A), indicating that the stimulus, although irrelevant for the task at hand, tend to automatically activate the ipsilateral response (30, 33). From the vincentized distributions of correct trials, the size of the congruency effect (Incongruent minus Congruent) was estimated for each class. This allowed the estimation of the evolution of the congruency effect (also called “delta plots”) to be plotted as a function of reaction time. As shown in Fig. S1B the congruency effect decreases as reaction time increases, as consistently reported in the literature. This has been interpreted as reflecting the engagement of an active top-down suppression of the automatically activated response (34, 35). This process takes time to build-up during the course of a trial and is, therefore, most effective for slow responses, hence reducing the size of the Simon effect for those slow responses.

Thus RT and error rate patterns indicated that subjects in the present study behaved as healthy subjects in this task.
## Note S1

It should be noted that a sixth subject, a 20 year old left-handed female having electrodes implanted in the medial frontal cortex (one of which was in the caudal part of the SMA and another in the posterior part of the RCZ) performed the Simon task. This subject was not included in the study because iEEG data analysis revealed no EMG-locked LFPs evoked by errors, whether partial or complete, in any of the implanted electrodes. Nevertheless EMG-locked LFPs could be observed on correct responses exclusively in the SMA. In this subject, two surface electrodes were available, allowing a bipolar derivation between Cz and Fz to be obtained. In these surface recordings, EMG-locked ERPs could be observed on correct trials with a time course comparable to that obtained from SMA, but no evoked activity could be observed for either overt or covert errors. The latency of the correct response EMG-locked LFPs was 65 ms, and its amplitude 16 µV. A total of 10 electrodes were implanted in the right hemisphere, exploring SMA, posterior RCZ, Insula, parietal operculum, superior parietal lobulus, Heschl's gyrus, Cuneus, anterior calcarine fissure, posterior hippocampus. This subject committed 31 errors and 77 partial errors.

## Note S2

Although intracerebral electrodes are sensitive to current within only a small volume of cerebral tissue, it is possible that the recorded activity may have been volume conducted from a remote generator outside the SMA. However three findings exclude this possibility: firstly, LFP amplitude decreased sharply over a short distance in a direction leading away from the medial (SMA) and towards the lateral contacts, suggesting a local source (Fig. S2A); secondly, in one patient with two active electrodes within the SMA, the characteristics of the LFPs (namely polarity inversion) indicated a local generator between the two electrodes, i.e. within the SMA (Fig. S2B,C); and lastly, one patient provided a valuable experimental condition in which electrodes were implanted in both the SMA and in neighboring areas including the posterior division of the RCZ.
This subject (n° 1) had two electrodes in the SMA (electrodes SC and SA), one in the posterior RCZ (RCZp, electrode CC) and another one situated rostral to the VAC boundary and above the calloso-marginal fissure (electrode PM) (Fig S3, left panel). A triphasic high-amplitude performance-sensitive response was recorded from anterior and posterior parts of SMA (respectively electrode SA and SC), with voltage sharply decreasing from medial to lateral contacts (Fig S3, right panel). No EMG-locked LFP was detectable in the recording site anterior to the VCA boundary, either for correct responses, or for overt or covert errors. This indicates that the activity recorded in SMA does not arise from a more anterior region. Moreover the amplitude of LFPs in the electrode located in the RCZp was clearly weaker with respect to SMA's activity and did not show any abrupt decrease from medial to lateral contacts, indicating that the recorded activity arose from a remote source i.e. the SMA.

## Note S3

In two subjects (subject 3 and 5), the overt error-evoked LFP was detectable on a trial-by-trial basis (Fig. S3). In subject 3 this activity was visible in 21/24 trials and showed the same morphology as the averaged potential, appearing as a phasic activity without any clear oscillatory component. This single trial LFP varied in amplitude from 92 to 414 µV, and it peaked at 100 to 413 ms from EMG onset (this last LFP being related to a longer EMG burst with delayed mechanical response). In subject 5 the error-evoked LFP was clearly identifiable on 64/72 trials in electrode contacts placed in the SMA. As for subject 3, morphology, amplitude (54 to 230 µV) and latency (peaking at 66 to 191 ms from EMG onset) of this single trial evoked LFP was comparable to those of the averaged potential. Similarly to patient 3, this single trial LFP manifests as phasic activity and does not show any clear oscillation.
Note S4

Correlation between the latencies of LFPs and EMG activity during covert error trials

LFPs evoked by covert errors were detectable on a trial-by trial basis in three subjects (subjects 2, 3 and 5), allowing for correlations between the latency of the LFP and the EMG activity.

We extracted latencies of SMA activity (represented by the onset, peak and end of the LFP of SMA), response interruption (represented by the offset of an incorrect EMG burst) and covert error correction (represented by the onset of the corrective EMG burst) (Fig. S6).

ERP peak was determined by the visual identification of polarity change in the evoked potential (Fig. S6), while LFP onset and end could be identified by slope change at the beginning and respectively at the end of the evoked activity.

We found that the peak of the LFP (36) strongly correlated with the offset of the incorrect-trial EMG activation (z-score, coefficient correlation of 0.61, p<0.01) (Fig. S7A), while it was less strongly correlated with corrective EMG onset (coefficient correlation 0.27, p<0.01). By contrast, the end of the LFP was strongly correlated with the onset of the corrective EMG activation, and, less strongly, with the offset of the incorrect EMG (coefficient correlation respectively 0.7, p<0.01 and 0.27, p<0.05) (Fig. S7B).

This difference in latency and amplitude of error-related potentials between covert and overt errors has been shown by previous scalp recording studies (10). Moreover scalp EEG studies have shown that error-evoked activities peak earlier when an overt error is followed by an immediate (but ineffective) correction, than in the case of uncorrected errors (22).
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36. LFP onset and peak are actually strongly correlated to each other, thus showing very similar patterns of correlation with EMG latencies. We decided to report data about the LFP peak because its latency can be unambiguously detected by visual inspection.
Figures' legends

**Fig. S1.** Behavioral pattern. (A) Percentage of correct responses on congruent (black line) and incongruent (grey line) condition as a function of reaction time: the two lines show the typical reduction in correct response rate on incongruent trials for short reaction times only. (B) Size of the congruency effect (reaction time on incongruent trials minus reaction time on congruent trials) as a function of reaction time. The curve shows the typical decrease in the congruency effect as a function of reaction time.

**Fig. S2.** Localization of action monitoring activity in the SMA. (A) EMG-locked LFPs showed decreasing amplitude from medial to lateral contacts. The amplitude of error-evoked LFPs recorded along the electrode in the SMA was averaged over subjects and is shown on a coronal and an axial view of an MNI template. The color scale represents these averaged LFPs normalized to the maximum LFP amplitude and expressed as a percentage. (B) LFPs evoked by correct responses and covert errors recorded from two overlying electrodes implanted in the SMA in subject 2. LFPs recorded from these overlying electrodes (electrode 1 and 2 respectively solid and dotted lines) showed the same morphology, the same time course and the same amplitude, but with inverted polarity. The polarity inversion could be ascertained also on single trial data, by measuring latency and amplitude of LFPs on 31 out of the 32 partial-error trials. High correlations were observed for both latencies ($\rho = 0.94$; $p < .01$) and amplitudes ($\rho = 0.66$; $p < .01$) demonstrating that the two recording sites captured the activity of the same source located in the SMA. (C) Sagittal view of patient's MRI/CT fusion scan, showing the anatomical location of electrode 1 in the upper part of the caudal SMA, and of electrode 2, underneath, implanted in the rostral SMA, at the level of VCA boundary.

**Fig. S3.** Spatial sampling of the caudal part of medial frontal lobe in subject 1. Left panel: LFPs recorded from the most medial contact of four electrodes implanted in the medial frontal cortex and a reconstruction of the electrodes' trajectory based on individual MRI/CT fusion. Right panel: sketch of an intracerebral electrode (numbers denote contacts from medial to lateral locations) and LFPs recorded from each contact. SC medial: caudal SMA;
SC lateral: motor cortex, hand area; SA medial: rostral SMA; SA lateral: premotor cortex, area 6; PM medial: pre-SMA; PM lateral: area 8; CC medial: posterior RCZ; CC lateral: ventral premotor cortex, area 6.

**Fig. S4.** Single trial LFPs time-locked to EMG onset in error trials. (A) as an example 18 trials are shown for subject 3 and (B) 17 trials for subject 5.

**Fig. S5.** Positive correlations between activities of medial prefrontal cortices (MPFC) and SMA activity in terms of latencies (A and C) and amplitude (B and D). Error-evoked LFPs were detectable on a trial-by-trial basis at both SMA (subject 3: 21 trials out of 24; subject 5: 64 trials out of 72) and medial prefrontal electrodes (pACC for subject 3: 18 trials; OMPFC for subject 5: 35 trials). The intercept of the regression shows the latency shift between SMA and MPFC.

**Fig. S6.** Example of a covert error trial and corresponding SMA LFP. Latencies of SMA activity are represented by the peak and end of the LFP in SMA, covert error interruption is represented by the offset of an incorrect EMG burst and covert error correction is represented by the onset of the corrective EMG burst.

**Fig. S7.** Correlation between the latencies of LFPs and EMG activity during covert error trials. (A) correlation between peak of LFP and covert error interruption. (B) correlation between LFP's offset and onset of corrective response.

**Fig. S8.** Caudo-rostral latency of activation in different medial frontal areas in patient 3 (top) and 5 (bottom). The anatomical location of electrodes placed in SMA, pACC and OMPFC, converted into normalized MNI brain, are shown on a RD MNI standard brain in its medial aspect (left).
A

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mean RT (msec)

B

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mean RT (msec)

19
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Accepted Manuscript

2.1

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A

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B
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24
anonical
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Peak of SMA activity

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End of incorrect EMG

End of SMA activity

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Onset of corrective EMG

Accepted Manuscript

25
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