Frontal and occipito-temporal Theta activity as marker of error monitoring in Human-Avatar joint performance

The discrepancy between expected outcome and real outcome is at the base of error coding, a crucial process during adaptive behaviours. Previous studies indicate that performing or observing errors elicits specific EEG markers (e.g. Theta). Here we show how unexpected changes in the movement trajectory of the virtual co-actor in a human-avatar dyadic paradigm are mapped into the error-monitoring system of the human partner. We asked individuals to synchronize their reach-to-grasp movements with those of a virtual partner in conditions that did (Interactive condition), or did not, require (Cued condition) spatio-temporal adaptation to the partner’s actions. Crucially, in certain trials the virtual partner suddenly changed its movement trajectory; thereby violating the human participant’s expectation. These trials showed that fronto-central error-related EEG markers increased as a function of the individual’s reliance on their partner’s behaviour. Source localization showed that observing violations of the expected movements also generated a Theta increase over occipito-temporal regions, highlighting visuo-motor processing during erroneous interactions. Significance Statement Our ability to coordinate with peers relies upon moment-to-moment prediction and integration of visual (i.e. observing the movements of others) and motor (completing our own actions) information. However, when the behaviour of our partners changes unexpectedly, our prediction appears to be incorrect. Here, we describe EEG error-related neuromarkers (ERN/Pe - Theta/Alpha modulations): when human participants perform a joint reach-to-grasp task with a virtual partner. We show that unexpected changes of the avatar trajectory are mapped into EEG error-markers according to the degree of interpersonal interdependence. Moreover, source analysis highlights that fronto-central and occipito-temporal regions generate Theta activity associated with processing visuo-motor information during social interactions.