Error, rather than its probability, elicits specific electrocortical signatures: a combined EEG-immersive virtual reality study of action observation

Abstract

Detecting errors in one's own actions, and in the actions of others, is a crucial ability for adaptable and flexible behavior. Studies show that specific EEG signatures underpin the monitoring of observed erroneous actions (error-related negativity, error positivity, mid-frontal theta oscillations). However, the majority of studies on action observation used sequences of trials where erroneous actions were less frequent than correct actions. Therefore, it was not possible to disentangle whether the activation of the performance monitoring system was due to an error, as a violation of the intended goal, or to a surprise/novelty effect, associated with a rare and unexpected event. Combining EEG and immersive virtual reality (IVR-CAVE system), we recorded the neural signal of 25 young adults who observed, in first-person perspective, simple reach-to-grasp actions performed by an avatar aiming for a glass. Importantly, the proportion of erroneous actions was higher than correct actions. Results showed that the observation of erroneous actions elicits the typical electrocortical signatures of error monitoring, and therefore the violation of the action goal is still perceived as a salient event. The observation of correct actions elicited stronger alpha suppression. This confirmed the role of the alpha-frequency band in the general orienting response to novel and infrequent stimuli. Our data provide novel evidence that an observed goal error (the action slip) triggers the activity of the performance-monitoring system even when erroneous actions, which are, typically, relevant events, occur more often than correct actions and thus are not salient because of their rarity. NEW & NOTEWORTHY Activation of the performance-monitoring system (PMS) is typically investigated when errors in a sequence are comparatively rare. However, whether the PMS is activated by errors per se or by their infrequency is not known. Combining EEG-virtual reality techniques, we found that observing frequent (70%) action errors performed by avatars elicits electrocortical error signatures suggesting that deviation from the prediction of how learned actions should correctly deploy, rather than its frequency, is coded in the PMS.

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

“…The interaction type (Complementary/Imitative) and the movement type (Precision/Power) factors were randomized trial-by-trial and pooled together. While an unequal number of Correction and No-Correction trials is usually used to emphasize the salience of one condition with respect to another we demonstrated that randomly selecting an equal number of trials for the two distributions does not change the results (Pezzetta et al, 2018).…”

“…Although reported separately in the analysis, Theta and Alpha modulation shows a similar and correlated pattern (see Table 2). In previous error-related literature, Theta and Alpha have both been found over fronto-central electrodes during the processing of errors , Pezzetta et al, 2018. However, Trujillo and Allen (2007) have argued that activity in the lower Alpha band is due to leakage of the Theta frequency to the neighbouring bands.…”

“…A recent study showed that inducing Theta over FCz by means of transcranial alternating current stimulation (tACS) resulted in modulation in behavioural adjustment after error execution (Fusco et al, 2018). More recently, Theta and Alpha synchronizations have also been detected during the observation of motor errors performed by an embodied avatar seen from a first-person perspective Spinelli et al, 2017;Pezzetta et al, 2018).…”

Hand blink reflex in virtual reality: The role of vision and proprioception in modulating defensive responses

“…Thus, a source for the reduced feeling of ownership over the avatar limb may also be the fact that the participants' and the avatar's body never assumed a matched position. However, previous evidence reported illusory ownership even when participants were still and the virtual limb performed reach‐to‐grasp movement (Pavone et al, ; Pezzetta, Nicolardi, Tidoni, & Aglioti, ; Spinelli, Tieri, Pavone, & Aglioti, ). A possible explanation of this difference might rely on the number of trials, consistently greater in these previous experiments (i.e., a greater number of trials could increase the illusory sensation).…”

A different state of mind: neural activity related to volitionally up- versus downregulating cortical excitability

“…While changes in alpha and gamma were specific to the hemisphere from which feedback was provided, theta showed a bilateral pattern of modulation, being higher in the DOWN than the UP state in motor areas in both hemispheres. While mid-frontal theta activity has been linked to error monitoring 46 the role of lateralized theta activity close to the sensorimotor hotspot electrode and its symmetric counterpart is less clear. Slower rhythms exert effects over larger distances, and are thought to be involved in long-range communication 40 .…”