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

J Neurophysiol. 2018 Sep 1;120(3):1107-1118. doi: 10.1152/jn.00130.2018. Epub 2018 Jun 6.

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.

Keywords: action observation; error; event probability; theta; virtual reality.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Alpha Rhythm / physiology
  • Analysis of Variance
  • Cerebral Cortex / physiology
  • Electroencephalography*
  • Female
  • Humans
  • Male
  • Models, Psychological*
  • Movement / physiology
  • Probability
  • Theta Rhythm / physiology
  • Virtual Reality*
  • Visual Perception / physiology*
  • Young Adult