Wronger than wrong: Graded mapping of the errors of an avatar in the performance monitoring system of the onlooker

• Published in: NeuroImage (Orlando, Fla.) Vol. 167; pp. 1 - 10
• Main Authors: Spinelli, G., Tieri, G., Pavone, E.F., Aglioti, S.M.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 15.02.2018; Elsevier Limited
• Subjects: Adaptation; Adult; Computer applications; Cortex; EEG; Electroencephalography Phase Synchronization - physiology; ERN; Error correction & detection; Error magnitude; Error observation; Evoked Potentials - physiology; Female; Frontal Lobe - physiology; Human performance; Humans; Male; Neural networks; Psychomotor Performance - physiology; Studies; Synchronization; Theta oscillations; Theta Rhythm - physiology; Theta rhythms; User-Computer Interface; Virtual reality; Young Adult; ERN; Error observation; Theta oscillations; Virtual reality; Error magnitude
• ISSN: 1053-8119; 1095-9572
• DOI: 10.1016/j.neuroimage.2017.11.019

EEG studies show that observing errors in one's own or others' actions triggers specific electro-cortical signatures in the onlooker's brain, but whether the brain error-monitoring system operates according to graded or discrete rules is still largely unknown. To explore this issue, we combined immersive virtual reality with EEG recording in participants who observed an avatar reaching-to-grasp a glass from a first-person perspective. The avatar could perform correct or erroneous actions. Erroneous grasps were defined as small or large depending on the magnitude of the trajectory deviation from the to-be-grasped glass. Results show that electro-cortical indices of error detection (indexed by ERN and mid-frontal theta oscillations), but not those of error awareness (indexed by error-Positivity), were gradually modulated by the magnitude of the observed errors. Moreover, the phase connectivity analysis revealed that enhancement of mid-frontal theta phase synchronization paralleled the magnitude of the observed error. Thus, theta oscillations represent an electro-cortical index of the degree of control exerted by mid-frontal regions whose activation depends on how much an observed action outcome results maladaptive for the onlooker. Our study provides novel neurophysiological evidence that the error monitoring system maps observed errors of different magnitude according to fine-grain, graded rather than all-or-none rules. •Seeing avatar's action errors activates the onlooker's error detection brain system.•ERN and theta power are modulated analogically by amplitude of observed errors.•Mid-frontal theta phase synchronization parallels the observed error magnitude.•Virtual reality is a powerful tool to study action observation ecologically.