Neural mechanisms of awareness of action.

Awareness of action (AoA)—the conscious awareness of one's own actions—is crucial for daily life, yet its neural basis is poorly understood. By developing a game where participants repeatedly made nearly identical moves while distracted, then reported awareness or unawareness of those moves, the authors compared neural activity between aware and unaware actions. On short timescales, aware actions showed larger neurophysiological signals both before and after movement, including volitional and perceptual event-related potentials, frontal midline theta, alpha/beta desynchronization, and increased blink rates. On longer timescales, a novel positive event-related potential preceded only unaware moves, and behavioral and pupillometric evidence indicated decreased attention and arousal concurrent with AoA loss. Three synergistic neural mechanisms were identified: long-term increases in arousal/attentional state, increased motor volitional signals, and increased sensory perceptual signals.

Study at a glance

Abstract

Awareness of action (AoA), or conscious awareness of an action just performed, is an important part of daily experience with major practical and ethical relevance, yet the neural mechanisms of AoA remain largely unknown. The main barrier to studying AoA is a lack of experimental paradigms to directly compare neural activity in aware versus unaware actions. Borrowing from the field of perceptual awareness, where exciting progress has been made by contrastive analysis of aware versus unaware stimuli, we developed a game where participants repeatedly perform nearly identical moves while engaged in a distractor task, and the participants then report awareness or unawareness of the moves they just performed. We found that on short timescales, aware actions had larger neurophysiological signals both preceding and following movement. The differences included both volitional and perceptual event-related potentials (premovement positivity, N140, and P300), as well as frontal midline theta, event-related alpha/beta desynchronization, and postmove blink rates. On longer time scales, we identified a novel positive event-related potential only preceding unaware moves and found behavioral and pupillometric evidence for decreased attention and arousal over minutes concurrent with AoA loss. Our findings reveal three neural mechanisms that may synergistically contribute to AoA: (i) long-term increases in arousal/attentional state at time of action; (ii) increased action-related motor volitional signals; and (iii) increased action-related sensory perceptual signals. Deeper understanding of AoA may ultimately elucidate the causes of variable AoA in daily life and lead to better treatments for impaired AoA in neuropsychiatric disorders.