Neural correlates of implicit agency during the transition from adolescence to adulthood: An ERP study

Abstract

Sense of agency (SoA), the experience of being in control of our voluntary actions and their outcomes, is a key feature of normal human experience. Frontoparietal brain circuits associated with SoA undergo a major maturational process during adolescence. To examine whether this translates to neurodevelopmental changes in agency experience, we investigated two key neural processes associated with SoA, the activity that is leading to voluntary action (Readiness Potential) and the activity that is associated with the action outcome processing (attenuation of auditory N1 and P2 event related potentials, ERPs) in mid-adolescents (13–14), late-adolescents (18–20) and adults (25–28) while they perform an intentional binding task. In this task, participants pressed a button (action) that delivered a tone (outcome) after a small delay and reported the time of the tone using the Libet clock. This action-outcome condition alternated with a no-action condition where an identical tone was triggered by a computer. Mid-adolescents showed greater outcome binding, such that they perceived self-triggered tones as being temporally closer to their actions compared to adults. Suggesting greater agency experience over the outcomes of their voluntary actions during mid-adolescence. Consistent with this, greater levels of attenuated neural response to self-triggered auditory tones (specifically P2 attenuation) were found during mid-adolescence compared to older age groups. This enhanced attenuation decreased with age as observed in outcome binding. However, there were no age-related differences in the readiness potential leading to the voluntary action (button press) as well as in the N1 attenuation to the self-triggered tones. Notably, in mid-adolescents greater outcome binding scores were positively associated with greater P2 attenuation, and smaller negativity in the late readiness potential. These findings suggest that the greater experience of implicit agency observed during mid-adolescence may be mediated by a neural over-suppression of action outcomes (auditory P2 attenuation), and over-reliance on motor preparation (late readiness potential), which we found to become adult-like during late-adolescence. Implications for adolescent development and SoA related neurodevelopmental disorders are discussed.