L-DOPA and oxytocin influence the neural correlates of performance monitoring for self and others

• Published in: Psychopharmacology Vol. 241; no. 5; pp. 1079 - 1092
• Main Authors: Jansen, Myrthe, Overgaauw, Sandy, de Bruijn, Ellen R. A.
• Format: Journal Article
• Language: English
• Published: Berlin/Heidelberg Springer Berlin Heidelberg 01-05-2024; Springer Nature B.V
• Subjects: Biomedical and Life Sciences; Biomedicine; Brain mapping; Cortex (cingulate); Dopamine; Functional magnetic resonance imaging; Hormones; Levodopa; Magnetic resonance imaging; Neostriatum; Neuroimaging; Neurosciences; Original Investigation; Oxytocin; Pharmacology/Toxicology; Placebos; Psychiatry; Social performance monitoring; Dopamine; Functional magnetic resonance imaging (fMRI); Oxytocin; Prosocial
• ISSN: 0033-3158; 1432-2072
• DOI: 10.1007/s00213-024-06541-9

Rationale
The ability to monitor the consequences of our actions for others is imperative for flexible and adaptive behavior, and allows us to act in a (pro)social manner. Yet, little is known about the neurochemical mechanisms underlying alterations in (pro)social performance monitoring.
Objective
The aim of this functional magnetic resonance imaging (fMRI) study was to improve our understanding of the role of dopamine and oxytocin and their potential overlap in the neural mechanisms underlying performance monitoring for own versus others’ outcomes.
Method
Using a double-blind placebo-controlled cross-over design, 30 healthy male volunteers were administered oxytocin (24 international units), the dopamine precursor L-DOPA (100 mg + 25 mg carbidopa), or placebo in three sessions. Participants performed a computerized cannon shooting game in two recipient conditions where mistakes resulted in negative monetary consequences for (1) oneself or (2) an anonymous other participant.
Results
Results indicated reduced error-correct differentiation in the ventral striatum after L-DOPA compared to placebo, independent of recipient. Hence, pharmacological manipulation of dopamine via L-DOPA modulated performance-monitoring activity in a brain region associated with reward prediction and processing in a domain-general manner. In contrast, oxytocin modulated the BOLD response in a recipient-specific manner, such that it specifically enhanced activity for errors that affected the other in the pregenual anterior cingulate cortex (pgACC), a region previously implicated in the processing of social rewards and prediction errors. Behaviorally, we also found reduced target sizes—indicative of better performance—after oxytocin, regardless of recipient. Moreover, after oxytocin lower target sizes specifically predicted higher pgACC activity when performing for others.
Conclusions
These different behavioral and neural patterns after oxytocin compared to L-DOPA administration highlight a divergent role of each neurochemical in modulating the neural mechanisms underlying social performance monitoring.