Winning and losing experiences differentially alter learning performance and forebrain protein expression in mangrove rivulus killifish, Kryptolebias marmoratus

Abstract

Contest outcomes alter future social behavior, but whether and how a single win or loss influences non-social learning-task performance and triggers rapid forebrain molecular responses remains unclear. The self-fertilizing mangrove rivulus killifish, Kryptolebias marmoratus , offers a useful system because contest outcomes can be standardized while reducing genetic background variation. We predicted that winning and losing would produce distinct post-contest behavioral profiles rather than equivalent or opposite shifts across tasks. We tested whether standardized winning, losing, or control experiences altered aggression, landmark-guided spatial task performance, and risk-avoidance task performance 1 h, 3 h, or 48 h after experience. In a separate experiment, we quantified whole-forebrain protein abundance 1 h after the same manipulation to identify outcome-associated molecular responses. Winners showed increased aggression and improved landmark-guided spatial task performance, whereas losers showed reduced aggression and improved risk-avoidance task performance. Proteomic analysis identified 23 outcome-associated proteins, including candidates linked to synaptic plasticity, cytoskeletal regulation, and neural energetics. Because behavioral and proteomic measurements used independent animals, these data do not establish within-individual or causal relationships between protein abundance and behavior performance. Instead, the proteomic results identify outcome-associated candidate molecules that may contribute to experience-dependent behavioral plasticity and should be tested directly in future studies.