Social experience alters different types of learning abilities controlled by distinct brain nuclei inKryptolebias marmoratus

Abstract

Fighting experiences strongly influence aggressive behavior and physiology (winner-loser effects). These effects are conserved from invertebrates to vertebrates, but the underlying mechanisms remain unclear. Recent studies indicate that the brain social decision-making network (SDN) plays a key role in guiding experience-induced behavioral change. Also, while most studies have focused on how winning and losing experiences alter aggression, growing evidence points to these experiences driving multiple behavioral effects, including changes in the ability to learn. In mangrove rivulus fish (Kryptolebias marmoratus), we discovered that single winning experiences significantly improved spatial learning but not risk-avoidance learning, whereas single losing experiences drove the exact opposite to occur. These results provide strong evidence that winning and losing modulate diverse behaviors served by key nodes within the SDN, specifically the dorsolateral pallium (Dl; fish homolog to mammalian hippocampus, which serves spatial learning) and dorsomedial pallium (Dm; fish homolog to mammalian basolateral amygdala, which responds to fear). We therefore quantified whole-proteome expression within the forebrain (where Dm and Dl are located) of adult rivulus with divergent social experiences. We discovered 23 proteins were significantly differentially expressed in the forebrains of winners and losers. Differentially expressed proteins in losers related to modulation of cellular processes, apoptosis and learning while those in winners related to neuronal plasticity, neuroendocrine homeostasis, energy utilization, and learning. These results imply that winner-loser effects might be governed by very different patterns of protein expression, which could explain why winners and losers show such pronounced differences in behavioral performance.Significance StatementSocial interactions permeate the daily lives of most animals and often result in changes in behavior for all parties. This implies that social experiences reorganize the brain in ways that promote the expression of alternative behaviors, or that help individuals cope with the outcome of such interactions. But how do aggressive interactions sculpt the brain at the molecular level? We used an emerging model organism, Kryptolebias marmoratus, to examine whether experiences modulate learning ability and then probe the potential neural mechanisms underlying these behavioral changes. We discovered that single winning and losing experiences dramatically altered spatial learning and risk-avoidance learning, respectively, indicating that winning and losing experiences have markedly different effects on the brain and cognitive processes.ClassificationBiological Sciences, Ecology