Historical loss weakens competitive behavior by remodeling ventral hippocampal dynamics.

Abstract

Competitive interactions are pervasive within biological populations, where individuals engage in fierce disputes over vital resources for survival. Before the establishment of a social hierarchy within the population, this competition becomes even more intense. Historical experiences of competition significantly influence the competitive performance; individuals with a history of persistent loss are less likely to initiate attacks or win escalated contests. However, it remains unclear how historical loss directly affects the evolution of mental processes during competition and alters responses to ongoing competitive events. Here, we utilized a naturalistic food competition paradigm to track the competitive patterns of mutually unfamiliar competitors and found that a history of loss leads to reduced competitive performance. By tracking the activity of ventral hippocampal neuron ensembles, we identified clusters of neurons that responded differently to behavioral events during the competition, with their reactivity modulated by previous losses. Using a Recurrent Switch Linear Dynamical System (rSLDS), we revealed rotational dynamics in the ventral hippocampus (vHPC) during food competition, where different discrete internal states corresponded to different behavioral strategies. Moreover, historical loss modulates competitive behavior by remodeling the characteristic attributes of this rotational dynamic system. Finally, we found that an evolutionarily conserved glutamate receptor-associated protein, glutamate receptor-associated protein 1 (Grina), plays an important role in this process. By continuously monitoring the association between the attributes of the dynamic system and competitiveness, we found that restoring Grina expression effectively reversed the impact of historical loss on competitive performance. Together, our study reveals the rotational dynamics in the ventral hippocampus during competition and elucidates the underlying mechanisms through which historical loss shapes these processes.