Cortical ensembles orchestrate social competition through hypothalamic outputs

Abstract

How do we know our social rank? Most social species, from insects to humans, self-organize into social dominance hierarchies (1-4). The establishment of social ranks serves to decrease aggression, conserve energy, and maximize survival for the entire group (5-8). Despite dominance behaviors being critical for successful interactions and ultimately, survival, we have only begun to learn how the brain represents social rank (9-12) and guides behavior based on this representation. The medial prefrontal cortex (mPFC) has been implicated in the expression of social dominance in rodents (10,11), and in social rank learning in humans (13,14). Yet precisely how the mPFC encodes rank and which circuits mediate this computation is not known. We developed a trial-based social competition assay in which mice compete for rewards, as well as a computer vision tool to track multiple, unmarked animals. With the development of a deep learning computer vision tool (AlphaTracker) and wireless electrophysiology recording devices, we have established a novel platform to facilitate quantitative examination of how the brain gives rise to social behaviors. We describe nine behavioral states during social competition that were accurately decoded from mPFC ensemble activity using a hidden Markov model combined with generalized linear models (HMM-GLM). Population dynamics in the mPFC were predictive of social rank and competitive success. This population-level rank representation translated into differences in the individual cell responses to task-relevant events across ranks. Finally, we demonstrate that mPFC cells that project to the lateral hypothalamus contribute to the prediction of social rank and promote dominance behavior during the reward competition. Thus, we reveal a cortico-hypothalamic circuit by which mPFC exerts topdown modulation of social dominance. Main TextThe medial prefrontal cortex (mPFC) is best known for its role in working memory, decision-making, reward learning and goal-oriented behavior [15][16][17][18][19] . Theories about mPFC function emphasize that it integrates sensory and limbic information to exibly guide behavior based on task rules 20,21 . mPFC circuitry has also been broadly implicated in social cognition [22][23][24] , social behaviors 25,26 , social

Hearing, touching, and multisensory integration during mate choice

“…This connection could be a potential top down control on how the cortex impinges on the social behavior network thereby driving a preference. A similar circuit has been described during social dominance behavior (Padilla-Coreano et al, 2022). Whether this is mediated by the integration of multisensory cues has been left open.…”

Increased paternal corticosterone exposure preconception shifts offspring social behaviours and expression of urinary pheromones

“…There is extensive literature on dominance and social hierarchy priming response to stress (Sapolsky, 2005), as it is known that hierarchical rank modulates the HPA system reactivity (Yohn et al, 2019), possibly due to higher-order impacts of the prefrontal cortex on hypothalamic function. Studies on stressful exposures modulating social dominance and hierarchical rank are less studied, but it has been reported that a cortico-hypothalamic circuit modulates social dominance (Padilla-Coreano et al, 2022) and maternal separation reduces adult dominance in a competition for water in water-restricted mice (Benner et al, 2014). Furthermore, chronic restraint decreases social dominance in the tube test (Park et al, 2018) and severe immobilisation stress heavily reduces social dominance in anxious mice (Lucion and Vogel, 1994).…”

“…For instance, studies have shown that the synaptic efficacy regulated by AMPA receptors in this region controls the expression of social dominance (Wang et al, 2011), that the increase in social dominance as assessed in the tube test accompanies modifications of the stable actin fraction in synaptic spikes in this region (Tada et al, 2016), and that social dominance is followed by differential gene expression in this region (Pallé et al, 2019). Lastly, neuronal population activity in the mPFC predicts social rank and success in competitive settings (Padilla-Coreano et al, 2022).…”

Social dominance status and social stability in spiny mice (Acomys cahirinus) and its relation to ear-hole regeneration and glucocorticoids

“…Briefly, other studies measuring social dominance in rodents use a diverse set of methods to measure dyadic social relationships (22) through social conflict in a narrow tube (55,56) or competing for rewards (57), for example. While these tests are not guaranteed to correlate with home-cage behavior or one another (58,59), they provide further insight into the social relationship and can be used in a round-robin tournament to measure dominance relationships with equal numbers of social interactions.…”