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The desire to understand how the brain generates and patterns behavior has driven rapid methodological innovation in tools to quantify natural animal behavior. While advances in deep learning and computer vision have enabled markerless pose estimation in individual animals, extending these to multiple animals presents unique challenges for studies of social behaviors or animals in their natural environments. Here we present Social LEAP Estimates Animal Poses (SLEAP), a machine learning system for multi-animal pose tracking. This system enables versatile workflows for data labeling, model training and inference on previously unseen data. SLEAP features an accessible graphical user interface, a standardized data model, a reproducible configuration system, over 30 model architectures, two approaches to part grouping and two approaches to identity tracking. We applied SLEAP to seven datasets across flies, bees, mice and gerbils to systematically evaluate each approach and architecture, and we compare it with other existing approaches. SLEAP achieves greater accuracy and speeds of more than 800 frames per second, with latencies of less than 3.5 ms at full 1,024 × 1,024 image resolution. This makes SLEAP usable for real-time applications, which we demonstrate by controlling the behavior of one animal on the basis of the tracking and detection of social interactions with another animal. SLEAP is a versatile deep learning-based multi-animal pose-tracking tool designed to work on videos of diverse animals, including during social behavior.

The authors show that the ventrolateral aspect of the ventromedial hypothalamus (VMHvl), a region previously implicated in attack behavior, can also drive flexible aggression-seeking behavior. When male mice learn a task to seek out attack opportunities, activity in the VMHvl tracks and bidirectionally modulates the seeking behavior that leads to future attack. In many vertebrate species, certain individuals will seek out opportunities for aggression, even in the absence of threat-provoking cues. Although several brain areas have been implicated in the generation of attack in response to social threat, little is known about the neural mechanisms that promote self-initiated or 'voluntary' aggression-seeking when no threat is present. To explore this directly, we utilized an aggression-seeking task in which male mice self-initiated aggression trials to gain brief and repeated access to a weaker male that they could attack. In males that exhibited rapid task learning, we found that the ventrolateral part of the ventromedial hypothalamus (VMHvl), an area with a known role in attack, was essential for aggression-seeking. Using both single-unit electrophysiology and population optical recording, we found that VMHvl neurons became active during aggression-seeking and that their activity tracked changes in task learning and extinction. Inactivation of the VMHvl reduced aggression-seeking behavior, whereas optogenetic stimulation of the VMHvl accelerated moment-to-moment aggression-seeking and intensified future attack. These data demonstrate that the VMHvl can mediate both acute attack and flexible seeking actions that precede attack.

Chronic stress can have lasting adverse consequences in some individuals, yet others are resilient to the same stressor 1 , 2 . Susceptible and resilient individuals exhibit differences in the intrinsic properties of mesolimbic dopamine (DA) neurons after the stressful experience is over 3 – 8 . However, the causal links between DA, behaviour during stress and individual differences in resilience are unknown. Here we recorded behaviour in mice simultaneously with DA neuron activity in projections to the nucleus accumbens (NAc) (which signals reward 9 – 12 ) and the tail striatum (TS) (which signals threat 13 – 16 ) during social defeat. Supervised and unsupervised behavioural quantification revealed that during stress, resilient and susceptible mice use different behavioural strategies and have distinct activity patterns in DA terminals in the NAc (but not the TS). Neurally, resilient mice have greater activity near the aggressor, including at the onset of fighting back. Conversely, susceptible mice have greater activity at the offset of attacks and onset of fleeing. We also performed optogenetic stimulation of NAc-projecting DA neurons in open loop (randomly timed) during defeat or timed to specific behaviours using real-time behavioural classification. Both open-loop and fighting-back-timed activation promoted resilience and reorganized behaviour during defeat towards resilience-associated patterns. Together, these data provide a link between DA neural activity, resilience and resilience-associated behaviour during the experience of stress. Neural recording and closed-loop manipulation during chronic stress in mice reveal causal links between dopamine, behavior and resilience.

Persistent negative emotional states, such as anxiety, suppress social behavior and vice versa. A new report identifies a novel neural circuit that generates persistent anxiety states and describes how competing excitatory and inhibitory components of this circuit battle to pattern social behavior.

Social behaviors often consist of a motivational phase followed by action. Here we show that neurons in the ventromedial hypothalamus ventrolateral area (VMHvl) of mice encode the temporal sequence of aggressive motivation to action. The VMHvl receives local inhibitory input (VMHvl shell) and long-range input from the medial preoptic area (MPO) with functional coupling to neurons with specific temporal profiles. Encoding models reveal that during aggression, VMHvl shell vgat+ activity peaks at the start of an attack, whereas activity from the MPO–VMHvl vgat+ input peaks at specific interaction endpoints. Activation of the MPO–VMHvl vgat+ input promotes and prolongs a low motivation state, whereas activation of VMHvl shell vgat+ results in action-related deficits, acutely terminating attack. Moreover, stimulation of MPO–VMHvl vgat+ input is positively valenced and anxiolytic. Together, these data demonstrate how distinct inhibitory inputs to the hypothalamus can independently gate the motivational and action phases of aggression through a single locus of control. Minakuchi et al. find that separable inhibitory inputs to a critical hypothalamic aggression-control node can influence the evolution of an aggressive state by independently modulating either the motivational phase or the action phase.

Persistent negative emotional states, such as anxiety, suppress social behavior and vice versa. A new report identifies a novel neural circuit that generates persistent anxiety states and describes how competing excitatory and inhibitory components of this circuit battle to pattern social behavior.

In naturalistic conditions, animals must routinely make ongoing self-motivated choices about whether to initiate interactions with same or opposite-sex partners and whether to re-initiate social contact when interactions have ended. However, it remains unclear what governs these choices, and whether they are motivated by drive states that exhibit signatures of moment-to-moment social satiety when these interactions have ended. Here, to explicitly test this at the behavioral level, we designed a novel fully-automated two-choice social operant paradigm where individuals can choose between same and opposite-sex social rewards and rewards are delivered for interaction with systematically varying durations. We trained cohorts of both sexes on this task and quantified the patterns of choices. We used choice latency as a metric to infer moment-to-moment satiety to test whether increased interaction duration leads to increased moment-to-moment satiety. We find that although both males and females have stable choice biases across sessions, with males showing consistent opposite sex biases, only males exhibit behavioral signatures of moment-to-moment social satiety and are sensitive to the duration of interaction. Using a simple normative model to capture patterns of social choice, we observe that behavior is better fit by a model that has a single evolving social drive and choice bias, rather than a model with multiple, independent drives for same and opposite-sex interactions. Together, our data reveal behavioral signatures of social satiety and offer new insights into the underlying homeostatic and motivational drives that govern social choices.