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Main In recent years, substantial advances in social neuroscience have been realized, including the generation of numerous rodent models of autism spectrum disorder. Still, it can be argued that those methods currently being used to analyze animal social behavior create a bottleneck that significantly slows down progress in this field. Indeed, the bulk of research still relies on a small number of simple behavioral paradigms, the results of which are assessed without considering behavioral dynamics. Moreover, only few variables are examined in each paradigm, thus overlooking a significant portion of the complexity that characterizes social interaction between two conspecifics, subsequently hindering our understanding of the neural mechanisms governing different aspects of social behavior. We further demonstrate these constraints by discussing the most commonly used paradigm for assessing rodent social behavior, the three-chamber test. We also point to the fact that although emotions greatly influence human social behavior, we lack reliable means for assessing the emotional state of animals during social tasks. As such, we also discuss current evidence supporting the existence of pro-social emotions and emotional cognition in animal models. We further suggest that adequate social behavior analysis requires a novel multimodal approach that employs automated and simultaneous measurements of multiple behavioral and physiological variables at high temporal resolution in socially interacting animals. We accordingly describe several computerized systems and computational tools for acquiring and analyzing such measurements. Finally, we address several behavioral and physiological variables that can be used to assess socio-emotional states in animal models and thus elucidate intricacies of social behavior so as to attain deeper insight into the brain mechanisms that mediate such behaviors. Conclusions In summary, we suggest that combining automated multimodal measurements with machine-learning algorithms will help define socio-emotional states and determine their dynamics during various types of social tasks, thus enabling a more thorough understanding of the complexity of social behavior.

Rhythmic activity in the theta range is thought to promote neuronal communication between brain regions. In this study, we performed chronic telemetric recordings in socially behaving rats to monitor electrophysiological activity in limbic brain regions linked to social behavior. Social encounters were associated with increased rhythmicity in the high theta range (7–10 Hz) that was proportional to the stimulus degree of novelty. This modulation of theta rhythmicity, which was specific for social stimuli, appeared to reflect a brain-state of social arousal. In contrast, the same network responded to a fearful stimulus by enhancement of rhythmicity in the low theta range (3–7 Hz). Moreover, theta rhythmicity showed different pattern of coherence between the distinct brain regions in response to social and fearful stimuli. We suggest that the two types of stimuli induce distinct arousal states that elicit different patterns of theta rhythmicity, which cause the same brain areas to communicate in different modes. For the brain to function correctly, the activities of multiple regions must be coordinated. This coordination is thought to be carried out by waves of electrical activity in the brain. One of the most prominent signals within these waves is called the theta rhythm. The theta rhythm is thought to help coordinate neural activity between the regions of the brain that are involved in learning and memory. However, theta rhythms also appear when subjects encounter emotional stimuli, which suggests that they might have a role in social cognition. Consistent with this idea, theta rhythms are reduced in individuals with autism spectrum disorders, but the exact nature of the relationship between theta rhythms and social behavior has remained unclear. Tendler and Wagner have now addressed this question directly by implanting electrodes into five brain regions that are active when rats engage in social interactions. Exposing a rat to a social stimulus, such as an unfamiliar visitor rat, caused the intensity of theta rhythms to increase in this network. This change was temporary, with the theta rhythms gradually returning to normal as the novelty of the visitor wore off. An increase in the intensity of theta rhythms also occurred in the same network when the rats encountered a fearful stimulus, such as a tone that had previously signaled the delivery of a mild electric shock. Notably, however, the fearful stimulus led to an increase in low frequency theta rhythms, whereas the social stimulus led to an increase in high frequency theta rhythms. These results suggest that social and fearful stimuli give rise to two different forms of alertness or arousal, which are reflected by the two types of theta rhythms in this network within the brain. Tendler and Wagner also suggest that the distinct frequencies of theta rhythms might be used to support different forms of communication between various regions of the brain, depending on the emotional value of the stimuli (for example, are they social or fearful stimuli?) encountered by the animal. This means that emotional states might be dictating cognitive processes such as learning and memory.

Background Social decision-making is influenced by multiple factors such as age, sex, emotional state, and the individual’s social environment. While various behavioural readouts have been commonly used to study social behaviour in rodents, the role of fine head movements during social interactions remains underexplored despite the presence of accelerometers in many electrophysiological recording systems. Results Here, we used head acceleration data to analyse head movement kinematics in adult male and female mice across several social discrimination tests in various time scales. Our findings demonstrate the complementary nature of two variables derived from the raw acceleration, namely overall static (OSHA) and dynamic (ODHA) head acceleration, as well as specific head angles (Pitch and Roll). Together, these variables provide a comprehensive, detailed analysis of head movement, which cannot be easily achieved by video analysis systems such as DeepLabCut. Overall, our results suggest that head movement patterns are significantly influenced by sex, stimulus preference, and social context. Specifically, ODHA exhibited strong sex dependence and appeared to be more sensitive to internal states such as arousal and alertness. The static components were primarily influenced by social context, particularly stimulus preference, and seemed to reflect the subject's motivation to engage with the stimulus. The Roll angle also appeared strongly modulated by the broader social context. Conclusions Our study provides a novel method and analysis pipeline for studying the social behaviour of small rodents in high-time resolution using a head-based accelerometer. Our findings suggest that such measurements may inform the affective and motivational states of the subject during social interactions.

Adolescent social interactions are essential for shaping adult behavior in humans. While rodent studies have highlighted the impact of social isolation on behavior, many extend isolation into adulthood, making it challenging to pinpoint the long-term consequences of juvenile isolation. To address these challenges, we examined the effects of social isolation using two independent protocols with male and female Sprague Dawley rats. In both prfotocols, rats were isolated during the juvenile stage; however, in one protocol, rats were re-socialized following isolation and tested in adulthood, while in the other, rats were tested immediately after isolation. This approach allowed us to determine whether social deficits emerged following adolescent isolation and if they could be reversed by re-socialization before adulthood. We found that juvenile isolation had no lasting effects but increased motivation for social interaction immediately after isolation. These findings underscore the need to account for housing conditions and isolation protocols when assessing the effects of social isolation.

Mice and rats are widely used to explore mechanisms of mammalian social behavior in health and disease, raising the question whether they actually differ in their social behavior. Here we address this question by directly comparing social investigation behavior between two mouse and rat strains used most frequently for behavioral studies and as models of neuropathological conditions: C57BL/6 J mice and Sprague Dawley (SD) rats. Employing novel experimental systems for behavioral analysis of both subjects and stimuli during the social preference test, we reveal marked differences in behavioral dynamics between the strains, suggesting stronger and faster induction of social motivation in SD rats. These different behavioral patterns, which correlate with distinctive c-Fos expression in social motivation-related brain areas, are modified by competition with non-social rewarding stimuli, in a strain-specific manner. Thus, these two strains differ in their social behavior, which should be taken into consideration when selecting an appropriate model organism. Laboratory rat and mouse strains serve as animal models to explore brain mechanisms underlying social behavior. Here, the authors describe differences in social behavior between commonly used rat and mouse strains, which may reflect distinct dynamics of social motivation.

Social isolation poses a severe mental and physiological burden on humans. Most animal models that investigate this effect are based on prolonged isolation, which does not mimic the milder conditions experienced by people in the real world. We show that in adult male rats, acute social isolation causes social memory loss. This memory loss is accompanied by significant changes in the expression of specific mRNAs and proteins in the medial amygdala, a brain structure that is crucial for social memory. These changes particularly involve the neurotrophic signaling and axon guidance pathways that are associated with neuronal network remodeling. Upon regrouping, memory returns, and most molecular changes are reversed within hours. However, the expression of some genes, especially those associated with neurodegenerative diseases remain modified for at least a day longer. These results suggest that acute social isolation and rapid resocialization, as experienced by millions during the COVID-19 pandemic, are sufficient to induce significant changes to neuronal networks, some of which may be pathological.

If a fear engram is too crucial to be ignored, its strength must be amplified to allow it to dominate behavior. Here we report a learning-induced amplification mechanism that promotes an engram to dominance. The amplification mechanism is mediated by CaMKII-dependent increase of the conductance of all AMPA and GABA A channels in each of the neurons that compose the engram in male mice. Moreover, we show that only crucial fear engrams are amplified and that the amplification mechanism is induced days after training completion. The engram amplification is correlated with intense and enduring freezing response upon retrieval; blocking the amplification dramatically reduces the freezing response. Thus, days after training, engrams that encode crucial information are promoted to dominance through the induction of the amplification mechanism. We introduce a learning functionality in which the strength of a critical engram is biasedly increased, therefore ensuring its dominance of the behavioral response. Neural mechanisms underlying long-lasting traumatic memories are not fully understood. Here authors show that only crucial fear engram, induced by intense fear conditioning, will be amplified. Furthermore, then authors identify the precise biophysical and molecular mechanism that underlies the amplification mechanism.

In many mammals, including rodents, social interactions are often accompanied by active urination (micturition), which is considered a mechanism for spatial scent marking. Urine and fecal deposits contain a variety of chemosensory signals that convey information about the individual’s identity, genetic strain, social rank, and physiological or hormonal state. Furthermore, scent marking has been shown to be influenced by the social context and by the individual’s internal state and experience. Therefore, analyzing scent-marking behavior during social interactions can provide valuable insight into the structure of mammalian social interactions in health and disease. However, conducting such analyses has been hindered by several technical challenges. For example, the widely used void spot assay lacks temporal resolution and is prone to artifacts, such as urine smearing. To solve these issues, recent studies employed thermal imaging for the spatio-temporal analysis of urination activity. However, this method involved manual analysis, which is time-consuming and susceptible to observer bias. Moreover, defecation activity was hardly analyzed by previous studies. In the present study, we integrate thermal imaging with an open-source algorithm based on a transformer-based video classifier for automatic detection and classification of urine and fecal deposits made by male and female mice during various social behavior assays. Our results reveal distinct dynamics of urination and defecation in a test-, strain-, and sex-dependent manner, indicating two separate processes of scent marking in mice. We validate this algorithm, termed by us DeePosit, and show that its accuracy is comparable to that of a human annotator and that it is efficient in various setups and conditions. Thus, the method and tools introduced here enable efficient and unbiased automatic spatio-temporal analysis of scent-marking behavior in the context of behavioral experiments in small rodents. Scientists conduct behavioral experiments on animals to study brain mechanisms that govern social behavior and how these may be affected by various conditions. For example, in rodents, urination and defecation are important social activities used for communication and territory marking, and they are influenced by the emotional state of an individual. In the past, these activities were analyzed at the end of an experiment by shining ultraviolet light on a filter paper placed on the floor of the cages. However, this method does not provide information on when urination or defecation occurred. Also, in many cases, urine drops are smeared on the filter paper due to the animal's movement during the experiment, which reduces the accuracy of this method. To bridge this gap, Peles et al. developed a computer-vision algorithm – named DeePosit – to automatically track mice's urination and defecation activities during social behavior experiments recorded with a thermal camera. To examine the efficiency of the tool, the researchers analyzed the urination and defecation activities of mice during several social behavior tests. They then tested whether these activities changed over time and if there were differences between male and female mice, or between different strains of laboratory mice. The analysis revealed that the tool could identify the time and location of each urination and defecation event with an accuracy similar to that of a human observer. Using this tool, Peles et al. demonstrated that urination and defecation activities changed during a social encounter, for example, urination became more frequent. They observed that males urinated more often than females, which may be attributed to differences in their territorial behavior. It also revealed differences between laboratory strains. Peles et al. are confident that this rapid, unbiased and cost-effective tool can improve the analysis of social behavior in animals, particularly rodents. This will be especially relevant for researchers investigating the effect of treatments in mouse models of various disorders. The tool can also be trained and adapted to different behavioral and experimental contexts. It may allow a comparison of an additional important aspect of social behavior in treated and non-treated animals, and in health and disease.

Background Deciphering the biological mechanisms underlying social behavior in animal models requires standard behavioral paradigms that can be unbiasedly employed in an observer- and laboratory-independent manner. During the past decade, the three-chamber test has become such a standard paradigm used to evaluate social preference (sociability) and social novelty preference in mice. This test suffers from several caveats, including its reliance on spatial navigation skills and negligence of behavioral dynamics. Methods Here, we present a novel experimental apparatus and an automated analysis system which offer an alternative to the three-chamber test while solving the aforementioned caveats. The custom-made apparatus is simple for production, and the analysis system is publically available as an open-source software, enabling its free use. We used this system to compare the dynamics of social behavior during the social preference and social novelty preference tests between male and female C57BL/6J mice. Results We found that in both tests, male mice keep their preference towards one of the stimuli for longer periods than females. We then employed our system to define several new parameters of social behavioral dynamics in mice and revealed that social preference behavior is segregated in time into two distinct phases. An early exploration phase, characterized by high rate of transitions between stimuli and short bouts of stimulus investigation, is followed by an interaction phase with low transition rate and prolonged interactions, mainly with the preferred stimulus. Finally, we compared the dynamics of social behavior between C57BL/6J and BTBR male mice, the latter of which are considered as asocial strain serving as a model for autism spectrum disorder. We found that BTBR mice ( n  = 8) showed a specific deficit in transition from the exploration phase to the interaction phase in the social preference test, suggesting a reduced tendency towards social interaction. Conclusions We successfully employed our new experimental system to unravel previously unidentified sex- and strain-specific differences in the dynamics of social behavior in mice. Thus, the system presented here facilitates a more thorough and detailed analysis of social behavior in small rodent models, enabling a better comparison between strains and treatments.

Mammalian social organizations require the ability to recognize and remember individual conspecifics. This social recognition memory (SRM) can be examined in rodents using their innate tendency to investigate novel conspecifics more persistently than familiar ones. Here we used the SRM paradigm to examine the influence of housing conditions on the social memory of adult rats. We found that acute social isolation caused within few days a significant impairment in acquisition of short-term SRM of male and female rats. Moreover, SRM consolidation into long-term memory was blocked following only one day of social isolation. Both impairments were reversible, but with different time courses. Furthermore, only the impairment in SRM consolidation was reversed by systemic administration of arginine-vasopressin (AVP). In contrast to SRM, object recognition memory was not affected by social isolation. We conclude that acute social isolation rapidly induces reversible changes in the brain neuronal and molecular mechanisms underlying SRM, which hamper its acquisition and completely block its consolidation. These changes occur via distinct, AVP sensitive and insensitive mechanisms. Thus, acute social isolation of rats swiftly causes changes in their brain and interferes with their normal social behavior.