Many mammals have evolved to be social creatures. In humans, the ability to learn from others' experiences is essential to survival; and from an early age, individuals are surrounded by a social environment that helps them develop a variety of skills, such as walking, talking, and avoiding danger. Similarly, in rodents, behaviors, such as food preference, exploration of novel contexts, and social approach, can be learned through social interaction. Social encounters facilitate new learning and help modify preexisting memories throughout the lifespan of an organism. Moreover, social encounters can help buffer stress or the effects of negative memories, as well as extinguish maladaptive behaviors. Given the importance of such interactions, there has been increasing work studying social learning and applying its concepts in a wide range of fields, including psychotherapy and medical sociology. The process of social learning, including its neural and behavioral mechanisms, has also been a rapidly growing field of interest in neuroscience. However, the term "social learning" has been loosely applied to a variety of psychological phenomena, often without clear definition or delineations. Therefore, this review gives a definition for specific aspects of social learning, provides an overview of previous work at the circuit, systems, and behavioral levels, and finally, introduces new findings on the social modulation of learning. We contextualize such social processes in the brain both through the role of the hippocampus and its capacity to process "social engrams" as well as through the brainwide realization of social experiences. With the integration of new technologies, such as optogenetics, chemogenetics, and calcium imaging, manipulating social engrams will likely offer a novel therapeutic target to enhance the positive buffering effects of social experiences or to inhibit fear-inducing social stimuli in models of anxiety and post-traumatic stress disorder.

Systems consolidation (SC) theory proposes that recent, contextually rich memories are stored in the hippocampus (HPC). As these memories become remote, they are believed to rely more heavily on cortical structures within the prefrontal cortex (PFC), where they lose much of their contextual detail and become schematized. Odor is a particularly evocative cue for intense remote memory recall and despite these memories being remote, they are highly contextual. In instances such as posttraumatic stress disorder (PTSD), intense remote memory recall can occur years after trauma, which seemingly contradicts SC. We hypothesized that odor may shift the organization of salient or fearful memories such that when paired with an odor at the time of encoding, they are delayed in the de-contextualization process that occurs across time, and retrieval may still rely on the HPC, where memories are imbued with contextually rich information, even at remote time points. We investigated this by tagging odor-and non-odor-associated fear memories in male c57BL/6 mice and assessed recall and c-Fos expression in the dorsal CA1 (dCA1) and prelimbic cortex (PL) 1 or 21 d later. In support of SC, our data showed that recent memories were more dCA1-dependent whereas remote memories were more PL-dependent. However, we also found that odor influenced this temporal dynamic, biasing the memory system from the PL to the dCA1 when odor cues were present. Behaviorally, inhibiting the dCA1 with activity-dependent DREADDs had no effect on recall at 1 d and unexpectedly caused an increase in freezing at 21 d. Together, these findings demonstrate that odor can shift the organization of fear memories at the systems level.

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Significance Social interactions can bolster and protect memory performance. However, the relationship between social stimuli and individually learned memories remains enigmatic. Our work reveals that exposure to a stressed, naïve nonfamiliar conspecific or to the ambient olfactory–auditory cues of a recently stressed familiar conspecific induces reactivation of the cellular ensembles associated with a fear memory in the hippocampus. Artificially stimulating the hippocampal ensemble active during the social experience induces fearful behaviors in animals that have previously acquired a negative memory, revealing the interaction between individual history and social experience. The neural resurgence of fear-driving ensembles during social experiences leads to a context-specific enhancement of fear recall. Our findings provide evidence that unlike direct stressors, social stimuli reactivate and amplify an individual’s memories.

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