Linking Social Cognition to Learning and Memory

Abstract

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.

Keywords: behavior; engram; learning; memory; optogenetics; social.

Figure 1.

The formation of a social engram. When a rodent has a social interaction with a novel conspecific, ensembles of cells embedded across neural circuits activate to form a stable representation of a social memory (depicted as the ensemble of green neurons on the right). Olfactory (purple traces between the novel conspecific and observer) and auditory (blue wave traces next to novel conspecific) information is relayed throughout the brain, including the hippocampus, which communicates with social loci of the brain, such as the nucleus accumbens and basolateral amygdala. Of the many brain regions involved in social cognition, the social engram is hypothesized to be formed in the hippocampus during sleep, primarily through SWRs from dorsal CA2 to ventral CA1, inducing synaptic consolidation (Okuyama, 2018; Oliva et al., 2020).

Figure 2.

STFP. A rodent (“demonstrator”) is exposed to a flavored food and allowed to eat it for a specified period of time. Next, the demonstrator is removed and placed near a conspecific (“observer”). The scent of the food and the chemical carbon disulfide (CS₂), a volatile from the demonstrator's breath, are detected by the “observer” during the social interaction. This single exposure leads the observer to prefer the scent and flavor associated with the demonstrator over a novel flavor when given the choice at a later time. This preference can last up to weeks in the observer rodents.

Figure 3.

Social fear learning paradigms. The two primary paradigms used to study social fear learning in rodents are observational fear conditioning and fear conditioning by proxy. Observational fear conditioning consists of a rodent (mouse or rat) observing a demonstrator conspecific receiving shocks (left). This paradigm elicits relatively robust learning in observer rodents whether the shock is paired with auditory stimuli or with context alone (represented by a yellow circle with stripes). In fear conditioning by proxy, a demonstrator rat undergoes auditory fear conditioning when alone (right). The following day, an observer rat is placed with the demonstrator conspecific, which is presented with tones from the previous fear-conditioning session without delivery of unconditioned stimuli. The fearful response of the demonstrator can elicit fear learning in the observer that is detectable the next day during a recall session.

Figure 4.

Two types of social buffering. In all paradigms, a rodent is fear-conditioned to auditory cues alone and then tested for recall 24 h later (see Kiyokawa et al., 2007). Recall in the solitary condition induces significant activation of CeA, LA, BA, and PAG, as indicated by red on the schematics of brain sections in the figure. Recall is also accompanied by activity in the HPA axis, SIH, and freezing behavior. In pair-housing, the rodent is housed with a conspecific for the 24 h between conditioning and recall. In this group, there is significant activation of the LA and PAG, but not of the BA and CeA. Although freezing behavior is still observed, there is reduced HPA activation and SIH. In pair exposure, the conditioned rodent is housed overnight in isolation but placed with a conspecific during recall. In this case, there is significant BA activation, and reduced HPA axis, CeA, and LA activity than when animals are housed and tested without conspecifics present. Freezing behavior is abolished in this condition, but SIH remains high. When a conspecific is present overnight as well as during testing, activation is reduced in all the aforementioned fear-associated regions, as well as a significant decrease in HPA axis activation, SIH, and freezing behavior.

Figure 5.

Proposed neural mechanisms of social buffering. During recall of a negative memory in rodents, fear is classically quantified as increases in freezing, which can be buffered with the presence of a conspecific (A–C). When placed back into the fear conditioning context with a conspecific, this shifts the scales of pro-fear (red weights) and reduced fear (green weights) toward the side of a mitigated fear response. The neural mechanisms are still unclear, but they include putative “buffering” olfactory information traveling from the medial olfactory bulb (MOB) to the anterior olfactory peduncle (AOP). This activation leads to excitation (depicted as green arrows) of the bundles of GABAergic neurons (ITCs) scattered around the amygdala. The excitation of the ITCs leads to inhibition (depicted as red blunted arrows) of the CeA and LA, leading to a decreased activation of the HPA axis (PVN activation) and corticotropin-releasing hormone (CRH) secretion. If the unfamiliar conspecific was also previously fear-conditioned and is therefore anxious in the chamber, the alarm pheromones and ultrasonic vocalizations elicited by the conspecific work against the buffering (A), leading to a less robust attention of freezing compared with a conspecific that is has not been fear-conditioned in the chamber with the subject (B). If the conspecific is nonfearful and familiar, the classical social-buffering neural circuit still applies. but the olfactory information of a familiar conspecific also travels from the MOB to the AOP, which activates the “social engram” in ventral CA1 (C). This activates the IL cortex of the mPFC, which is known to control fear responses by activating ITCs. The added excitation of the ITCs leads to an increased inhibition of the amygdala fear response and subsequent attenuation of the HPA axis response.