Direct exposure to stimuli in their environment is not the only way that animals learn about important information. Individuals can infer fear from a social context through observation. Like humans, rats are very social animals, and may learn to infer information about their environment through their interactions with conspecifics. Here, we first review different models for social transmission of information in rodents. Second, we examine different modes of communication that are important to social learning. Then, we cover the different proximate factors that are thought to modulate the social transmission of information. Next, we identify social and environmental conditions that impact social learning, and finally, we conclude by revisiting social transmission through the lens of the Tinbergen framework.

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Fear conditioning is widely employed to study dysregulations of the fear system. The repeated presentation of a conditioned stimulus in the absence of a reinforcer leads to a decrease in fear responding-a phenomenon known as extinction. From a translational perspective, identifying whether an individual might respond well to extinction prior to intervention could prove important to treatment outcomes. Here, we test the hypothesis that CO reactivity predicts extinction phenotype in rats, and that variability in CO reactivity as well as extinction long-term memory (LTM) significantly predicts orexin activity in the lateral hypothalamus (LH). Our results validate a rat model of CO reactivity and show that subcomponents of behavioral reactivity following acute CO exposure explain a significant portion of the variance in extinction LTM. Furthermore, we show evidence that variability in CO reactivity is also significantly predictive of orexin activity in the LH, and that orexin activity, in turn, significantly accounts for LTM variance. Our findings open the possibility that we may be able to use CO reactivity as a screening tool to determine if individuals are good candidates for an extinction/exposure-based approach.

In the social transmission of food preference paradigm, naive observer rats acquire safety information about novel food sources in the environment through social interaction with a demonstrator rat that has recently eaten said food. Research into the behavioural mechanisms governing this form of learning has found that observers show increased reliance on socially acquired information when the state of the environment makes personal examination of their surroundings risky. We aimed to (1) determine whether reliance on social information would decrease if previous reliance on social learning was unsuccessful, and (2) whether reliance on the specific demonstrator that had transmitted poor information would similarly decrease. By inducing illness in observers following consumption of a socially demonstrated food, we created an environmental situation in which reliance on socially acquired information was maladaptive. We found that under these conditions, observers showed no change in their reliance on a specific demonstrator or socially learned information in general. Our experiment also unexpectedly produced results showing that recent demonstrators were more influential in later transmissions than demonstrators that had been learned from less recently. Notably, this effect only emerged when the observer simultaneously interacted with both demonstrators, indicating that demonstrators must be in direct competition for this effect to manifest.

We describe a method of social fear transmission to a discrete auditory cue in freely behaving rats. Extending beyond traditional observer/demonstrator paradigms, rats are allowed to physically interact and integrate cues from all sensory modalities. In the protocol described in this article, "observer" rats experience social fear conditioning through a proxy cage mate that serves as a "demonstrator" during retrieval of a cued fear memory. We find that a specific auditory cue can come to elicit fear expression in an animal with no foot shock experience simply by interacting with a conspecific expressing a conditioned response in the presence of an otherwise benign stimulus. In this "fear conditioning by proxy" paradigm, we have demonstrated that some, but not all, rats display conditioned responding (e.g., freezing) to a cue after interacting with a cage mate during fear memory retrieval. The amount of freezing exhibited by this fear conditioned "by proxy" rat 24 hr after learning critically depends on social influences, including social relationships and social interactions during learning. © 2018 by John Wiley & Sons, Inc.

Renewal of appetitive behavior depends on the gonadal hormonal state of the female rat. In this experiment the effect of female rat estrous cycle stage on renewal of appetitive behaviors is replicated and extended upon to understand how endogenous hormonal states around the estrous cycle drive renewal at the neuronal population level. Estrous cycle stage (i.e., proestrus (P, high hormone) or metestrus/diestrus (M/D, low hormone)) was considered during two important learning and behavioral expression windows: at extinction training and during LTM/renewal testing. First, rats in P during context-dependent extinction training but in some other stage of the estrous cycle during long-term memory and renewal testing (Different) were shown to exhibit more renewal of conditioned foodcup (but not conditioned orienting) behavior compared to rats in other estrous cycle groups. Next, cellular compartment analysis of temporal activity using fluorescence in situ hybridization (catFISH) was used to examine immediate early gene activity of Arc mRNA in neuronal populations after distinct context-stimulus exposures (i.e., extinction and acquisition test contexts). Arc mRNA expression patterns were examined in the prefrontal cortex (PFC), amygdala, hippocampus (HPC), and paraventricular nucleus of the thalamus. P-different rats showed differential neuronal population activity in the infralimbic cortex of the PFC, the lateral amygdaloid nucleus, and both CA1 and CA3 regions of the dorsal HPC. In each region P-different rats exhibited more co-expression and less specificity of Arc mRNA compared to other hormonal groups, indicating that renewal of appetitive foodcup behavior induces Arc mRNA in overlapping neuronal populations in female rats.

Learning can occur via direct experience or through observation of another individual (i.e., social learning). While research focused on understanding the neural mechanisms of direct learning is prevalent, less work has examined the brain circuitry mediating the acquisition and recall of socially acquired information. Here, we aimed to further elucidate the mechanisms underlying recall of socially acquired information by having male and female rats sequentially recall a socially transmitted food preference (STFP) and a fear association via fear conditioning by-proxy (FCbP). Brain tissue was processed for mRNA expression of the immediate early gene (IEG) Arc, which expresses in the nucleus following transcription before migrating to the cytoplasm over the next 25 min. Given this timeframe, we could identify whether Arc transcription was triggered by STFP recall, FCbP recall, or both. Contrary to past research, we found no differences in any Arc expression measures across a number of prefrontal regions and the ventral CA3 of the hippocampus between controls, demonstrators, and observers. We theorize that these results may indicate that relatively little Arc-dependent neural restructuring is taking place in the prefrontal cortices and ventral CA3 following recall of recently socially acquired information or directly acquired fear associations in these areas.

IntroductionRenewal is a behavioral phenomenon wherein extinction learning fails to generalize between different contextual environments, thereby representing a significant challenge to extinction-based rehabilitative therapies. Previously, we have shown that renewal of extinguished appetitive behavior differs across the estrous cycle of the female rat. In this experiment that effect is replicated and extended upon to understand how the estrous cycle may modulate contextual representation at the neuronal population level to drive renewal.MethodsEstrous cycle stage [i.e., proestrus (P, high hormone) or metestrus/diestrus (M/D, low hormone)] was considered during two important learning and behavioral expression windows: at extinction training and during long-term memory (LTM)/renewal testing. Cellular compartment analysis of temporal activity using fluorescence in situ hybridization (catFISH) for Arc mRNA was conducted after the distinct context-stimulus exposures.ResultsRats in P during context-dependent extinction training but in a different stage of the estrous cycle during LTM and renewal testing (P-different) were shown to exhibit more renewal of conditioned foodcup (but not conditioned orienting) behavior compared to rats in other estrous cycle groups. Importantly, we discovered this depends on the order of tests. P-different rats showed differential Arc mRNA expression in regions of the prefrontal cortex (PFC), amygdala, and hippocampus (HPC). For each case P-different rats had more co-expression (i.e., expression of both nuclear and cytoplasmic) of Arc mRNA compared to other groups; specific to the dorsal HPC, P-different rats also had a more robust Arc mRNA response to the extinction context exposure.ConclusionThese data suggest female rats show estrous cycle state-dependent renewal of appetitive behavior, and differences in context and conditioned stimulus representation at the neuronal level may drive this effect.