Optogenetic reactivation of prefrontal social neural ensembles mimics social buffering of fear

Gutzeit, Vanessa A.; Ahuna, Kylia; Santos, Tabia; Cunningham, Ashley M.; Rooney, Meghin Sadsad; Zamora, Andrea; Denny, Christine A.; Donaldson, Zoe R.

doi:10.1038/s41386-020-0631-1

Cited by 35 publications

(28 citation statements)

References 80 publications

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“…Of note, reactivating the IL neuronal ensembles involved in the original memory engram during remote fear extinction is thought to be required for fear attenuation 53 . Similarly, recruiting the IL neuronal population activated during social interaction can alleviate conditioned fear responses 54 . Collectively, data suggest that activity and plasticity in the IL during initial learning stages are essential for posterior suppression of fear.…”

Section: Discussionmentioning

confidence: 99%

Infralimbic cortex controls fear memory generalization and susceptibility to extinction during consolidation

Bayer

Bertoglio

2020

Sci Rep

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Lesioning or inactivating the infralimbic (IL) subregion of the medial prefrontal cortex before acquisition produces more generalized and extinction-resistant fear memories. However, whether and how it modulates memory specificity and extinction susceptibility while consolidation takes place is still unknown. The present study aims to investigate these questions using muscimol-induced temporary inactivation and anisomycin-induced protein synthesis inhibition in the rat IL following contextual fear conditioning. Results indicate that the IL activity immediately after acquisition, but not six hours later, controls memory generalization over a week, regardless of its strength. Such IL function depends on the context-shock pairing since muscimol induced no changes in animals exposed to immediate shocks or the conditioning context only. Animals in which the IL was inactivated during consolidation extinguished similarly to controls within the session but were unable to recall the extinction memory the following day. Noteworthy, these post-acquisition IL inactivation-induced effects were not associated with changes in anxiety, as assessed in the elevated plus-maze test. Anisomycin results indicate that the IL protein synthesis during consolidation contributes more to producing extinction-sensitive fear memories than memory specificity. Collectively, present results provide evidence for the IL's role in controlling generalization and susceptibility to extinction during fear memory consolidation.

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Section: Discussionmentioning

confidence: 99%

Infralimbic cortex controls fear memory generalization and susceptibility to extinction during consolidation

Bayer

Bertoglio

2020

Sci Rep

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“…S. Smith et al, 2016;Meira et al, 2018), ventral CA1 (Dudek et al, 2016;Mitre et al, 2016;A. S. Smith et al, 2016;Meira et al, 2018), and nucleus accumbens (Okuyama et al, 2016;Okuyama, 2018), as well as modulatory roles for the mPFC (Tanimizu et al, 2017;Gutzeit et al, 2020), ACC (Tanimizu et al, 2017), amygdala (Tanimizu et al, 2017;Fernández et al, 2018), lateral septum (Fernández et al, 2018), and hypothalamus (Dudek et al, 2016;Mitre et al, 2016;A. S. Smith et al, 2016).…”

Section: The Hippocampus and The Social Engrammentioning

confidence: 99%

“…We propose that the social engram in vCA1 may play a role in the enhanced effect with familiar conspecifics, given its various outputs to areas, including the PFC and amygdala. More specifically, odor of the conspecific is associated with the social engram of the familiar conspecific, which activates the IL cortex of the PFC (Spehr et al, 2006;Lungwitz et al, 2014;Levy et al, 2019;Gutzeit et al, 2020). The IL cortex, a major region for inhibition of fear expression, has direct projections to the ITCs of the amygdala (Amano et al, 2010;Ciocchi et al, 2010).…”

Section: Extinction Bufferingmentioning

confidence: 99%

Linking Social Cognition to Learning and Memory

Leblanc

Ramirez

2020

J. Neurosci.

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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.

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“…Therefore, the pair-exposed condition in this study provided more of a social buffering effect than a social contagion effect. Previous studies have also shown that the application of social buffering to the fear expression session or learning session reduces the animals’ freezing behavior compared to the isolated condition [ 27 , 28 ]. Therefore, we think that social buffering not only reduces the formation of fear memory but can also affect the increase in fear extinction.…”

Section: Discussionmentioning

confidence: 99%

Role of Medial Prefrontal Cortical Neurons and Oxytocin Modulation in the Establishment of Social Buffering

2021

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Fear-related behaviors are rigidly controlled by the medial prefrontal cortex (mPFC). The mPFC is activated by the prosocial hormone oxytocin, which plays an important role in social buffering. We used a slice patch current-clamp recording in single- and pair-exposed rats who were subjected to electric shocks, to determine the cellular mechanism of the action of oxytocin in the mPFC under social buffering conditions. Pair-exposed rats showed a significant reduction in both freezing and passive avoidance behaviors compared to single-exposed rats. It was observed that input resistance in pyramidal neurons decreased in both single- and pair-exposed rats than na?ve rats, but input resistance in interneurons increased in pair-exposed rats than single-exposed rats. We found that the number of action potential (AP) spikes in the mPFC pyramidal neurons decreased significantly in pair-exposed rats than in single-exposed rats. The pyramidal neurons in the mPFC were similarly regulated by oxytocin in singleand pair-exposed rats, while the number of AP spikes in interneurons by oxytocin decreased in single-exposed rats, but there was no significant change in pair-exposed rats. Therefore, our findings reveal that a decrease in mPFC pyramidal neuronal activity in pair-exposed rats through social interaction induces a reduction in fear-related behavior via obstruction of fear-memory formation; however, no such reduction was observed in single-exposed rats. Moreover, we suggest that the oxytocin-mediated decrease in neuronal activity in the mPFC could facilitate social buffering.

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Optogenetic reactivation of prefrontal social neural ensembles mimics social buffering of fear

Cited by 35 publications

References 80 publications

Infralimbic cortex controls fear memory generalization and susceptibility to extinction during consolidation

Infralimbic cortex controls fear memory generalization and susceptibility to extinction during consolidation

Linking Social Cognition to Learning and Memory

Role of Medial Prefrontal Cortical Neurons and Oxytocin Modulation in the Establishment of Social Buffering

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