Correlated Neural Activity and Encoding of Behavior across Brains of Socially Interacting Animals

Kingsbury, Lyle; Huang, Shan; Wang, Jun; Gu, Ken; Golshani, Peyman; Wu, Ye; Hong, Weizhe

doi:10.1016/j.cell.2019.05.022

Cited by 255 publications

(265 citation statements)

References 48 publications

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“…Multiple lines of evidence indicate that the IL-PFC processes social information and modulates fear responses, although few studies have examined the potential convergence of these functions. The IL-PFC exhibits robust neuronal activity during social interaction [31][32][33], and we confirmed that interaction with either a novel or familiar conspecific results in increased c-fos + expression within this region [52]. Likewise, the IL-PFC is required for extinction of fear [44,53,54].…”

Section: Discussionsupporting

confidence: 76%

“…Given the highly conserved nature of social buffering, its underlying neural mechanisms are hypothesized to be shared across taxa [12,30]. In particular, the PFC modulates social behavior [31][32][33], fear responses [34,35], and resilience to stressors [36][37][38]. Critically, inhibition of the PFC with the GABA agonist, muscimol, blocks the effects of social familiarity in reducing anxiety-like behaviors (Lungwitz et al, 2014), suggesting a potentially direct role for the PFC in social buffering of fear and/or anxiety.…”

Section: Introductionmentioning

confidence: 99%

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Optogenetic reactivation of prefrontal social memory trace mimics social buffering of fear

Ahuna

Santos

et al. 2019

Preprint

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Social buffering occurs when the presence of a companion attenuates the physiological and/or behavioral effects of a stressful or fear-provoking event. It represents a way in which social interactions can immediately and potently modulate behavior. As such, social buffering is one mechanism by which strong social support increases resilience to mental illness. While the behavioral and neuroendocrine impacts of social buffering are well studied in multiple species, including humans, the neuronal bases of this behavioral phenomenon remain largely unexplored. Previous work has shown that the infralimbic prefrontal cortex (IL-PFC) is important for processing social information and, in separate studies, for modulating fear and anxiety. Thus, we hypothesized that socially-active cells within the IL-PFC may integrate social information to modulate fear responsivity. To test this hypothesis, we employed social buffering paradigms in male and female mice. Similar to prior studies in rats, we found that the presence of a cagemate reduced freezing in fear and anxiety-provoking contexts. In accordance with previous work, we demonstrated that interaction with a novel or familiar conspecific induces activity in the IL-PFC as evidenced by increased immediate early gene (IEG) expression. We then utilized an activity-dependent tagging murine line, the ArcCreER T2 mice, to express channelrhodopsin (ChR2) in neurons active during the social encoding of a new cagemate. We found that optogenetic reactivation of these sociallyactive neuronal ensembles phenocopied the effects of cagemate presence in male and female mice in learned and innate fear contexts without being inherently rewarding or altering locomotion. These data suggest that a social neuronal ensemble within the IL-PFC may contribute to social buffering of fear. These neurons may represent a novel therapeutic target for fear and anxiety disorders.

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Section: Discussionsupporting

confidence: 76%

Section: Introductionmentioning

confidence: 99%

Optogenetic reactivation of prefrontal social memory trace mimics social buffering of fear

Ahuna

Santos

et al. 2019

Preprint

View full text Add to dashboard Cite

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“…Thus, imaging approaches can reveal how individual cells embedded in a larger network display coordinated activity during different stages of behavior or training (Wagner et al 2017;Heffley et al 2018;Galiñanes, Bonardi, and Huber 2018;Giovannucci et al 2017) . Moreover, because of their ability to record in freely moving animals, miniscopes have been instrumental in uncovering neural activity patterns occurring during natural behaviors and related brain-states including social interactions (Murugan et al 2017;Remedios et al 2017;Liang et al 2018;Kingsbury et al 2019) or sleep Cox, Pinto, and Dan 2016) with fully intact vestibular input.…”

Section: Introductionmentioning

confidence: 99%

NINscope: a versatile miniscope for multi-region circuit investigations

Groot

Boom

Genderen

et al. 2019

Preprint

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Miniaturized fluorescence microscopes (miniscopes) have been instrumental to monitor neural activity during unrestrained behavior and their open-source versions have helped to distribute them at an affordable cost. Generally, the footprint and weight of open-source miniscopes is sacrificed for added functionality. Here, we present NINscope: a light-weight, small footprint open-source miniscope that incorporates a high-sensitivity image sensor, an inertial measurement unit (IMU), and an LED driver for an external optogenetic probe. We highlight the advantages of NINscope by performing the first simultaneous cellular resolution (dual scope) recordings from cerebellum and cerebral cortex in unrestrained mice, revealing that the activity of both regions generally precede the onset of behavioral acceleration. At the same time, we demonstrate the optogenetic stimulation capabilities of NINscope and show that cerebral cortical activity can be driven strongly by cerebellar stimulation. Finally, we combine optogenetic stimulation of cortex with imaging in the dorsal striatum and replicate previous studies that show action space is encoded by neurons in this subcortical region. In combination with cross-platform control software NINscope is a versatile addition to the expanding toolbox of open-source miniscopes and will aid multi-region circuit investigations during unrestrained behavior.

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“…RM is an unconscious, congruent, and rapid response (less than 1 s) during which human and non-human animals automatically mimic others' expressions and movements [13,32]. RM has been demonstrated not only in humans but also in several primate [33][34][35][36], rodent [27,37], and carnivore species [31,38,39].…”

Section: Rapid Mimicry: the Key For Fair Play And Bonding Successmentioning

confidence: 99%

Intraspecific Motor and Emotional Alignment in Dogs and Wolves: The Basic Building Blocks of Dog–Human Affective Connectedness

Palagi

Cordoni

2020

Animals

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Involuntary synchronization occurs when individuals perform the same motor action patterns during a very short time lapse. This phenomenon serves an important adaptive value for animals permitting them to socially align with group fellows thus increasing integration and fitness benefits. Rapid mimicry (RM) and yawn contagion (YC) are two behavioral processes intermingled in the animal synchronization domain. Several studies demonstrated that RM and YC are socially modulated being more frequently performed by individuals sharing close relationships. This evidence highlights the relation between RM/YC and emotional contagion that is the capacity of two or more individuals to share the same affective state. In this review, we try to delineate a possible developmental trajectory of emotional sharing phenomena by using, as a model species, the domestic dog (Canis lupus familiaris), a valid example of empathic predisposition towards individuals belonging both to the same and the different species. We contrast available findings on RM and YC in dog–dog and dog–human dyads with those in wolf–wolf dyads, in order to investigate if the ability to emotionally engage with conspecifics (wolf–wolf and dog–dog) is evolutionary rooted in canids and if provides the basis for the development of inter-specific emotional sharing (dog–human).

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Correlated Neural Activity and Encoding of Behavior across Brains of Socially Interacting Animals

Cited by 255 publications

References 48 publications

Optogenetic reactivation of prefrontal social memory trace mimics social buffering of fear

Optogenetic reactivation of prefrontal social memory trace mimics social buffering of fear

NINscope: a versatile miniscope for multi-region circuit investigations

Intraspecific Motor and Emotional Alignment in Dogs and Wolves: The Basic Building Blocks of Dog–Human Affective Connectedness

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