Dynamics of a disinhibitory prefrontal microcircuit in controlling social competition

Zhang, Chaoyi; Hong, Zhu; Ni, Zheyi; Xin, Qiuhong; Zhou, Tingting; Wu, Runlong; Gao, Guangping; Gao, Zhihua; Ma, Hongxia; Li, Hao‐Hong; He, Miao; Zhang, Jue; Cheng, Heping; Hu, Hailan

doi:10.1016/j.neuron.2021.10.034

Cited by 53 publications

(36 citation statements)

References 99 publications

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“…Therefore, how these neurons encode relevant but distinct social information is unknown. In addition, although we know that GABAergic (gamma-aminobutyric acid-releasing) interneurons (INs) within the mPFC are associated with social behaviors ( 10 , 19 – 22 ), how this normal social information is processed at the single-cell level is still unknown.…”

Section: Introductionmentioning

confidence: 99%

Encoding of social novelty by sparse GABAergic neural ensembles in the prelimbic cortex

et al. 2022

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Although the prelimbic (PrL) area is associated with social behaviors, the neural ensembles that regulate social preference toward novelty or familiarity remain unknown. Using miniature two-photon microscopy (mTPM) to visualize social behavior–associated neuronal activity within the PrL in freely behaving mice, we found that the Ca 2+ transients of GABAergic neurons were more highly correlated with social behaviors than those of glutamatergic neurons. Chemogenetic suppression of social behavior–activated GABAergic neurons in the PrL disrupts social novelty behaviors. Restoring the MeCP2 level in PrL GABAergic neurons in MECP2 transgenic ( MECP2 -TG) mice rescues the social novelty deficits. Moreover, we identified and characterized sparsely distributed NewPNs and OldPNs of GABAergic interneurons in the PrL preferentially responsible for new and old mouse exploration, respectively. Together, we propose that social novelty information may be encoded by the responses of NewPNs and OldPNs in the PrL area, possibly via synergistic actions on both sides of the seesaw.

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Section: Introductionmentioning

confidence: 99%

Encoding of social novelty by sparse GABAergic neural ensembles in the prelimbic cortex

et al. 2022

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“…Firstly, it is unknown whether pain and itch activate the same population of ZI PV neurons. This issue could be addressed by in vivo miniscope, miniature two-photon imaging or multi-channel extracellular recordings ( de Groot et al, 2020 ; Zhang et al, 2021 ), which helps determine whether individual ZI PV neuron responds to both pain and itch stimuli. In addition, the utilization of the targeted recombination in active populations system in Fos-CreER transgenic mice ( Sanders et al, 2019 ) allows to determine whether selective manipulation of itching-responsive ZI neurons influences pain behaviors.…”

Section: Discussionmentioning

confidence: 99%

Parvalbumin Neurons in Zona Incerta Regulate Itch in Mice

Bai

Liang

et al. 2022

Front. Mol. Neurosci.

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Pain and itch are intricately entangled at both circuitry and behavioral levels. Emerging evidence indicates that parvalbumin (PV)-expressing neurons in zona incerta (ZI) are critical for promoting nocifensive behaviors. However, the role of these neurons in itch modulation remains elusive. Herein, by combining FOS immunostaining, fiber photometry, and chemogenetic manipulation, we reveal that ZI PV neurons act as an endogenous negative diencephalic modulator for itch processing. Morphological data showed that both histamine and chloroquine stimuli induced FOS expression in ZI PV neurons. The activation of these neurons was further supported by the increased calcium signal upon scratching behavior evoked by acute itch. Behavioral data further indicated that chemogenetic activation of these neurons reduced scratching behaviors related to histaminergic and non-histaminergic acute itch. Similar neural activity and modulatory role of ZI PV neurons were seen in mice with chronic itch induced by atopic dermatitis. Together, our study provides direct evidence for the role of ZI PV neurons in regulating itch, and identifies a potential target for the remedy of chronic itch.

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“…Notably, cingulate parvalbumin-positive interneurons seem to be required for hierarchical behavior as well, since the chemogenetic inhibition of this inhibitory population leads to a pronounced decline in competitive performance among dominant mice, whereas chemogenetic excitation causes a striking increase in competitive performance among subordinate mice (Nelson et al, 2019 ). More recently, an interneuron-based gating mechanism was described in PFC capable of acting as a switch between dominance and subordination (Zhang et al, 2022 ; Figure 3B-1 ). Increased activity of local vasoactive intestinal polypeptide (VIP) interneurons in PFC leads to direct inhibition of local parvalbumin (PV) interneurons, generating a window of opportunity for increased excitability in L5 pyramidal neurons, resulting in dominance.…”

Section: Mesoscale and Microscale Mechanisms Supporting Social Hierar...mentioning

confidence: 91%

“…It would be relevant to assess if SWR could evoke plasticity changes in prefrontal layer 5 pyramidal neurons by strengthening the vCA1-PFC synapses and whether this mechanism would impact the social rank and hierarchical behavior. In light of the recent findings of an interneuron-based gating mechanism for dominance and subordination in PFC (Zhang et al, 2022 ), it would be also relevant to test whether vCA1 can modulate the gate since there is a well-known projection from vCA1 to the PV interneurons in PFC, whose inhibition produces deficits in social memory (Sun et al, 2020 ). It would be expected that excitation of PV interneurons in PFC by the same pathway would modulate hierarchical behavior, specifically leading to subordination, establishing a definitive link between hierarchical behavior and social memory, thus explaining the former observation that stress prior to a social encounter leads to long-term subordinate behavior, due to amplification of memory, or, more specifically, due to a putative increase in vCA1-triggered excitation of PV interneurons in PFC.…”

Section: New Directions: Emerging Candidates In Social Hierarchiesmentioning

confidence: 99%

The Neural Circuit Architecture of Social Hierarchy in Rodents and Primates

Ferreira-Fernandes

Peça

2022

Front. Cell. Neurosci.

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Social status is recognized as a major determinant of social behavior and health among animals; however, the neural circuits supporting the formation and navigation of social hierarchies remain under extensive research. Available evidence suggests the prefrontal cortex is a keystone in this circuit, but upstream and downstream candidates are progressively emerging. In this review, we compare and integrate findings from rodent and primate studies to create a model of the neural and cellular networks supporting social hierarchies, both from a macro (i.e., circuits) to a micro-scale perspective (microcircuits and synapses). We start by summarizing the literature on the prefrontal cortex and other relevant brain regions to expand the current “prefrontal-centric” view of social hierarchy behaviors. Based on connectivity data we also discuss candidate regions that might inspire further investigation, as well as the caveats and strategies that have been used to further our understanding of the biological substrates underpinning social hierarchy and dominance.

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Dynamics of a disinhibitory prefrontal microcircuit in controlling social competition

Cited by 53 publications

References 99 publications

Encoding of social novelty by sparse GABAergic neural ensembles in the prelimbic cortex

Encoding of social novelty by sparse GABAergic neural ensembles in the prelimbic cortex

Parvalbumin Neurons in Zona Incerta Regulate Itch in Mice

The Neural Circuit Architecture of Social Hierarchy in Rodents and Primates

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