Rescue-like Behavior in a Bystander Mouse Toward Anesthetized Conspecifics Promotes Arousal Via a Tongue-brain Connection

Overview

Journal Sci Adv

Date 2025 Jan 22

PMID 39841840

Authors

Peng Cao

Ying Liu

Ziyun Ni

Mingjun Zhang

Hong-Rui Wei

An Liu

Jin-Rong Guo

Yumeng Yang

Zheng Xu

Yuyu Guo

Zhi Zhang

Wenjuan Tao

Likui Wang

Affiliations

Soon will be listed here.

Abstract

Prosocial behaviors are advantageous to social species, but the neural mechanism(s) through which others receive benefit remain unknown. Here, we found that bystander mice display rescue-like behavior (tongue dragging) toward anesthetized cagemates and found that this tongue dragging promotes arousal from anesthesia through a direct tongue-brain circuit. We found that a direct circuit from the tongue → glutamatergic neurons in the mesencephalic trigeminal nucleus (MTN) → noradrenergic neurons in the locus coeruleus (LC) drives rapid arousal in the anesthetized mice that receive the rescue-like behavior from bystanders. Artificial inhibition of this circuit abolishes the rapid arousal effect induced by the rescue-like behavior. Further, we revealed that glutamatergic neurons in the paraventricular nucleus of the thalamus (PVT) that project to the nucleus accumbens shell (NAcSh) mediate the rescue-like behavior. These findings reveal a tongue-brain connection underlying the rapid arousal effects induced by rescue-like behavior and the circuit basis governing this specific form of prosocial behavior.

References

Tachikawa K, Yoshihara Y, Kuroda K . Behavioral transition from attack to parenting in male mice: a crucial role of the vomeronasal system. J Neurosci. 2013; 33(12):5120-6. PMC: 6705007. DOI: 10.1523/JNEUROSCI.2364-12.2013. View

Dauvergne C, Smit A, Valla J, Diagne M, Buisseret-Delmas C, Buisseret P . Are locus coeruleus neurons involved in blinking?. Neurosci Res. 2008; 61(2):182-91. DOI: 10.1016/j.neures.2008.02.005. View

Wei D, Talwar V, Lin D . Neural circuits of social behaviors: Innate yet flexible. Neuron. 2021; 109(10):1600-1620. PMC: 8141016. DOI: 10.1016/j.neuron.2021.02.012. View

Labouebe G, Boutrel B, Tarussio D, Thorens B . Glucose-responsive neurons of the paraventricular thalamus control sucrose-seeking behavior. Nat Neurosci. 2016; 19(8):999-1002. PMC: 4964931. DOI: 10.1038/nn.4331. View

Langford D, Tuttle A, Briscoe C, Harvey-Lewis C, Baran I, Gleeson P . Varying perceived social threat modulates pain behavior in male mice. J Pain. 2010; 12(1):125-32. DOI: 10.1016/j.jpain.2010.06.003. View

Sivaselvachandran S, Acland E, Abdallah S, Martin L . Behavioral and mechanistic insight into rodent empathy. Neurosci Biobehav Rev. 2016; 91:130-137. DOI: 10.1016/j.neubiorev.2016.06.007. View

Ci H, Wu N, Su Y . Clock gene modulates roles of OXTR and AVPR1b genes in prosociality. PLoS One. 2014; 9(10):e109086. PMC: 4195688. DOI: 10.1371/journal.pone.0109086. View

Rogers-Carter M, Djerdjaj A, Gribbons K, Varela J, Christianson J . Insular Cortex Projections to Nucleus Accumbens Core Mediate Social Approach to Stressed Juvenile Rats. J Neurosci. 2019; 39(44):8717-8729. PMC: 6820210. DOI: 10.1523/JNEUROSCI.0316-19.2019. View

Menon R, Neumann I . Detection, processing and reinforcement of social cues: regulation by the oxytocin system. Nat Rev Neurosci. 2023; 24(12):761-777. DOI: 10.1038/s41583-023-00759-w. View

10.

Yokomizo Y, Murai Y, Tanaka E, Inokuchi H, Kusukawa J, Higashi H . Excitatory GABAergic synaptic potentials in the mesencephalic trigeminal nucleus of adult rat in vitro. Neurosci Res. 2005; 51(4):463-74. DOI: 10.1016/j.neures.2004.12.016. View

11.

Rogers-Carter M, Djerdjaj A, Culp A, Elbaz J, Christianson J . Familiarity modulates social approach toward stressed conspecifics in female rats. PLoS One. 2018; 13(10):e0200971. PMC: 6168124. DOI: 10.1371/journal.pone.0200971. View

12.

Zeng Q, Shan W, Zhang H, Yang J, Zuo Z . Paraventricular thalamic nucleus plays a critical role in consolation and anxious behaviors of familiar observers exposed to surgery mice. Theranostics. 2021; 11(8):3813-3829. PMC: 7914349. DOI: 10.7150/thno.45690. View

13.

Stanek 4th E, Cheng S, Takatoh J, Han B, Wang F . Monosynaptic premotor circuit tracing reveals neural substrates for oro-motor coordination. Elife. 2014; 3:e02511. PMC: 4041139. DOI: 10.7554/eLife.02511. View

14.

Fortin S, Chen J, Grill H, Hayes M . The Mesencephalic Trigeminal Nucleus Controls Food Intake and Body Weight via Hindbrain POMC Projections. Nutrients. 2021; 13(5). PMC: 8152732. DOI: 10.3390/nu13051642. View

15.

Takatoh J, Park J, Lu J, Li S, Thompson P, Han B . Constructing an adult orofacial premotor atlas in Allen mouse CCF. Elife. 2021; 10. PMC: 8137149. DOI: 10.7554/eLife.67291. View

16.

Wu Y, Hong W . Neural basis of prosocial behavior. Trends Neurosci. 2022; 45(10):749-762. PMC: 10039809. DOI: 10.1016/j.tins.2022.06.008. View

17.

Wu Y, Dang J, Kingsbury L, Zhang M, Sun F, Hu R . Neural control of affiliative touch in prosocial interaction. Nature. 2021; 599(7884):262-267. PMC: 8605624. DOI: 10.1038/s41586-021-03962-w. View

18.

de Waal F . Putting the altruism back into altruism: the evolution of empathy. Annu Rev Psychol. 2007; 59:279-300. DOI: 10.1146/annurev.psych.59.103006.093625. View

19.

Shemesh Y, Forkosh O, Mahn M, Anpilov S, Sztainberg Y, Manashirov S . Ucn3 and CRF-R2 in the medial amygdala regulate complex social dynamics. Nat Neurosci. 2016; 19(11):1489-1496. DOI: 10.1038/nn.4346. View

20.

Cao P, Zhang M, Ni Z, Song X, Yang C, Mao Y . Green light induces antinociception via visual-somatosensory circuits. Cell Rep. 2023; 42(4):112290. DOI: 10.1016/j.celrep.2023.112290. View