A dedicated hypothalamic oxytocin circuit controls aversive social learning.
Journal
Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462
Informations de publication
Date de publication:
24 Jan 2024
24 Jan 2024
Historique:
received:
11
09
2022
accepted:
08
12
2023
medline:
25
1
2024
pubmed:
25
1
2024
entrez:
24
1
2024
Statut:
aheadofprint
Résumé
To survive in a complex social group, one needs to know who to approach and, more importantly, who to avoid. In mice, a single defeat causes the losing mouse to stay away from the winner for weeks
Identifiants
pubmed: 38267576
doi: 10.1038/s41586-023-06958-w
pii: 10.1038/s41586-023-06958-w
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Qi, C. C. et al. Interaction of basolateral amygdala, ventral hippocampus and medial prefrontal cortex regulates the consolidation and extinction of social fear. Behav. Brain Funct. 14, 7 (2018).
pubmed: 29554926
pmcid: 5858134
doi: 10.1186/s12993-018-0139-6
Martinez, M., Calvo‐Torrent, A. & Pico‐Alfonso, M. A. Social defeat and subordination as models of social stress in laboratory rodents: a review. Aggress. Behav. 24, 241–256 (1998).
doi: 10.1002/(SICI)1098-2337(1998)24:4<241::AID-AB1>3.0.CO;2-M
Schlund, M. W. et al. Human social defeat and approach-avoidance: escalating social-evaluative threat and threat of aggression increases social avoidance. J. Exp. Anal. Behav. 115, 157–184 (2021).
pubmed: 33369748
doi: 10.1002/jeab.654
Banks, R. ERIC Clearinghouse on Elementary and Early Childhood Education (ERIC Development Team, 1997).
Huhman, K. L. et al. Conditioned defeat in male and female Syrian hamsters. Horm. Behav. 44, 293–299 (2003).
pubmed: 14609551
doi: 10.1016/j.yhbeh.2003.05.001
Markham, C. M., Taylor, S. L. & Huhman, K. L. Role of amygdala and hippocampus in the neural circuit subserving conditioned defeat in Syrian hamsters. Learn. Mem. 17, 109–116 (2010).
pubmed: 20154357
pmcid: 2825696
doi: 10.1101/lm.1633710
Day, D. E., Cooper, M. A., Markham, C. M. & Huhman, K. L. NR2B subunit of the NMDA receptor in the basolateral amygdala is necessary for the acquisition of conditioned defeat in Syrian hamsters. Behav. Brain Res. 217, 55–59 (2011).
pubmed: 20933543
doi: 10.1016/j.bbr.2010.09.034
Markham, C. M., Luckett, C. A. & Huhman, K. L. The medial prefrontal cortex is both necessary and sufficient for the acquisition of conditioned defeat. Neuropharmacology 62, 933–939 (2012).
pubmed: 22001285
doi: 10.1016/j.neuropharm.2011.09.026
Sakurai, K. et al. Capturing and manipulating activated neuronal ensembles with CANE delineates a hypothalamic social–fear circuit. Neuron 92, 739–753 (2016).
pubmed: 27974160
pmcid: 5172402
doi: 10.1016/j.neuron.2016.10.015
Silva, B. A. et al. Independent hypothalamic circuits for social and predator fear. Nat. Neurosci. 16, 1731–1733 (2013).
pubmed: 24212674
pmcid: 4194278
doi: 10.1038/nn.3573
Wang, L. et al. Hypothalamic control of conspecific self-defense. Cell Rep. 26, 1747–1758.e5 (2019).
pubmed: 30759387
pmcid: 6431082
doi: 10.1016/j.celrep.2019.01.078
Diaz, V. & Lin, D. Neural circuits for coping with social defeat. Curr. Opin. Neurobiol. 60, 99–107 (2020).
pubmed: 31837481
doi: 10.1016/j.conb.2019.11.016
Krzywkowski, P., Penna, B. & Gross, C. T. Dynamic encoding of social threat and spatial context in the hypothalamus. eLife 9, e57148 (2020).
pubmed: 32955014
pmcid: 7505658
doi: 10.7554/eLife.57148
Newman, S. W. The medial extended amygdala in male reproductive behavior. A node in the mammalian social behavior network. Ann. NY Acad. Sci. 877, 242–257 (1999).
pubmed: 10415653
doi: 10.1111/j.1749-6632.1999.tb09271.x
Lin, D. et al. Functional identification of an aggression locus in the mouse hypothalamus. Nature 470, 221–226 (2011).
pubmed: 21307935
pmcid: 3075820
doi: 10.1038/nature09736
Toth, I. & Neumann, I. D. Animal models of social avoidance and social fear. Cell Tissue Res. 354, 107–118 (2013).
pubmed: 23760888
doi: 10.1007/s00441-013-1636-4
Nasanbuyan, N. et al. Oxytocin–oxytocin receptor systems facilitate social defeat posture in male mice. Endocrinology 159, 763–775 (2018).
pubmed: 29186377
doi: 10.1210/en.2017-00606
Lee, H. et al. Scalable control of mounting and attack by Esr1
pubmed: 24739975
pmcid: 4098836
doi: 10.1038/nature13169
Hashikawa, K. et al. Esr1
pubmed: 28920934
pmcid: 5953764
doi: 10.1038/nn.4644
Isosaka, T. et al. Htr2a-expressing cells in the central amygdala control the hierarchy between innate and learned fear. Cell 163, 1153–1164 (2015).
pubmed: 26590419
doi: 10.1016/j.cell.2015.10.047
Mahn, M. et al. High-efficiency optogenetic silencing with soma-targeted anion-conducting channelrhodopsins. Nat. Commun. 9, 4125 (2018).
pubmed: 30297821
pmcid: 6175909
doi: 10.1038/s41467-018-06511-8
Armbruster, B. N., Li, X., Pausch, M. H., Herlitze, S. & Roth, B. L. Evolving the lock to fit the key to create a family of G protein-coupled receptors potently activated by an inert ligand. Proc. Natl Acad. Sci. USA 104, 5163–5168 (2007).
pubmed: 17360345
pmcid: 1829280
doi: 10.1073/pnas.0700293104
Thompson, K. J. et al. DREADD agonist 21 is an effective agonist for muscarinic-based DREADDs in vitro and in vivo. ACS Pharmacol. Transl. Sci. 1, 61–72 (2018).
pubmed: 30868140
pmcid: 6407913
doi: 10.1021/acsptsci.8b00012
Liao, P. Y., Chiu, Y. M., Yu, J. H. & Chen, S. K. Mapping central projection of oxytocin neurons in unmated mice using Cre and alkaline phosphatase reporter. Front. Neuroanat. 14, 559402 (2020).
pubmed: 33192340
pmcid: 7604466
doi: 10.3389/fnana.2020.559402
Rhodes, C. H., Morrell, J. I. & Pfaff, D. W. Immunohistochemical analysis of magnocellular elements in rat hypothalamus: distribution and numbers of cells containing neurophysin, oxytocin, and vasopressin. J. Comp. Neurol. 198, 45–64 (1981).
pubmed: 7014660
doi: 10.1002/cne.901980106
Castel, M. & Morris, J. F. The neurophysin-containing innervation of the forebrain of the mouse. Neuroscience 24, 937–966 (1988).
pubmed: 3380308
doi: 10.1016/0306-4522(88)90078-4
Ludwig, M. Dendritic release of vasopressin and oxytocin. J. Neuroendocrinol. 10, 881–895 (1998).
pubmed: 9870745
doi: 10.1046/j.1365-2826.1998.00279.x
Pow, D. V. & Morris, J. F. Dendrites of hypothalamic magnocellular neurons release neurohypophysial peptides by exocytosis. Neuroscience 32, 435–439 (1989).
pubmed: 2586758
doi: 10.1016/0306-4522(89)90091-2
Kim, D.-W. Multimodal Analysis of Cell Types in a Hypothalamic Node Controlling Social Behavior in Mice. PhD thesis, California Institute of Technology (2020).
Klapoetke, N. C. et al. Independent optical excitation of distinct neural populations. Nat. Methods 11, 338–346 (2014).
pubmed: 24509633
pmcid: 3943671
doi: 10.1038/nmeth.2836
Yamaguchi, T. et al. Posterior amygdala regulates sexual and aggressive behaviors in male mice. Nat. Neurosci. 23, 1111–1124 (2020).
pubmed: 32719562
pmcid: 7483354
doi: 10.1038/s41593-020-0675-x
Stagkourakis, S., Spigolon, G., Liu, G. & Anderson, D. J. Experience-dependent plasticity in an innate social behavior is mediated by hypothalamic LTP. Proc. Natl Acad. Sci. USA 117, 25789–25799 (2020).
pubmed: 32973099
pmcid: 7568289
doi: 10.1073/pnas.2011782117
Zha, X. et al. VMHvl-projecting Vglut1
pubmed: 32320666
doi: 10.1016/j.celrep.2020.03.081
Bekkers, J. M. Changes in dendritic axial resistance alter synaptic integration in cerebellar Purkinje cells. Biophys. J. 100, 1198–1206 (2011).
pubmed: 21354392
pmcid: 3043206
doi: 10.1016/j.bpj.2011.01.042
Malinow, R. & Miller, J. P. Postsynaptic hyperpolarization during conditioning reversibly blocks induction of long-term potentiation. Nature 320, 529–530 (1986).
pubmed: 3008000
doi: 10.1038/320529a0
Saito, M. et al. Diphtheria toxin receptor-mediated conditional and targeted cell ablation in transgenic mice. Nat. Biotechnol. 19, 746–750 (2001).
pubmed: 11479567
doi: 10.1038/90795
Froemke, R. C. & Young, L. J. Oxytocin, neural plasticity, and social behavior. Annu. Rev. Neurosci. 44, 359–381 (2021).
pubmed: 33823654
pmcid: 8604207
doi: 10.1146/annurev-neuro-102320-102847
Zoicas, I., Slattery, D. A. & Neumann, I. D. Brain oxytocin in social fear conditioning and its extinction: involvement of the lateral septum. Neuropsychopharmacology 39, 3027–3035 (2014).
pubmed: 24964815
pmcid: 4229574
doi: 10.1038/npp.2014.156
Williams, A. V. et al. Social approach and social vigilance are differentially regulated by oxytocin receptors in the nucleus accumbens. Neuropsychopharmacology 45, 1423–1430 (2020).
pubmed: 32198453
pmcid: 7360746
doi: 10.1038/s41386-020-0657-4
Menon, R. et al. Oxytocin signaling in the lateral septum prevents social fear during lactation. Curr. Biol. 28, 1066–1078.e6 (2018).
pubmed: 29551417
doi: 10.1016/j.cub.2018.02.044
Guzman, Y. F. et al. Fear-enhancing effects of septal oxytocin receptors. Nat. Neurosci. 16, 1185–1187 (2013).
pubmed: 23872596
pmcid: 3758455
doi: 10.1038/nn.3465
Duque-Wilckens, N. et al. Extrahypothalamic oxytocin neurons drive stress-induced social vigilance and avoidance. Proc. Natl Acad. Sci. USA 117, 26406–26413 (2020).
pubmed: 33020267
pmcid: 7585015
doi: 10.1073/pnas.2011890117
Carcea, I. et al. Oxytocin neurons enable social transmission of maternal behaviour. Nature 596, 553–557 (2021).
pubmed: 34381215
pmcid: 8387235
doi: 10.1038/s41586-021-03814-7
Yu, H. et al. Social touch-like tactile stimulation activates a tachykinin 1–oxytocin pathway to promote social interactions. Neuron 110, 1051–1067.e7 (2022).
pubmed: 35045339
doi: 10.1016/j.neuron.2021.12.022
Tang, Y. et al. Social touch promotes interfemale communication via activation of parvocellular oxytocin neurons. Nat. Neurosci. 23, 1125–1137 (2020).
pubmed: 32719563
doi: 10.1038/s41593-020-0674-y
Resendez, S. L. et al. Social stimuli induce activation of oxytocin neurons within the paraventricular nucleus of the hypothalamus to promote social behavior in male mice. J. Neurosci. 40, 2282–2295 (2020).
pubmed: 32024781
pmcid: 7083279
doi: 10.1523/JNEUROSCI.1515-18.2020
Erdozain, A. M. & Penagarikano, O. Oxytocin as treatment for social cognition, not there yet. Front. Psychiatry 10, 930 (2020).
pubmed: 31998152
pmcid: 6962227
doi: 10.3389/fpsyt.2019.00930
Daigle, T. L. et al. A suite of transgenic driver and reporter mouse lines with enhanced brain-cell-type targeting and functionality. Cell 174, 465–480.e22 (2018).
pubmed: 30007418
pmcid: 6086366
doi: 10.1016/j.cell.2018.06.035
Vong, L. et al. Leptin action on GABAergic neurons prevents obesity and reduces inhibitory tone to POMC neurons. Neuron 71, 142–154 (2011).
pubmed: 21745644
pmcid: 3134797
doi: 10.1016/j.neuron.2011.05.028
Lee, H. J., Caldwell, H. K., Macbeth, A. H., Tolu, S. G. & Young, W. S. 3rd A conditional knockout mouse line of the oxytocin receptor. Endocrinology 149, 3256–3263 (2008).
pubmed: 18356275
pmcid: 2453083
doi: 10.1210/en.2007-1710
Madisen, L. et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 13, 133–140 (2010).
pubmed: 20023653
doi: 10.1038/nn.2467
Franklin, K. B. J. & Paxinos, G. Paxinos and Franklin’s The Mouse Brain in Stereotaxic Coordinates. 4th edn (Academic Press, 2013).
Osborne, J. E. & Dudman, J. T. RIVETS: a mechanical system for in vivo and in vitro electrophysiology and imaging. PLoS ONE 9, e89007 (2014).
pubmed: 24551206
pmcid: 3925229
doi: 10.1371/journal.pone.0089007
Mathis, A. et al. DeepLabCut: markerless pose estimation of user-defined body parts with deep learning. Nat. Neurosci. 21, 1281–1289 (2018).
pubmed: 30127430
doi: 10.1038/s41593-018-0209-y
Yin, L. et al. VMHvll
pubmed: 35896109
pmcid: 9509472
doi: 10.1016/j.neuron.2022.06.026
Wong, L. C. et al. Effective modulation of male aggression through lateral septum to medial hypothalamus projection. Curr. Biol. 26, 593–604 (2016).
pubmed: 26877081
pmcid: 4783202
doi: 10.1016/j.cub.2015.12.065
Falkner, A. L. et al. Hierarchical representations of aggression in a hypothalamic–midbrain circuit. Neuron 106, 637–648.e6 (2020).
pubmed: 32164875
pmcid: 7571490
doi: 10.1016/j.neuron.2020.02.014
Fang, Y. Y., Yamaguchi, T., Song, S. C., Tritsch, N. X. & Lin, D. A hypothalamic midbrain pathway essential for driving maternal behaviors. Neuron 98, 192–207.e10 (2018).
pubmed: 29621487
pmcid: 5890946
doi: 10.1016/j.neuron.2018.02.019