Mechanically evoked defensive attack is controlled by GABAergic neurons in the anterior hypothalamic nucleus.

Animals Anterior Hypothalamic Nucleus GABAergic Neurons / physiology Mice Periaqueductal Gray / physiology

Journal

Nature neuroscience
ISSN: 1546-1726
Titre abrégé: Nat Neurosci
Pays: United States
ID NLM: 9809671

Informations de publication

Date de publication:
01 2022
Historique:
received: 02 11 2020
accepted: 11 11 2021
pubmed: 5 1 2022
medline: 7 4 2022
entrez: 4 1 2022
Statut: ppublish

Résumé

Innate defensive behaviors triggered by environmental threats are important for animal survival. Among these behaviors, defensive attack toward threatening stimuli (for example, predators) is often the last line of defense. How the brain regulates defensive attack remains poorly understood. Here we show that noxious mechanical force in an inescapable context is a key stimulus for triggering defensive attack in laboratory mice. Mechanically evoked defensive attacks were abrogated by photoinhibition of vGAT

Identifiants

DOI: 10.1038/s41593-021-00985-4 PMID: 34980925
pubmed: 34980925
doi: 10.1038/s41593-021-00985-4
pii: 10.1038/s41593-021-00985-4
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

72-85

Informations de copyright

© 2022. The Author(s), under exclusive licence to Springer Nature America, Inc.

Références

Fanselow, M. S. & Lester, L. S. A functional behavioristic approach to aversively motivated behavior: predatory imminence as a determinant of the topography of defensive behavior. In: Evolution and Learning, 185–211 (Lawrence Erlbaum Associates, 1988).
De Franceschi, G., Vivattanasarn, T., Saleem, A. B. & Solomon, S. G. Vision guides selection of freeze or flight defense strategies in mice. Curr. Biol. 26, 2150–2154 (2016).
pubmed: 27498569 doi: 10.1016/j.cub.2016.06.006
Yilmaz, M. & Meister, M. Rapid innate defensive responses of mice to looming visual stimuli. Curr. Biol. 23, 2011–2015 (2013).
pubmed: 24120636 doi: 10.1016/j.cub.2013.08.015
Blanchard, R. J. & Blanchard, D. C. Attack and defense in rodents as ethoexperimental models for the study of emotion. Prog. Neuropsychopharmacol. Biol. Psychiatry 13, S3–S14 (1989).
pubmed: 2694228 doi: 10.1016/0278-5846(89)90105-X
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., Chen, I. Z. & Lin, D. Collateral pathways from the ventromedial hypothalamus mediate defensive behaviors. Neuron 85, 1344–1358 (2015).
pubmed: 25754823 pmcid: 4368499 doi: 10.1016/j.neuron.2014.12.025
Kunwar, P. S. et al. Ventromedial hypothalamic neurons control a defensive emotion state. eLife 4, e06633 (2015).
Kennedy, A. et al. Stimulus-specific hypothalamic encoding of a persistent defensive state. Nature 586, 730–734 (2020).
pubmed: 32939094 pmcid: 7606611 doi: 10.1038/s41586-020-2728-4
Wang, W. et al. Coordination of escape and spatial navigation circuits orchestrates versatile flight from threats. Neuron 109, 1848–1860 (2021).
pubmed: 33861942 doi: 10.1016/j.neuron.2021.03.033
Wei, P. et al. Processing of visually evoked innate fear by a non-canonical thalamic pathway. Nat. Commun. 6, 6756 (2015).
pubmed: 25854147 doi: 10.1038/ncomms7756
Shang, C. et al. BRAIN CIRCUITS. A parvalbumin-positive excitatory visual pathway to trigger fear responses in mice. Science 348, 1472–1477 (2015).
pubmed: 26113723 doi: 10.1126/science.aaa8694
Tovote, P. et al. Midbrain circuits for defensive behaviour. Nature 534, 206–212 (2016).
pubmed: 27279213 doi: 10.1038/nature17996
Evans, D. A. et al. A synaptic threshold mechanism for computing escape decisions. Nature 558, 590–594 (2018).
pubmed: 29925954 pmcid: 6235113 doi: 10.1038/s41586-018-0244-6
Shang, C. et al. Divergent midbrain circuits orchestrate escape and freezing responses to looming stimuli in mice. Nat. Commun. 9, 1232 (2018).
pubmed: 29581428 pmcid: 5964329 doi: 10.1038/s41467-018-03580-7
Salay, L. D., Ishiko, N. & Huberman, A. D. A midline thalamic circuit determines reactions to visual threat. Nature 557, 183–189 (2018).
pubmed: 29720647 pmcid: 8442544 doi: 10.1038/s41586-018-0078-2
Han, S., Soleiman, M. T., Soden, M. E., Zweifel, L. S. & Palmiter, R. D. Elucidating an affective pain circuit that creates a threat memory. Cell 162, 363–374 (2015).
pubmed: 26186190 pmcid: 4512641 doi: 10.1016/j.cell.2015.05.057
Gross, C. T. & Canteras, N. S. The many paths to fear. Nat. Rev. Neurosci. 13, 651–658 (2012).
pubmed: 22850830 doi: 10.1038/nrn3301
Branco, T. & Redgrave, P. The neural basis of escape behavior in vertebrates. Annu. Rev. Neurosci. 43, 417–439 (2020).
pubmed: 32259462 doi: 10.1146/annurev-neuro-100219-122527
Canteras, N. S., Chiavegatto, S., Ribeiro do Valle, L. E. & Swanson, L. W. Severe reduction of rat defensive behavior to a predator by discrete hypothalamic chemical lesions. Brain Res. Bull. 44, 297–305 (1997).
pubmed: 9323445 doi: 10.1016/S0361-9230(97)00141-X
Canteras, N. S. The medial hypothalamic defensive system: hodological organization and functional implications. Pharmacol. Biochem. Behav. 71, 481–491 (2002).
pubmed: 11830182 doi: 10.1016/S0091-3057(01)00685-2
Cezario, A. F., Ribeiro-Barbosa, E. R., Baldo, M. V. & Canteras, N. S. Hypothalamic sites responding to predator threats—the role of the dorsal premammillary nucleus in unconditioned and conditioned antipredatory defensive behavior. Eur. J. Neurosci. 28, 1003–1015 (2008).
pubmed: 18691328 doi: 10.1111/j.1460-9568.2008.06392.x
Paschoalin-Maurin, T. et al. The rodent-versus-wild snake paradigm as a model for studying anxiety- and panic-like behaviors: face, construct and predictive validities. Neuroscience 369, 336–349 (2018).
pubmed: 29183829 doi: 10.1016/j.neuroscience.2017.11.031
Zylka, M. J., Rice, F. L. & Anderson, D. J. Topographically distinct epidermal nociceptive circuits revealed by axonal tracers targeted to Mrgprd. Neuron 45, 17–25 (2005).
pubmed: 15629699 doi: 10.1016/j.neuron.2004.12.015
Cavanaugh, D. J. et al. Distinct subsets of unmyelinated primary sensory fibers mediate behavioral responses to noxious thermal and mechanical stimuli. Proc. Natl Acad. Sci. USA 106, 9075–9080 (2009).
pubmed: 19451647 pmcid: 2683885 doi: 10.1073/pnas.0901507106
Olson, W. et al. Sparse genetic tracing reveals regionally specific functional organization of mammalian nociceptors. eLife 6, e29507 (2017).
Buch, T. et al. A Cre-inducible diphtheria toxin receptor mediates cell lineage ablation after toxin administration. Nat. Methods 2, 419–426 (2005).
pubmed: 15908920 doi: 10.1038/nmeth762
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
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
Govorunova, E. G., Sineshchekov, O. A., Janz, R., Liu, X. & Spudich, J. L. NEUROSCIENCE. Natural light-gated anion channels: a family of microbial rhodopsins for advanced optogenetics. Science 349, 647–650 (2015).
pubmed: 26113638 pmcid: 4764398 doi: 10.1126/science.aaa7484
Falkner, A. L. et al. Hierarchical representations of aggression in a hypothalamic-midbrain circuit. Neuron 106, 637–648 (2020).
pubmed: 32164875 pmcid: 7571490 doi: 10.1016/j.neuron.2020.02.014
Gunaydin, L. A. et al. Natural neural projection dynamics underlying social behavior. Cell 157, 1535–1551 (2014).
pubmed: 24949967 pmcid: 4123133 doi: 10.1016/j.cell.2014.05.017
Dana, H. et al. High-performance calcium sensors for imaging activity in neuronal populations and microcompartments. Nat. Methods 16, 649–657 (2019).
pubmed: 31209382 doi: 10.1038/s41592-019-0435-6
Cohen, J. Y., Haesler, S., Vong, L., Lowell, B. B. & Uchida, N. Neuron-type-specific signals for reward and punishment in the ventral tegmental area. Nature 482, 85–88 (2012).
pubmed: 22258508 pmcid: 3271183 doi: 10.1038/nature10754
Wickersham, I. R., Finke, S., Conzelmann, K. K. & Callaway, E. M. Retrograde neuronal tracing with a deletion-mutant rabies virus. Nat. Methods 4, 47–49 (2007).
pubmed: 17179932 doi: 10.1038/nmeth999
Huang, T. et al. Identifying the pathways required for coping behaviours associated with sustained pain. Nature 565, 86–90 (2019).
pubmed: 30532001 doi: 10.1038/s41586-018-0793-8
Chiang, M. C. et al. Divergent neural pathways emanating from the lateral parabrachial nucleus mediate distinct components of the pain response. Neuron 106, 927–939 (2020).
pubmed: 32289251 doi: 10.1016/j.neuron.2020.03.014
Choi, S. et al. Parallel ascending spinal pathways for affective touch and pain. Nature 587, 258–263 (2020).
pubmed: 33116307 pmcid: 7666110 doi: 10.1038/s41586-020-2860-1
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
Leroy, F. et al. A circuit from hippocampal CA2 to lateral septum disinhibits social aggression. Nature 564, 213–218 (2018).
pubmed: 30518859 pmcid: 6364572 doi: 10.1038/s41586-018-0772-0
Isogai, Y. et al. Molecular organization of vomeronasal chemoreception. Nature 478, 241–245 (2011).
pubmed: 21937988 pmcid: 3192931 doi: 10.1038/nature10437
Risold, P. Y., Canteras, N. S. & Swanson, L. W. Organization of projections from the anterior hypothalamic nucleus: a Phaseolus vulgaris-leucoagglutinin study in the rat. J. Comp. Neurol. 348, 1–40 (1994).
pubmed: 7814679 doi: 10.1002/cne.903480102
Park, S. G. et al. Medial preoptic circuit induces hunting-like actions to target objects and prey. Nat. Neurosci. 21, 364–372 (2018).
pubmed: 29379117 doi: 10.1038/s41593-018-0072-x
Papes, F., Logan, D. W. & Stowers, L. The vomeronasal organ mediates interspecies defensive behaviors through detection of protein pheromone homologs. Cell 141, 692–703 (2010).
pubmed: 20478258 pmcid: 2873972 doi: 10.1016/j.cell.2010.03.037
Wang, Y. et al. Large-scale forward genetics screening identifies Trpa1 as a chemosensor for predator odor-evoked innate fear behaviors. Nat. Commun. 9, 2041 (2018).
pubmed: 29795268 pmcid: 5966455 doi: 10.1038/s41467-018-04324-3
Lischinsky, J. E. & Lin, D. Neural mechanisms of aggression across species. Nat. Neurosci. 23, 1317–1328 (2020).
pubmed: 33046890 doi: 10.1038/s41593-020-00715-2
Olivier, B., Olivier-Aardema, R. & Wiepkema, P. R. Effect of anterior hypothalamic and mammillary area lesions on territorial aggressive behaviour in male rats. Behav. Brain Res. 9, 59–81 (1983).
pubmed: 6411099 doi: 10.1016/0166-4328(83)90014-1
Fuchs, S. A., Edinger, H. M. & Siegel, A. The role of the anterior hypothalamus in affective defense behavior elicited from the ventromedial hypothalamus of the cat. Brain Res. 330, 93–107 (1985).
pubmed: 4039214 doi: 10.1016/0006-8993(85)90010-1
Delville, Y., De Vries, G. J. & Ferris, C. F. Neural connections of the anterior hypothalamus and agonistic behavior in golden hamsters. Brain Behav. Evol. 55, 53–76 (2000).
pubmed: 10838477 doi: 10.1159/000006642
Gobrogge, K. L., Liu, Y., Jia, X. & Wang, Z. Anterior hypothalamic neural activation and neurochemical associations with aggression in pair-bonded male prairie voles. J. Comp. Neurol. 502, 1109–1122 (2007).
pubmed: 17444499 doi: 10.1002/cne.21364
Goodson, J. L., Kelly, A. M., Kingsbury, M. A. & Thompson, R. R. An aggression-specific cell type in the anterior hypothalamus of finches. Proc. Natl Acad. Sci. USA 109, 13847–13852 (2012).
pubmed: 22872869 pmcid: 3427066 doi: 10.1073/pnas.1207995109
Lee, H. et al. Scalable control of mounting and attack by Esr1
pubmed: 24739975 pmcid: 4098836 doi: 10.1038/nature13169
Falkner, A. L., Grosenick, L., Davidson, T. J., Deisseroth, K. & Lin, D. Hypothalamic control of male aggression-seeking behavior. Nat. Neurosci. 19, 596–604 (2016).
pubmed: 26950005 pmcid: 4853470 doi: 10.1038/nn.4264
Yang, T. et al. Social control of hypothalamus-mediated male aggression. Neuron 95, 955–970 (2017).
pubmed: 28757304 pmcid: 5648542 doi: 10.1016/j.neuron.2017.06.046
Paxinos, G. & Franklin, K. B. J. The Mouse Brain in Stereotaxic Coordinates (Academic Press, 2001).
Chen, J. et al. A vagal-NTS neural pathway that stimulates feeding. Curr. Biol. 30, 3986–3998 (2020).
pubmed: 32822608 doi: 10.1016/j.cub.2020.07.084
Liu, Z. et al. IGF1-dependent synaptic plasticity of mitral cells in olfactory memory during social learning. Neuron 95, 106–122 (2017).
pubmed: 28683263 pmcid: 5559288 doi: 10.1016/j.neuron.2017.06.015

Auteurs

Zhiyong Xie (Z)

National Institute of Biological Sciences, Beijing, China.

Huating Gu (H)

National Institute of Biological Sciences, Beijing, China.
College of Life Sciences, Beijing Normal University, Beijing, China.

Meizhu Huang (M)

Bioland Laboratories, Guangzhou, China.

Xinyu Cheng (X)

National Institute of Biological Sciences, Beijing, China.
Graduate School of Peking Union Medical College, Chinese Academy of Medical Sciences, Beijing, China.

Congping Shang (C)

Bioland Laboratories, Guangzhou, China.

Ting Tao (T)

National Institute of Biological Sciences, Beijing, China.

Dapeng Li (D)

Department of Neurobiology, School of Basic Medical Sciences, Beijing Key Laboratory of Neural Regeneration and Repair, Advanced Innovation Center for Human Brain Protection, Capital Medical University, Beijing, China.

Yuan Xie (Y)

The Key Laboratory of Neural and Vascular Biology, Ministry of Education, Department of Biochemistry and Molecular Biology, Hebei Medical University, Shijiazhuang, China.

Jidong Zhao (J)

State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China.

Wei Lu (W)

State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China.

Zhibin Zhang (Z)

State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China.

Cheng Zhan (C)

National Institute of Biological Sciences, Beijing, China.
Tsinghua Institute of Multidisciplinary Biomedical Research, Tsinghua University, Beijing, China.
ORCID: 0000-0001-9397-0871

Zongxiang Tang (Z)

School of Medicine and Holistic Integrative Medicine, Nanjing University of Chinese Medicine, Nanjing, China.

Fan Zhang (F)

The Key Laboratory of Neural and Vascular Biology, Ministry of Education, Department of Biochemistry and Molecular Biology, Hebei Medical University, Shijiazhuang, China. zhangfan86@hebmu.edu.cn.
ORCID: 0000-0003-0458-6742

Peng Cao (P)

National Institute of Biological Sciences, Beijing, China. caopeng@nibs.ac.cn.
Tsinghua Institute of Multidisciplinary Biomedical Research, Tsinghua University, Beijing, China. caopeng@nibs.ac.cn.
ORCID: 0000-0001-7739-6857

Articles similaires

Evaluating the efficacy of telesurgery with dual console SSI Mantra Surgical Robotic System: experiment on animal model and clinical trials.

Sudhir Prem Srivastava, Vishwajyoti Pascual Srivastava, Avinesh Singh et al.
1.00
Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell

FBXO22 inhibits colitis and colorectal carcinogenesis by regulating the degradation of the S2448-phosphorylated form of mTOR.

Minle Li, Xuan Chen, Pengfei Qu et al.
1.00
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice

Use of organic material provided by an automatic enrichment device by weaner pigs and its influence on tail lesions.

Philipp Heseker, Jeanette Probst, Stefanie Ammer et al.
1.00
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › Mechanically evoked defensive attack is...
questionsmedicales.fr › Système nerveux › Système nerveux central › Encéphale › Prosencéphale › Diencéphale › Hypothalamus › Hypothalamus antérieur › Noyau hypothalamique antérieur › Mechanically evoked defensive attack is...
questionsmedicales.fr › Cellules › Neurones › Neurones GABAergiques › Mechanically evoked defensive attack is...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Souris › Mechanically evoked defensive attack is...
questionsmedicales.fr › Système nerveux › Système nerveux central › Encéphale › Tronc cérébral › Mésencéphale › Pédoncule cérébral › Tegmentum du mésencéphale › Substance grise centrale du mésencéphale › Mechanically evoked defensive attack is...