Zona Incerta GABAergic Neurons Facilitate Emergence from Isoflurane Anesthesia in Mice.

Emergence time GABAergic Neurons Isoflurane Anesthesia Optogenetic Zona Incerta

Journal

Neurochemical research
ISSN: 1573-6903
Titre abrégé: Neurochem Res
Pays: United States
ID NLM: 7613461

Informations de publication

Date de publication:
23 Sep 2024
Historique:
received: 28 05 2024
accepted: 14 08 2024
revised: 09 08 2024
medline: 23 9 2024
pubmed: 23 9 2024
entrez: 23 9 2024
Statut: aheadofprint

Résumé

The zona incerta (ZI) predominantly consists of gamma-aminobutyric acid (GABAergic) neurons, located adjacent to the lateral hypothalamus. GABA, acting on GABAA receptors, serves as a crucial neuromodulator in the initiation and maintenance of general anesthesia. In this study, we aimed to investigate the involvement of ZI GABAergic neurons in the general anesthesia process. Utilizing in-vivo calcium signal optical fiber recording, we observed a decrease in the activity of ZI GABAergic neurons during isoflurane anesthesia, followed by a significant increase during the recovery phase. Subsequently, we selectively ablated ZI GABAergic neurons to explore their role in general anesthesia, revealing no impact on the induction of isoflurane anesthesia but a prolonged recovery time, accompanied by a reduction in delta-band power in mice under isoflurane anesthesia. Finally, through optogenetic activation/inhibition of ZI GABAergic neurons during isoflurane anesthesia, we discovered that activation of these neurons facilitated emergence without affecting the induction process, while inhibition delayed emergence, leading to fluctuations in delta band activity. In summary, these findings highlight the involvement of ZI GABAergic neurons in modulating the emergence of isoflurane anesthesia.

Identifiants

DOI: 10.1007/s11064-024-04230-9 PMID: 39312079
pubmed: 39312079
doi: 10.1007/s11064-024-04230-9
pii: 10.1007/s11064-024-04230-9
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : National Natural Science Foundation of China
ID : 81760259 and 81971298
Organisme : The Science and Technology Department of Guizhou Province
ID : Qiankehe JichuZK[2022]597 and Qiankehe JichuZK[2022]630

Informations de copyright

© 2024. The Author(s).

Références

Franks NP, Wisden W (2021) The inescapable drive to sleep: overlapping mechanisms of sleep and sedation. Science 374(6567):556–559
doi: 10.1126/science.abi8372 pubmed: 34709918
Liu C et al (2021) Lateral habenula glutamatergic neurons modulate isoflurane anesthesia in mice. Front Mol Neurosci 14:628996
doi: 10.3389/fnmol.2021.628996 pubmed: 33746711 pmcid: 7969819
Wang D et al (2021) GABAergic neurons in the dorsal-intermediate lateral septum regulate sleep-wakefulness and anesthesia in mice. Anesthesiology 135(3):463–481
doi: 10.1097/ALN.0000000000003868 pubmed: 34259824
Franks NP (2008) General anaesthesia: from molecular targets to neuronal pathways of sleep and arousal. Nat Rev Neurosci 9(5):370–386
doi: 10.1038/nrn2372 pubmed: 18425091
Vlasov K et al (2021) Activation of GABAergic neurons in the Rostromedial Tegmental Nucleus and other Brainstem regions promotes sedation and facilitates sevoflurane anesthesia in mice. Anesth Analg 132(4):e50–e55
doi: 10.1213/ANE.0000000000005387 pubmed: 33560660 pmcid: 7969415
Yin L et al (2019) Optogenetic/Chemogenetic Activation of GABAergic Neurons in the ventral Tegmental Area facilitates General Anesthesia via projections to the lateral hypothalamus in mice. Front Neural Circuits 13:73
doi: 10.3389/fncir.2019.00073 pubmed: 31798420 pmcid: 6878851
Cai S et al (2021) Effect of basal forebrain somatostatin and parvalbumin neurons in propofol and isoflurane anesthesia. CNS Neurosci Ther 27(7):792–804
doi: 10.1111/cns.13635 pubmed: 33764684 pmcid: 8193699
Venner A et al (2016) A Novel Population of Wake-promoting GABAergic neurons in the ventral lateral hypothalamus. Curr Biol 26(16):2137–2143
doi: 10.1016/j.cub.2016.05.078 pubmed: 27426511 pmcid: 5160020
Mitrofanis J (2005) Some certainty for the zone of uncertainty? Exploring the function of the zona incerta. Neuroscience 130(1):1–15
doi: 10.1016/j.neuroscience.2004.08.017 pubmed: 15561420
Chou XL et al (2018) Inhibitory gain modulation of defense behaviors by zona incerta. Nat Commun 9(1):1151
doi: 10.1038/s41467-018-03581-6 pubmed: 29559622 pmcid: 5861117
Shang C et al (2019) A subcortical excitatory circuit for sensory-triggered predatory hunting in mice. Nat Neurosci 22(6):909–920
doi: 10.1038/s41593-019-0405-4 pubmed: 31127260
Zhang X, van den Pol AN (2017) Rapid binge-like eating and body weight gain driven by zona incerta GABA neuron activation. Science 356(6340):853–859
doi: 10.1126/science.aam7100 pubmed: 28546212 pmcid: 6602535
Liu K et al (2017) Lhx6-positive GABA-releasing neurons of the zona incerta promote sleep. Nature 548(7669):582–587
doi: 10.1038/nature23663 pubmed: 28847002 pmcid: 5958617
Bao WW et al (2021) Nucleus accumbens neurons expressing dopamine D1 receptors modulate states of consciousness in sevoflurane anesthesia. Curr Biol 31(9):1893 –1902.e5
doi: 10.1016/j.cub.2021.02.011 pubmed: 33705720
Zhao ZD et al (2019) Zona incerta GABAergic neurons integrate prey-related sensory signals and induce an appetitive drive to promote hunting. Nat Neurosci 22(6):921–932
doi: 10.1038/s41593-019-0404-5 pubmed: 31127258
Liu C et al (2020) Dopamine neurons in the ventral periaqueductal gray modulate isoflurane anesthesia in rats. CNS Neurosci Ther 26(11):1121–1133
doi: 10.1111/cns.13447 pubmed: 32881314 pmcid: 7564192
Taylor NE et al (2016) Optogenetic activation of dopamine neurons in the ventral tegmental area induces reanimation from general anesthesia. Proc Natl Acad Sci U S A 113(45):12826–12831
doi: 10.1073/pnas.1614340113 pubmed: 27791160 pmcid: 5111696
Tarnal V, Vlisides PE, Mashour GA (2016) Neurobiol Anesthetic Emergence J Neurosurg Anesthesiol 28(3):250–255
Luo T et al (2018) Parabrachial neurons promote Behavior and Electroencephalographic Arousal from General Anesthesia. Front Mol Neurosci 11:420
doi: 10.3389/fnmol.2018.00420 pubmed: 30564094 pmcid: 6288364
Fu B et al (2017) Noradrenergic transmission in the central medial thalamic nucleus modulates the electroencephalographic activity and emergence from propofol anesthesia in rats. J Neurochem 140(6):862–873
doi: 10.1111/jnc.13939 pubmed: 28092095
Zhang LN et al (2012) Orexin-A facilitates emergence from propofol anesthesia in the rat. Anesth Analg 115(4):789–796
doi: 10.1213/ANE.0b013e3182645ea3 pubmed: 22798527
Li J et al (2019) Orexin activated emergence from isoflurane anaesthesia involves excitation of ventral tegmental area dopaminergic neurones in rats. Br J Anaesth 123(4):497–505
doi: 10.1016/j.bja.2019.07.005 pubmed: 31399212
Wang Y et al (2021) Norepinephrine modulates wakefulness via α1 adrenoceptors in paraventricular thalamic nucleus. iScience 24(9):103015
doi: 10.1016/j.isci.2021.103015 pubmed: 34522858 pmcid: 8426266
Ren S et al (2018) The paraventricular thalamus is a critical thalamic area for wakefulness. Science 362(6413):429–434
doi: 10.1126/science.aat2512 pubmed: 30361367
Li J et al (2018) Involvement of Ventral Periaqueductal Gray Dopaminergic Neurons in Propofol Anesthesia. Neurochem Res 43(4):838–847
doi: 10.1007/s11064-018-2486-y pubmed: 29417470
Gui H et al (2021) Dopaminergic projections from the Ventral Tegmental Area to the Nucleus Accumbens modulate Sevoflurane Anesthesia in mice. Front Cell Neurosci 15:671473
doi: 10.3389/fncel.2021.671473 pubmed: 33994950 pmcid: 8119636
Liu D et al (2020) A common hub for sleep and motor control in the substantia nigra. Science 367(6476):440–445
doi: 10.1126/science.aaz0956 pubmed: 31974254
Caggiano V et al (2018) Midbrain circuits that set locomotor speed and gait selection. Nature 553(7689):455–460
doi: 10.1038/nature25448 pubmed: 29342142 pmcid: 5937258
Kroeger D et al (2017) Cholinergic, Glutamatergic, and GABAergic neurons of the Pedunculopontine Tegmental Nucleus have distinct effects on Sleep/Wake Behavior in mice. J Neurosci 37(5):1352–1366
doi: 10.1523/JNEUROSCI.1405-16.2016 pubmed: 28039375 pmcid: 5296799
Lee AM et al (2014) Identification of a brainstem circuit regulating visual cortical state in parallel with locomotion. Neuron 83(2):455–466
doi: 10.1016/j.neuron.2014.06.031 pubmed: 25033185 pmcid: 4151326
Holstege JC, Kuypers HG (1987) Brainstem projections to spinal motoneurons: an update. Neuroscience 23(3):809–821
doi: 10.1016/0306-4522(87)90160-6 pubmed: 2893995

Auteurs

Hong Chen (H)

Key Laboratory of Anesthesia and Organ Protestion of Ministry of Education (In Cultivation), Zunyi Medical University, Zunyi, China.
Guizhou Key Laboratory of Anesthesia and Organ Protection, Zunyi Medical University, Zunyi, China.
Department of Anesthesiology, KweiChow Moutai Hospital, Renhuai, Guizhou, China.
Guizhou Key Laboratory of Brain Science, Zunyi Medical University, Zunyi, China.

Chengxi Liu (C)

Key Laboratory of Anesthesia and Organ Protestion of Ministry of Education (In Cultivation), Zunyi Medical University, Zunyi, China.
Guizhou Key Laboratory of Anesthesia and Organ Protection, Zunyi Medical University, Zunyi, China.
Department of Anesthesiology, The Second Affiliated Hospital, Hengyang Medical School, University of South China, Hengyang, China.

Junxiao Liu (J)

Key Laboratory of Anesthesia and Organ Protestion of Ministry of Education (In Cultivation), Zunyi Medical University, Zunyi, China.
Guizhou Key Laboratory of Anesthesia and Organ Protection, Zunyi Medical University, Zunyi, China.
Department of Anesthesiology, Zunyi Hospital of Traditional Chinese Medicine, Zunyi, Guizhou, China.
Guizhou Key Laboratory of Brain Science, Zunyi Medical University, Zunyi, China.

Chengdong Yuan (C)

Key Laboratory of Anesthesia and Organ Protestion of Ministry of Education (In Cultivation), Zunyi Medical University, Zunyi, China.
Guizhou Key Laboratory of Anesthesia and Organ Protection, Zunyi Medical University, Zunyi, China.
Department of Anesthesiology, The Second Affiliated Hospital of Zunyi Medical University, Zunyi, China.
Guizhou Key Laboratory of Brain Science, Zunyi Medical University, Zunyi, China.

Haifeng He (H)

Key Laboratory of Anesthesia and Organ Protestion of Ministry of Education (In Cultivation), Zunyi Medical University, Zunyi, China.
Guizhou Key Laboratory of Anesthesia and Organ Protection, Zunyi Medical University, Zunyi, China.
Guizhou Key Laboratory of Brain Science, Zunyi Medical University, Zunyi, China.

Yu Zhang (Y)

Key Laboratory of Anesthesia and Organ Protestion of Ministry of Education (In Cultivation), Zunyi Medical University, Zunyi, China.
Guizhou Key Laboratory of Anesthesia and Organ Protection, Zunyi Medical University, Zunyi, China.

Shouyang Yu (S)

Key Laboratory of Anesthesia and Organ Protestion of Ministry of Education (In Cultivation), Zunyi Medical University, Zunyi, China.
Guizhou Key Laboratory of Anesthesia and Organ Protection, Zunyi Medical University, Zunyi, China.
Guizhou Key Laboratory of Brain Science, Zunyi Medical University, Zunyi, China.

Tianyuan Luo (T)

Key Laboratory of Anesthesia and Organ Protestion of Ministry of Education (In Cultivation), Zunyi Medical University, Zunyi, China.
Guizhou Key Laboratory of Anesthesia and Organ Protection, Zunyi Medical University, Zunyi, China.
Guizhou Key Laboratory of Brain Science, Zunyi Medical University, Zunyi, China.

Wei Shen (W)

School of Life Science and Technology and Shanghai Institute of Advanced Immunochemical Studies, ShanghaiTech University, Shanghai, China.

Tian Yu (T)

Key Laboratory of Anesthesia and Organ Protestion of Ministry of Education (In Cultivation), Zunyi Medical University, Zunyi, China. anesthesiayutian@163.com.
Guizhou Key Laboratory of Anesthesia and Organ Protection, Zunyi Medical University, Zunyi, China. anesthesiayutian@163.com.

Classifications MeSH