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Journal of Anesthesia

Erschienen in:

19.07.2016 | Original Article

Heightened stress response and cognitive impairment after repeated neonatal sevoflurane exposures might be linked to excessive GABA_AR-mediated depolarization

verfasst von: Guanghai Liu, Tiangui Zhu, Aihua Zhang, Feng Li, Weidong Qian, Bin Qian

Erschienen in: Journal of Anesthesia | Ausgabe 5/2016

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Abstract

Objective

Children with repeated exposures to anesthesia at an early age are at an increased risk of cognitive impairment. Data in the literature link increased developmental depolarizing γ-aminobutyric acid (GABA) type A receptor (GABA_AR) at younger age to neurodevelopmental disorders. Here we investigated the involvement of GABAergic signaling during development in mediating the adverse effects of repeated sevoflurane exposures.

Methods

Sprague–Dawley male rats received repeated exposures to 3 % sevoflurane for 2 h daily for 3 consecutive days on postnatal days (P) 4, 5, and 6; maternally separated and unseparated rats served as controls. A subgroup of rats received three injections of the Na⁺–K⁺–2Cl⁻ cotransporter inhibitor, bumetanide (1.82 mg/kg, intraperitoneally) 15 min prior to initiation of each sevoflurane exposure.

Results

The results showed that repeated neonatal sevoflurane exposures contribute to learning and memory impairment in the Morris water maze (MWM) at P60. The corticosterone level was significantly increased immediately after repeated neonatal sevoflurane exposures. Repeated neonatal sevoflurane exposures heightened the secretion of corticosterone in response to stress in P7 and P60 rats. Pretreatment of male rats prior to each sevoflurane exposure with bumetanide attenuated the corticosterone level immediately after repeated neonatal sevoflurane exposures, normalized endocrine response to stress at P7 and P60, and attenuated the sevoflurane-induced learning and memory impairment in the MWM.

Conclusion

These data suggested that the heightened stress response and cognitive impairment after repeated neonatal sevoflurane exposures might be linked to excessive GABA_AR-mediated depolarization.

Stratmann G. Neurotoxicity of anesthetic drugs in the developing brain. Anesth Analg. 2011;113:1170–9.CrossRefPubMed

Edwards DA, Shah HP, Cao W, Gravenstein N, Seubert CN, Martynyuk AE. Bumetanide alleviates epileptogenic and neurotoxic effects of sevoflurane in neonatal rat brain. Anesthesiology. 2010;112:567–75.CrossRefPubMed

Bormann J, Hamill OP, Sakmann B. Mechanism of anion permeation through channels gated by glycine and gamma-aminobutyric acid in mouse cultured spinal neurones. J Physiol. 1987;385:243–86.CrossRefPubMedPubMedCentral

Owens DF, Boyce LH, Davis MB, Kriegstein AR. Excitatory GABA responses in embryonic and neonatal cortical slices demonstrated by gramicidin perforated-patch recordings and calcium imaging. J Neurosci. 1996;16:6414–23.PubMed

Zhang L-L, Pathak HR, Coulter DA, Freed MA, Vardi N. Shift of intracellular chloride concentration in ganglion and amacrine cells of developing mouse retina. J Neurophysiol. 2006;95:2404–16.CrossRefPubMed

Dzhala VI, Talos DM, Sdrulla DA, Brumback AC, Mathews GC, Benke TA, Delpire E, Jensen FE, Staley KJ. NKCC1 transporter facilitates seizures in the developing brain. Nat Med. 2005;11:1205–13.CrossRefPubMed

Ben-Ari Y, Gaiarsa J-L, Tyzio R, Khazipov R. GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol Rev. 2007;87:1215–84.CrossRefPubMed

Yamada J, Okabe A, Toyoda H, Kilb W, Luhmann HJ, Fukuda A. Cl− uptake promoting depolarizing GABA actions in immature rat neocortical neurones is mediated by NKCC1. J Physiol. 2004;557:829–41.CrossRefPubMedPubMedCentral

Khazipov R, Khalilov I, Tyzio R, Morozova E, Ben-Ari Y, Holmes GL. Developmental changes in GABAergic actions and seizure susceptibility in the rat hippocampus. Eur J Neurosci. 2004;19:590–600.CrossRefPubMed

10.

Glykys J, Dzhala VI, Kuchibhotla KV, Feng G, Kuner T, Augustine G, Bacskai BJ, Staley KJ. Differences in cortical versus subcortical GABAergic signaling: a candidate mechanism of electroclinical uncoupling of neonatal seizures. Neuron. 2009;63:657–72.CrossRefPubMedPubMedCentral

11.

Rivera C, Voipio J, Payne JA, Ruusuvuori E, Lahtinen H, Lamsa K, Pirvola U, Saarma M, Kaila K. The K+/Cl− co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature. 1999;397:251–5.CrossRefPubMed

12.

Lee H, Chen CXQ, Liu YJ, Aizenman E, Kandler K. KCC2 expression in immature rat cortical neurons is sufficient to switch the polarity of GABA responses. Eur J Neurosci. 2005;21:2593–9.CrossRefPubMedPubMedCentral

13.

Rivera C, Voipio J, Kaila K. Two developmental switches in GABAergic signalling: the K+–Cl− cotransporter KCC2 and carbonic anhydrase CAVII. J Physiol. 2005;562:27–36.CrossRefPubMed

14.

Tyzio R, Nardou R, Ferrari DC, Tsintsadze T, Shahrokhi A, Eftekhari S, Khalilov I, Tsintsadze V, Brouchoud C, Chazal G. Oxytocin-mediated GABA inhibition during delivery attenuates autism pathogenesis in rodent offspring. Science. 2014;343:675–9.CrossRefPubMed

15.

Mody I, Maguire J. The reciprocal regulation of stress hormones and GABAA receptors. Front Cell Neurosci. 2012;6:4.CrossRefPubMedPubMedCentral

16.

Crowley SK, Girdler SS. Neurosteroid, GABAergic and hypothalamic pituitary adrenal (HPA) axis regulation: what is the current state of knowledge in humans? Psychopharmacology. 2014;231:3619–34.CrossRefPubMedPubMedCentral

17.

Gao X-B, Van Den Pol AN. GABA, not glutamate, a primary transmitter driving action potentials in developing hypothalamic neurons. J Neurophysiol. 2001;85:425–34.PubMed

18.

Li Y, Xu Y, van den Pol AN. Reversed synaptic effects of hypocretin and NPY mediated by excitatory GABA-dependent synaptic activity in developing MCH neurons. J Neurophysiol. 2013;109:1571–8.CrossRefPubMed

19.

Mitev Y, Darwish M, Wolf S, Holsboer F, Almeida O, Patchev V. Gender differences in the regulation of 3α-hydroxysteroid dehydrogenase in rat brain and sensitivity to neurosteroid-mediated stress protection. Neuroscience. 2003;120:541–9.CrossRefPubMed

20.

Morris RGM, Garrud P, Rawlins JNP, Okeefe J. Place navigation impaired in rats with hippocampal-lesions. Nature. 1982;297:681–3.CrossRefPubMed

21.

Macrí S, Mason GJ, Würbel H. Dissociation in the effects of neonatal maternal separations on maternal care and the offspring’s HPA and fear responses in rats. Eur J Neurosci. 2004;20:1017–24.CrossRefPubMed

22.

Sousa VC, Vital J, Costenla AR, Batalha VL, Sebastião AM, Ribeiro JA, Lopes LV. Maternal separation impairs long term-potentiation in CA1-CA3 synapses and hippocampal-dependent memory in old rats. Neurobiol Aging. 2014;35:1680–5.CrossRefPubMed

23.

Brunson KL, Kramár E, Lin B, Chen Y, Colgin LL, Yanagihara TK, Lynch G, Baram TZ. Mechanisms of late-onset cognitive decline after early-life stress. J Neurosci. 2005;25:9328–38.CrossRefPubMedPubMedCentral

24.

Willis J, Zhu W, Perez-Downes J, Tan S, Xu C, Seubert C, Gravenstein N, Martynyuk A. Propofol-induced electroencephalographic seizures in neonatal rats: the role of corticosteroids and γ-aminobutyric acid type A receptor-mediated excitation. Anesth Analg. 2015;120:433–9.CrossRefPubMedPubMedCentral

25.

Huot RL, Plotsky PM, Lenox RH, McNamara RK. Neonatal maternal separation reduces hippocampal mossy fiber density in adult Long Evans rats. Brain Res. 2002;950:52–63.CrossRefPubMed

26.

Amaral DG, Dent JA. Development of the mossy fibers of the dentate gyrus: I. A light and electron microscopic study of the mossy fibers and their expansions. J Comp Neurol. 1981;195:51–86.CrossRefPubMed

27.

Wilder RT, Flick RP, Sprung J. Early exposure to anesthesia and learning disabilities in a population-based birth cohort. Anesthesiology. 2009;110:796–804.CrossRefPubMedPubMedCentral

Titel: Heightened stress response and cognitive impairment after repeated neonatal sevoflurane exposures might be linked to excessive GABAAR-mediated depolarization
verfasst von: Guanghai Liu
Tiangui Zhu
Aihua Zhang
Feng Li
Weidong Qian
Bin Qian
Publikationsdatum: 19.07.2016
Verlag: Springer Japan
Erschienen in: Journal of Anesthesia / Ausgabe 5/2016
Print ISSN: 0913-8668
Elektronische ISSN: 1438-8359
DOI: https://doi.org/10.1007/s00540-016-2215-0

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Heightened stress response and cognitive impairment after repeated neonatal sevoflurane exposures might be linked to excessive GABA_AR-mediated depolarization

Abstract

Objective

Methods

Results

Conclusion

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