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BMC Anesthesiology

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Open Access 01-12-2017 | Research article

Ketamine attenuates the glutamatergic neurotransmission in the ventral posteromedial nucleus slices of rats

Authors: Bao Fu, Chengxi Liu, Yajun Zhang, Xiaoyun Fu, Lin Zhang, Tian Yu

Published in: BMC Anesthesiology | Issue 1/2017

Abstract

Background

Ketamine is a frequently used intravenous anesthetic, which can reversibly induce loss of consciousness (LOC). Previous studies have demonstrated that thalamocortical system is critical for information transmission and integration in the brain. The ventral posteromedial nucleus (VPM) is a critical component of thalamocortical system. Glutamate is an important excitatory neurotransmitter in the brain and may be involved in ketamine-induced LOC.

Methods

The study used whole-cell patch-clamp to observe the effect of ketamine (30 μM–1000 μM) on glutamatergic neurotransmission in VPM slices.

Results

Ketamine significantly decreased the amplitude of glutamatergic spontaneous excitatory postsynaptic currents (sEPSCs), but only higher concentration of ketamine (300 μM and 1000 μM) suppressed the frequency of sEPSCs. Ketamine (100 μM–1000 μM) also decreased the amplitude of glutamatergic miniature excitatory postsynaptic currents (mEPSCs), without altering the frequency.

Conclusions

In VPM neurons, ketamine attenuates the glutamatergic neurotransmission mainly through postsynaptic mechanism and action potential may be involved in the process.

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Edelman GM. Naturalizing consciousness: a theoretical framework. Proc Natl Acad Sci U S A. 2003;100(9):5520–4.CrossRefPubMedPubMedCentral

Tononi G, Koch C. The neural correlates of consciousness: an update. Ann N Y Acad Sci. 2008;1124:239–61.CrossRefPubMed

Zhang Y, Li Z, Dong H, Yu T. Effects of general anesthesia with propofol on thalamocortical sensory processing in rats. J Pharmacol Sci. 2014;126(4):370–81.CrossRefPubMed

Zhang Y, He JC, Liu XK, Wang Y, Yu T. Assessment of the effect of etomidate on voltage-gated sodium channels and action potentials in rat primary sensory cortex pyramidal neurons. Eur J Pharmacol. 2014;736:55–62.CrossRefPubMed

Li Z, Liu X, Zhang Y, Shi J, Xie P, Yu T. Connection changes in somatosensory cortex induced by different doses of propofol. PLoS One. 2014;9(2):e87829.CrossRefPubMedPubMedCentral

Zhang Y, Wang C, Zhang L, Yu T. GABAA receptor in the thalamic specific relay system contributes to the propofol-induced somatosensory cortical suppression in rat. PLoS One. 2013;8(12):e82377.CrossRefPubMedPubMedCentral

Rath M, Fohr KJ, Weigt HU, Gauss A, Engele J, Georgieff M, Koster S, Adolph O. Etomidate reduces glutamate uptake in rat cultured glial cells: involvement of PKA. Br J Pharmacol. 2008;155(6):925–33.CrossRefPubMedPubMedCentral

Fu B, Wang Y, Yang H, Yu T. Effects of etomidate on GABAergic and glutamatergic transmission in rat Thalamocortical slices. Neurochem Res. 2016;41(12):3181–91.CrossRefPubMed

Magalhaes A, Valentim A, Venancio C, Pereira M, Melo P, Summavielle T, Antunes L. Ketamine alone or combined with midazolam or dexmedetomidine does not affect anxiety-like behaviours and memory in adult Wistar rats. Lab Anim. 2017;51(2):147–59.CrossRefPubMed

10.

Chau PL. New insights into the molecular mechanisms of general anaesthetics. Br J Pharmacol. 2010;161(2):288–307.CrossRefPubMedPubMedCentral

11.

Jin J, Gong K, Zou X, Wang R, Lin Q, Chen J. The blockade of NMDA receptor ion channels by ketamine is enhanced in developing rat cortical neurons. Neurosci Lett. 2013;539:11–5.CrossRefPubMedPubMedCentral

12.

Franks NP. General anaesthesia: from molecular targets to neuronal pathways of sleep and arousal. Nat Rev Neurosci. 2008;9(5):370–86.CrossRefPubMed

13.

Yuan C, Zhang Y, Cao S, Wang Y, Fu B, Yu T. Effects of ketamine on neuronal spontaneous excitatory postsynaptic currents and miniature excitatory postsynaptic currents in the somatosensory cortex of rats. Iranian journal of medical sciences. 2016;41(4):275–82.PubMed

14.

Chakraborty S, Elvezio V, Kaczocha M, Rebecchi M, Puopolo M. Presynaptic inhibition of transient receptor potential vanilloid type 1 (TRPV1) receptors by noradrenaline in nociceptive neurons. J Physiol. 2017;595(8):2639–60.CrossRefPubMed

15.

Fu B, Yu T, Yuan J, Gong X, Zhang M. Noradrenergic transmission in the central medial thalamic nucleus modulates the electroencephalographic activity and emergence from propofol anesthesia in rats. J Neurochem. 2017;140(6):862–73.CrossRefPubMed

16.

Puopolo M, Bean BP, Raviola E. Spontaneous activity of isolated dopaminergic periglomerular cells of the main olfactory bulb. J Neurophysiol. 2005;94(5):3618–27.CrossRefPubMed

17.

Haseneder R, Kurz J, Dodt HU, Kochs E, Zieglgansberger W, Scheller M, Rammes G, Hapfelmeier G: Isoflurane reduces glutamatergic transmission in neurons in the spinal cord superficial dorsal horn: evidence for a presynaptic site of an analgesic action. Anesthesia and analgesia 2004, 98(6):1718–1723, table of contents.

18.

Zhang Y, He JC, Liu XK, Zhang Y, Wang Y, Yu T. Assessment of the effect of etomidate on voltage-gated sodium channels and action potentials in rat primary sensory cortex pyramidal neurons. Eur J Pharmacol. 2014;736:55–62.CrossRefPubMed

19.

Bai D, Pennefather PS, MacDonald JF, Orser BA. The general anesthetic propofol slows deactivation and desensitization of GABA(a) receptors. The Journal of neuroscience : the official journal of the Society for Neuroscience. 1999;19(24):10635–46.

20.

Purdon PL, Pierce ET, Bonmassar G, Walsh J, Harrell PG, Kwo J, Deschler D, Barlow M, Merhar RC, Lamus C, et al. Simultaneous electroencephalography and functional magnetic resonance imaging of general anesthesia. Ann N Y Acad Sci. 2009;1157:61–70.CrossRefPubMedPubMedCentral

21.

Velly LJ, Rey MF, Bruder NJ, Gouvitsos FA, Witjas T, Regis JM, Peragut JC, Gouin FM. Differential dynamic of action on cortical and subcortical structures of anesthetic agents during induction of anesthesia. Anesthesiology. 2007;107(2):202–12.CrossRefPubMed

22.

Ferrarelli F, Massimini M, Sarasso S, Casali A, Riedner BA, Angelini G, Tononi G, Pearce RA. Breakdown in cortical effective connectivity during midazolam-induced loss of consciousness. Proc Natl Acad Sci U S A. 2010;107(6):2681–6.CrossRefPubMedPubMedCentral

23.

Rudolph U, Antkowiak B. Molecular and neuronal substrates for general anaesthetics. Nat Rev Neurosci. 2004;5(9):709–20.CrossRefPubMed

24.

Fu B, Wang Y, Yang H, Yu T. Effects of etomidate on GABAergic and glutamatergic transmission in rat Thalamocortical slices. Neurochem Res. 2016;

25.

Morgan CJ, Mofeez A, Brandner B, Bromley L, Curran HV. Acute effects of ketamine on memory systems and psychotic symptoms in healthy volunteers. Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology. 2004;29(1):208–18.CrossRef

26.

Gili T, Saxena N, Diukova A, Murphy K, Hall JE, Wise RG. The thalamus and brainstem act as key hubs in alterations of human brain network connectivity induced by mild propofol sedation. The Journal of neuroscience : the official journal of the Society for Neuroscience. 2013;33(9):4024–31.CrossRef

27.

Wang X, Gorini C, Sharp D, Bateman R, Mendelowitz D. Anaesthetics differentially modulate the trigeminocardiac reflex excitatory synaptic pathway in the brainstem. J Physiol. 2011;589(Pt 22):5431–42.CrossRefPubMedPubMedCentral

28.

Banks MI, Pearce RA. Dual actions of volatile anesthetics on GABA(a) IPSCs: dissociation of blocking and prolonging effects. Anesthesiology. 1999;90(1):120–34.CrossRefPubMed

29.

McBain CJ, Mayer ML. N-methyl-D-aspartic acid receptor structure and function. Physiol Rev. 1994;74(3):723–60.PubMed

30.

Shibuta S, Morita T, Kosaka J, Kamibayashi T, Fujino Y. Only extra-high dose of ketamine affects l-glutamate-induced intracellular ca(2+) elevation and neurotoxicity. Neurosci Res. 2015;98:9–16.CrossRefPubMed

Title: Ketamine attenuates the glutamatergic neurotransmission in the ventral posteromedial nucleus slices of rats
Authors: Bao Fu
Chengxi Liu
Yajun Zhang
Xiaoyun Fu
Lin Zhang
Tian Yu
Publication date: 01-12-2017
Publisher: BioMed Central
Published in: BMC Anesthesiology / Issue 1/2017
Electronic ISSN: 1471-2253
DOI: https://doi.org/10.1186/s12871-017-0404-5

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Ketamine attenuates the glutamatergic neurotransmission in the ventral posteromedial nucleus slices of rats

Abstract

Background

Methods

Results

Conclusions

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

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