Distinct effects of volatile and intravenous anaesthetics on presynaptic calcium dynamics in mouse hippocampal GABAergic neurones.

BACKGROUND General anaesthetics have marked effects on synaptic transmission, but their neuronal and circuit-level effects remain unclear. The volatile anaesthetic isoflurane differentially inhibits synaptic vesicle exocytosis in specific neuronal subtypes, but whether other common anaesthetics also have neurone-subtype-specific actions is unknown. METHODS We used the genetically encoded fluorescent Ca2+ sensor GCaMP6f to compare the pharmacological effects of isoflurane, sevoflurane, propofol, and ketamine on presynaptic excitability in hippocampal glutamatergic neurones and in hippocampal parvalbumin-, somatostatin-, and vasoactive intestinal peptide-expressing (PV+, SST+, and VIP+, respectively) GABAergic interneurones. RESULTS Isoflurane and sevoflurane depressed activity-driven presynaptic Ca2+ transients in a neurone-type-specific manner, with greater potency for inhibition of glutamate and SST+ compared with PV+ and VIP+ neurone presynaptic activation. In contrast, clinical concentrations of propofol (1 μM) or ketamine (15 μM) had no significant effects on presynaptic activation. Propofol potentiated evoked Ca2+ entry in PV+ interneurones but only at a supraclinical concentration (3 μM). CONCLUSIONS Anaesthetic-agent-selective effects on presynaptic Ca2+ entry have functional implications for hippocampal circuit function during i.v. or volatile anaesthetic-mediated anaesthesia. Hippocampal interneurones have distinct subtype-specific sensitivities to volatile anaesthetic actions on presynaptic Ca2+, which are similar between isoflurane and sevoflurane.

• Publication year

  2022

• Venue

  British Journal of Anaesthesia

• Publication date

  2022-02-01

• Fields of study

  Medicine

• Identifiers
  DOI 10.1016/j.bja.2022.01.014PMID 35164969PMCID PMC9204660
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• GABAergic Inhibition of Presynaptic Ca2+ Transients in Respiratory PreBötzinger Neurons in Organotypic Slice Cultures

  2021cited by this paper
• Sleep down state-active ID2/Nkx2.1 interneurons in the neocortex

  2021cited by this paper
• Selective inhibition of gamma aminobutyric acid release from mouse hippocampal interneurone subtypes by the volatile anaesthetic isoflurane.

  2021cited by this paper
• Proportional Downscaling of Glutamatergic Release Sites by the General Anesthetic Propofol at Drosophila Motor Nerve Terminals

  2020cited by this paper
• Sevoflurane induces neuronal activation and behavioral hyperactivity in young mice

  2020cited by this paper
• Antidepressant mechanisms of ketamine: Focus on GABAergic inhibition.

  2020cited by this paper
• Imaging and Analysis of Presynaptic Calcium Influx in Cultured Neurons Using synGCaMP6f

  2019cited by this paper
• Role of specific presynaptic calcium channel subtypes in isoflurane inhibition of synaptic vesicle exocytosis in rat hippocampal neurones.

  2019cited by this paper
• Isoflurane Inhibits Dopaminergic Synaptic Vesicle Exocytosis Coupled to CaV2.1 and CaV2.2 in Rat Midbrain Neurons

  2019cited by this paper
• Interpreting in vivo calcium signals from neuronal cell bodies, axons, and dendrites: a review

  2019cited by this paper
• Ketamine disinhibits dendrites and enhances calcium signals in prefrontal dendritic spines

  2019cited by this paper
• The diversity of GABAergic neurons and neural communication elements

  2019cited by this paper
• Towards a Comprehensive Understanding of Anesthetic Mechanisms of Action: A Decade of Discovery.

  2019cited by this paper
• Trapping of Syntaxin1a in Presynaptic Nanoclusters by a Clinically Relevant General Anesthetic.

  2018cited by this paper
• Recent progress on the molecular pharmacology of propofol

  2018cited by this paper
• An allosteric propofol-binding site in kinesin disrupts kinesin-mediated processive movement on microtubules

  2018cited by this paper
• Presynaptic GCaMP expression decreases vesicle release probability at the calyx of Held

  2018cited by this paper
• Sevoflurane increases locomotion activity in mice

  2018cited by this paper
• Sevoflurane activates hippocampal CA3 kainate receptors (Gluk2) to induce hyperactivity during induction and recovery in a mouse model

  2017cited by this paper
• An inhibitory gate for state transition in cortex

  2017cited by this paper
• Hippocampal GABAergic Inhibitory Interneurons.

  2017cited by this paper
• Propofol-induced spike firing suppression is more pronounced in pyramidal neurons than in fast-spiking neurons in the rat insular cortex.

  2016cited by this paper
• Transgenic mice for intersectional targeting of neural sensors and effectors with high specificity and performance.

  2015cited by this paper
• Interneuronal GABAA receptors inside and outside of synapses.

  2014cited by this paper
• alpha2delta expression sets presynaptic calcium channel abundance and release probability

  2012cited by this paper
• A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex.

  2011cited by this paper
• Driving fast-spiking cells induces gamma rhythm and controls sensory responses

  2009cited by this paper
• HCN1 Channel Subunits Are a Molecular Substrate for Hypnotic Actions of Ketamine

  2009cited by this paper
• Fate mapping Nkx2.1‐lineage cells in the mouse telencephalon

  2008cited by this paper
• A Specific Role for NR2A-Containing NMDA Receptors in the Maintenance of Parvalbumin and GAD67 Immunoreactivity in Cultured Interneurons

  2006cited by this paper
• Differential Modulation of Human N-Methyl-d-Aspartate Receptors by Structurally Diverse General Anesthetics

  2006cited by this paper
• Electrophysiological characterization of N-methyl-d-aspartate receptors in rat dorsal root ganglia neurons

  2004cited by this paper
• Origins of Cortical Interneuron Subtypes

  2004cited by this paper
• Molecular and neuronal substrates for general anaesthetics

  2004cited by this paper
• General anesthetic actions in vivo strongly attenuated by a point mutation in the GABAA receptor β3 subunit

  2003cited by this paper
• Isoflurane and propofol inhibit voltage-gated sodium channels in isolated rat neurohypophysial nerve terminals.

  2003cited by this paper
• Agent-selective Effects of Volatile Anesthetics on GABAA Receptor–mediated Synaptic Inhibition in Hippocampal Interneurons

  2001cited by this paper
• Inhibition of Presynaptic Sodium Channels by Halothane

  1998cited by this paper
• Effects of Intravenous General Anesthetics on [(3) H]GABA Release from Rat Cortical Synaptosomes

  1998cited by this paper

• Aging and perioperative brain health: Mechanisms, management, and future

  2025cites this paper
• Propofol inhibits norepinephrine release in vivo at presynaptic varicosities of locus coeruleus neurones in zebrafish larvae.

  2025cites this paper
• Preoperative Sleep Deprivation Exacerbates Anesthesia/Surgery-induced Abnormal GABAergic Neurotransmission and Neuronal Damage in the Hippocampus in Aged Mice

  2025cites this paper
• Optimizing esketamine administration for postoperative depression: a comprehensive study on laparoscopic bariatric surgery patients

  2024cites this paper
• Alterations in hippocampal somatostatin interneurons, GABAergic metabolism, and ASL perfusion in an aged male mouse model of POCD aggravated by sleep fragmentation

  2024cites this paper
• Functionally important binding site for a volatile anesthetic in a voltage-gated sodium channel identified by X-ray crystallography

  2024cites this paper
• Time to Wake Up! The Ongoing Search for General Anesthetic Reversal Agents.

  2024cites this paper
• Synapse-Specific Trapping of SNARE Machinery Proteins in the Anesthetized Drosophila Brain

  2024cites this paper
• Synapse-specific trapping of Syntaxin1a into nanoclusters by the general anesthetic isoflurane

  2023cites this paper
• Simultaneous Observation of Mouse Cortical and Hippocampal Neural Dynamics under Anesthesia through a Cranial Microprism Window

  2022cites this paper