ArticleThe Journal of physiology2014
Optogenetic identification of an intrinsic cholinergically driven inhibitory oscillator sensitive to cannabinoids and opioids in hippocampal CA1.
Article in The Journal of physiology, 2014. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 25 papers.
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Who cites it
25 citing papers in PubMed, 52 citations in OpenAlex.
- EEG-based network dynamics in cannabis and polydrug use: a directed transfer function approach.Psychopharmacology · 2026Article
- Acetylcholine Engages Distinct Amygdala Microcircuits to Gate Internal Theta Rhythm.The Journal of neuroscience : the official journal of the Society for Neuroscience · 2024Article
- Article
- Neuromodulation of inhibitory synaptic transmission in the basolateral amygdala during fear and anxiety.Frontiers in cellular neuroscience · 2024Review
- Opioid Receptor-Mediated Regulation of Neurotransmission in the Brain.Frontiers in molecular neuroscience · 2022Review
- Disrupted inhibitory plasticity and homeostasis in Fragile X syndrome.Neurobiology of disease · 2020Article
- Molecular Specialization of GABAergic Synapses on the Soma and Axon in Cortical and Hippocampal Circuit Function and Dysfunction.Frontiers in molecular neuroscience · 2019Article
- Cannabinoid disruption of learning mechanisms involved in reward processing.Learning & memory (Cold Spring Harbor, N.Y.) · 2018Review
- Optogenetic Entrainment of Hippocampal Theta Oscillations in Behaving Mice.Journal of visualized experiments : JoVE · 2018Article
- Persistent inhibitory circuit defects and disrupted social behaviour following in utero exogenous cannabinoid exposure.Molecular psychiatry · 2017Article
- Modulation of Hippocampal Circuits by Muscarinic and Nicotinic Receptors.Frontiers in neural circuits · 2017Review
- Cannabinoids and Vanilloids in Schizophrenia: Neurophysiological Evidence and Directions for Basic Research.Frontiers in pharmacology · 2017Review
- Neuronal Dystroglycan Is Necessary for Formation and Maintenance of Functional CCK-Positive Basket Cell Terminals on Pyramidal Cells.The Journal of neuroscience : the official journal of the Society for Neuroscience · 2016Article
- Synergy of direct and indirect cholinergic septo-hippocampal pathways coordinates firing in hippocampal networks.The Journal of neuroscience : the official journal of the Society for Neuroscience · 2015Article
- Activation of muscarinic receptors by ACh release in hippocampal CA1 depolarizes VIP but has varying effects on parvalbumin-expressing basket cells.The Journal of physiology · 2015Article
- Parvalbumin and GAD65 interneuron inhibition in the ventral hippocampus induces distinct behavioral deficits relevant to schizophrenia.The Journal of neuroscience : the official journal of the Society for Neuroscience · 2014Article
- Permanent suppression of cortical oscillations in mice after adolescent exposure to cannabinoids: receptor mechanisms.Neuropharmacology · 2014Article
- Direct excitation of parvalbumin-positive interneurons by M1 muscarinic acetylcholine receptors: roles in cellular excitability, inhibitory transmission and cognition.The Journal of physiology · 2014Article
- Endogenous cannabinoid signaling at inhibitory interneurons.Current opinion in neurobiology · 2014Review
- Modulating excitation through plasticity at inhibitory synapses.Frontiers in cellular neuroscience · 2014Review
Corrections and comments
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Authors and funding
4 authors at 2 institutions in 2 countries.
Funding
Abstract
Neuronal electrical oscillations in the theta (4-14 Hz) and gamma (30-80 Hz) ranges are necessary for the performance of certain animal behaviours and cognitive processes. Perisomatic GABAergic inhibition is prominently involved in cortical oscillations driven by ACh release from septal cholinergic afferents. In neocortex and hippocampal CA3 regions, parvalbumin (PV)-expressing basket cells, activated by ACh and glutamatergic agonists, largely mediate oscillations. However, in CA1 hippocampus in vitro, cholinergic agonists or the optogenetic release of endogenous ACh from septal afferents induces rhythmic, theta-frequency inhibitory postsynaptic currents (IPSCs) in pyramidal cells, even with glutamatergic transmission blocked. The IPSCs are regulated by exogenous and endogenous cannabinoids, suggesting that they arise from type 1 cannabinoid receptor-expressing (CB1R+) interneurons - mainly cholecystokinin (CCK)-expressing cells. Nevertheless, an occult contribution of PV-expressing interneurons to these rhythms remained conceivable. Here, we directly test this hypothesis by selectively silencing CA1 PV-expressing cells optogenetically with halorhodopsin or archaerhodopsin. However, this had no effect on theta-frequency IPSC rhythms induced by carbachol (CCh). In contrast, the silencing of glutamic acid decarboxylase 2-positive interneurons, which include the CCK-expressing basket cells, strongly suppressed inhibitory oscillations; PV-expressing interneurons appear to play no role. The low-frequency IPSC oscillations induced by CCh or optogenetically stimulated ACh release were also inhibited by a μ-opioid receptor (MOR) agonist, which was unexpected because MORs in CA1 are not usually associated with CCK-expressing cells. Our results reveal novel properties of an inhibitory oscillator circuit within CA1 that is activated by muscarinic agonists. The oscillations could contribute to behaviourally relevant, atropine-sensitive, theta rhythms and link cannabinoid and opioid actions functionally.
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Registered trials
Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.