Cannabinoids attenuate hippocampal gamma oscillations by suppressing excitatory synaptic input onto CA3 pyramidal neurons and fast spiking basket cells

Non‐Technical Summary  Administration of cannabinoids can impair several cognitive functions, including memory by altering synchronous activities in cortical networks. We show that the gamma frequency (40 Hz) oscillations in hippocampal slices, that are prominent oscillations in electroencephalogram during awake states in vivo, are reduced by cannabinoids. This effect can be explained by the suppression of the excitatory synaptic transmission onto fast spiking basket cells, GABAergic cells that are key players in oscillogenesis. The reduced excitatory drive onto these interneurons leads to a reduction in neuronal firing frequency and precision, and thus to smaller field potentials. Our data further our understanding of the synaptic mechanisms of how cannabinoids alter neuronal operation.

• Publication year

  2011

• Venue

  Journal of Physiology

• Publication date

  2011-08-22

• Fields of study

  Biology, Medicine

• Identifiers
  DOI 10.1113/jphysiol.2011.216259PMID 21859823PMCID 3224883
• 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.

• The role of phase synchronization in memory processes

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  2010cited by this paper
• Instantaneous modulation of gamma oscillation frequency by balancing excitation with inhibition.

  2009cited by this paper
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  2009cited by this paper
• stablishing a physiological environment for visualized in vitro brain slice ecordings by increasing oxygen supply and modifying aCSF content

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• Alteration of Theta Timescale Dynamics of Hippocampal Place Cells by a Cannabinoid Is Associated with Memory Impairment

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• Reporting ethical matters in The Journal of Physiology: standards and advice

  2009influential reference
• Hippocampal CA3 output is crucial for ripple-associated reactivation and consolidation of memory.

  2009cited by this paper
• Endocannabinoid-mediated control of synaptic transmission.

  2009cited by this paper
• 2009 Special Issue: Network mechanisms of gamma oscillations in the CA3 region of the hippocampus

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• Endocannabinoid signaling as a synaptic circuit breaker in neurological disease

  2008influential reference
• Recurrent Synaptic Input and the Timing of Gamma-Frequency-Modulated Firing of Pyramidal Cells during Neocortical “UP” States

  2008cited by this paper
• Complementary Modulation of Somatic Inhibition by Opioids and Cannabinoids

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• Excitatory afferents to CA3 pyramidal cells display differential sensitivity to CB1 dependent inhibition of synaptic transmission.

  2008influential reference
• Input-specific plasticity at excitatory synapses mediated by endocannabinoids in the dentate gyrus.

  2008cited by this paper
• Activation of cannabinoid-1 receptors disrupts sensory gating and neuronal oscillation: relevance to schizophrenia.

  2008cited by this paper
• Coincidence Detection of Place and Temporal Context in a Network Model of Spiking Hippocampal Neurons

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• Gamma oscillations dynamically couple hippocampal CA3 and CA1 regions during memory task performance

  2007cited by this paper
• Postsynaptic origin of CB1‐dependent tonic inhibition of GABA release at cholecystokinin‐positive basket cell to pyramidal cell synapses in the CA1 region of the rat hippocampus

  2007cited by this paper
• Recruitment of parvalbumin-positive interneurons determines hippocampal function and associated behavior.

  2007cited by this paper
• Pharmacological profile of the selective FAAH inhibitor KDS-4103 (URB597).

  2006cited by this paper
• Molecular Composition of the Endocannabinoid System at Glutamatergic Synapses

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• Cannabinoids reveal importance of spike timing coordination in hippocampal function

  2006influential reference
• Synaptic Currents in Anatomically Identified CA3 Neurons during Hippocampal Gamma Oscillations In Vitro

  2006cited by this paper
• Conditional dendritic spike propagation following distal synaptic activation of hippocampal CA1 pyramidal neurons

  2005cited by this paper
• Perisomatic feedback inhibition underlies cholinergically induced fast network oscillations in the rat hippocampus in vitro.

  2005cited by this paper
• Two distinct classes of muscarinic action on hippocampal inhibitory synapses: M2‐mediated direct suppression and M1/M3‐mediated indirect suppression through endocannabinoid signalling

  2004cited by this paper
• Segregation of two endocannabinoid‐hydrolyzing enzymes into pre‐ and postsynaptic compartments in the rat hippocampus, cerebellum and amygdala

  2004cited by this paper
• Immunocytochemical study of GABAergic neurons containing the calcium-binding protein parvalbumin in the rat hippocampus

  2004cited by this paper
• Spike Timing of Distinct Types of GABAergic Interneuron during Hippocampal Gamma Oscillations In Vitro

  2004cited by this paper
• Mechanisms of gamma oscillations in the hippocampus of the behaving rat.

  2003cited by this paper
• The high-conductance state of neocortical neurons in vivo

  2003cited by this paper
• Functional localization of cannabinoid receptors and endogenous cannabinoid production in distinct neuron populations of the hippocampus

  2003influential reference
• Theta and Gamma Oscillations during Encoding Predict Subsequent Recall

  2003cited by this paper
• Presynaptic Cannabinoid Sensitivity Is a Major Determinant of Depolarization-Induced Retrograde Suppression at Hippocampal Synapses

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• Mu opioid receptors are in discrete hippocampal interneuron subpopulations

  2002cited by this paper
• Place Cells and Place Recognition Maintained by Direct Entorhinal-Hippocampal Circuitry

  2002cited by this paper
• Cannabinoids inhibit hippocampal GABAergic transmission and network oscillations

  2000cited by this paper
• A model of gamma‐frequency network oscillations induced in the rat CA3 region by carbachol in vitro

  2000influential reference
• Increased mortality, hypoactivity, and hypoalgesia in cannabinoid CB1 receptor knockout mice.

  1999cited by this paper
• Mechanism of Cannabinoid Effects on Long-Term Potentiation and Depression in Hippocampal CA1 Neurons

  1999cited by this paper
• Presynaptically Located CB1 Cannabinoid Receptors Regulate GABA Release from Axon Terminals of Specific Hippocampal Interneurons

  1999influential reference
• Role of cannabinoid receptors in memory storage.

  1998influential reference
• Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro

  1998influential reference
• Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation

  1995cited by this paper
• Systemic or intrahippocampal cannabinoid administration impairs spatial memory in rats

  1995cited by this paper
• Synchronization of cortical activity and its putative role in information processing and learning.

  1993cited by this paper
• Selective attention enhances the auditory 40-Hz transient response in humans

  1993cited by this paper
• High-frequency network oscillation in the hippocampus.

  1992cited by this paper
• Two-stage model of memory trace formation: a role for "noisy" brain states.

  1989cited by this paper

• Dialectics of perisomatic inhibition—The unity and conflict of opposites

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  2021cites this paper
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• Perinatal Fentanyl Exposure Leads to Long-Lasting Impairments in Somatosensory Circuit Function and Behavior

  2020cites this paper
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  2020cites this paper
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  2020cites this paper
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  2019influential citation
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  2018cites this paper
• Effects of Adolescent THC Exposure on the Prefrontal GABAergic System: Implications for Schizophrenia-Related Psychopathology

  2018cites this paper
• Hippocampal GABAergic Inhibitory Interneurons.

  2017cites this paper
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  2017cites this paper
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  2016cites this paper
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  2016cites this paper
• Disruption of hippocampal synaptic transmission and long‐term potentiation by psychoactive synthetic cannabinoid ‘Spice’ compounds: comparison with Δ9‐tetrahydrocannabinol

  2016cites this paper
• Dissecting the cannabinergic control of behavior: The where matters

  2015cites this paper
• Development of sensory gamma oscillations and cross-frequency coupling from childhood to early adulthood.

  2015cites this paper
• Hippocampal Representations on the Spatial Delay Discounting Task

  2015cites this paper
• Long-term changes in the CA3 associative network of fear-conditioned mice

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• Optogenetic identification of an intrinsic cholinergically driven inhibitory oscillator sensitive to cannabinoids and opioids in hippocampal CA1

  2014influential citation
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  2014influential citation
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