Literature DB >> 21115639

Cholinergic modulation amplifies the intrinsic oscillatory properties of CA1 hippocampal cholecystokinin-positive interneurons.

Christian A Cea-del Rio1, J Josh Lawrence, Ferenc Erdelyi, Gabor Szabo, Chris J McBain.   

Abstract

In the mammalian hippocampus, the neurotransmitter acetylcholine (ACh) promotes learning and memory storage. During sensory processing and learning, large ACh-dependent electrical oscillatory events are observed, which involve the synchronization of both inhibitory and excitatory neural circuits. While the actions of ACh are known on excitatory hippocampal circuits, its actions on specific inhibitory circuits are poorly understood. We show that two types of cholecystokinin-positive local circuit inhibitory interneuron, the so-called 'basket cells' and 'Schaffer collateral-associated' cells, which innervate separately the cell body and dendritic regions of principal cells, are modulated similarly by cholinergic receptor activation. In both cell types activation of their muscarinic receptors triggers a general increase of excitability and intrinsic oscillatory activity, and a more efficient engagement to slow network oscillations. Knowledge of how cholinergic neuromodulation acts on neurochemically identical but morphologically distinct inhibitory interneurons will allow us to understand the role played by this important neuromodulator during hippocampal-dependent tasks in vivo.

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Year:  2010        PMID: 21115639      PMCID: PMC3055546          DOI: 10.1113/jphysiol.2010.199422

Source DB:  PubMed          Journal:  J Physiol        ISSN: 0022-3751            Impact factor:   5.182


  47 in total

1.  Muscarinic receptor activity has multiple effects on the resting membrane potentials of CA1 hippocampal interneurons.

Authors:  A R McQuiston; D V Madison
Journal:  J Neurosci       Date:  1999-07-15       Impact factor: 6.167

Review 2.  Structural basis of the cholinergic and serotonergic modulation of GABAergic neurons in the hippocampus.

Authors:  A I Gulyás; L Acsády; T F Freund
Journal:  Neurochem Int       Date:  1999-05       Impact factor: 3.921

3.  Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons.

Authors:  I Katona; B Sperlágh; A Sík; A Käfalvi; E S Vizi; K Mackie; T F Freund
Journal:  J Neurosci       Date:  1999-06-01       Impact factor: 6.167

4.  Cell type-specific dependence of muscarinic signalling in mouse hippocampal stratum oriens interneurones.

Authors:  J Josh Lawrence; Jeffrey M Statland; Zachary M Grinspan; Chris J McBain
Journal:  J Physiol       Date:  2005-12-01       Impact factor: 5.182

5.  Complementary roles of cholecystokinin- and parvalbumin-expressing GABAergic neurons in hippocampal network oscillations.

Authors:  Thomas Klausberger; Laszlo F Marton; Joseph O'Neill; Jojanneke H J Huck; Yannis Dalezios; Pablo Fuentealba; Wai Yee Suen; Edit Papp; Takeshi Kaneko; Masahiko Watanabe; Jozsef Csicsvari; Peter Somogyi
Journal:  J Neurosci       Date:  2005-10-19       Impact factor: 6.167

6.  Theta-frequency resonance in hippocampal CA1 neurons in vitro demonstrated by sinusoidal current injection.

Authors:  L S Leung; H W Yu
Journal:  J Neurophysiol       Date:  1998-03       Impact factor: 2.714

7.  Distinct timing in the activity of cannabinoid-sensitive and cannabinoid-insensitive basket cells.

Authors:  Lindsey L Glickfeld; Massimo Scanziani
Journal:  Nat Neurosci       Date:  2006-04-30       Impact factor: 24.884

8.  Intrinsic theta-frequency membrane potential oscillations in hippocampal CA1 interneurons of stratum lacunosum-moleculare.

Authors:  C A Chapman; J C Lacaille
Journal:  J Neurophysiol       Date:  1999-03       Impact factor: 2.714

9.  Total number and ratio of excitatory and inhibitory synapses converging onto single interneurons of different types in the CA1 area of the rat hippocampus.

Authors:  A I Gulyás; M Megías; Z Emri; T F Freund
Journal:  J Neurosci       Date:  1999-11-15       Impact factor: 6.167

10.  Regulation of fast-spiking basket cell synapses by the chloride channel ClC-2.

Authors:  Csaba Földy; Sang-Hun Lee; Robert J Morgan; Ivan Soltesz
Journal:  Nat Neurosci       Date:  2010-08-01       Impact factor: 24.884

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  29 in total

Review 1.  An update on cholinergic regulation of cholecystokinin-expressing basket cells.

Authors:  Christian A Cea-del Rio; Chris J McBain; Kenneth A Pelkey
Journal:  J Physiol       Date:  2011-12-23       Impact factor: 5.182

2.  Persistent sodium current drives conditional pacemaking in CA1 pyramidal neurons under muscarinic stimulation.

Authors:  Jason Yamada-Hanff; Bruce P Bean
Journal:  J Neurosci       Date:  2013-09-18       Impact factor: 6.167

3.  Functional specification of CCK+ interneurons by alternative isoforms of Kv4.3 auxiliary subunits.

Authors:  Viktor János Oláh; David Lukacsovich; Jochen Winterer; Antónia Arszovszki; Andrea Lőrincz; Zoltan Nusser; Csaba Földy; János Szabadics
Journal:  Elife       Date:  2020-06-03       Impact factor: 8.140

4.  Direct excitation of parvalbumin-positive interneurons by M1 muscarinic acetylcholine receptors: roles in cellular excitability, inhibitory transmission and cognition.

Authors:  Feng Yi; Jackson Ball; Kurt E Stoll; Vaishali C Satpute; Samantha M Mitchell; Jordan L Pauli; Benjamin B Holloway; April D Johnston; Neil M Nathanson; Karl Deisseroth; David J Gerber; Susumu Tonegawa; J Josh Lawrence
Journal:  J Physiol       Date:  2014-05-30       Impact factor: 5.182

Review 5.  Physiological roles of CNS muscarinic receptors gained from knockout mice.

Authors:  Morgane Thomsen; Gunnar Sørensen; Ditte Dencker
Journal:  Neuropharmacology       Date:  2017-09-11       Impact factor: 5.250

Review 6.  Hippocampal GABAergic Inhibitory Interneurons.

Authors:  Kenneth A Pelkey; Ramesh Chittajallu; Michael T Craig; Ludovic Tricoire; Jason C Wester; Chris J McBain
Journal:  Physiol Rev       Date:  2017-10-01       Impact factor: 37.312

Review 7.  Neuronal Network Oscillations in Neurodegenerative Diseases.

Authors:  Volker Nimmrich; Andreas Draguhn; Nikolai Axmacher
Journal:  Neuromolecular Med       Date:  2015-04-29       Impact factor: 3.843

8.  Muscarinic excitation of parvalbumin-positive interneurons contributes to the severity of pilocarpine-induced seizures.

Authors:  Feng Yi; Evan DeCan; Kurt Stoll; Eric Marceau; Karl Deisseroth; J Josh Lawrence
Journal:  Epilepsia       Date:  2014-12-13       Impact factor: 5.864

9.  Gating of hippocampal activity, plasticity, and memory by entorhinal cortex long-range inhibition.

Authors:  Jayeeta Basu; Jeffrey D Zaremba; Stephanie K Cheung; Frederick L Hitti; Boris V Zemelman; Attila Losonczy; Steven A Siegelbaum
Journal:  Science       Date:  2016-01-08       Impact factor: 47.728

Review 10.  Behavioral state-dependent modulation of distinct interneuron subtypes and consequences for circuit function.

Authors:  Jason C Wester; Chris J McBain
Journal:  Curr Opin Neurobiol       Date:  2014-07-22       Impact factor: 6.627

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