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

Christian A. Cea-Del Rio, J. Josh Lawrence, Ferenc Erdelyi, Gabor Szabo, Chris J. Mcbain

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37 Citations (Scopus)

Abstract

Cholecystokinin (CCK)-containing interneuron subpopulations provide GABAergic inhibition to multiple surface domains of CA1 hippocampal pyramidal cells. CCK-basket cells (BCs) control AP initiation through perisomatic inhibition, whereas dendritically projecting Schaffer collateral-associated (SCAs) cells probably shape dendritic excitability and synaptic integration. We have shown previously that muscarinic receptor (mAChR) activation regulates firing properties and excitability of CCK-BCs; however, little is known about mAChR modulation of the related but anatomically distinct CCK-SCA population. Here, using whole-cell recordings and single-cell RT-PCR, we show that muscarine elicited a biphasic hyperpolarizing-depolarizing voltage response in CCK-SCAs, which was mediated by opposing actions of M1 and M3 mAChRs, respectively. In addition, like CCK-BCs, CCK-SCAs exhibited an M3-mediated increase in AP firing frequency and an afterdepolarization mediated synergistically by both M1 and M3 mAChRs. Spontaneous M3-mediated membrane potential oscillations (1-2 Hz) were observed in both CCK-SCAs and CCK-BCs. Using sinusoidal current injection we examined how mAChR activation of CCK interneurons alters intrinsic oscillatory properties and AP frequency preference. In CCK-BCs and CCK-SCAs, APs occurred preferentially at delta/theta frequencies (1-7 Hz) under control conditions. mAChR activation extended the AP phase-locking bandwidth into the theta and beta frequency range for CCK-SCAs and CCK-BCs respectively. This was accompanied by changes in both AP phase and precision. In conclusion, anatomically distinct CCK+ cells show similar changes in excitability, firing pattern activity and oscillatory preferences during cholinergic modulation suggesting that CCK+ interneurons probably act cooperatively to collectively synchronize the hippocampal network along the somatodendritic axis of the CA1 pyramidal cells during muscarinic receptor activation.

Original languageEnglish
Pages (from-to)609-627
Number of pages19
JournalJournal of Physiology
Volume589
Issue number3
DOIs
Publication statusPublished - Feb 1 2011

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ASJC Scopus subject areas

  • Physiology

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