Cholinergic modulation of excitatory synaptic input integration in hippocampal CA1: Acetylcholine and excitatory synaptic integration in hippocampal CA1
Open accessAbstract
During theta rhythm, the timing of inputs to hippocampal CA1 from the perforant path (PP) of the entorhinal cortex and the Schaffer collaterals (SCs) from individual CA3 pyramidal neurons can vary within an individual theta period. Importantly, during theta rhythms these interactions occur during elevated acetylcholine concentrations. Thus, I examined the effect that PP inputs have on SC inputs in hippocampal CA1 during cholinergic receptor activation. To do this I measured the impact that a single electrical stimulus of the stratum lacunosum-moleculare (SLM, which contains the PP) had on excitation evoked by stimulation of the stratum radiatum (SR, which contains the SC) using voltage-sensitive dye imaging, field excitatory postsynaptic potentials and whole cell patch clamping in rat hippocampal brain slices. My data showed that SLM stimulation one half a theta cycle or less (25-75 ms) before SR stimulation resulted in the summation of excitatory events in SR and SP of hippocampal CA1. The summation was unaffected by cholinergic receptor activation by carbachol. SLM stimulation one theta cycle (150-225 ms) preceding SR stimulation significantly suppressed excitatory events measured in SR and SP. This SLM stimulus inhibition of SR-driven excitatory events was augmented by carbachol application. The carbachol effect was blocked by atropine and SLM-driven suppression of excitatory events was blocked by the GABA(B) receptor antagonist CGP 54626. SR field EPSP slopes were unaffected by SLM prepulses. Carbachol increased the probability of SR input to drive action potential firing in CA1 pyramidal neurons, which was inhibited by SLM prepulses (150-225 ms). Together these data provide important information regarding the integration of inputs in hippocampal CA1 during theta rhythms. More specifically, SR inputs can be differentially gated by SLM feedforward inhibition at varying temporal intervals within a theta cycle.
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Cholinergic signaling is important in the integration of excitatory inputs, specifically via α4β2 nAChRs.
“Recent voltage-sensitive dye imaging (VSDi) studies have demonstrated the importance of cholinergic signaling in the integration of excitatory inputs, specifically via a4b2 nAChRs (Bell et al, 2011; McQuiston, 2010).”
From Divergent Functional Effects of Sazetidine-A and Varenicline During Nicotine Withdrawal (2013) · cites this paper as McQuiston, 2010
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Divergent Functional Effects of Sazetidine-A and Varenicline During Nicotine Withdrawal
Turner, J. R., Wilkinson, D. S., Poole, R. L., Gould, T. J., Carlson, G. C., & Blendy, J. A. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.105 · Cited by 29 · see citing works
- Authors
- McQuiston, A. R.
- Affiliations
- Virginia Commonwealth University (US)
- Corresponding author
- McQuiston, A. Rory
- Venue
- The Journal of Physiology
- Publisher
- Wiley
- Published
- 2010-09-30
- Volume
- 588
- Issue
- 19
- Pages
- 3727-3742
- ISSN
- 0022-3751 (ISSN-L)
- PMC
- PMC2998223
- OpenAlex
- W1543933280
- Cited by
- 16
- References
- 52
- Citations by year
- 2024: 1 · 2023: 1 · 2021: 1 · 2019: 2 · 2017: 1 · 2016: 3 · 2015: 2 · 2013: 2 · 2012: 1
- FWCI
- 0.65
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- The Journal of Physiology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute on Drug Abuse (R01DA017110, DA017110)
- National Institute of Neurological Disorders and Stroke (NS063059, R21NS063059)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- cholinergic modulation, hippocampal CA1, theta oscillations, perforant path, Schaffer collaterals, feedforward inhibition, GABAB receptors, carbachol, CA3 pyramidal cells, stratum lacunosum-moleculare, stratum radiatum, action potential firing, temporal summation
- MeSH terms
- Action Potentials, Animals, Carbachol, Coloring Agents, Evoked Potentials, Extracellular Matrix, Male, Organophosphorus Compounds, Parasympathetic Nervous System, Receptors, Cholinergic, Reflex, Startle, Rats, Sprague-Dawley, Receptors, GABA-B, Patch-Clamp Techniques, Muscarinic Agonists, GABA Agonists, GABA Antagonists, Excitatory Postsynaptic Potentials, Rats, Electrophysiological Phenomena, CA1 Region, Hippocampal, In Vitro Techniques
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