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Muscarinic Modulation of the Oscillatory and Repetitive Firing Properties of Entorhinal Cortex Layer II Neurons

Klink, Ruby, Alonso, Angel·1997·Journal of Neurophysiology
DOI 10.1152/jn.1997.77.4.1813
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Abstract

Klink, Ruby and Angel Alonso. Muscarinic modulation of the oscillatory and repetitive firing properties of entorhinal cortex layer II neurons. J. Neurophysiol. 77: 1813–1828, 1997. Neurons in layer II of the entorhinal cortex (EC) are key elements in the temporal lobe memory system because they integrate and transfer into the hippocampal formation convergent sensory input from the entire cortical mantle. EC layer II also receives a profuse cholinergic innervation from the basal forebrain that promotes oscillatory dynamics in the EC network and may also implement memory function. To understand the cellular basis of cholinergic actions in EC, we investigated by intracellular recording in an in vitro rat brain slice preparation the muscarinic modulation of the electroresponsive properties of the two distinct classes of medial EC layer II projection neurons, the stellate cells (SCs) and non-SCs. In both SCs and non-SCs, muscarinic receptor activation with carbachol (CCh, 10–50 μM) caused atropine-sensitive (300 nM) membrane depolarization. In SCs, the CCh-induced membrane depolarization was associated with subthreshold membrane potential oscillations and “spike cluster” discharge, which are typically expressed by these cells on depolarization. CCh, however, caused a decrease of the dominant frequency of the membrane potential oscillations from 9.2 ± 1.1 (SD) Hz to 6.3 ± 1.1 Hz, as well as a decrease of the intracluster firing frequency from 18.1 ± 1.7 Hz to 13.6 ± 1.3 Hz. In addition, spike cluster discharge was less robust, and the cells tended to shift into tonic firing during CCh. In contrast to SCs, in non-SCs, CCh drastically affected firing behavior by promoting the development of voltage-dependent, long-duration (1–5 s) slow bursts of action potentials that could repeat rhythmically at slow frequencies (0.2–0.5 Hz). Concomitantly, the slow afterhyperpolarization (sAHP) was replaced by long-lasting plateau postdepolarizations. In both SCs and non-SCs, CCh also produced conspicuous changes on the action potential waveform and its afterpotentials. Notably, CCh significantly decreased spike amplitude and rate of rise, which suggests muscarinic modulation of a voltage-dependent Na+conductance. Finally, we also observed that whereas CCh abolished the sAHP in both SCs and non-SCs, the membrane-permeant analogues of adenosine 3′,5′-cyclic monophosphate, 8-(4-chlorophenylthio)-adenosine-cyclic monophosphate and 8-bromo-adenosine-cyclic-monophosphate, abolished the sAHP in SCs but not in non-SCs. The data demonstrate that cholinergic modulation further differentiates the intrinsic electroresponsiveness of SCs and non-SCs, and add support to the presence of two parallel processing systems in medial EC layer II that could thereby differentially influence their hippocampal targets. The results also indicate an important role for the cholinergic system in tuning the oscillatory dynamics of entorhinal neurons.

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  • ACh enhances persistent spiking or plateau potentials within cortical structures, as demonstrated in brain slice preparations of the entorhinal cortex, prefrontal cortex, postsubiculum and perirhinal cortex.

    “ACh enhances persistent spiking or plateau potentials within cortical structures, as demonstrated in brain slice preparations of the entorhinal cortex (Klink and Alonso, 1997; Egorov et al., 2002; Fransen et al., 2006; Tahvildari et al., 2007), prefrontal cortex (Haj-Dahmane and Andrade, 1996, 1997, 1998), postsubiculum (Yoshida and Hasselmo, 2009) and perirhinal cortex (Leung et al., 2006).”

    From Modes and models of forebrain cholinergic neuromodulation of cognition (2011) · cites this paper as Klink and Alonso, 1997

  • The cholinergic enhancement of persistent spiking is reduced by muscarinic antagonists such as scopolamine, indicating a dependence on mechanisms activated by mAChRs.

    “The cholinergic enhancement of persistent spiking is reduced by muscarinic antagonists such as scopolamine, indicating a dependence on mechanisms activated by mAChRs (Klink and Alonso 1997; Egorov et al, 2002; Yoshida and Hasselmo, 2009).”

    From Modes and models of forebrain cholinergic neuromodulation of cognition (2011) · cites this paper as Klink and Alonso 1997

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Authors
Klink, R., & Alonso, A.
Affiliations
  • Montreal Neurological Institute and Hospital (CA)
  • Department of Neurology and Neurosurgery, Montreal Neurological Institute and McGill University, Montreal, Quebec H3A 2B4, Canada
ORCID
Klink, Ruby
Venue
Journal of Neurophysiology
Publisher
American Physiological Society
Published
1997-04-01
Volume
77
Issue
4
Pages
1813-1828
ISSN
  • 0022-3077 (ISSN-L)
  • 1522-1598
DOI
10.1152/jn.1997.77.4.1813
OpenAlex
W5055497
Cited by
228
References
82
Citations by year
2026: 2 · 2025: 2 · 2024: 3 · 2023: 2 · 2022: 2 · 2021: 1 · 2020: 3 · 2019: 5 · 2018: 8 · 2017: 4 · 2016: 5 · 2015: 6 · 2014: 11 · 2013: 13 · 2012: 17
FWCI
4.77
Type
journal article
Language
en
Open access
closed
Locations
  • Journal of Neurophysiology (publishedVersion)
  • PubMed (publishedVersion)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
Keywords
muscarinic receptors, cholinergic modulation, stellate cells, membrane potential oscillations, slow afterhyperpolarization, carbachol, atropine, repetitive firing, hippocampal formation, action potential waveform
MeSH terms
Action Potentials, Cyclic AMP, Animals, Biological Clocks, Carbachol, Male, Membrane Potentials, Neurons, Receptors, Muscarinic, Tetrodotoxin, Pyramidal Cells, Muscarinic Agonists, Entorhinal Cortex, Rats, In Vitro Techniques

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