The role of hyperpolarization-activated cationic current in spike-time precision and intrinsic resonance in cortical neurons in vitro

Philippe Gastrein, Émilie Campanac, Célia Gasselin, Robert H. Cudmore, Andrzej Bialowas, Edmond Carlier, Laure Fronzaroli-Molinieres, Norbert Ankri, Dominique Debanne

Research output: Contribution to journalArticle

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Abstract

Non-technical summary: We determined here the role of the hyperpolarization-activated cationic (h) current on the temporal organization of hippocampal activity in vitro. In CA1 pyramidal neurons the h-current has three main actions. In addition to setting intrinsic resonance frequency at ~4 Hz, the h-current determines, through two main mechanisms, the temporal precision of action potentials evoked by excitatory postsynaptic potentials or following stimulation of inhibitory postsynaptic potentials (rebound spiking). We propose that h-channels participate in the fine tuning of oscillatory activity in hippocampal and neocortical networks. Hyperpolarization-activated cyclic nucleotide modulated current (I h) sets resonance frequency within the θ-range (5-12 Hz) in pyramidal neurons. However, its precise contribution to the temporal fidelity of spike generation in response to stimulation of excitatory or inhibitory synapses remains unclear. In conditions where pharmacological blockade of I h does not affect synaptic transmission, we show that postsynaptic h-channels improve spike time precision in CA1 pyramidal neurons through two main mechanisms. I h enhances precision of excitatory postsynaptic potential (EPSP)-spike coupling because I h reduces peak EPSP duration. I h improves the precision of rebound spiking following inhibitory postsynaptic potentials (IPSPs) in CA1 pyramidal neurons and sets pacemaker activity in stratum oriens interneurons because I h accelerates the decay of both IPSPs and after-hyperpolarizing potentials (AHPs). The contribution of h-channels to intrinsic resonance and EPSP waveform was comparatively much smaller in CA3 pyramidal neurons. Our results indicate that the elementary mechanisms by which postsynaptic h-channels control fidelity of spike timing at the scale of individual neurons may account for the decreased theta-activity observed in hippocampal and neocortical networks when h-channel activity is pharmacologically reduced.

Original languageEnglish (US)
Pages (from-to)3753-3773
Number of pages21
JournalJournal of Physiology
Volume589
Issue number15
DOIs
StatePublished - Aug 1 2011
Externally publishedYes

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Pyramidal Cells
Excitatory Postsynaptic Potentials
Inhibitory Postsynaptic Potentials
Neurons
Cyclic Nucleotides
Interneurons
Synaptic Transmission
Synapses
Action Potentials
In Vitro Techniques
Pharmacology

ASJC Scopus subject areas

  • Physiology

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The role of hyperpolarization-activated cationic current in spike-time precision and intrinsic resonance in cortical neurons in vitro. / Gastrein, Philippe; Campanac, Émilie; Gasselin, Célia; Cudmore, Robert H.; Bialowas, Andrzej; Carlier, Edmond; Fronzaroli-Molinieres, Laure; Ankri, Norbert; Debanne, Dominique.

In: Journal of Physiology, Vol. 589, No. 15, 01.08.2011, p. 3753-3773.

Research output: Contribution to journalArticle

Gastrein, P, Campanac, É, Gasselin, C, Cudmore, RH, Bialowas, A, Carlier, E, Fronzaroli-Molinieres, L, Ankri, N & Debanne, D 2011, 'The role of hyperpolarization-activated cationic current in spike-time precision and intrinsic resonance in cortical neurons in vitro', Journal of Physiology, vol. 589, no. 15, pp. 3753-3773. https://doi.org/10.1113/jphysiol.2011.209148
Gastrein, Philippe ; Campanac, Émilie ; Gasselin, Célia ; Cudmore, Robert H. ; Bialowas, Andrzej ; Carlier, Edmond ; Fronzaroli-Molinieres, Laure ; Ankri, Norbert ; Debanne, Dominique. / The role of hyperpolarization-activated cationic current in spike-time precision and intrinsic resonance in cortical neurons in vitro. In: Journal of Physiology. 2011 ; Vol. 589, No. 15. pp. 3753-3773.
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AU - Gastrein, Philippe

AU - Campanac, Émilie

AU - Gasselin, Célia

AU - Cudmore, Robert H.

AU - Bialowas, Andrzej

AU - Carlier, Edmond

AU - Fronzaroli-Molinieres, Laure

AU - Ankri, Norbert

AU - Debanne, Dominique

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N2 - Non-technical summary: We determined here the role of the hyperpolarization-activated cationic (h) current on the temporal organization of hippocampal activity in vitro. In CA1 pyramidal neurons the h-current has three main actions. In addition to setting intrinsic resonance frequency at ~4 Hz, the h-current determines, through two main mechanisms, the temporal precision of action potentials evoked by excitatory postsynaptic potentials or following stimulation of inhibitory postsynaptic potentials (rebound spiking). We propose that h-channels participate in the fine tuning of oscillatory activity in hippocampal and neocortical networks. Hyperpolarization-activated cyclic nucleotide modulated current (I h) sets resonance frequency within the θ-range (5-12 Hz) in pyramidal neurons. However, its precise contribution to the temporal fidelity of spike generation in response to stimulation of excitatory or inhibitory synapses remains unclear. In conditions where pharmacological blockade of I h does not affect synaptic transmission, we show that postsynaptic h-channels improve spike time precision in CA1 pyramidal neurons through two main mechanisms. I h enhances precision of excitatory postsynaptic potential (EPSP)-spike coupling because I h reduces peak EPSP duration. I h improves the precision of rebound spiking following inhibitory postsynaptic potentials (IPSPs) in CA1 pyramidal neurons and sets pacemaker activity in stratum oriens interneurons because I h accelerates the decay of both IPSPs and after-hyperpolarizing potentials (AHPs). The contribution of h-channels to intrinsic resonance and EPSP waveform was comparatively much smaller in CA3 pyramidal neurons. Our results indicate that the elementary mechanisms by which postsynaptic h-channels control fidelity of spike timing at the scale of individual neurons may account for the decreased theta-activity observed in hippocampal and neocortical networks when h-channel activity is pharmacologically reduced.

AB - Non-technical summary: We determined here the role of the hyperpolarization-activated cationic (h) current on the temporal organization of hippocampal activity in vitro. In CA1 pyramidal neurons the h-current has three main actions. In addition to setting intrinsic resonance frequency at ~4 Hz, the h-current determines, through two main mechanisms, the temporal precision of action potentials evoked by excitatory postsynaptic potentials or following stimulation of inhibitory postsynaptic potentials (rebound spiking). We propose that h-channels participate in the fine tuning of oscillatory activity in hippocampal and neocortical networks. Hyperpolarization-activated cyclic nucleotide modulated current (I h) sets resonance frequency within the θ-range (5-12 Hz) in pyramidal neurons. However, its precise contribution to the temporal fidelity of spike generation in response to stimulation of excitatory or inhibitory synapses remains unclear. In conditions where pharmacological blockade of I h does not affect synaptic transmission, we show that postsynaptic h-channels improve spike time precision in CA1 pyramidal neurons through two main mechanisms. I h enhances precision of excitatory postsynaptic potential (EPSP)-spike coupling because I h reduces peak EPSP duration. I h improves the precision of rebound spiking following inhibitory postsynaptic potentials (IPSPs) in CA1 pyramidal neurons and sets pacemaker activity in stratum oriens interneurons because I h accelerates the decay of both IPSPs and after-hyperpolarizing potentials (AHPs). The contribution of h-channels to intrinsic resonance and EPSP waveform was comparatively much smaller in CA3 pyramidal neurons. Our results indicate that the elementary mechanisms by which postsynaptic h-channels control fidelity of spike timing at the scale of individual neurons may account for the decreased theta-activity observed in hippocampal and neocortical networks when h-channel activity is pharmacologically reduced.

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