TY - JOUR
T1 - The role of hyperpolarization-activated cationic current in spike-time precision and intrinsic resonance in cortical neurons in vitro
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
PY - 2011/8
Y1 - 2011/8
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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U2 - 10.1113/jphysiol.2011.209148
DO - 10.1113/jphysiol.2011.209148
M3 - Article
C2 - 21624967
AN - SCOPUS:79960833196
SN - 0022-3751
VL - 589
SP - 3753
EP - 3773
JO - Journal of Physiology
JF - Journal of Physiology
IS - 15
ER -