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Dorsoventral differences in Kv7/M‐current and its impact on resonance, temporal summation and excitability in rat hippocampal pyramidal cells
Author(s) -
Hönigsperger Christoph,
Marosi Máté,
Murphy Ricardo,
Storm Johan F.
Publication year - 2015
Publication title -
the journal of physiology
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 1.802
H-Index - 240
eISSN - 1469-7793
pISSN - 0022-3751
DOI - 10.1113/jphysiol.2014.280826
Subject(s) - hippocampal formation , neuroscience , pyramidal cell , electrophysiology , patch clamp , chemistry , hyperpolarization (physics) , gating , hippocampus , biophysics , current clamp , biology , stereochemistry , nuclear magnetic resonance spectroscopy
Key points Kv7 (KCNQ/M) channels are known to control excitability and generate subthreshold M‐resonance in CA1 hippocampal pyramidal cells, but their properties and functions have not previously been compared along the dorsoventral (septotemporal) axis We used whole‐cell recordings to compare electrophysiological properties of dorsal and ventral CA1 pyramidal cells in hippocampal slices from 3‐ to 4‐week‐old rats Blockade of Kv7/M‐channels with 10,10‐ bis (4‐pyridinylmethyl)‐9(10 H )‐anthracenone dihydrochloride (XE991) had a stronger impact on electrical properties in dorsal than ventral pyramidal cells, including input resistance, temporal summation, M‐resonance, spike threshold, medium after‐hyperpolarization, excitability, and spike frequency adaptation. Voltage‐clamp recordings revealed a larger amplitude and left‐shifted voltage dependence of XE991‐sensitive current ( I M ) in dorsal vs . ventral cells. I M ‐dependent differences in excitability and resonance may be important for rate and phase coding of CA1 place cells along the dorsoventral axis and may enhance epileptiform activity in ventral pyramidal cells.Abstract In rodent hippocampi, the connections, gene expression and functions differ along the dorsoventral (D–V) axis. CA1 pyramidal cells show increasing excitability along the D–V axis, although the underlying mechanism is not known. In the present study, we investigated how the M‐current ( I M ), caused by Kv7/M (KCNQ) potassium channels, and known to often control neuronal excitability, contributes to D–V differences in intrinsic properties of CA1 pyramidal cells. Using whole‐cell patch clamp recordings and the selective Kv7/M blocker 10,10‐ bis (4‐pyridinylmethyl)‐9(10 H )‐anthracenone dihydrochloride (XE991) in hippocampal slices from 3‐ to 4‐week‐old rats, we found that: (i) I M had a stronger impact on subthreshold electrical properties in dorsal than ventral CA1 pyramidal cells, including input resistance, temporal summation of artificial synaptic potentials, and M‐resonance; (ii) I M activated at more negative potentials (left‐shifted) and had larger peak amplitude in the dorsal than ventral CA1; and (iii) the initial spike threshold (during ramp depolarizations) was elevated, and the medium after‐hyperpolarization and spike frequency adaptation were increased (i.e. excitability was lower) in the dorsal rather than ventral CA1. These differences were abolished or reduced by application of XE991, indicating that they were caused by I M . Thus, it appears that I M has stronger effects in dorsal than in ventral rat CA1 pyramidal cells because of a larger maximal M‐conductance and left‐shifted activation curve in the dorsal cells. These mechanisms may contribute to D–V differences in the rate and phase coding of position by CA1 place cells, and may also enhance epileptiform activity in ventral CA1.