Journal of Neurophysiology 2014-08-01

Intrinsic Ca2+-dependent theta oscillations in apical dendrites of hippocampal CA1 pyramidal cells in vitro.

Allan Kjeldsen Hansen, Steen Nedergaard, Mogens Andreasen

Index: J. Neurophysiol. 112(3) , 631-43, (2014)

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Abstract

Behavior-associated theta-frequency oscillation in the hippocampal network involves a patterned activation of place cells in the CA1, which can be accounted for by a somatic-dendritic interference model predicting the existence of an intrinsic dendritic oscillator. Here we describe an intrinsic oscillatory mechanism in apical dendrites of in vitro CA1 pyramidal cells, which is induced by suprathreshold depolarization and consists of rhythmic firing of slow spikes in the theta-frequency band. The incidence of slow spiking (29%) increased to 78% and 100% in the presence of the β-adrenergic agonist isoproterenol (2 μM) or 4-aminopyridine (2 mM), respectively. Prior depolarization facilitated the induction of slow spiking. Applied electrical field polarization revealed a distal dendritic origin of slow spikes. The oscillations were largely insensitive to tetrodotoxin, but blocked by nimodipine (10 μM), indicating that they depend on activation of L-type Ca2+ channels. Antagonists of T-, R-, N-, and P/Q-type Ca2+ channels had no detectable effect. The slow spike dimension and frequency was sensitive to 4-aminopyridine (0.1-2 mM) and TEA (10 mM), suggesting the contribution from voltage-dependent K+ channels to the oscillation mechanism. α-Dendrotoxin (10 μM), stromatoxin (2 μM), iberiotoxin (0.2 μM), apamin (0.5 μM), linorpidine (30 μM), and ZD7288 (20 μM) were without effect. Oscillations induced by sine-wave current injection or theta-burst synaptic stimulation were voltage-dependently attenuated by nimodipine, indicating an amplifying function of L-type Ca2+ channels on imposed signals. These results show that the apical dendrites have intrinsic oscillatory properties capable of generating rhythmic voltage fluctuations in the theta-frequency band.Copyright © 2014 the American Physiological Society.