The presence of pacemaker HCN channels identifies theta rhythmic GABAergic neurons in the medial septum
- 15 August 2008
- journal article
- Published by Wiley in Journal Of Physiology-London
- Vol. 586 (16), 3893-3915
- https://doi.org/10.1113/jphysiol.2008.155242
Abstract
The medial septum (MS) is an indispensable component of the subcortical network which synchronizes the hippocampus at theta frequency during specific stages of information processing. GABAergic neurons exhibiting highly regular firing coupled to the hippocampal theta rhythm are thought to form the core of the MS rhythm-generating network. In recent studies the hyperpolarization-activated, cyclic nucleotide-gated non-selective cation (HCN) channel was shown to participate in theta synchronization of the medial septum. Here, we tested the hypothesis that HCN channel expression correlates with theta modulated firing behaviour of MS neurons by a combined anatomical and electrophysiological approach. HCN-expressing neurons represented a subpopulation of GABAergic cells in the MS partly overlapping with parvalbumin (PV)-containing neurons. Rhythmic firing in the theta frequency range was characteristic of all HCN-expressing neurons. In contrast, only a minority of HCN-negative cells displayed theta related activity. All HCN cells had tight phase coupling to hippocampal theta waves. As a group, PV-expressing HCN neurons had a marked bimodal phase distribution, whereas PV-immunonegative HCN neurons did not show group-level phase preference despite significant individual phase coupling. Microiontophoretic blockade of HCN channels resulted in the reduction of discharge frequency, but theta rhythmic firing was perturbed only in a few cases. Our data imply that HCN-expressing GABAergic neurons provide rhythmic drive in all phases of the hippocampal theta activity. In most MS theta cells rhythm genesis is apparently determined by interactions at the level of the network rather than by the pacemaking property of HCN channels alone.Keywords
This publication has 74 references indexed in Scilit:
- The Hippocamposeptal Pathway Generates Rhythmic Firing of GABAergic Neurons in the Medial Septum and Diagonal Bands: An Investigation Using a Complete Septohippocampal PreparationIn VitroJournal of Neuroscience, 2008
- Noncholinergic Lesions of the Medial Septum Impair Sequential Learning of Different Spatial LocationsJournal of Neuroscience, 2007
- Pacemaking by HCN Channels Requires Interaction with PhosphoinositidesNeuron, 2006
- Activity-dependent decrease of excitability in rat hippocampal neurons through increases in IhNature Neuroscience, 2005
- 5-HT1A receptor mRNA and immunoreactivity in the rat medial septum/diagonal band of Broca—relationships to GABAergic and cholinergic neuronsJournal of Chemical Neuroanatomy, 2005
- A Behavioral Role for Dendritic Integration: HCN1 Channels Constrain Spatial Memory and Plasticity at Inputs to Distal Dendrites of CA1 Pyramidal NeuronsCell, 2004
- Phase Segregation of Medial Septal GABAergic Neurons during Hippocampal Theta ActivityJournal of Neuroscience, 2004
- In vivo contribution of h‐channels in the septal pacemaker to theta rhythm generationEuropean Journal of Neuroscience, 2004
- Distinct electrophysiological properties of glutamatergic, cholinergic and GABAergic rat septohippocampal neurons: novel implications for hippocampal rhythmicityJournal Of Physiology-London, 2003
- Cross-correlation analysis of septohippocampal neurons during ≡-rhythmBrain Research, 1987