Serotonergic modulation of hyperpolarization-activated current in acutely isolated rat dorsal root ganglion neurons

The effect of serotonin (5-HT) on the hyperpolarization-activated cation current ( I H ) was studied in small-, medium- and large-diameter acutely isolated rat dorsal root ganglion (DRG) cells, including cells categorized as type 1, 2, 3 and 4 based on membrane properties. 5-HT increased I H in 91 %...

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Bibliographic Details
Published in:The Journal of physiology 1999-07, Vol.518 (2), p.507-523
Main Authors: Cardenas, Carla G., Mar, Lucinda P. Del, Vysokanov, Alexander V., Arnold, Peter B., Cardenas, Luz M., Surmeier, D. James, Scroggs, Reese S.
Format: Article
Language:English
Subjects:
8-Hydroxy-2-(di-n-propylamino)tetralin - pharmacology
Action Potentials - drug effects
Animals
Cell Size
Cyclic Nucleotide-Gated Cation Channels
Dopamine Antagonists - pharmacology
Ganglia, Spinal - cytology
Ganglia, Spinal - drug effects
Ganglia, Spinal - metabolism
Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels
In Vitro Techniques
Ion Channels - drug effects
Ion Channels - genetics
Ion Channels - metabolism
Male
Membrane Potentials - drug effects
Membrane Potentials - physiology
Neurons, Afferent - drug effects
Neurons, Afferent - metabolism
Neurons, Afferent - ultrastructure
Original
Patch-Clamp Techniques
Pindolol - analogs & derivatives
Pindolol - pharmacology
Potassium Channels
Rats
Rats, Sprague-Dawley
Receptors, Serotonin - drug effects
Receptors, Serotonin - metabolism
Reverse Transcriptase Polymerase Chain Reaction
Serotonin - analogs & derivatives
Serotonin - pharmacology
Serotonin Antagonists - pharmacology
Serotonin Receptor Agonists - pharmacology
Spiperone - pharmacology
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Summary:The effect of serotonin (5-HT) on the hyperpolarization-activated cation current ( I H ) was studied in small-, medium- and large-diameter acutely isolated rat dorsal root ganglion (DRG) cells, including cells categorized as type 1, 2, 3 and 4 based on membrane properties. 5-HT increased I H in 91 % of medium-diameter DRG cells (including type 4) and in 67 % of large-diameter DRG cells, but not other DRG cell types. The increase of I H by 5-HT was antagonized by spiperone but not cyanopindolol, and was mimicked by 5-carboxyamidotryptamine, but not (+)-8-hydroxydipropylaminotetralin (8-OH-DPAT) or cyanopindolol. These data suggested the involvement of 5-HT 7 receptors, which were shown to be expressed by medium-diameter DRG cells using RT-PCR analysis. 5-HT shifted the conductance-voltage relationship of I H by +6 mV without changing peak conductance. The effects of 5-HT on I H were mimicked and occluded by forskolin, but not by inactive 1,9-dideoxy forskolin. At holding potentials negative to -50 mV, 5-HT increased steady-state inward current and instantaneous membrane conductance (fast current). The 5-HT-induced inward current and fast current were blocked by Cs + but not Ba 2+ and reversed at -23 mV, consistent with the properties of tonically activated I H . In medium-diameter neurons recorded from in the current clamp mode, 5-HT depolarized the resting membrane potential, decreased input resistance and facilitated action potential generation by anode-break excitation. The above data suggest that in distinct subpopulations of DRG neurons, 5-HT increases cAMP levels via activation of 5-HT 7 receptors, which shifts the voltage dependence of I H to more depolarized potentials and increases neuronal excitability.
ISSN:0022-3751
1469-7793
DOI:10.1111/j.1469-7793.1999.0507p.x