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The Journal of Neuroscience, May 1, 2001, 21(9):2974-2982
Ionotropic Histamine Receptors and H2 Receptors
Modulate Supraoptic Oxytocin Neuronal Excitability and Dye Coupling
Glenn I.
Hatton and
Qin Zhao
Yang
Department of Cell Biology and Neuroscience, University of
California, Riverside, California 92521
Histaminergic neurons of the tuberomammillary nucleus (TM) project
monosynaptically to the supraoptic nucleus (SON). This projection
remains intact in our hypothalamic slices and permits investigation of
both brief synaptic responses and the effects of repetitively
activating this pathway. SON oxytocin (OX) neurons respond to single TM
stimuli with fast IPSPs, whose kinetics resemble those of
GABAA or glycine receptors. IPSPs were blocked by the Cl channel blocker picrotoxin, but not by
bicuculline or strychnine, and by histamine H2, but
not by H1 or H3 receptor antagonists, suggesting the presence of an ionotropic histamine receptor and the
possible nonspecificity of currently used H2 antagonists. G-protein mediation of the IPSPs was ruled out using
guanosine 5'-O-(2-thiodiphosphate) (GDP- S), pertussis
toxin, and Rp-adenosine 3',5'-cyclic monophosphothioate triethylamine
(Rp-cAMPs), none of which blocked evoked IPSPs. We also
investigated the effects of synaptically released histamine on dye
coupling and neuronal excitability. One hundred seventy-three OX
neurons were Lucifer yellow-injected in horizontal slices. Repetitive
TM stimulation (10 Hz, 5-10 min) reduced coupling, an effect blocked
by H2, but not by H1 or
H3, receptor antagonists. Because H2
receptors are linked to activation of adenylyl cyclase, TM-stimulated
reduction in coupling was blocked by GDP-S, pertussis toxin, and
Rp-cAMPs and was mimicked by 8-bromo-cAMP,
3-isobutyl-1-methylxanthine, and Sp-cAMP. Membrane
potentials of OX and vasopressin neurons were hyperpolarized,
accompanied by decreased conductances, in response to bath
application of 8-bromo-cAMP but not the membrane-impermeable cAMP.
These results suggest that synaptically released histamine, in addition
to evoking fast IPSPs in OX cells, mediates a prolonged decrease in
excitability and uncoupling of the neurons.
Key words:
chloride channels; cAMP; G-protein blockade; histamine
receptor antagonists; IPSPs; tuberomammillary nucleus
Copyright © 2001 Society for Neuroscience 0270-6474/01/2192974-09$05.00/0
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