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The Journal of Neuroscience, May 15, 2003, 23(10):4270-4277

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Vasopressin Differentially Modulates Non-NMDA Receptors in Vasopressin and Oxytocin Neurons in the Supraoptic Nucleus

Michiru Hirasawa,¹ Didier Mouginot,² Michael G. Kozoriz,¹ Samuel B. Kombian,³ and Quentin J. Pittman¹

¹Neuroscience Research Group, Department of Physiology and Biophysics, University of Calgary, Calgary, Alberta, T2N 4N1 Canada, ²Centre de Recherché en Neurosciences, Centre Hospitalier de l'Université Laval, Sainte-Foy, Quebec, G1Y 4G2 Canada, and ³Faculty of Pharmacy, Kuwait University, Safat, 13110 Kuwait

Magnocellular neurons of the supraoptic nucleus release the neuropeptides oxytocin and vasopressin from their dendrites to regulate their synaptic inputs. This study aims to determine the cellular mechanism by which vasopressin modulates excitatory synaptic transmission. Presumably by electroporation through perforated patch, we were able to successfully introduce biocytin into cells in which we performed an electrophysiological study. This method enabled us to determine that roughly half of the recorded neurons were immunoreactive to oxytocin-associated neurophysin and showed two characteristic features: an inward rectification and a sustained outward rectification. The remaining half showed a linear voltage-current relationship and was immunoreactive to vasopressin-associated neurophysin. Using these electrophysiological characteristics and post hoc immunohistochemistry to identify vasopressin or oxytocin neurons, we found that vasopressin decreased evoked EPSCs in vasopressin neurons while increasing EPSCs in oxytocin neurons. In both types of neurons, EPSC decay constants were not affected, indicating that desensitization of non-NMDA receptors did not underlie the EPSC amplitude change. In vasopressin neurons, both vasopressin and a V1a receptor agonist, F-180, decreased AMPA-induced currents, an effect blocked by a V1a receptor antagonist SR49059. In oxytocin neurons, AMPA-induced currents were facilitated by vasopressin, whereas F-180 had no effect. An oxytocin receptor antagonist blocked the facilitatory effect of vasopressin. Thus, we conclude that vasopressin inhibits EPSCs in vasopressin neurons via postsynaptic V1a receptors, whereas it facilitates EPSCs in oxytocin neurons through oxytocin receptors.

Key words: EPSC; non-NMDA receptor; V1a receptor; oxytocin receptor; vasopressin; supraoptic nucleus; dendritic release

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Received Oct. 31, 2002; revised Feb. 12, 2003; accepted Feb. 26, 2003.

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