Vasopressin (AVP) and oxytocin (OT) magnocellular neurons of the hypothalamic supraoptic nuclei autocontrol their electrical activity through the somatodendritic release of their respective peptides. These neurons belong to specific networks, respond to distinct physiological stimuli, display highly characteristic electrical activities and influence the release of AVP and OT at axon terminals in the neurohypophysis as well. The membrane mechanisms supporting AVP and OT action on the electrical activity of SON neurons involve specific autoreceptors and induce an increase in [Ca²⁺]_i in these cells. AVP involves the phospholipase C and adenylate cyclase intracellular pathways that are activated, in the periphery, by V1 (V1a and V1b)- and V2-type vasopressin receptors, respectively. In AVP neurons, [Ca²⁺]_i measurements in response to V1a and V2 agonists and antagonists revealed the functional expression of these two types of receptors, but V2-type mRNA is not detectable within AVP cells. While investigating the intracellular messengers, using various second messenger pathway activators and inhibitors, involved in the [Ca²⁺]_i response to V1a and V2 agonists, [Ca²⁺]_i measurements and AVP release experiments revealed the activation in hypothalamic supraoptic neurons of V1a receptors involved in both the phospholipase C and the adenylate cyclase pathways. Similarly, both signal transduction pathways are involved following V2 receptor activation, suggesting the functional expression of these two types of receptors in AVP neurons. Together, the physiological responses and pharmacological profiles of AVP receptors in the SON neurons are atypical and do not fit with what has been described in the peripheral system. Therefore, there is a need to further characterize the AVP receptors using newly developed tools to understand the physiology of AVP receptors in the CNS neurons.