Short‐term potentiation of GABAergic synaptic inputs to vasopressin and oxytocin neurones

<jats:title>Key points</jats:title><jats:sec><jats:label/><jats:p><jats:list list-type="bullet"> <jats:list-item><jats:p>Hypothalamic neurones that release the hormones vasopressin and oxytocin from the posterior pituitary are controlled, in part, by synaptic inputs mediated by the neurotransmitter GABA.</jats:p></jats:list-item> <jats:list-item><jats:p>GABA synapses on the vasopressin neurones, but not the oxytocin neurones, have been shown to elicit excitation.</jats:p></jats:list-item> <jats:list-item><jats:p>We show that brief (1 s) electrical stimulation of hypothalamus slices causes release of GABA lasting several minutes at synapses on vasopressin and oxytocin neurones.</jats:p></jats:list-item> <jats:list-item><jats:p>Consistent with GABA being excitatory in vasopressin neurones, brief electrical stimulation of GABA synaptic inputs elicited activation of vasopressin neurones, but not oxytocin neurones, that lasted for several minutes.</jats:p></jats:list-item> <jats:list-item><jats:p>Prolonged GABA release following a brief stimulus together with GABA excitation of vasopressin neurones constitute a basic synaptic mechanism for controlling vasopressin release.</jats:p></jats:list-item> </jats:list></jats:p></jats:sec><jats:sec><jats:title>Abstract</jats:title><jats:p>The magnocellular vasopressin (VP) and oxytocin (OT) neurones undergo long‐term synaptic plasticity to accommodate prolonged hormone demand. By contrast, rapidly induced, transient synaptic plasticity in response to brief stimuli could enable the activation of magnocellular neurones in response to acute challenges. Here, we report a robust short‐term potentiation of asynchronous GABAergic synaptic inputs (STP<jats:sub>GABA</jats:sub>) to VP and OT neurones of the hypothalamic supraoptic nucleus elicited by repetitive extracellular electrical stimulation. The STP<jats:sub>GABA</jats:sub> required extracellular Ca<jats:sup>2+</jats:sup>, but did not require activation of glutamate, VP or OT receptors or nitric oxide synthesis. Presynaptic action potential generation was necessary for the induction, but not the maintenance, of STP<jats:sub>GABA</jats:sub>. The STP<jats:sub>GABA</jats:sub> led to a minutes‐long GABA<jats:sub>A</jats:sub> receptor‐dependent increase in spike frequency in VP neurones, but not in OT neurones, consistent with an excitatory function of GABA in only VP neurones and with the generation of prolonged bursts of action potentials in VP neurones. Therefore, this short‐term plasticity of GABAergic synaptic inputs is likely to play very different roles in the regulation of OT and VP neurones and their distinct patterns of physiological activation.</jats:p></jats:sec>