Vasopressin facilitates glycinergic and GABAergic synaptic transmission in developing hypoglossal motoneurons

Abstract

The hypoglossal nucleus of young rats contains vasopressin binding sites and vasopressin can directly excite hypoglossal motoneurons. In addition, indirect evidence suggests that vasopressin can enhance the synaptic input to motoneurons. We have characterized this latter effect by using brainstem slices and whole-cell recordings. We found that, in the presence of blockers of fast glutamatergic transmission, vasopressin strongly facilitated inhibitory synaptic activity. On average, vasopressin caused a six-fold increase in the frequency and a 1.5-fold increase in the amplitude of GABAergic postsynaptic currents. The effect of vasopressin on glycinergic postsynaptic currents was similar in magnitude. Vasopressin did not affect the frequency of GABAergic or glycinergic miniature postsynaptic currents, indicating that the peptide-induced facilitation of inhibitory transmission was mediated by receptors located on the somatodendritic region rather than on axon terminals of presynaptic neurons. The pharmacological profile of these receptors was determined by using d[Cha4]AVP and dVDAVP, selective agonists of V1b and V2 vasopressin receptors, respectively, and Phaa-D-Tyr-(Et)-Phe-Gln-Pro-Arg-Arg-NH2, a selective antagonist of V1a vasopressin receptors. The two agonists had no effect on the frequency of inhibitory postsynaptic currents. By contrast, the antagonist suppressed the vasopressin-induced facilitation of these currents, indicating that the receptors involved were exclusively of the V1a type. Thus, vasopressin exerts a dual action on hypoglossal motoneurons: a direct excitatory action and an indirect action mediated by GABAergic and glycinergic synapses. By virtue of this dual effect, vasopressin could alter the input-output properties of these motoneurons. Alternatively, it could play a role in generating or modulating specific motor patterns.

Vasopressin indirectly excites dorsal raphe serotonin neurons through activation of the vasopressin1A receptor

“…In the lateral septum most cells responded to AVP with an increase in IPSC frequency; only a small subset of a cells show a direct depolarization (Allaman-Exertier et al, 2007). A similar multi-synaptic effect has been observed in brainstem and spinal cord motor neurons where increases in EPSCs and IPSCs have been observed in different neuron populations (Liu et al, 2003, Reymond-Marron et al, 2005). It is also important to note here that the observed response was not due to oxytocin receptors; the response could be fully blocked by d(CH 2 ) 5 [Tyr(Me) 2 , Dab 5 ]AVP, a V 1A R antagonist with no affinity for the oxytocin receptor (Manning et al, 2008).…”

Spinal vasopressin alleviates formalin-induced nociception by enhancing GABAA receptor function in mice

“…Elevating intracellular calcium by activation of V 1 A receptors may thus play a role in AVPinduced potentiation of GABA A receptor functions, which needs to further be verified. In developing hypoglossal motoneurons, AVP increases also spontaneous GABAergic IPSCs' amplitude through V 1A receptors [21].…”

Vasopressin modulates lateral septal network activity via two distinct electrophysiological mechanisms

“…Vasopressin appears to act in a dual, apparently paradoxical manner: (i) by acting postsynaptically, it causes excitation in a specific neuronal population; (ii) by acting indirectly, it causes synaptic inhibition in this same neuronal population. This is the case for VII and XII brainstem motoneurons and for spinal motoneurons, where vasopressin, in addition to evoking an inward current or inducing depolarization, also enhances the GABAergic and glycinergic synaptic input (Liu et al, 2003;Reymond-Marron et al, 2005). In the amygdala, vasopressin directly excites neurons located in the central amygdaloid nucleus, but in addition oxytocin (or vasopressin) [ 3 H]AVP binding is expressed in DLU ⁄ mm 2 .…”