Vasopressin Regularizes the Phasic Firing Pattern of Rat Hypothalamic Magnocellular Vasopressin Neurons

Abstract

Vasopressin (AVP) magnocellular neurons of hypothalamic nuclei express specific phasic firing (successive periods of activity and silence), which conditions the mode of neurohypophyseal vasopression release. In situations favoring plasmatic secretion of AVP, the hormone is also released at the somatodendritic level, at which it is believed to modulate the activity of AVP neurons. We investigated the nature of this autocontrol by testing the effects of juxtamembrane applications of AVP on the extracellular activity of presumed AVP neurons in paraventricular and supraoptic nuclei of anesthetized rats. AVP had three effects depending on the initial firing pattern: (1) excitation of faintly active neurons (periods of activity of <10 sec), which acquired or reinforced their phasic pattern; (2) inhibition of quasi-continuously active neurons (periods of silences of <10 sec), which became clearly phasic; and (3) no effect on neurons already showing an intermediate phasic pattern (active and silent periods of 10-30 sec). Consequently, AVP application resulted in a narrower range of activity patterns of the population of AVP neurons, with a Gaussian distribution centered around a mode of 57% of time in activity, indicating a homogenization of the firing pattern. The resulting phasic pattern had characteristics close to those established previously for optimal release of AVP from neurohypophyseal endings. These results suggest a new role for AVP as an optimizing factor that would foster the population of AVP neurons to discharge with a phasic pattern known to be most efficient for hormone release.

The chemokine SDF-1/CXCL12 modulates the firing pattern of vasopressin neurons and counteracts induced vasopressin release through CXCR4

“…AVP neurons display in vitro an electrical activity almost comparable with that observed in vivo, characterized by a succession of shorter periods of activity and silence than in vivo (23). Electrical stimulations of isolated neurohypophysial terminals led to the demonstration that the silent and active periods in the firing activity of AVP neurons are equally necessary for optimal release (24,25). SDF-1, as shown here, has various effects on the electrical activity of SON neurons, resulting probably from the heterogeneity of the population recorded or from a variety of actions on the AVP neuronal population (26).…”

Apelin, a potent diuretic neuropeptide counteracting vasopressin actions through inhibition of vasopressin neuron activity and vasopressin release

“…During dehydration, while the increased somatodendritic release of AVP (33) will optimize phasic activity, facilitating systemic AVP release (ref. 32 and see references therein), apelin accumulates in SON and PVN neurons, instead of being systemically and probably intranuclearly released. Thus, decreased local supply of apelin to SON and PVN AVP cell bodies may facilitate the expression by AVP neurons of an optimized phasic activity, by lowering the inhibitory action of apelin on these neurons.…”

“…In response to osmotic stimulation, an increased somatodendritic release of AVP from SON and PVN cell bodies occurs (32,33), enhancing by means of V1 autoreceptors the phasic activity pattern of AVP neurons (32) and thereby facilitating systemic AVP release. In a similar way, apelin may be involved in autocrine somatodendritic feedback regulation of neurohypophyseal AVP neurons.…”

Over-expression of V1A receptors in PVN modulates autonomic cardiovascular control

“…Also, we have shown that during exposure of rats to air-jet stress, selective blockade of central VP receptors do not affect the response of the hypothalamo-pituitary axis as judged by the concentration of blood corticosterone (Stojičić et al, 2008), suggesting that VP released into the portal circulation during air-jet stress does not modulate ACTH release into the blood stream. Nonetheless, physiological stimuli know to increase VP release into the blood stream, such as hyperosmotic challenge, have been reported to increase intranuclear release of VP (Son et al, 2013) and that its role is to coordinate the optimal firing rate of the whole population of magnocellular neurons (Gouzènes et al, 1998), and also to activate pre-sympathetic neurons in the parvocellular division of PVN. This inter-neural cross-talk has been shown to involve V1aRs in PVN (Son et al, 2013), supporting the present findings.…”