Neuronal-derived nitric oxide and somatodendritically released vasopressin regulate neurovascular coupling in the rat hypothalamic supraoptic nucleus

Wenting Du, Javier E. Stern, Jessica A. Filosa

Research output: Contribution to journalArticle

11 Citations (Scopus)

Abstract

The classical model of neurovascular coupling (NVC) implies that activity-dependent axonal glutamate release at synapses evokes the production and release of vasoactive signals from both neurons and astrocytes, which dilate arterioles, increasing in turn cerebral blood flow (CBF) to areas with increased metabolic needs. However, whether this model is applicable to brain areas that also use less conventional neurotransmitters, such as neuropeptides, is currently unknown. To this end, we studied NVC in the rat hypothalamic magnocellular neurosecretory system (MNS) of the supraoptic nucleus (SON), in which dendritic release of neuropeptides, including vasopressin (VP), constitutes a key signaling modality influencing neuronal and network activity. Using a multidisciplinary approach, we investigated vasopressin-mediated vascular responses in SON arterioles of hypothalamic brain slices of Wistar or VP-eGFP Wistar rats. Bathapplied VP significantly constricted SON arterioles (▵ - 41 ± 7%) via activation of the V1a receptor subtype. Vasoconstrictions were also observed in response to single VP neuronal stimulation (▵ - 18 ± 2%), an effect prevented by V1a receptor blockade (V2255), supporting local dendritic VP release as the key signal mediating activity-dependent vasoconstrictions. Conversely, osmotically driven magnocellular neurosecretory neuronal population activity leads to a predominant nitric oxide-mediated vasodilation (▵19 ± 2%). Activitydependent vasodilations were followed by a VP-mediated vasoconstriction, which acted to limit the magnitude of the vasodilation and served to reset vascular tone following activity-dependent vasodilation. Together, our results unveiled a unique and complex form of NVC in the MNS, supporting a competitive balance between nitric oxide and activity-dependent dendritic released VP, in the generation of proper NVC responses.

Original languageEnglish (US)
Pages (from-to)5330-5341
Number of pages12
JournalJournal of Neuroscience
Volume35
Issue number13
DOIs
StatePublished - Apr 1 2015

Fingerprint

Supraoptic Nucleus
Vasopressins
Nitric Oxide
Vasodilation
Arterioles
Vasoconstriction
Neurosecretory Systems
Neuropeptides
Blood Vessels
Cerebrovascular Circulation
Neurovascular Coupling
Brain
Astrocytes
Synapses
Neurotransmitter Agents
Wistar Rats
Glutamic Acid
Neurons

Keywords

  • Arteriole
  • Dendrite
  • Hypothalamus
  • Neurovascular
  • Nitric oxide
  • Vasopressin

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Neuronal-derived nitric oxide and somatodendritically released vasopressin regulate neurovascular coupling in the rat hypothalamic supraoptic nucleus. / Du, Wenting; Stern, Javier E.; Filosa, Jessica A.

In: Journal of Neuroscience, Vol. 35, No. 13, 01.04.2015, p. 5330-5341.

Research output: Contribution to journalArticle

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