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Nutritional state-dependent ghrelin activation of vasopressin neurons via retrograde trans-neuronal-glial stimulation of excitatory GABA circuits.
- Source :
-
The Journal of neuroscience : the official journal of the Society for Neuroscience [J Neurosci] 2014 Apr 30; Vol. 34 (18), pp. 6201-13. - Publication Year :
- 2014
-
Abstract
- Behavioral and physiological coupling between energy balance and fluid homeostasis is critical for survival. The orexigenic hormone ghrelin has been shown to stimulate the secretion of the osmoregulatory hormone vasopressin (VP), linking nutritional status to the control of blood osmolality, although the mechanism of this systemic crosstalk is unknown. Here, we show using electrophysiological recordings and calcium imaging in rat brain slices that ghrelin stimulates VP neurons in the hypothalamic paraventricular nucleus (PVN) in a nutritional state-dependent manner by activating an excitatory GABAergic synaptic input via a retrograde neuronal-glial circuit. In slices from fasted rats, ghrelin activation of a postsynaptic ghrelin receptor, the growth hormone secretagogue receptor type 1a (GHS-R1a), in VP neurons caused the dendritic release of VP, which stimulated astrocytes to release the gliotransmitter adenosine triphosphate (ATP). ATP activation of P2X receptors excited presynaptic GABA neurons to increase GABA release, which was excitatory to the VP neurons. This trans-neuronal-glial retrograde circuit activated by ghrelin provides an alternative means of stimulation of VP release and represents a novel mechanism of neuronal control by local neuronal-glial circuits. It also provides a potential cellular mechanism for the physiological integration of energy and fluid homeostasis.
- Subjects :
- Adenosine Triphosphate metabolism
Anesthetics, Local pharmacology
Animals
Calcium metabolism
Dose-Response Relationship, Drug
Enzyme Inhibitors pharmacology
Green Fluorescent Proteins genetics
Green Fluorescent Proteins metabolism
In Vitro Techniques
Male
Nerve Net drug effects
Nerve Net physiology
Neuroglia drug effects
Neurons physiology
Neurotransmitter Agents pharmacology
Rats
Rats, Wistar
Synaptic Potentials drug effects
Synaptic Potentials genetics
Tetrodotoxin pharmacology
Vasopressins genetics
Ghrelin pharmacology
Neuroglia metabolism
Neurons drug effects
Paraventricular Hypothalamic Nucleus cytology
Vasopressins metabolism
gamma-Aminobutyric Acid metabolism
Subjects
Details
- Language :
- English
- ISSN :
- 1529-2401
- Volume :
- 34
- Issue :
- 18
- Database :
- MEDLINE
- Journal :
- The Journal of neuroscience : the official journal of the Society for Neuroscience
- Publication Type :
- Academic Journal
- Accession number :
- 24790191
- Full Text :
- https://doi.org/10.1523/JNEUROSCI.3178-13.2014