Multi-factorial somato-dendritic regulation of phasic spike discharge in vasopressin neurons
Section snippets
Phasic spike discharge patterning in vasopressin neurons
Secretion of the antidiuretic hormone, vasopressin, is stimulated by increased plasma osmolality or decreased blood volume to return plasma osmolality and blood pressure towards their set-points by promoting antidiuresis and vasoconstriction (Holmes et al., 2001). The somata of vasopressin neurons (and neighbouring oxytocin neurons) are largely found within the hypothalamic paraventricular nucleus and supraoptic nucleus; these neurons project to the posterior pituitary gland and release their
Somato-dendritic neuropeptide release from vasopressin neurons
Vasopressin (and oxytocin) neurons also contain large amounts of neuropeptides within their soma and dendrites (Fig. 1), from which release occurs by exocytosis (Pow and Morris, 1989; Ludwig and Pittman, 2003). This somato-dendritic neuropeptide release is activity dependent (de Kock et al., 2003; Brown et al., 2004b), although it is unlikely that there is tight coupling between individual spikes and individual exocytotic events in the somata/dendrites (Brown et al., 2007). Nevertheless,
Autocrine modulation of phasic spike discharge by somato-dendritic vasopressin release
Vasopressin is released into the supraoptic nucleus in measurable quantities under basal conditions (Ludwig and Pittman, 2003) and vasopressin administration excites irregular or weakly phasic vasopressin neurons (Gouzenes et al., 1998) but inhibits vasopressin neurons displaying robust phasic spike discharge or continuous spike discharge (Ludwig and Leng, 1997; Gouzenes et al., 1998). Hence, it has been proposed that somato-dendritic vasopressin functions as a ‘population feedback signal’ that
Autocrine modulation of phasic spike discharge by co-released neuropeptides
In addition to vasopressin itself, vasopressin neurons synthesize and secrete several other neuropeptides that have been implicated in modulation of phasic spike discharge in vasopressin neurons, including dynorphin (Watson et al., 1982), galanin (Landry et al., 2003) and apelin (De Mota et al., 2004). Vasopressin neurons express receptors for each of these peptides (O’Donnell et al., 1999; Shuster et al., 1999; Burazin et al., 2001; O’Carroll and Lolait, 2003), providing a mechanism for each
Adenosine
In addition to activity-dependent release of adenosine and adenosine triphosphate (ATP) from glial cells or synaptic inputs, the magnocellular neurons themselves (via a combination of adenosine secretion and the rapid catabolism of exocytosed ATP (Song and Sladek, 2005)) contribute to the extracellular adenosine concentration. Similar to other neurons, vasopressin neurosecretory granules contain ATP (Poisner and Douglas, 1968), which is presumably co-released upon somato-dendritic exocytosis of
Conclusion
It is clear that several autocrine mechanisms (of which we have highlighted only a select few) serve essentially the same function; to restrain the activity of vasopressin neurons, particularly at times when secretion is stimulated. The question remains as to why so many different mechanisms do so? The simple answer might be that prevention of vasopressin over-secretion is so important for the survival of the organism that multiple redundancies are built in to the system; failure in any one (or
Abbreviations
- ADP
afterdepolarization
- AHP
afterhyperpolarization
- ATP
adenosine triphosphate
- EPSC
excitatory postsynaptic current
- GABA
γ-aminobutyric acid
- IPSC
inhibitory postsynaptic current
- mAHP
medium afterhyperpolarization
- PLC
phospholipase C
- V1aR
vasopressin V1a receptor
- V1bR
vasopressin V1b receptor
Acknowledgements
This work was supported by grants from the BBSRC (Mike Ludwig), the Wellcome Trust (Colin H. Brown) and the Lottery Grants Board of New Zealand (Colin H. Brown).
References (68)
- et al.
Apelin-immunoreactivity in the rat hypothalamus and pituitary
Neurosci. Lett.
(2002) - et al.
Mechanisms of rhythmogenesis: insights from hypothalamic vasopressin neurons
Trends Neurosci.
(2006) - et al.
Temporal dissociation of the feedback effects of dendritically co-released peptides on rhythmogenesis in vasopressin cells
Neuroscience
(2004) - et al.
The hypothalamic–neurohypophysial system regulates the hypothalamic–pituitary–adrenal axis under stress: an old concept revisited
Front. Neuroendocrinol.
(2004) - et al.
Nitric oxide synthase-containing magnocellular neurons of the rat hypothalamus synthesize oxytocin and vasopressin and express Fos following stress stimuli
J. Chem. Neuroanat.
(1996) - et al.
Physiology of vasopressin relevant to management of septic shock
Chest
(2001) - et al.
Kappa-selective agonists decrease postsynaptic potentials and calcium components of action potentials in the supraoptic nucleus of rat hypothalamus in vitro
Neuroscience
(1994) - et al.
Behavioral, neuroendocrine and thermoregulatory actions of apelin-13
Neuroscience
(2004) - et al.
Centrally administered galanin inhibits osmotically stimulated arginine vasopressin release in conscious rats
Neurosci. Lett.
(1991) - et al.
Vasopressin and oxytocin release within the brain: a dynamic concept of multiple and variable modes of neuropeptide communication
Front. Neuroendocrinol.
(2004)
Physiological pathways regulating the activity of magnocellular neurosecretory cells
Prog. Neurobiol.
Nitric oxide inhibits neuronal activity in the supraoptic nucleus of the rat hypothalamic slices
Brain Res. Bull.
Talking back: dendritic neurotransmitter release
Trends Neurosci.
N-methyl-d-aspartate receptor antagonist ketamine selectively attenuates spontaneous phasic activity of supraoptic vasopressin neurons in vivo
Neuroscience
Dendrites of hypothalamic magnocellular neurons release neurohypophysial peptides by exocytosis
Neuroscience
Distribution of apelin-synthesizing neurons in the adult rat brain
Neuroscience
Does conversion of ATP to adenosine terminate ATP-stimulated vasopressin release from hypothalamo-neurohypophyseal explants?
Brain Res.
Neuronal nitric oxide synthase inhibition differentially affects oxytocin and vasopressin secretion in salt loaded rats
Neurosci. Lett.
Burst discharge in mammalian neuroendocrine cells involves an intrinsic regenerative mechanism
Science
Intraterminal recordings from the rat neurohypophysis in vitro
J. Physiol.
Rhythmogenesis in vasopressin cells
J. Neuroendocrinol.
Autocrine feedback inhibition of plateau potentials terminates phasic bursts in magnocellular neurosecretory cells of the rat supraoptic nucleus
J. Physiol.
Phasic bursts in rat magnocellular neurosecretory cells are not intrinsically regenerative in vivo
Eur. J. Neurosci.
Kappa-opioid receptor activation inhibits post-spike depolarizing after-potentials in rat supraoptic nucleus neurones in vitro
J. Neuroendocrinol.
Endogenous activation of supraoptic nucleus kappa-opioid receptors terminates spontaneous phasic bursts in rat magnocellular neurosecretory cells
J. Neurophysiol.
Kappa-opioid regulation of neuronal activity in the rat supraoptic nucleus in vivo
J. Neurosci.
Somatodendritic dynorphin release: orchestrating activity patterns of vasopressin neurons
Biochem. Soc. Trans.
Activity-dependent feedback modulation of spike patterning of supraoptic nucleus neurons by endogenous adenosine
Am. J. Physiol. Regul. Integr. Comp. Physiol.
Regulation by osmotic stimuli of galanin-R1 receptor expression in magnocellular neurones of the paraventricular and supraoptic nuclei of the rat
J. Neuroendocrinol.
Centrally administered galanin modifies vasopressin and oxytocin release from the hypothalamo-neurohypophysial system of euhydrated and dehydrated rats
J. Physiol. Pharmacol.
Somatodendritic secretion in oxytocin neurons is upregulated during the female reproductive cycle
J. Neurosci.
Apelin, a potent diuretic neuropeptide counteracting vasopressin actions through inhibition of vasopressin neuron activity and vasopressin release
Proc. Natl. Acad. Sci. U.S.A.
Excitatory role of the hyperpolarization-activated inward current in phasic and tonic firing of rat supraoptic neurons
J. Neurosci.
Muscarinic receptor modulation of slow afterhyperpolarization and phasic firing in rat supraoptic nucleus neurons
J. Neurosci.
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