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).
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