Multi-factorial somato-dendritic regulation of phasic spike discharge in vasopressin neurons

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Abstract

Classically, neuropeptide release occurs from axon terminals to influence post-synaptic neurons. However, it has become increasingly clear that many neurons in the central nervous system also release neuropeptide from their somata and dendrites. This somato-dendritic neuropeptide release can have many functions, amongst which is feedback modulation of activity. In addition, most central neurons also co-express other neurotransmitters/neuromodulators alongside their principal neurotransmitter, yet the function of these co-expressed factors is largely unknown. With regard to the function of somato-dendritic neuropeptide release, hypothalamic vasopressin neurons are amongst the best understood neurons in the central nervous system. Vasopressin neurons co-express a number of other neuropeptides including apelin, dynorphin and galanin as well as the purine, adenosine triphosphate. In addition to factors co-released during exocytosis, vasopressin neurons also generate nitric oxide. Each of these factors has been demonstrated to influence the activity of vasopressin neurons. For at least some of these factors, modulation of the activity of vasopressin neurons is activity dependent; suggesting that autocrine feedback regulation of activity might be an important role for somato-dendritic release of neuromodulators across the central nervous system.

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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