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J Physiol Volume 555, Number 3, 699-711, March 15, 2004 DOI: 10.1113/jphysiol.2003.051136
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Ca2+ and frequency dependence of exocytosis in isolated somata of magnocellular supraoptic neurones of the rat hypothalamus

Brandi L. Soldo1, David R. Giovannucci2, Edward L. Stuenkel1 and Hylan C. Moises1

1 Department of Molecular and Integrative Physiology, University of Michigan Medical School, Ann Arbor, MI 48109-0622, USA2 Department of Anatomy and Neurobiology, Medical College of Ohio, 3036 Arlington Avenue, Toledo, OH 43614, USA

In addition to action potential-evoked exocytotic release at neurohypophysial nerve terminals, the neurohormones arginine vasopressin (aVP) and oxytocin (OT) undergo Ca2+-dependent somatodendritic release within the supraoptic and paraventricular hypothalamic nuclei. However, the cellular and molecular mechanisms that underlie this release have not been elucidated. In the present study, the whole-cell patch-clamp technique was utilized in combination with high-time-resolved measurements of membrane capacitance (Cm) and microfluorometric measurements of cytosolic free Ca2+ concentration ([Ca2+]i) to examine the Ca2+ and stimulus dependence of exocytosis in the somata of magnocellular neurosecretory cells (MNCs) isolated from rat supraoptic nucleus (SON). Single depolarizing steps (>=20 ms) that evoked high-voltage-activated (HVA) Ca2+ currents (ICa) and elevations in intracellular Ca2+ concentration were accompanied by an increase in Cm in a majority (40/47) of SON neurones. The Cm responses were composed of an initial Ca2+-independent, transient component and a subsequent, sustained phase of increased Cm (termed {Delta}Cm) mediated by an influx of Ca2+, and increased with corresponding prolongation of depolarizing step durations (20–200 ms). From this relationship we estimated the rate of vesicular release to be 1533 vesicles s-1. Delivery of neurone-derived action potential waveforms (APWs) as stimulus templates elicited ICa and also induced a {Delta}Cm, provided APWs were applied in trains of greater than 13 Hz. A train of APWs modelled after the bursting pattern recorded from an OT-containing neurone during the milk ejection reflex was effective in supporting an exocytotic {Delta}Cm in isolated MNCs, indicating that the somata of SON neurones respond to physiological patterns of neuronal activity with Ca2+-dependent exocytotic activity.

(Received 11 July 2003; accepted after revision 20 November 2003; first published online 28 November 2003)
Corresponding author D. Giovannucci: Department of Anatomy and Neurobiology, Medical College of Ohio, 3036 Arlington Avenue, Toledo, OH 43614, USA.  Email: dgiovannucci{at}mco.edu

B. L. Soldo and D. R. Giovannucci contributed equally to this work.






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