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The Journal of Neuroscience, September 15, 2000, 20(18):6773-6780

Dependence of Transient and Residual Calcium Dynamics on Action-Potential Patterning during Neuropeptide Secretion

Martin Muschol¹ and B. M. Salzberg^{1, 2}

Departments of ¹ Neuroscience and ² Physiology, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania 19104-6074

Secretion of the neuropeptide arginine vasopressin (AVP) from the neurohypophysis is optimized by short phasic bursts of action potentials with a mean intraburst frequency around 10 Hz. Several hypotheses, most prominently action-potential broadening and buildup of residual calcium, have been proposed to explain this frequency dependence of AVP release. However, how either of these mechanisms would optimize release at any given frequency remains an open question. We have addressed this issue by correlating the frequency-dependence of intraterminal calcium dynamics and AVP release during action-potential stimulation.

By monitoring the intraterminal calcium changes with low-affinity indicator dyes and millisecond time resolution, the signal could be dissected into three separate components: rapid Ca²⁺ rises ([Ca²⁺]_tr) related to action-potential depolarization, Ca²⁺ extrusion and/or uptake, and a gradual increase in residual calcium ([Ca²⁺]_res) throughout the stimulus train. Action-potential stimulation modulated all three components in a manner dependent on both the stimulation frequency and number of stimuli. Overall, the cumulative [Ca²⁺]_tr amplitude initially increased with f_Stim and then rapidly deteriorated, with a maximum around f_Stim  5 Hz. Residual calcium levels, in contrast, increased monotonically with stimulation frequency.

Simultaneously with the calcium measurements we determined the amount of AVP release evoked by each stimulus train. Hormone release increased with f_Stim beyond the peak in [Ca²⁺]_tr amplitudes, reaching its maximum between 5 and 10 Hz before returning to its 1 Hz level. Thus, AVP release responds to the temporal patterning of stimulation, is sensitive to both [Ca²⁺]_tr and [Ca²⁺]_res, and is optimized at a frequency intermediate between the frequency-dependent maxima in [Ca²⁺]_tr and [Ca²⁺]_res.

Key words: calcium dynamics; excitation-secretion coupling; arginine vasopressin; exocytosis; neurohypophysis; action potential; residual calcium

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Copyright © 2000 Society for Neuroscience  0270-6474/00/20186773-08$05.00/0

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