In:
The Journal of Physiology, Wiley, Vol. 592, No. 22 ( 2014-11-15), p. 4931-4949
Abstract:
Because intracellular Ca 2+ is important for activity‐dependent growth and development, we studied action potential (AP)‐evoked dendritic Ca 2+ influx and Ca 2+ buffering in developing rat CA1 pyramidal cells during the first 1–4 weeks after birth. We show for the first time that active dendritic backpropagation of APs generates large Ca 2+ transients in pyramidal cell dendrites even after the first postnatal week. The amplitude of Ca 2+ transients at 1 week is similar to that at 4 weeks because a four‐fold upregulation of calcium influx per AP is balanced by a similar increase in endogenous Ca 2+ buffer capacity during this period. The calcium extrusion after APs was about five times slower at 1 week than at 4 weeks, resulting in a slower decay in young cells and a more effective temporal summation during brief bursts of APs. During continuous theta‐burst firing, dendritic calcium concentration was up to three‐fold larger in animals aged 1 week than in those aged 4 weeks, generated via an activity‐dependent slow‐down of Ca 2+ extrusion, which may allow Ca 2+ ‐dependent control of growth and development with a large dynamic range. Abstract Although Ca 2+ is critically important in activity‐dependent neuronal development, not much is known about the regulation of dendritic Ca 2+ signals in developing neurons. Here, we used ratiometric Ca 2+ imaging to investigate dendritic Ca 2+ signalling in rat hippocampal pyramidal cells during the first 1–4 weeks of postnatal development. We show that active dendritic backpropagation of Na v channel‐dependent action potentials (APs) evoked already large dendritic Ca 2+ transients in animals aged 1 week with amplitudes of ∼150 n m , similar to the amplitudes of ∼160 nM seen in animals aged 4 weeks. Although the AP‐evoked dendritic Ca 2+ load increased about four times during the first 4 weeks, the peak amplitude of free Ca 2+ concentration was balanced by a four‐fold increase in Ca 2+ buffer capacity κ s (∼70 vs . ∼280). Furthermore, Ca 2+ extrusion rates increased with postnatal development, leading to a slower decay time course (∼0.2 s vs . ∼0.1 s) and more effective temporal summation of Ca 2+ signals in young cells. Most importantly, during prolonged theta‐burst stimulation dendritic Ca 2+ signals were up to three times larger in cells at 1 week than at 4 weeks of age and much larger than predicted by linear summation, which is attributable to an activity‐dependent slow‐down of Ca 2+ extrusion. As Ca 2+ influx is four‐fold smaller in young cells, the larger Ca 2+ signals are generated using four times less ATP consumption. Taken together, the data suggest that active backpropagations regulate dendritic Ca 2+ signals during early postnatal development. Remarkably, during prolonged AP firing, Ca 2+ signals are several times larger in young than in mature cells as a result of activity‐dependent regulation of Ca 2+ extrusion rates.
Type of Medium:
Online Resource
ISSN:
0022-3751
,
1469-7793
DOI:
10.1113/jphysiol.2014.592.issue-22
DOI:
10.1113/jphysiol.2014.281931
Language:
English
Publisher:
Wiley
Publication Date:
2014
detail.hit.zdb_id:
1475290-6
SSG:
12
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