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Cholinergic stimulation enhances cytosolic calcium ion accumulation in mouse hippocampal CA1 pyramidal neurones during short action potential trains

Steven M. Beier and Michael E. Barish

1. Acetylcholine is a regulatory cofactor for numerous activity-dependent processes of central nervous system development and plasticity in which increases in cytosolic calcium ion concentration ([Ca²⁺]_cyto) couple membrane excitation to cellular changes. We examined how cholinergic receptor activation affects temporal and spatial aspects of increases in [Ca²⁺]_cyto during short trains of action potentials in hippocampal CA1 pyramidal neurones. Membrane-impermeant Ca²⁺-sensitive dye was introduced into the cytosol during whole-cell recordings, and Ca²⁺-dependent fluorescence was recorded from somatic, nuclear and proximal dendrite regions with high temporal resolution.

2. In all neuronal compartments, the cholinergic agonist carbachol (5 µM) increased resting [Ca²⁺]_cyto and the maximum [Ca²⁺]_cyto attained during a short action potential train. Carbachol also slowed the recovery of [Ca²⁺]_cyto towards resting levels. The largest increases in peak cytosolic Ca²⁺ concentration ([Ca²⁺]_cyto) were seen in the dendrite and apical cell body, while relaxations of the carbachol-induced increase in [Ca²⁺]_cyto showed greater prolongation in the nucleus and basal cell body.

3. Most significantly, the difference between Ca²⁺ signals recorded before and during exposure to carbachol consistently showed a monotonic rise and smooth fall in all cell compartments, suggesting that the increase in [Ca²⁺]_cyto associated with each action potential was not altered by carbachol. Consistent with this view, changes in Ca²⁺ signalling were not accompanied by changes in action potential waveforms.

4. The effects of carbachol were partially reversed by simultaneous exposure to atropine, or partially inhibited by inclusion of heparin in the intracellular solution, indicating the involvement of muscarinic acetylcholine receptors and InsP₃-sensitive Ca²⁺-release channels.

5. Our data indicate that carbachol-induced slowing of [Ca²⁺]_cyto relaxations after each action potential results in enhanced accumulation of Ca²⁺ in the cytosol in the absence of changes in action potential-driven Ca²⁺ entry. By modulating the time course of Ca²⁺ signals, cholinergic stimulation may regulate the activation of Ca²⁺-dependent intracellular processes dependent on patterns of [Ca²⁺]_cyto changes.

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