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The Journal of Neuroscience, August 2, 2006, 26(31):8183-8194; doi:10.1523/JNEUROSCI.1962-06.2006

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Cellular/Molecular
Nonlinear [Ca²⁺] Signaling in Dendrites and Spines Caused by Activity-Dependent Depression of Ca²⁺ Extrusion

Volker Scheuss,¹ Ryohei Yasuda,¹ Aleksander Sobczyk,^1,2 and Karel Svoboda¹

¹Howard Hughes Medical Institute, Cold Spring Harbor Laboratory, Cold Spring Harbor, New York 11724, and ²Department of Physics, State University of New York at Stony Brook, Stony Brook, New York 11794

Correspondence should be addressed to Dr. Karel Svoboda, Howard Hughes Medical Institute, Janelia Farm Research Campus, 19700 Helix Drive, Ashburn, VA 20147.

Spine Ca²⁺ triggers the induction of synaptic plasticity and other adaptive neuronal responses. The amplitude and time course of Ca²⁺ signals specify the activation of the signaling pathways that trigger different forms of plasticity such as long-term potentiation and depression. The shapes of Ca²⁺ signals are determined by the dynamics of Ca²⁺ sources, Ca²⁺ buffers, and Ca²⁺ extrusion mechanisms. Here we show in rat CA1 pyramidal neurons that plasma membrane Ca²⁺ pumps (PMCAs) and Na⁺/Ca²⁺ exchangers are the major Ca²⁺ extrusion pathways in spines and small dendrites. Surprisingly, we found that Ca²⁺ extrusion via PMCA and Na⁺/Ca²⁺ exchangers slows in an activity-dependent manner, mediated by intracellular Na⁺ and Ca²⁺ accumulations. This activity-dependent depression of Ca²⁺ extrusion is, in part, attributable to Ca²⁺-dependent inactivation of PMCAs. Ca²⁺ extrusion recovers from depression with a time constant of 0.5 s. Depression of Ca²⁺ extrusion provides a positive feedback loop, converting small differences in stimuli into large differences in Ca²⁺ concentration. Depression of Ca²⁺ extrusion produces Ca²⁺ concentration dynamics that depend on the history of neuronal activity and therefore likely modulates the induction of synaptic plasticity.

Key words: calcium extrusion; plasma membrane calcium pump; sodium calcium exchanger; dendritic spine; calcium imaging; two-photon glutamate uncaging

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Received March 17, 2006; revised June 21, 2006; accepted June 21, 2006.

Correspondence should be addressed to Dr. Karel Svoboda, Howard Hughes Medical Institute, Janelia Farm Research Campus, 19700 Helix Drive, Ashburn, VA 20147.

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