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The Journal of Neuroscience, April 25, 2007, 27(17):4776-4785; doi:10.1523/JNEUROSCI.0139-07.2007

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Cellular/Molecular
Differential Regulation of Action Potential- and Metabotropic Glutamate Receptor-Induced Ca²⁺ Signals by Inositol 1,4,5-Trisphosphate in Dopaminergic Neurons

Guohong Cui, Brian E. Bernier, Mark T. Harnett, and Hitoshi Morikawa

Waggoner Center for Alcohol and Addiction Research, Section of Neurobiology and Institute for Neuroscience, University of Texas, Austin, Texas 78712

Correspondence should be addressed to Hitoshi Morikawa, Waggoner Center for Alcohol and Addiction Research, University of Texas, 2500 Speedway, Molecular Biology Building 1.150A, Austin, TX 78712. Email: morikawa{at}mail.utexas.edu

Ca²⁺ signals associated with action potentials (APs) and metabotropic glutamate receptor (mGluR) activation exert distinct influences on neuronal activity and synaptic plasticity. However, it is not clear how these two types of Ca²⁺ signals are differentially regulated by neurotransmitter inputs in a single neuron. We investigated this issue in dopaminergic neurons of the ventral midbrain using brain slices. Intracellular Ca²⁺ was assessed by measuring Ca²⁺-sensitive K⁺ currents or imaging the fluorescence of Ca²⁺ indicator dyes. Tonic activation of metabotropic neurotransmitter receptors (mGluRs, 1 adrenergic receptors, and muscarinic acetylcholine receptors), attained by superfusion of agonists or weak, sustained (1 s) synaptic stimulation, augmented AP-induced Ca²⁺ transients. In contrast, Ca²⁺ signals elicited by strong, transient (50–200 ms) activation of mGluRs with aspartate iontophoresis were suppressed by superfusion of agonists. These opposing effects on Ca²⁺ signals were both mediated by an increase in intracellular inositol 1,4,5-trisphosphate (IP₃) levels, because they were blocked by heparin, an IP₃ receptor antagonist, and reproduced by photolytic application of IP₃. Evoking APs repetitively at low frequency (2 Hz) caused inactivation of IP₃ receptors and abolished IP₃ facilitation of single AP-induced Ca²⁺ signals, whereas facilitation of Ca²⁺ signals triggered by bursts of APs (five at 20 Hz) was attenuated by less than half. We further obtained evidence suggesting that the psychostimulant amphetamine may augment burst-induced Ca²⁺ signals via both depression of basal firing and production of IP₃. We propose that intracellular IP₃ tone provides a mechanism to selectively amplify burst-induced Ca²⁺ signals in dopaminergic neurons.

Key words: calcium (Ca); intracellular signaling; IP₃ receptor; metabotropic glutamate receptor; burst; dopaminergic neuron

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Received Jan. 12, 2007; revised March 28, 2007; accepted March 28, 2007.

Correspondence should be addressed to Hitoshi Morikawa, Waggoner Center for Alcohol and Addiction Research, University of Texas, 2500 Speedway, Molecular Biology Building 1.150A, Austin, TX 78712. Email: morikawa{at}mail.utexas.edu

This article has been cited by other articles:

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				M. A. Sullivan, H. Chen, and H. Morikawa Recurrent Inhibitory Network among Striatal Cholinergic Interneurons J. Neurosci., August 27, 2008; 28(35): 8682 - 8690. [Abstract] [Full Text] [PDF]

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