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The Journal of Neuroscience, January 24, 2007, 27(4):860-867; doi:10.1523/JNEUROSCI.3579-06.2007

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Cellular/Molecular
Cell Type-Specific Expression of a Genetically Encoded Calcium Indicator Reveals Intrinsic Calcium Oscillations in Adult Gonadotropin-Releasing Hormone Neurons

Christine L. Jasoni,¹ Martin G. Todman,¹ Max M. Strumia,² and Allan E. Herbison¹

¹Centre for Neuroendocrinology and Department of Physiology, and ²Department of Mathematics, University of Otago School of Medical Sciences, Dunedin 9054, New Zealand

Correspondence should be addressed to Allan E. Herbison, Centre for Neuroendocrinology, Department of Physiology, University of Otago School of Medical Sciences, P.O. Box 913, Dunedin 9054, New Zealand. Email: allan.herbison{at}stonebow.otago.ac.nz

The gonadotropin-releasing hormone (GnRH) neurons exhibit a unique pattern of episodic activity to control fertility in all mammals. To enable the measurement of intracellular calcium concentration ([Ca²⁺]_i) in adult GnRH neurons in situ, we generated transgenic mice in which the genetically encodable calcium indicator ratiometric Pericam was expressed by 95% of GnRH neurons. Real-time monitoring of [Ca²⁺]_i within adult male GnRH neurons in the acute brain slice revealed that 70% of GnRH neurons exhibited spontaneous, 10–15 s duration [Ca²⁺]_i transients with a mean frequency of 7 per hour. The remaining 30% of GnRH neurons did not exhibit calcium transients nor did a population of non-GnRH cells located within the lateral septum that express Pericam. Pharmacological studies using antagonists to the inositol-1,4,5-trisphosphate receptor (InsP₃R) and several calcium channels, demonstrated that [Ca²⁺]_i transients in GnRH neurons were generated by an InsP₃R-dependent store-release mechanism and were independent of plasma membrane ligand- or voltage-gated calcium channels. Interestingly, the abolition of action potential-mediated transmission with tetrodotoxin reduced the number of [Ca²⁺]_i transients in GnRH neurons by 50% (p < 0.05), suggesting a modulatory role for synaptic inputs on [Ca²⁺]_i transient frequency. Using a novel transgenic strategy that enables [Ca²⁺]_i to be examined in a specific neuronal phenotype in situ, we provide evidence for spontaneous [Ca²⁺]_i fluctuations in adult GnRH neurons. This represents the initial description of spontaneous [Ca²⁺]_i transients in mature neurons and shows that they arise from an InsP₃R-generating mechanism that is further modulated by synaptic inputs.

Key words: calcium; IP₃R; GnRH; transgenic; Pericam; inositol

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Received Aug. 18, 2006; revised Dec. 14, 2006; accepted Dec. 15, 2006.

Correspondence should be addressed to Allan E. Herbison, Centre for Neuroendocrinology, Department of Physiology, University of Otago School of Medical Sciences, P.O. Box 913, Dunedin 9054, New Zealand. Email: allan.herbison{at}stonebow.otago.ac.nz

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