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The Journal of Neuroscience, July 16, 2003, 23(15):6223-6231

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Priming of Excitatory Synapses by ₁ Adrenoceptor-Mediated Inhibition of Group III Metabotropic Glutamate Receptors

Grant R. J. Gordon and Jaideep S. Bains

Neuroscience Research Group, Department of Physiology and Biophysics, University of Calgary, Alberta, T2N 4N1, Canada

Adaptive responses mediated by the hypothalamus require sustained activation until homeostasis is achieved. Increases in excitatory drive to the magnocellular neuroendocrine cells that mediate these responses, however, result in the activation of a presynaptic metabotropic glutamate receptor (mGluR) that curtails synaptic excitability. Recent evidence that group III mGluRs can be inhibited by protein kinase C prompted us to test the hypothesis that activation of PKC by noradrenaline (NA) inhibits group III mGluRs and increases excitatory synaptic input to these cells. To examine the effects of NA on miniature EPSCs (mEPSCs), we obtained whole-cell recordings from magnocellular vasopressin and oxytocin neurons in the paraventricular nucleus of the hypothalamus. All of the neurons tested in the current study displayed an ₁ adrenoceptor-mediated increase in mEPSC frequency in response to NA (1–200 µM). The excitatory effects of NA were mimicked by the phorbol ester PMA and blocked by the PKC inhibitor calphostin C. The activation of PKC inhibits the efficacy of group III mGluRs, resulting in an increase in mEPSC frequency in response to a subsequent exposure to NA. By removing feedback inhibition, this mechanism effectively primes the synapses such that subsequent activation is more efficacious. The novel form of synaptic rescaling afforded by this cross-talk between distinct metabotropic receptors provides a means by which ascending catecholamine inputs can facilitate the control of homeostasis by hypothalamic networks.

Key words: magnocellular; hypothalamus; presynaptic inhibition; G-protein-coupled receptors; noradrenaline; paraventricular nucleus

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Received Dec. 23, 2002; revised May. 16, 2003; accepted May. 16, 2003.

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