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The Journal of Neuroscience, June 20, 2007, 27(25):6684-6691; doi:10.1523/JNEUROSCI.0934-07.2007

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Cellular/Molecular
Integration of Asynchronously Released Quanta Prolongs the Postsynaptic Spike Window

Karl J. Iremonger and Jaideep S. Bains

Hotchkiss Brain Institute and Department of Physiology and Biophysics, University of Calgary, Calgary, Alberta, Canada T2N 4N1

Correspondence should be addressed to Jaideep S. Bains, Hotchkiss Brain Institute and Department of Physiology and Biophysics, University of Calgary, 3330 Hospital Drive, NW, Calgary, Alberta, Canada T2N 4N1. Email: jsbains{at}ucalgary.ca

Classically, the release of glutamate in response to a presynaptic action potential causes a brief increase in postsynaptic excitability. Previous reports indicate that at some central synapses, a single action potential can elicit multiple, asynchronous release events. This raises the possibility that the temporal dynamics of neurotransmitter release may determine the duration of altered postsynaptic excitability. In response to physiological challenges, the magnocellular neurosecretory cells (MNCs) in the paraventricular nucleus of the hypothalamus (PVN) exhibit robust and prolonged increases in neuronal activity. Although the postsynaptic conductances that may facilitate this form of activity have been investigated thoroughly, the role of presynaptic release has been largely overlooked. Because the specific patterns of activity generated by MNCs require the activation of excitatory synaptic inputs, we sought to characterize the release dynamics at these synapses and determine whether they contribute to prolonged excitability in these cells. We obtained whole-cell recordings from MNCs in brain slices of postnatal day 21–44 rats. Stimulation of glutamatergic inputs elicited large and prolonged postsynaptic events that resulted from the summation of multiple, asynchronously released quanta. Asynchronous release was selectively inhibited by the slow calcium buffer EGTA-AM and potentiated by brief high-frequency stimulus trains. These trains caused a prolonged increase in postsynaptic spike activity that could also be eliminated by EGTA-AM. Our results demonstrate that glutamatergic terminals in PVN exhibit asynchronous release, which is important in generating large postsynaptic depolarizations and prolonged spiking in response to brief, high-frequency bursts of presynaptic activity.

Key words: asynchronous release; glutamate; paraventricular; synaptic transmission; spiking; prolonged depolarization

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Received March 1, 2007; revised May 14, 2007; accepted May 14, 2007.

Correspondence should be addressed to Jaideep S. Bains, Hotchkiss Brain Institute and Department of Physiology and Biophysics, University of Calgary, 3330 Hospital Drive, NW, Calgary, Alberta, Canada T2N 4N1. Email: jsbains{at}ucalgary.ca

This article has been cited by other articles:

				K. J. Iremonger and J. S. Bains Retrograde Opioid Signaling Regulates Glutamatergic Transmission in the Hypothalamus J. Neurosci., June 3, 2009; 29(22): 7349 - 7358. [Abstract] [Full Text] [PDF]

				M. E. Quinlan, C. O. Alberto, and M. Hirasawa Short-term potentiation of mEPSCs requires N-, P/Q- and L-type Ca2+ channels and mitochondria in the supraoptic nucleus J. Physiol., July 1, 2008; 586(13): 3147 - 3161. [Abstract] [Full Text] [PDF]

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