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The Journal of Neuroscience, February 7, 2007, 27(6):1325-1333; doi:10.1523/JNEUROSCI.2676-06.2007

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Cellular/Molecular
Retrograde Regulation of GABA Transmission by the Tonic Release of Oxytocin and Endocannabinoids Governs Postsynaptic Firing

Stéphane H. R. Oliet,^1 * Dinara V. Baimoukhametova,^2 * Richard Piet,¹ and Jaideep S. Bains²

¹Institut National de la Santé et de la Recherche Médicale, Unité 862, Université Victor Segalen Bordeaux 2, Bordeaux 33077, France, and ²Department of Biophysics and Physiology, The Hotchkiss Brain Institute, University of Calgary, Calgary, Alberta, Canada T2N 4N1

Correspondence should be addressed to Jaideep S. Bains, Department of Biophysics and Physiology, The Hotchkiss Brain Institute, University of Calgary, Calgary, Alberta, Canada T2N 1N4. Email: jsbains{at}ucalgary.ca

The probability of neurotransmitter release at the nerve terminal is an important determinant of synaptic efficacy. At some central synapses, the postsynaptic, or target, neuron determines neurotransmitter release probability (P_r) at the presynaptic terminal. The mechanisms responsible for this target-cell dependent control of P_r have not been elucidated. Using whole-cell patch-clamp recordings from magnocellular neurosecretory cells in the paraventricular and supraoptic nuclei of the hypothalamus, we demonstrate that inhibitory, GABA synapses specifically onto oxytocin (OT)-producing neurosecretory cells exhibit a low P_r that is relatively uniform at multiple synapses onto the same cell. This low P_r results from a two-step process that requires the tonic release of OT from the postsynaptic cell. The ambient extracellular levels of neuropeptide are sufficient to activate postsynaptic OT receptors and trigger the Ca²⁺-dependent production of endocannabinoids, which act in a retrograde manner at presynaptic cannabinoid CB₁ receptors to decrease GABA release. The functional consequence of this tonic inhibition of GABA release is that all inhibitory inputs facilitate uniformly when activated at high rates of activity. This causes inhibition in the postsynaptic cell that is sufficiently powerful to disrupt firing. Blockade of CB₁ receptors increases P_r at these synapses, resulting in a rapid depression of IPSCs at high rates of activity, thereby eliminating the ability of afferent inputs to inhibit postsynaptic firing. By playing a deterministic role in GABA release at the afferent nerve terminal, the postsynaptic OT neuron effectively filters synaptic signals and thereby modulates its own activity patterns.

Key words: endocannabinoid; GABAergic modulation; neuropeptide; oxytocin; paraventricular; pituitary; presynaptic; supraoptic; synaptic transmission

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Received June 23, 2006; revised Oct. 6, 2006; accepted Oct. 19, 2006.

Correspondence should be addressed to Jaideep S. Bains, Department of Biophysics and Physiology, The Hotchkiss Brain Institute, University of Calgary, Calgary, Alberta, Canada T2N 1N4. Email: jsbains{at}ucalgary.ca

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