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The Journal of Neuroscience, August 22, 2007, 27(34):9022-9031; doi:10.1523/JNEUROSCI.1954-07.2007

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Cellular/Molecular
Activation of Presynaptic GABA_A Receptors Induces Glutamate Release from Parallel Fiber Synapses

Brandon M. Stell,¹ Philippe Rostaing,² Antoine Triller,² and Alain Marty¹

¹Laboratoire de Physiologie Cérébrale, Unité de Formation et de Recherche Biomédicale, Université Paris Descartes, 75006 Paris, France, and ²Inserm, Unité 789, Ecole Normale Supérieure, 75005 Paris, France

Correspondence should be addressed to Brandon M. Stell, Laboratoire de Physiologie Cérébrale, Unité de Formation et de Recherche Biomédicale, Université Paris Descartes, 45 rue des Saints Pères, 75006 Paris, France. Email: brandon.stell{at}univ-paris5.fr

The parallel fibers relay information coming into the cerebellar cortex from the mossy fibers, and they form synapses with molecular layer interneurons (MLIs) and Purkinje cells. Here we show that activation of ionotropic GABA receptors (GABA_ARs) induces glutamate release from parallel fibers onto both MLIs and Purkinje cells. These GABA-induced EPSCs have kinetics and amplitudes identical to random spontaneous currents (sEPSCs), but, unlike sEPSCs, they occur in bursts of between one and five successive events. The variation in amplitude of events within bursts is significantly less than the variation of all sEPSC amplitudes, suggesting that the bursts result from repetitive activation of single presynaptic fibers. Electron microscopy of immunogold-labeled -1 subunits revealed GABA_ARs on parallel fiber terminals. We suggest that the activation of these receptors underlies the increased amplitude of parallel fiber-evoked Purkinje cell EPSCs seen with application of exogenous GABA or after the release of GABA from local interneurons. These results occur only when molecular layer GABA_ARs are activated, and the effects are abolished when the receptors are blocked by the GABA_AR antagonist gabazine (5 µM). From these data, we conclude that GABA_ARs located on parallel fibers depolarize parallel fiber terminals beyond the threshold for Na⁺ channel activation and thereby induce glutamate release onto MLIs and Purkinje cells.

Key words: cerebellum; GABA_A receptors; AMPA receptors; synaptic terminal; parallel fiber; Purkinje cell

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Received April 30, 2007; revised July 2, 2007; accepted July 2, 2007.

Correspondence should be addressed to Brandon M. Stell, Laboratoire de Physiologie Cérébrale, Unité de Formation et de Recherche Biomédicale, Université Paris Descartes, 45 rue des Saints Pères, 75006 Paris, France. Email: brandon.stell{at}univ-paris5.fr

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