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The Journal of Neuroscience, January 11, 2006, 26(2):597-608; doi:10.1523/JNEUROSCI.4493-05.2006

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Development/Plasticity/Repair
GABAergic Signaling at Mossy Fiber Synapses in Neonatal Rat Hippocampus

Victoria F. Safiulina,¹ Giorgia Fattorini,² Fiorenzo Conti,² and Enrico Cherubini¹

¹Neuroscience Programme, International School for Advanced Studies, 34014 Trieste, Italy, and ²Department of Neurosciences, Università Politecnica delle Marche, 60020 Ancona, Italy

In the adult rat hippocampus, granule cell mossy fibers (MFs) form excitatory glutamatergic synapses with CA3 principal cells and local inhibitory interneurons. However, evidence has been provided that, in young animals and after seizures, the same fibers can release in addition to glutamate GABA. Here we show that, during the first postnatal week, stimulation of granule cells in the dentate gyrus gave rise to monosynaptic GABA_A-mediated responses in principal cells and in interneurons. These synapses were indeed made by MFs because they exhibited strong paired-pulse facilitation, high sensitivity to the metabotropic glutamate receptor agonist L-AP-4, and short-term frequency-dependent facilitation. MF responses were potentiated by blocking the plasma membrane GABA transporter GAT-1 with NO-711 or by allosterically modulating GABA_A receptors with flurazepam. Chemical stimulation of granule cell dendrites with glutamate induced barrages of GABA_A-mediated postsynaptic currents into target neurons. Furthermore, immunocytochemical experiments demonstrated colocalization of vesicular GABA transporter with vesicular glutamate transporter-1 and zinc transporter 3, suggesting that GABA can be taken up and stored in synaptic vesicles of MF terminals.

Additional fibers releasing both glutamate and GABA into principal cells and interneurons were recruited by increasing the strength of stimulation. Both the GABAergic and the glutamatergic component of synaptic currents occurred with the same latency and were reversibly abolished by L-AP-4, indicating that they originated from the MFs. GABAergic signaling may play a crucial role in tuning hippocampal network during postnatal development. Low-threshold GABA-releasing fibers may undergo elimination, and this may occur when GABA shifts from the depolarizing to the hyperpolarizing direction.

Key words: mossy fiber synapses; immature hippocampus; GABA release; spontaneous synaptic events; pyramidal cells and interneurons; VGAT; VGLUT1

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Received Aug 2, 2005; revised November 25, 2005; accepted November 25, 2005.

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