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The Journal of Neuroscience, February 23, 2005, 25(8):2010-2023; doi:10.1523/JNEUROSCI.2383-04.2005

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Development/Plasticity/Repair
Differential Postnatal Maturation of GABA_A, Glycine Receptor, and Mixed Synaptic Currents in Renshaw Cells and Ventral Spinal Interneurons

David González-Forero and Francisco J. Alvarez

Department of Anatomy and Physiology, Wright State University, Dayton, Ohio 45435

Renshaw cells (RCs) receive excitatory inputs from motoneurons to which then they inhibit. The gain of this spinal recurrent inhibitory circuit is modulated by inhibitory synapses on RCs. Inhibitory synapses on RCs mature postnatally, developing unusually large postsynaptic gephyrin clusters that colocalize glycine and GABA_A receptors. We hypothesized that these features potentiate inhibitory currents in RCs. Thus, we analyzed glycinergic and GABAergic "inhibitory" miniature postsynaptic currents (mPSCs) in neonatal [postnatal day 1 (P1) to P5] and mature (P9-P15) RCs and compared them to other ventral interneurons (non-RCs). Recorded neurons were Neurobiotin filled and identified as RCs or non-RCs using post hoc immunohistochemical criteria. Glycinergic, GABAergic, and mixed glycine/GABA mPSCs matured differently in RCs and non-RCs. In RCs, glycinergic and GABA_A mPSC peak amplitudes increased 230 and 45%, respectively, from P1-P5 to P9-P15, whereas in non-RCs, glycinergic peak amplitudes changed little and GABA_A amplitudes decreased. GABA_A mPSCs were slower in RCs (P1-P5, = 58 ms; P9-P15, = 43 ms) compared with non-RCs (P1-P5, = 27 ms; P9-P15, = 14 ms). Thus, fast glycinergic currents dominated "mixed" mPSC peak amplitudes in mature RCs, and GABA_A currents dominated their long decays. In non-RCs, GABAergic and mixed events had shorter durations, and their frequencies decreased with development. Functional maturation of inhibitory synapses on RCs correlates well with increased glycine receptor recruitment to large gephyrin patches, colocalization with 3/5-containing GABA_A receptors, and maintenance of GABA/glycine corelease. As a result, charge transfer in GABA, glycine, or mixed mPSCs was larger in mature RCs than in non-RCs, suggesting RCs receive potent inhibitory synapses.

Key words: development; subunit composition; corelease; gephyrin; GABA; synapse; motor

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Received June 16, 2004; revised January 4, 2005; accepted January 6, 2005.

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