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The Journal of Neuroscience, January 12, 2005, 25(2):417-429; doi:10.1523/JNEUROSCI.3725-04.2005

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Development/Plasticity/Repair
Regulation of Gephyrin Cluster Size and Inhibitory Synaptic Currents on Renshaw Cells by Motor Axon Excitatory Inputs

David Gonzalez-Forero,^1,2 Angel M. Pastor,² Eric J. Geiman,¹ Beatriz Benítez-Temiño,² and Francisco J. Alvarez¹

¹Department of Anatomy and Physiology, Wright State University, Dayton, Ohio 45435, and ²Departamento de Fisiología y Zoología, Facultad de Biología, Universidad de Sevilla, 41012-Sevilla, Spain

Renshaw cells receive a high density of inhibitory synapses characterized by large postsynaptic gephyrin clusters and mixed glycinergic/GABAergic inhibitory currents with large peak amplitudes and long decays. These properties appear adapted to increase inhibitory efficacy over Renshaw cells and mature postnatally by mechanisms that are unknown. We tested the hypothesis that heterosynaptic influences from excitatory motor axon inputs modulate the development of inhibitory synapses on Renshaw cells. Thus, tetanus (TeNT) and botulinum neurotoxin A (BoNT-A) were injected intramuscularly at postnatal day 5 (P5) to, respectively, elevate or reduce motor axon firing activity for 2 weeks. After TeNT injections, the average gephyrin cluster areas on Renshaw cells increased by 18.4% at P15 and 28.4% at P20 and decreased after BoNT-A injections by 17.7% at P15 and 19.9% at P20. The average size differences resulted from changes in the proportions of small and large gephyrin clusters. Whole-cell recordings in P9-P15 Renshaw cells after P5 TeNT injections showed increases in the peak amplitude of glycinergic miniature postsynaptic currents (mPSCs) and the fast component of mixed (glycinergic/GABAergic) mPSCs compared with controls (60.9% and 78.9%, respectively). GABAergic mPSCs increased in peak amplitude to a smaller extent (45.8%). However, because of the comparatively longer decays of synaptic GABAergic currents, total current transfer changes after TeNT were similar for synaptic glycine and GABA_A receptors (56 vs 48.9% increases, respectively). We concluded that motor axon excitatory synaptic activity modulates the development of inhibitory synapse properties on Renshaw cells, influencing recruitment of postsynaptic gephyrin and glycine receptors and, to lesser extent, GABA_A receptors.

Key words: motoneurons; development; spinal cord; botulinum toxin; tetanus toxin; GABA_A receptor; glycine receptor; recurrent inhibition

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Received July 21, 2003; revised November 19, 2004; accepted November 20, 2004.

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