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The Journal of Neuroscience, February 14, 2007, 27(7):1725-1737; doi:10.1523/JNEUROSCI.4116-06.2007

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Cellular/Molecular
The Role of Physiological Afferent Nerve Activity during In Vivo Maturation of the Calyx of Held Synapse

Emilio Erazo-Fischer,¹ Jörg Striessnig,² and Holger Taschenberger¹

¹Max Planck Institute for Biophysical Chemistry, D-37077 Göttingen, Germany, and ²Pharmacology and Toxicology, Institute of Pharmacy, University of Innsbruck, A-6020 Innsbruck, Austria

Correspondence should be addressed to Holger Taschenberger, Max Planck Institute for Biophysical Chemistry, Am Fassberg 11, D-37077 Göttingen, Germany. Email: Holger.Taschenberger{at}mpi-bpc.mpg.de

We studied how afferent nerve activity affects the in vivo maturation of a fast glutamatergic CNS synapse, the calyx of Held. To address this question, we exploited the distinct presynaptic Ca²⁺ channel subtypes governing transmitter release at the cochlear inner hair cell (IHC)–spiral neuron synaptic junction compared with those at higher synapses along the auditory pathways. We characterized the functional properties of calyx synapses in wild type (wt) compared with those developing in Ca_V1.3 subunit-deficient (Ca_V1.3^–/–) mice. Ca_V1.3^–/– mice are deaf because of an absence of glutamate release from IHC, which results in a complete lack of cochlea-driven nerve activity. Presynaptic Ca²⁺ channel properties, Ca²⁺ dependence of exocytosis, number of readily releasable quanta, and AMPA mEPSCs were unchanged in postnatal day 14 (P14) to P17 calyx synapses of Ca_V1.3^–/– mice. However, synaptic strength was augmented because presynaptic action potentials were broader, leading to increased quantal release, consistent with lower paired-pulse ratios and stronger depression during repetitive synaptic stimulation. Furthermore, asynchronous release after trains was elevated presumably because of higher residual Ca²⁺ accumulating in the presynaptic terminals. Finally, we measured larger NMDA EPSCs with higher sensitivity to the NR2B subunit-specific antagonist ifenprodil in P14–P17 synapses of Ca_V1.3^–/– compared with wt mice. These results suggest that auditory activity is required for the adjustment of synaptic strength as well as for the downregulation of synaptic NMDA receptors during postnatal development of the calyx of Held. In contrast, properties of the presynaptic release machinery and postsynaptic AMPA receptors are unaffected by chronic changes in the level of afferent activity at this synapse.

Key words: development; EPSC; MNTB; calyx of Held; maturation; synaptic plasticity

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Received Sept. 20, 2006; revised Dec. 14, 2006; accepted Dec. 15, 2006.

Correspondence should be addressed to Holger Taschenberger, Max Planck Institute for Biophysical Chemistry, Am Fassberg 11, D-37077 Göttingen, Germany. Email: Holger.Taschenberger{at}mpi-bpc.mpg.de

This article has been cited by other articles:

				M. Sonntag, B. Englitz, C. Kopp-Scheinpflug, and R. Rubsamen Early Postnatal Development of Spontaneous and Acoustically Evoked Discharge Activity of Principal Cells of the Medial Nucleus of the Trapezoid Body: An In Vivo Study in Mice J. Neurosci., July 29, 2009; 29(30): 9510 - 9520. [Abstract] [Full Text] [PDF]

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