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The Journal of Neuroscience, May 17, 2006, 26(20):5511-5523; doi:10.1523/JNEUROSCI.5525-05.2006
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Cellular/Molecular
Synaptogenesis of the Calyx of Held: Rapid Onset of Function and One-to-One Morphological Innervation
Brian K. Hoffpauir, Janelle L. Grimes, Peter H. Mathers, andGeorge A. Spirou Sensory Neuroscience Research Center, Department of Otolaryngology, West Virginia University School of Medicine, Morgantown, West Virginia 26506-9303
Correspondence should be addressed to Dr. George A. Spirou, Sensory Neuroscience Research Center, West Virginia University School of Medicine, P.O. Box 9303 Health Sciences Center, One Medical Center Drive, Morgantown, WV 26506-9303. Email: gspirou{at}hsc.wvu.edu
Synaptogenesis during early development is thought to follow a canonical program whereby synapses increase rapidly in number and individual axons multiply-innervate nearby targets. Typically, a subset of inputs then out-competes all others through experience-driven processes to establish stable, long-lasting contacts. We investigated the formation of the calyx of Held, probably the largest nerve terminal in the mammalian CNS. Many basic functional and morphological features of calyx growth have not been studied previously, including whether mono-innervation, a hallmark of this system in adult animals, is established early in development. Evoked postsynaptic currents, recorded from neonatal mice between postnatal day 1 (P1) and P4, increased dramatically from –0.14 ± 0.04 nA at P1 to –6.71 ± 0.65 nA at P4 with sharp jumps between P2 and P4. These are the first functional assays of these nascent synapses for ages less than P3. AMPA and NMDA receptor-mediated currents were prominent across this age range. Electron microscopy (EM) revealed a concomitant increase, beginning at P2, in the prevalence of postsynaptic densities (16-fold) and adhering contacts (73-fold) by P4. Therefore, both functional and structural data showed that young calyces could form within 2 d, well before the onset of hearing around P8. Convergence of developing calyces onto postsynaptic targets, indicative of competitive processes that precede mono-innervation, was rare (4 of 29) at P4 as assessed using minimal stimulation electrophysiology protocols. Serial EM sectioning through 19 P4 cells further established the paucity (2 of 19) of convergence. These data indicate that calyces of Held follow a noncanonical program to establish targeted innervation that occurs over a rapid time course and precedes auditory experience.
Key words: development; NMDA; AMPA; topography; electron microscopy; 3-D reconstruction
Received Dec. 23, 2005; revised April 11, 2006; accepted April 11, 2006.
Correspondence should be addressed to Dr. George A. Spirou, Sensory Neuroscience Research Center, West Virginia University School of Medicine, P.O. Box 9303 Health Sciences Center, One Medical Center Drive, Morgantown, WV 26506-9303. Email: gspirou{at}hsc.wvu.edu
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