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Articles, 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 and George A. Spirou
Journal of Neuroscience 17 May 2006, 26 (20) 5511-5523; DOI: https://doi.org/10.1523/JNEUROSCI.5525-05.2006
Brian K. Hoffpauir
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Janelle L. Grimes
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Peter H. Mathers
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George A. Spirou
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Abstract

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.

  • development
  • NMDA
  • AMPA
  • topography
  • electron microscopy
  • 3-D reconstruction
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The Journal of Neuroscience: 26 (20)
Journal of Neuroscience
Vol. 26, Issue 20
17 May 2006
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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, George A. Spirou
Journal of Neuroscience 17 May 2006, 26 (20) 5511-5523; DOI: 10.1523/JNEUROSCI.5525-05.2006

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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, George A. Spirou
Journal of Neuroscience 17 May 2006, 26 (20) 5511-5523; DOI: 10.1523/JNEUROSCI.5525-05.2006
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