Fine-tuning an auditory synapse for speed and fidelity: Developmental changes in presynaptic waveform, EPSC kinetics, and synaptic plasticity

Holger Taschenberger, Henrique Von Gersdorff

Research output: Contribution to journalArticle

352 Citations (Scopus)

Abstract

Fast, precise, and sustained synaptic transmission at high frequency is thought to be crucial for the task of sound localization in the auditory brainstem. However, recordings from the calyx of Held synapse have revealed severe frequency-dependent synaptic depression, which tends to degrade the exact timing of postsynaptic spikes. Here we investigate the functional changes occurring throughout the critical period of synapse refinement from immature calyx terminal [postnatal day 5 (P5)] to after the onset of hearing (P12-P14). Surprisingly, for recordings near physiological temperature (35°C), we find that P14 synapses are already able to follow extremely high input rates of up to 800 Hz. This ability stems in part from a remarkable shortening of presynaptic action potentials, which may lead to a lowering of release probability and decrease in synaptic delays during development. In addition, AMPA receptor-mediated EPSCs as well as quantal synaptic currents acquired progressively faster kinetics, although their mean amplitudes did not change significantly. NMDA receptor-mediated EPSCs, however, diminished with age, as indicated by a 50% reduction in mean amplitude and faster decay kinetics. Finally, the degree of synaptic depression was greatly attenuated with age, presumably because of a 2.5-fold or larger increase in the releasable pool of vesicles, which together with a decreasing release probability produces a fairly constant EPSC amplitude. This finely tuned orchestra of developmental changes thus simultaneously promotes speed while preventing premature vesicle pool depletion during prolonged bouts of firing. A few critical days in postnatal development can thus have a large impact on synaptic function.

Original languageEnglish (US)
Pages (from-to)9162-9173
Number of pages12
JournalJournal of Neuroscience
Volume20
Issue number24
StatePublished - Dec 15 2000

Fingerprint

Neuronal Plasticity
Synapses
Sound Localization
Aptitude
AMPA Receptors
N-Methyl-D-Aspartate Receptors
Synaptic Transmission
Hearing
Action Potentials
Brain Stem
Temperature

Keywords

  • AMPA and NMDA EPSCs
  • Calyx of Held
  • Development
  • MNTB
  • Neuronal reliability
  • Patch-clamp
  • Quantal and mEPSCs
  • Short-term synaptic depression

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

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title = "Fine-tuning an auditory synapse for speed and fidelity: Developmental changes in presynaptic waveform, EPSC kinetics, and synaptic plasticity",
abstract = "Fast, precise, and sustained synaptic transmission at high frequency is thought to be crucial for the task of sound localization in the auditory brainstem. However, recordings from the calyx of Held synapse have revealed severe frequency-dependent synaptic depression, which tends to degrade the exact timing of postsynaptic spikes. Here we investigate the functional changes occurring throughout the critical period of synapse refinement from immature calyx terminal [postnatal day 5 (P5)] to after the onset of hearing (P12-P14). Surprisingly, for recordings near physiological temperature (35°C), we find that P14 synapses are already able to follow extremely high input rates of up to 800 Hz. This ability stems in part from a remarkable shortening of presynaptic action potentials, which may lead to a lowering of release probability and decrease in synaptic delays during development. In addition, AMPA receptor-mediated EPSCs as well as quantal synaptic currents acquired progressively faster kinetics, although their mean amplitudes did not change significantly. NMDA receptor-mediated EPSCs, however, diminished with age, as indicated by a 50{\%} reduction in mean amplitude and faster decay kinetics. Finally, the degree of synaptic depression was greatly attenuated with age, presumably because of a 2.5-fold or larger increase in the releasable pool of vesicles, which together with a decreasing release probability produces a fairly constant EPSC amplitude. This finely tuned orchestra of developmental changes thus simultaneously promotes speed while preventing premature vesicle pool depletion during prolonged bouts of firing. A few critical days in postnatal development can thus have a large impact on synaptic function.",
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