Auditory hair cell-afferent fiber synapses are specialized to operate at their best frequencies

Neuron. 2005 Jul 21;47(2):243-54. doi: 10.1016/j.neuron.2005.06.004.

Abstract

Auditory afferent fiber activity is driven by high-fidelity information transfer from the sensory hair cell. Presynaptic specializations, posited to maintain fidelity, are investigated at synapses with characteristic frequencies of 120 Hz and 320 Hz. Morphological data indicate that high-frequency cells have more synapses and higher vesicle density near dense bodies (DBs). Tracking vesicular release via capacitance changes identified three overlapping kinetic components of release corresponding to morphologically identified vesicle pools. High-frequency cells released faster; however, when normalized to release site number, low-frequency cells released faster, likely due to a greater Ca2+ load per synapse. The Ca(2+)-dependence of release was nonsaturating and independent of frequency, suggesting that release, not refilling, was rate limiting. A model of release derived from vesicle equilibration between morphologically defined pools reproduced the capacitance data, supporting a critical role in vesicle trafficking for DBs. The model suggests that presynaptic specializations enable synapses to operate most efficiently at their characteristic frequencies.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Auditory Pathways / physiology*
  • Cadmium / pharmacology
  • Calcium / metabolism
  • Diagnostic Imaging / methods
  • Dose-Response Relationship, Radiation
  • Electric Capacitance
  • Electric Stimulation / methods
  • Hair Cells, Auditory / physiology*
  • In Vitro Techniques
  • Membrane Potentials / drug effects
  • Membrane Potentials / physiology
  • Microscopy, Electron, Transmission
  • Models, Neurological
  • Organ of Corti / cytology*
  • Organ of Corti / physiology
  • Patch-Clamp Techniques / methods
  • Presynaptic Terminals / physiology
  • Presynaptic Terminals / radiation effects
  • Synapses / classification
  • Synapses / physiology*
  • Synapses / ultrastructure
  • Synaptic Transmission / physiology*
  • Synaptic Vesicles / physiology
  • Synaptic Vesicles / ultrastructure
  • Time Factors
  • Turtles

Substances

  • Cadmium
  • Calcium