Mechanisms, pools, and sites of spontaneous vesicle release at synapses of rod and cone photoreceptors

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Abstract

Photoreceptors have depolarized resting potentials that stimulate calcium-dependent release continuously from a large vesicle pool but neurons can also release vesicles without stimulation. We characterized the Ca2+ dependence, vesicle pools, and release sites involved in spontaneous release at photoreceptor ribbon synapses. In whole-cell recordings from light-adapted horizontal cells (HCs) of tiger salamander retina, we detected miniature excitatory post-synaptic currents (mEPSCs) when no stimulation was applied to promote exocytosis. Blocking Ca2+ influx by lowering extracellular Ca2+, by application of Cd2+ and other agents reduced the frequency of mEPSCs but did not eliminate them, indicating that mEPSCs can occur independently of Ca2+. We also measured release presynaptically from rods and cones by examining quantal glutamate transporter anion currents. Presynaptic quantal event frequency was reduced by Cd2+ or by increased intracellular Ca2+ buffering in rods, but not in cones, that were voltage clamped at −70 mV. By inhibiting the vesicle cycle with bafilomycin, we found the frequency of mEPSCs declined more rapidly than the amplitude of evoked excitatory post-synaptic currents (EPSCs) suggesting a possible separation between vesicle pools in evoked and spontaneous exocytosis. We mapped sites of Ca2+-independent release using total internal reflectance fluorescence (TIRF) microscopy to visualize fusion of individual vesicles loaded with dextran-conjugated pHrodo. Spontaneous release in rods occurred more frequently at non-ribbon sites than evoked release events. The function of Ca2+-independent spontaneous release at continuously active photoreceptor synapses remains unclear, but the low frequency of spontaneous quanta limits their impact on noise.

Original languageEnglish (US)
Pages (from-to)2015-2027
Number of pages13
JournalEuropean Journal of Neuroscience
Volume44
Issue number3
DOIs
StatePublished - Aug 1 2016

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Keywords

  • calcium
  • exocytosis
  • retina
  • ribbon synapse
  • spontaneous synaptic release
  • tiger salamander

ASJC Scopus subject areas

  • Neuroscience(all)

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