Endogenous calcium buffering at photoreceptor synaptic terminals in salamander retina

Synapse. 2014 Nov;68(11):518-28. doi: 10.1002/syn.21768. Epub 2014 Jul 30.

Abstract

Calcium operates by several mechanisms to regulate glutamate release at rod and cone synaptic terminals. In addition to serving as the exocytotic trigger, Ca2+ accelerates replenishment of vesicles in cones and triggers Ca2+-induced Ca2+ release (CICR) in rods. Ca2+ thereby amplifies sustained exocytosis, enabling photoreceptor synapses to encode constant and changing light. A complete picture of the role of Ca2+ in regulating synaptic transmission requires an understanding of the endogenous Ca2+ handling mechanisms at the synapse. We therefore used the "added buffer" approach to measure the endogenous Ca2+ binding ratio (κendo ) and extrusion rate constant (γ) in synaptic terminals of photoreceptors in retinal slices from tiger salamander. We found that κendo was similar in both cell types-∼25 and 50 in rods and cones, respectively. Using measurements of the decay time constants of Ca2+ transients, we found that γ was also similar, with values of ∼100 s(-1) and 160 s(-1) in rods and cones, respectively. The measurements of κendo differ considerably from measurements in retinal bipolar cells, another ribbon-bearing class of retinal neurons, but are comparable to similar measurements at other conventional synapses. The values of γ are slower than at other synapses, suggesting that Ca2+ ions linger longer in photoreceptor terminals, supporting sustained exocytosis, CICR, and Ca2+ -dependent ribbon replenishment. The mechanisms of endogenous Ca2+ handling in photoreceptors are thus well-suited for supporting tonic neurotransmission. Similarities between rod and cone Ca2+ handling suggest that neither buffering nor extrusion underlie differences in synaptic transmission kinetics.

Keywords: added buffer; calcium buffering; calcium extrusion; photoreceptor; retina; synapse; synaptic ribbon.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Ambystoma
  • Animals
  • Calcium Signaling*
  • Presynaptic Terminals / metabolism*
  • Retinal Cone Photoreceptor Cells / metabolism*
  • Retinal Rod Photoreceptor Cells / metabolism*