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Synaptic cleft acidification and modulation of short-term depression by exocytosed protons in retinal bipolar cells.

Publication ,  Journal Article
Palmer, MJ; Hull, C; Vigh, J; von Gersdorff, H
Published in: J Neurosci
December 10, 2003

The release of vesicular protons during exocytosis causes a feedback inhibition of Ca2+ channels in photoreceptor terminals; however, the effect of this inhibition on subsequent exocytosis has not been studied. Here we show that a similar L-type Ca2+ channel inhibition occurs in bipolar cell terminals in slices of goldfish retina, and we investigate the effect that this has on subsequent exocytosis with membrane capacitance measurements. We find that transient Ca2+ current inhibition is correlated with exocytosis and modulated by the concentration of extracellular pH buffer. Ca2+ current inhibition is negligible in acutely dissociated terminals, demonstrating the importance of an intact synaptic cleft. The sensitivity of bipolar cell Ca2+ currents to extracellular pH was assessed: channel conductance is reduced and activation is shifted to more positive potentials by acidification. The effect of Ca2+ current inhibition on subsequent exocytosis was investigated by measuring paired-pulse depression. Under conditions in which there is a large amount of inhibition of Ca2+ influx, the degree of paired-pulse depression is significantly reduced. Finally, we show that under physiological (bicarbonate) buffering conditions, pronounced Ca2+ current inhibition occurs after exocytosis ( approximately 60% peak inhibition), which can decrease subsequent exocytosis during single depolarizations. We estimate that exocytosis is accompanied by a transient change in synaptic cleft pH from 7.5 to approximately 6.9. We suggest that this effect serves as an activity-dependent modulator of exocytosis at ribbon-type synapses where a large and compact coterie of vesicles can fuse at each active zone.

Duke Scholars

Published In

J Neurosci

DOI

EISSN

1529-2401

Publication Date

December 10, 2003

Volume

23

Issue

36

Start / End Page

11332 / 11341

Location

United States

Related Subject Headings

  • Retina
  • Protons
  • Presynaptic Terminals
  • Patch-Clamp Techniques
  • Neurons
  • Neurology & Neurosurgery
  • Neural Inhibition
  • Kinetics
  • Hydrogen-Ion Concentration
  • HEPES
 

Citation

APA
Chicago
ICMJE
MLA
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Palmer, M. J., Hull, C., Vigh, J., & von Gersdorff, H. (2003). Synaptic cleft acidification and modulation of short-term depression by exocytosed protons in retinal bipolar cells. J Neurosci, 23(36), 11332–11341. https://doi.org/10.1523/JNEUROSCI.23-36-11332.2003
Palmer, Mary J., Court Hull, Jozsef Vigh, and Henrique von Gersdorff. “Synaptic cleft acidification and modulation of short-term depression by exocytosed protons in retinal bipolar cells.J Neurosci 23, no. 36 (December 10, 2003): 11332–41. https://doi.org/10.1523/JNEUROSCI.23-36-11332.2003.
Palmer MJ, Hull C, Vigh J, von Gersdorff H. Synaptic cleft acidification and modulation of short-term depression by exocytosed protons in retinal bipolar cells. J Neurosci. 2003 Dec 10;23(36):11332–41.
Palmer, Mary J., et al. “Synaptic cleft acidification and modulation of short-term depression by exocytosed protons in retinal bipolar cells.J Neurosci, vol. 23, no. 36, Dec. 2003, pp. 11332–41. Pubmed, doi:10.1523/JNEUROSCI.23-36-11332.2003.
Palmer MJ, Hull C, Vigh J, von Gersdorff H. Synaptic cleft acidification and modulation of short-term depression by exocytosed protons in retinal bipolar cells. J Neurosci. 2003 Dec 10;23(36):11332–11341.

Published In

J Neurosci

DOI

EISSN

1529-2401

Publication Date

December 10, 2003

Volume

23

Issue

36

Start / End Page

11332 / 11341

Location

United States

Related Subject Headings

  • Retina
  • Protons
  • Presynaptic Terminals
  • Patch-Clamp Techniques
  • Neurons
  • Neurology & Neurosurgery
  • Neural Inhibition
  • Kinetics
  • Hydrogen-Ion Concentration
  • HEPES