Calcium-dependent inactivation and depletion of synaptic cleft calcium ions combine to regulate rod calcium currents under physiological conditions

Katalin Rabl, Wallace B Thoreson

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41 Citations (Scopus)

Abstract

L-type Ca2+ currents (ICa) in rod photoreceptors exhibit Ca2+-dependent inactivation. Perforated-patch whole-cell recordings were obtained from isolated rods of the tiger salamander using 1.8 mM Ca2+ in the bathing medium to determine the extent of Ca2+-dependent inactivation of ICa with physiological [Ca2+] and endogenous buffering. ICa was measured with voltage ramps applied before and after 5-s steps to -40, -30, -20, or -10 mV. Long depolarizing steps in isolated rods produced inactivation of ICa ranging from 15% at -40 mV to > 80% at -10 mV. Because, in addition to Ca2+-dependent inactivation, depletion of synaptic cleft Ca2+ accompanying activation of ICa can reduce presynaptic ICa at calycal synapses, we investigated whether a similar mechanism worked at the invaginating rod synapse. Rods from retinal slices with intact synapses were compared with isolated rods in which synaptic cleft depletion is absent. ICa was more strongly depressed by depolarization of rods in retinal slices, with ICa reduced by 47% following voltage steps to -40 mV. The depression of currents by depolarization was also greater for rods from retinal slices than isolated rods when Ca2+ was replaced with Ba2+ to reduce Ca2+-dependent inactivation. The stronger depolarization-evoked inhibition of ICa in retinal slices compared to isolated rods probably reflects depletion of synaptic cleft Ca2+ arising from sustained Ca2+ influx. Inactivation of ICa exhibited slow onset and recovery. These findings suggest that Ca2+-dependent inactivation and depletion of synaptic cleft Ca2+ may combine to regulate ICa in response to light-evoked changes in rod membrane potential.

Original languageEnglish (US)
Pages (from-to)2070-2077
Number of pages8
JournalEuropean Journal of Neuroscience
Volume16
Issue number11
DOIs
StatePublished - Dec 24 2002

Fingerprint

Retinal Rod Photoreceptor Cells
Synapses
Ions
Calcium
Ambystoma
Architectural Accessibility
Patch-Clamp Techniques
Membrane Potentials
Light

Keywords

  • Ambystoma tigrinum
  • Electrophysiology
  • L-type calcium channel
  • Photoreceptor
  • Retina
  • Tiger salamander

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

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title = "Calcium-dependent inactivation and depletion of synaptic cleft calcium ions combine to regulate rod calcium currents under physiological conditions",
abstract = "L-type Ca2+ currents (ICa) in rod photoreceptors exhibit Ca2+-dependent inactivation. Perforated-patch whole-cell recordings were obtained from isolated rods of the tiger salamander using 1.8 mM Ca2+ in the bathing medium to determine the extent of Ca2+-dependent inactivation of ICa with physiological [Ca2+] and endogenous buffering. ICa was measured with voltage ramps applied before and after 5-s steps to -40, -30, -20, or -10 mV. Long depolarizing steps in isolated rods produced inactivation of ICa ranging from 15{\%} at -40 mV to > 80{\%} at -10 mV. Because, in addition to Ca2+-dependent inactivation, depletion of synaptic cleft Ca2+ accompanying activation of ICa can reduce presynaptic ICa at calycal synapses, we investigated whether a similar mechanism worked at the invaginating rod synapse. Rods from retinal slices with intact synapses were compared with isolated rods in which synaptic cleft depletion is absent. ICa was more strongly depressed by depolarization of rods in retinal slices, with ICa reduced by 47{\%} following voltage steps to -40 mV. The depression of currents by depolarization was also greater for rods from retinal slices than isolated rods when Ca2+ was replaced with Ba2+ to reduce Ca2+-dependent inactivation. The stronger depolarization-evoked inhibition of ICa in retinal slices compared to isolated rods probably reflects depletion of synaptic cleft Ca2+ arising from sustained Ca2+ influx. Inactivation of ICa exhibited slow onset and recovery. These findings suggest that Ca2+-dependent inactivation and depletion of synaptic cleft Ca2+ may combine to regulate ICa in response to light-evoked changes in rod membrane potential.",
keywords = "Ambystoma tigrinum, Electrophysiology, L-type calcium channel, Photoreceptor, Retina, Tiger salamander",
author = "Katalin Rabl and Thoreson, {Wallace B}",
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TY - JOUR

T1 - Calcium-dependent inactivation and depletion of synaptic cleft calcium ions combine to regulate rod calcium currents under physiological conditions

AU - Rabl, Katalin

AU - Thoreson, Wallace B

PY - 2002/12/24

Y1 - 2002/12/24

N2 - L-type Ca2+ currents (ICa) in rod photoreceptors exhibit Ca2+-dependent inactivation. Perforated-patch whole-cell recordings were obtained from isolated rods of the tiger salamander using 1.8 mM Ca2+ in the bathing medium to determine the extent of Ca2+-dependent inactivation of ICa with physiological [Ca2+] and endogenous buffering. ICa was measured with voltage ramps applied before and after 5-s steps to -40, -30, -20, or -10 mV. Long depolarizing steps in isolated rods produced inactivation of ICa ranging from 15% at -40 mV to > 80% at -10 mV. Because, in addition to Ca2+-dependent inactivation, depletion of synaptic cleft Ca2+ accompanying activation of ICa can reduce presynaptic ICa at calycal synapses, we investigated whether a similar mechanism worked at the invaginating rod synapse. Rods from retinal slices with intact synapses were compared with isolated rods in which synaptic cleft depletion is absent. ICa was more strongly depressed by depolarization of rods in retinal slices, with ICa reduced by 47% following voltage steps to -40 mV. The depression of currents by depolarization was also greater for rods from retinal slices than isolated rods when Ca2+ was replaced with Ba2+ to reduce Ca2+-dependent inactivation. The stronger depolarization-evoked inhibition of ICa in retinal slices compared to isolated rods probably reflects depletion of synaptic cleft Ca2+ arising from sustained Ca2+ influx. Inactivation of ICa exhibited slow onset and recovery. These findings suggest that Ca2+-dependent inactivation and depletion of synaptic cleft Ca2+ may combine to regulate ICa in response to light-evoked changes in rod membrane potential.

AB - L-type Ca2+ currents (ICa) in rod photoreceptors exhibit Ca2+-dependent inactivation. Perforated-patch whole-cell recordings were obtained from isolated rods of the tiger salamander using 1.8 mM Ca2+ in the bathing medium to determine the extent of Ca2+-dependent inactivation of ICa with physiological [Ca2+] and endogenous buffering. ICa was measured with voltage ramps applied before and after 5-s steps to -40, -30, -20, or -10 mV. Long depolarizing steps in isolated rods produced inactivation of ICa ranging from 15% at -40 mV to > 80% at -10 mV. Because, in addition to Ca2+-dependent inactivation, depletion of synaptic cleft Ca2+ accompanying activation of ICa can reduce presynaptic ICa at calycal synapses, we investigated whether a similar mechanism worked at the invaginating rod synapse. Rods from retinal slices with intact synapses were compared with isolated rods in which synaptic cleft depletion is absent. ICa was more strongly depressed by depolarization of rods in retinal slices, with ICa reduced by 47% following voltage steps to -40 mV. The depression of currents by depolarization was also greater for rods from retinal slices than isolated rods when Ca2+ was replaced with Ba2+ to reduce Ca2+-dependent inactivation. The stronger depolarization-evoked inhibition of ICa in retinal slices compared to isolated rods probably reflects depletion of synaptic cleft Ca2+ arising from sustained Ca2+ influx. Inactivation of ICa exhibited slow onset and recovery. These findings suggest that Ca2+-dependent inactivation and depletion of synaptic cleft Ca2+ may combine to regulate ICa in response to light-evoked changes in rod membrane potential.

KW - Ambystoma tigrinum

KW - Electrophysiology

KW - L-type calcium channel

KW - Photoreceptor

KW - Retina

KW - Tiger salamander

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U2 - 10.1046/j.1460-9568.2002.02277.x

DO - 10.1046/j.1460-9568.2002.02277.x

M3 - Article

VL - 16

SP - 2070

EP - 2077

JO - European Journal of Neuroscience

JF - European Journal of Neuroscience

SN - 0953-816X

IS - 11

ER -