Neuron
Volume 7, Issue 6, December 1991, Pages 915-926
Journal home page for Neuron

Article
Role of residual calcium in synaptic depression and posttetanic potentiation: Fast and slow calcium signaling in nerve terminals

https://doi.org/10.1016/0896-6273(91)90337-YGet rights and content

Abstract

Trains of action potentials evoked rises in presynaptic Ca2+ concentration ([Ca2+]i) at the squid giant synapse. These increases in [Ca2+]i were spatially nonuniform during the trains, but rapidly equilibrated after the trains and slowly declined over hundreds of seconds. The trains also elicited synaptic depression and augmentation, both of which developed during stimulation and declined within a few seconds afterward. Microinjection of the Ca2+ buffer EGTA into presynaptic terminals had no effect on transmitter release or synaptic depression. However, EGTA injection effectively blocked both the persistent Ca2+ signals and augmentation. These results suggest that transmitter release is triggered by a large, brief, and sharply localized rise in [Ca2+]i, while augmentation is produced by a smaller, slower, and more diffuse rise in [Ca2+]i.

References (60)

  • D.J. Adams et al.

    Inhibitors of calcium buffering depress evoked transmitter release at the squid giant synapse

    J. Physiol.

    (1985)
  • E.M. Adler et al.

    Alien intracellular calcium chelators attenuate neurotransmitter release at the squid giant synapse

    J. Neurosci.

    (1991)
  • Z. Ahmed et al.

    Intracellular pH changes induced by calcium influx during electrical activity in molluscan neurons

    J. Gen. Physiol.

    (1980)
  • E. Alnaes et al.

    On the role of mitochondria in transmitter release from motor nerve terminals

    J. Physiol.

    (1975)
  • G.J. Augustine et al.

    Calcium dependence of presynaptic calcium cu rrent and post-synaptic response at the squid giant synapse

    J. Physiol.

    (1986)
  • G.J. Augustine et al.

    Divalent cations differentially support transmitter release at the squid giant synapse

    J. Physiol.

    (1984)
  • G.J. Augustine et al.

    Calcium requirements for secretion in bovine chromaffin cells

    J. Physiol.

    (1991)
  • G.J. Augustine et al.

    Calcium action in synaptic transmitter release

    Annu. Rev. Neurosci.

    (1987)
  • G.J. Augustine et al.

    Fingering the trigger for neurotransmitter secretion: studies on the calcium channels of squid giant presynaptic terminals

  • E.E. Barrett et al.

    The kinetics of transmitter release at the frog neuromuscular junction

    J. Physiol.

    (1972)
  • W.J. Betz

    Depression of transmitter release at the neuromuscular junction of the frog

    J. Physiol.

    (1970)
  • M.P. Charlton et al.

    Facilitation of transmitter release at squid synapses

    J. Gen. Physiol.

    (1978)
  • M.P. Charlton et al.

    Role of presynaptic calcium ions and channels in synaptic facilitation and depression at the squid giant synapse

    J. Physiol.

    (1982)
  • J.A. Connor et al.

    Calcium levels measured in a presynaptic neurone of Aplysia under conditions that modulate transmitter release

    J. Physiol.

    (1986)
  • J. del Castillo et al.

    Statistical factors involved in neuromuscular facilitation and depression

    J. Physiol.

    (1954)
  • K.R. Delaney et al.

    Calcium in motor nerve terminals associated with posttetanic potentiation

    J. Neurosci.

    (1989)
  • J. Dudel

    The effect of reduced calcium on quantal unit current and release at the crayfish neuromuscular junction

    Pfl:lugers Arch.

    (1981)
  • S.D. Erulkar et al.

    The role of calcium ions in tetanic and post tetanic increase of miniature end plate potential frequency

    J. Physiol.

    (1978)
  • M.J. Gutnick et al.

    Voltage-dependent and calcium-dependent inactivation of calcium channel current in identified snail neurones

    J. Physiol.

    (1989)
  • H. Kasai et al.

    Cytosolic Ca2+ gradients triggering unidirectional fluid secretion from exocrine pancreas

    Nature

    (1990)
  • Cited by (165)

    • Dynamic compartmentalization of calcium channel signalling in neurons

      2020, Neuropharmacology
      Citation Excerpt :

      The spatial proximity of VGCCs to the calcium sensor of SVs is the key parameter of efficient coupling between VGCC opening and SV release that was discussed in detail in excellent recent reviews (Bohme et al., 2018; Eggermann et al., 2012; Stanley, 2016; Sudhof, 2013). Due to the defined readout of synaptic activity and the knowledge of conductance properties of VGCCs, the size and extension of calcium nanodomains can be well defined by exogenous calcium buffers (Adler et al., 1991; Schneggenburger and Neher, 2000; Swandulla et al., 1991) and have been used to explore nanodomain signalling along the neuronal membrane. Other examples for tight coupling between VGCC and calcium-gated or -modulated ion channels or calcium-sensitive enzymes revealed that tight coupling between VGCCs and effector molecules reflects a common feature of fast calcium signalling (Berkefeld et al., 2006; Constantin et al., 2017).

    • The emerging use of bioluminescence in medical research

      2018, Biomedicine and Pharmacotherapy
    • Calcium Channel Modulation as an All-Purpose Mechanism for Short-Term Synaptic Plasticity

      2008, Neuron
      Citation Excerpt :

      For example, at the squid giant synapse, both facilitation and depression clearly occur in the absence of any changes in presynaptic calcium currents (Charlton et al., 1982). At this synapse, augmentation also occurs in the absence of any obvious changes in presynaptic calcium influx (Swandulla et al., 1991). Even for the case of the synapses examined by Mochida et al. (2008), some facilitation persists after both of the CaS-protein-binding sites of the calcium channel were mutated (Figure 2B of Mochida et al., 2008), and some depression is evident during repeated synaptic activity even after the calmodulin binding domain is deleted (Figure 3B).

    View all citing articles on Scopus

    Present address: Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139.

    View full text