Neuron
Volume 6, Issue 3, March 1991, Pages 333-344
Journal home page for Neuron

Article
Control of postsynaptic Ca2+ influx in developing neocortex by excitatory and inhibitory neurotransmitters

https://doi.org/10.1016/0896-6273(91)90243-SGet rights and content

Abstract

We assessed the pathways by which excitatory and inhibitory neurotransmitters elicit postsynaptic changes in [Ca2+iin brain slices of developing rat and cat neocortex, using fura 2. Glutamate, NMDA, and quisqualate transiently elevated [Ca2+]i in all neurons. While the quisqualate response relied exclusively on voltage-gated Ca2+ channels, almost all of the NMDA-induced Ca2+ influx was via the NMDA ionophore itself, rather than through voltage-gated Ca2+ channels. Glutamate itself altered [Ca2+]i almost exclusively via the NMDA receptor. Furthermore, synaptically induced Ca2+ entry relied almost completely on NMDA receptor activation, even with low-frequency stimulation. The inhibitory neurotransmitter GABA also increased [Ca2+]i, probably via voltage-sensitive Ca2+ channels, whereas the neuromodulator acetylcholine caused Ca2+ release from intracellular stores via a muscarinic receptor. Low concentrations of these agonists produced nonperiodic [Ca2+]i oscillations, which were temporally correlated in neighboring cells. Optical recording with Ca2+-sensitive indicators may thus permit the visualization of functional networks in developing cortical circuits.

References (58)

  • H.E. Scharfman et al.

    Responses to gammaaminobutyric acid applied to cell bodies and dendrites of rat visual cortical neurons

    Brain Res.

    (1985)
  • R.W. Tsien et al.

    Multiple types of neuronal calcium channels and their selective modulation

    Trends Neurosci.

    (1988)
  • M. Armstrong-James

    The functional status and columnar organization of single cells responding to cutaneous stimulation in neonatal rat somatosensory cortex S1

    J. Physiol.

    (1975)
  • M. Armstrong-James et al.

    Quantitative studies of postnatal changes in synapses in rat superficial motor cortex

    Z. Zellforsch. Mikrosk. Anat.

    (1970)
  • A. Artola et al.

    Long-term potentiation and NMDA receptors in rat visual cortex.

    Nature

    (1987)
  • M.F. Bear et al.

    Modulation of visual cortical plasticity by acetylcholine and noradrenaline

    Nature

    (1986)
  • M.F. Bear et al.

    Disruption of experience-dependent synaptic modifications in striate cortex by infusion of an NMDA receptor antagonist

    J. Neurosci.

    (1990)
  • Y. Ben-Ari et al.

    Giant synaptic potentials in immature rat CA3 hippocampul neurones

    J. Physiol.

    (1989)
  • M.J. Berridge et al.

    Inositol phosphates and cell signalling

    Nature

    (1989)
  • T.V.P. Bliss et al.

    Long-lasting potentiation of synaptic transmission in the dentate area of the unanesthetized rabbit following stimulation of the perforant path

    J. Physiol.

    (1973)
  • J. Bolz et al.

    Generation of end-inhibition in the visual cortex via interlaminar connections

    Nature

    (1986)
  • H.T. Cline et al.

    N-methyl-D-aspartate receptor antagonist desegregates eyespecific stripes

  • G.L. Collingridge et al.

    Excitatory amino acids in synaptic transmission in the Schaffer collateralcommissural pathway of the rat hippocampus

    J. Physiol.

    (1983)
  • J.A. Connor et al.

    Depolarization-and transmitter-induced changes in intracellular Cal' of rat cerebellar granule cells in explant cultures

    J. Neurosci.

    (1987)
  • A.H. Cornell-Bell et al.

    Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling

    Science

    (1990)
  • D.A. Coulter et al.

    Characterization of ethosuximide reduction of low-threshold calcium current in thalamic neurons

    Ann. Neurol

    (1989)
  • K. Fox et al.

    The location and function of NMDA receptors in cat and kitten visual cortex

    J. Neurosci.

    (1989)
  • A. Grinvald et al.

    Optical imaging of neuronal activity

    Physiol. Rev.

    (1988)
  • P. Hess et al.

    Different modes of Ca2+ channel gating behavior favoured by dihydropyridine Cat' agonists and antagonists

    Nature

    (1984)
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    Present address: Department of Neurobiology, Box 3209, Duke University Medical Center, Durham, North Carolina 27710.

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