AMPA/kainate and NMDA-like glutamate receptors at the chromatophore neuromuscular junction of the squid: role in synaptic transmission and skin patterning

Eur J Neurosci. 2003 Feb;17(3):507-16. doi: 10.1046/j.1460-9568.2003.02477.x.

Abstract

Glutamate receptor types were examined at the chromatophore synapses of the squids Alloteuthis subulata and Loligo vulgaris, where nerve-induced muscle contraction causes chromatophore expansion. Immunoblotting with antibody raised against a squid AMPA receptor (sGluR) demonstrated that AMPA/kainate receptors are present in squid skin. Application of l-glutamate evoked chromatophore muscle contractions in both ventral and dorsal skins, while NMDA was only active on a subpopulation of dorsal chromatophores. In dorsal skin, neurotransmission was partly blocked by either AMPA/kainate receptor antagonists (CNQX and DNQX) or NMDA receptor antagonists (AP-5 and MK-801) or completely blocked by simultaneous application of both classes of antagonists. In isolated muscle fibres, ionophoretic application of l-glutamate evoked fast inward CNQX- and DNQX-sensitive currents with reversal potentials around +14 mV and a high conductance to Na+. In fibres from dorsal skin only, a slower outward glutamate-sensitive current appeared at positive holding potentials. At negative potentials, currents were potentiated by glycine or by removing external Mg2+ and were blocked by AP-5 and MK-801. Glutamate caused a fast, followed by a slow, transient increase in cytoplasmic Ca2+. The slow component was increased in amplitude and duration by glycine or by lowering external Mg2+ and decreased by AP-5 and MK-801. In cells from ventral skin, no 'NMDA-like responses' were detected. Thus, while AMPA/kainate receptors mediated fast excitatory synaptic transmission and rapid colour change over the whole skin, activation of both AMPA/kainate and NMDA-like receptors in a subpopulation of dorsal chromatophores prolonged the postsynaptically evoked Ca2+ elevation causing temporally extended colour displays with behavioural significance.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Calcium / metabolism
  • Chromatophores / metabolism*
  • Decapodiformes / physiology*
  • Electric Stimulation
  • Electrophoresis, Polyacrylamide Gel
  • Excitatory Postsynaptic Potentials / physiology
  • Fluorescent Dyes
  • Fura-2
  • Glutamic Acid / metabolism
  • Immunoblotting
  • Immunohistochemistry
  • In Vitro Techniques
  • Ion Channels / physiology
  • Iontophoresis
  • Muscle Contraction / physiology
  • Muscle Fibers, Skeletal / physiology
  • N-Methylaspartate / metabolism
  • Neuromuscular Junction / metabolism*
  • Receptors, AMPA / metabolism*
  • Receptors, Kainic Acid / metabolism*
  • Receptors, N-Methyl-D-Aspartate / metabolism*
  • Skin Physiological Phenomena*
  • Synaptic Transmission / physiology*

Substances

  • Fluorescent Dyes
  • Ion Channels
  • Receptors, AMPA
  • Receptors, Kainic Acid
  • Receptors, N-Methyl-D-Aspartate
  • Glutamic Acid
  • N-Methylaspartate
  • Calcium
  • Fura-2