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IP3-mediated octopamine-induced synaptic enhancement of crayfish LG neurons

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Abstract

The biogenic amines, octopamine and serotonin, modulate the synaptic activity of the lateral giant interneuron (LG) circuitry of the crayfish escape behavior. Bath application of both octopamine and serotonin enhances the synaptic responses of LG to sensory stimulation. We have shown previously (Araki et al. J Neurophysiol 94:2644–2652, 2005) that a serotonin-induced enhancement of the LG response was mediated by an increase in cAMP levels following activation of adenylate cyclase; however, octopamine acts independently. Here, we clarify how octopamine enhances the LG response during sensory stimulation using physiological and pharmacological analyses. When phospholipase C inhibitor U-73122 was directly injected into the LG before biogenic amine application, it abolished the enhancing effect of octopamine on direct sensory input to the LG, but did not block indirect input via sensory interneurons or the effect of serotonin. Direct injection of IP3, and its analogue adenophostin A, into the LG increased the synaptic response of the LG to sensory stimulation. Thus, IP3 mediates octopamine-induced synaptic enhancement of the LG, but serotonin acts independently. These results indicate that both octopamine and serotonin enhance the synaptic responses of the LG to sensory stimulation, but that they activate two different signaling cascades in the LG.

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Abbreviations

5-HT:

Serotonin

CaMK:

Ca++/calmodulin-dependent protein kinase

DMSO:

Dimethylsulphoxide

EPSP:

Excitatory postsynaptic potential

IP3 :

Inositol 1,4,5-trisphosphate

LG:

Lateral giant interneuron

OA:

Octopamine

PKA:

Protein kinase A

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Acknowledgments

This work was supported by Grants-in-Aid from the Ministry of Education, Science, Sport, and Culture to T.N. All experiments were carried out in accordance with the Guide for the care and use of Laboratory animals of Yamagata University (Japan).

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Authors and Affiliations

  1. Division of Biological Sciences, Graduate School of Science, Hokkaido University, Sapporo, 060-0810, Japan

    Makoto Araki

  2. Department of Biology, Faculty of Science, Yamagata University, Yamagata, 990-8560, Japan

    Toshiki Nagayama

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  1. Makoto Araki
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  2. Toshiki Nagayama
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Correspondence to Toshiki Nagayama.

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Araki, M., Nagayama, T. IP3-mediated octopamine-induced synaptic enhancement of crayfish LG neurons. J Comp Physiol A 198, 607–615 (2012). https://doi.org/10.1007/s00359-012-0733-2

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  • DOI: https://doi.org/10.1007/s00359-012-0733-2

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