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Coordination of rhythm-generating units via NO and extrasynaptic neurotransmitter release

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Abstract

The buccal ganglia of the mollusc, Lymnaea stagnalis, contain two distinct but interacting rhythm-generating units: the central pattern generator for the buccal rhythm and nitrergic B2 neurons controlling gut motility. Nitric oxide (NO) has previously been demonstrated to be involved in the activation of the buccal rhythm. Here, we found that NO-generating substances (SNP and SNAP) activated the buccal rhythm while slowing the endogenous rhythm of B2 bursters. The inhibitor of NO-synthase, L-NNA, the NO scavenger PTIO, or the inhibitor of soluble guanylyl cyclase, ODQ, each produced opposite, depolarising effects on the B2 neuron. In isolated B2 cells, only depolarising effects of substances interfering with NO production or function (PTIO, L-NNA and ODQ) were detected, whereas the NO donors had no hyperpolarising effects. However, when an isolated B2 cell was placed close to its initial position in the ganglion, hyperpolarising effects could be obtained with NO donors. This indicates that extrasynaptic release of some unidentified factor(s) mediates the hyperpolarising effects of NO donors on the B2 bursters. The results suggest that NO is involved in coordination between the radula and foregut movements and that the effects of NO are partially mediated by the volume chemical neurotransmission of as yet unknown origin.

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Abbreviations

L-NNA:

N-Nitro-l-arginine

ODQ:

1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one

PTIO:

2-Phenyl-4,4,5,5-tetramethylimidazonine-l-oxyl-3-oxide

SNAP:

s-Nitroso-N-acetylpenicillamine

SNP:

Sodium nitroprusside

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Acknowledgments

We thank Prof. D.A. Sakharov, Prof. I.S. Zakharov and our colleagues from the Laboratory of Comparative Physiology for helpful comments on this work. It is supported by the grant RFBR 08-04-00120.

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Authors and Affiliations

  1. Laboratory of Comparative Physiology, Institute of Developmental Biology of the Russian Academy of Sciences, Vavilov Str. 26, Moscow, 119991, Russia

    Varvara E. Dyakonova & Taisia L. Dyakonova

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  1. Varvara E. Dyakonova
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  2. Taisia L. Dyakonova
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Correspondence to Varvara E. Dyakonova.

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Dyakonova, V.E., Dyakonova, T.L. Coordination of rhythm-generating units via NO and extrasynaptic neurotransmitter release. J Comp Physiol A 196, 529–541 (2010). https://doi.org/10.1007/s00359-010-0541-5

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