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Phylogenetic, ontogenetic and adult adaptive plasticity of rhythmic neural networks: a common neuromodulatory mechanism?

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Abstract

Neuromodulatory inputs are known to play a major role in the adaptive plasticity of rhythmic neural networks in adult animals. Using the crustacean stomatogastric nervous system, we have investigated the role of modulatory inputs in the development of rhythmic neural networks. We found that the same neuronal population is organised into a single network in the embryo, as opposed to the two networks present in the adult. However, these adult networks pre-exist in the embryo and can be unmasked by specific alterations of the neuromodulatory environment. Similarly, adult networks may switch back to the embryonic phenotype by manipulating neuromodulatory inputs. During development, we found that the early established neuromodulatory population display alteration in expressed neurotransmitter phenotypes, and that although the population of modulatory neurones is established early, with morphology and projection pattern similar to adult ones, their neurotransmitter phenotype may appear gradually. Therefore the abrupt switch from embryonic to adult network expression occurring at metamorphosis may be due to network reconfiguration in response to changes in modulatory input, as found in adult adaptive plasticity. Strikingly, related crustacean species express different motor outputs using the same basic network circuitry, due to species-specific alteration in neuromodulatory substances within homologous projecting neurones. Therefore we propose that alterations within neuromodulatory systems to a given rhythmic neural network displaying the same basic circuitry may account for the generation of different motor outputs throughout development (ontogenetic plasticity), adulthood (adaptive plasticity) and evolution (phylogenetic plasticity).

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Fig. 1a–d
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Fig. 5a–d
Fig. 6a, b
Fig. 7

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Abbreviations

CoG:

Commissural ganglion

OG:

Oesophageal ganglion

STG:

Stomatogastric ganglion

STNS:

Stomatogastric nervous system

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Acknowledgements

We deeply thank Dr. Andrew Hill for carefull reading of an earlier version of the manuscript.

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  1. CNRS UMR 5816, University of Bordeaux I, Avenue des Facultés, 33405, Talence, France

    V. S. Fénelon, Y. Le Feuvre & P. Meyrand

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  1. V. S. Fénelon
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  3. P. Meyrand
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Correspondence to V. S. Fénelon.

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Fénelon, V.S., Le Feuvre, Y. & Meyrand, P. Phylogenetic, ontogenetic and adult adaptive plasticity of rhythmic neural networks: a common neuromodulatory mechanism?. J Comp Physiol A 190, 691–705 (2004). https://doi.org/10.1007/s00359-004-0533-4

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