Central inputs mask multiple adult neural networks within a single embryonic network

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Abstract

It is usually assumed that, after construction of basic network architecture in embryos1, immature networks undergo progressive maturation to acquire their adult properties2,3,4. We examine this assumption in the context of the lobster stomatogastric nervous system. In the lobster, the neuronal population5 that will form this system is at first orgnanized into a single embryonic network that generates a single rhythmic pattern6. The system then splits into different functional adult networks6 controlled by central descending systems7,8; these adult networks produce multiple motor programmes, distinctively different from the single output of the embryonic network. We show here that the single embryonic network can produce multiple adult-like programmes. This occurs after the embryonic network is silenced by removal of central inputs, then pharmacologically stimulated to restore rhythmicity. Furthermore, restoration of the flow of descending information reversed the adult-like pattern to an embryonic pattern. This indicates that the embryonic network possesses the ability to express adult-like network characteristics, but descending information prevents it from doing so. Functional adult networks may therefore not necessarily be derived from progressive ontogenetic changes in networks themselves, but may result from maturation of descending systems that unmask pre-existing adult networks in an embryonic system.

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Figure 1: Spontaneous rhythmic activity generated by the same neurons in adult and embryonic stomatogastric nervous system of H. gammarus.
Figure 2: The spontaneous rhythmic activity of the embryonic network depends on the presence of descending inputs.
Figure 3: The embryonic stomatogastric network has the potential to express multiple adult-like rhythmic motor outputs.
Figure 4: Descending inputs mask expression of multiple adult-like network activities in the embryonic STNS.

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Acknowledgements

We thank T. Bem, E. Marder, R. Miles, J. Simmers and S. Faumont for comments on an earlier version of the manuscript, and S. Faumont for providing the adult intracellular recordings shown in Fig. 1A.

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Correspondence to Pierre Meyrand.

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Le Feuvre, Y., Fénelon, V. & Meyrand, P. Central inputs mask multiple adult neural networks within a single embryonic network. Nature 402, 660–664 (1999) doi:10.1038/45238

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