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.
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Fénelon,V. S., Casasnovas,B., Simmers,J. & Meyrand,P. Development of rhythmic pattern generators. Curr. Opin. Neurobiol. 8, 705–709 (1998).
Sillar,K. T. Synaptic specificity: development of locomotor rhythmicity. Curr. Opin. Neurobiol. 4, 101–107 (1994).
Spitzer,N. C. Development of voltage-dependent and ligand-gated channels in excitable membranes. Prog. Brain Res. 102, 169–179 (1994).
Levine,R. B., Morton,D. B. & Restifo,L. L. Remodeling of the insect nervous system. Curr. Opin. Neurobiol. 5, 28–35 (1995).
Fénelon,V. S., Casasnovas,B., Faumont,S. & Meyrand,P. Ontogenetic alteration in peptidergic expression within a stable neuronal population in lobster stomatogastric nervous system. J. Comp. Neurol. 399, 289–305 (1998).
Casasnovas,B. & Meyrand,P. Functional differentiation of adult neural circuits from a single embryonic network. J. Neurosci. 15, 5703–5718 (1995).
Moulins,M. & Cournil,I. All-or-none control of the bursting properties of the pacemaker neurons of the lobster pyloric pattern generator. J. Neurobiol. 5, 447–458 (1982).
Selverston,A. I. & Moulins,M. The Crustacean Stomatogastric System (Springer, Berlin, 1987).
Harris-Warrick,R. M., Marder,E., Selverston,A. I. & Moulins,M. Dynamic Biological Networks. The Stomatogastric Nervous System (MIT Press, Cambridge, Massachusetts, 1992).
Meyrand,P., Simmers,J. & Moulins,M. Construction of a pattern-generating circuit with neurons of different networks. Nature 351, 60–63 (1991).
Faumont,S., Simmers,J. & Meyrand,P. Activation of a lobster motor rhythm-generating network by disinhibition of permissive modulatory inputs. J. Neurophysiol. 80, 2776–2780 (1998).
Masabuau,J.-C. & Meyrand,P. Modulation of a neural network by physiological levels of oxygen in lobster stomatogastric ganglion. J. Neurosci. 16, 3950–3959 (1996).
Robertson,R. M. & Moulins,M. Oscillatory command input to the motor pattern generators of the crustacean stomatogastric ganglion. II. The gastric rhythm. J. Comp. Physiol. A 154, 473–491 (1984).
Kilman,V. et al. Sequential developmental acquisition of cotransmitters in identified neurons of the stomatogastric nervous system of the lobsters, Homarus americanus and Homorus gammarus. J. Comp. Neurol. 408, 318–334 (1999).
Fénelon,V. S., Kilman,V., Myrand,P. & Marder,E. Sequential developmental acquisition of neuromodulatory inputs to a central pattern generating network. J. Comp. Neurol. 408, 335–351 (1999).
Hooper,S. L. & Marder,E. Modulation of a central pattern generator by two neuropeptides, proctolin and FMRFamide. Brain Res. 305, 186–191 (1984).
Flamm,R. E. & Harris-Warrick,R. M. Aminergic modulation in lobster stomatogastric ganglion. I. Effects on motor pattern and activity of neurons within the pyloric circuit. J. Neurophysiol. 55, 847–865 (1986).
Turrigiano,G. G. & Selverston,A. I. Cholecystokinin-like peptide is a modulator of a crustacean central pattern generator. J. Neurosci. 9, 2486–2501 (1989).
Elson,R. C. & Selverston,A. I. Mechanisms of gastric rhythm generation in the isolated stomatogastric ganglion of spiny lobsters: bursting pacemaker potentials, synaptic interactions, and muscarinic modulation. J. Neurophysiol. 68, 890–907 (1992).
Bal,T., Nagy,F. & Moulins,M. Muscarinic modulation of a pattern-generating network: control of neuronal properties. J. Neurosci. 14, 3019–3035 (1994).
Clemens,S., Massabuau,J.-C., Legeay,A., Meyrand,P. & Simmers,J. In vivo modulation of interacting central pattern generators in lobster stomatogastric ganglion: Influence of feeding and partial pressure of oxygen. J. Neurosci. 18, 2788–2799 (1998).
Bolshakov,V. Y. & Siegelbaum,S. A. Regulation of hippocampal release during development and long-term potentiation. Science 269, 1730–1734 (1995).
McCormick,D. A., Trent,F. & Ramoa,A. S. Postnatal development of synchronized network oscillations in the ferret dorsal lateral geniculate and perigeniculate nuclei. J. Neurosci. 15, 5739–5752 (1995).
Durand,G. M., Kovalchuk,Y. & Konnerth,A. Long-term potentiation and functional synapse induction in developing hippocampus. Nature 381, 71–75 (1996).
Katz,L. C. & Shatz,C. J. Synaptic activity and the construction of cortical circuits. Science 274, 1133–1138 (1996).
Nick,T. A., Kaczmarek,L. K. & Carew,T. J. Ionic currents underlying developmental regulation of repetitive firing in Aplysia bag cell neurons. J. Neurosci. 16, 7583–7598 (1996).
Warren,R. A. & Jones,E. G. Maturation of neuronal form and function in a mouse thalamo-cortical circuit. J. Neurosci. 17, 277–295 (1997).
Sun,Q.-Q. & Dale,N. Developmental changes in expression of ion currents accompany maturation of locomotor pattern in frog tadpoles. J. Physiol. (Lond.) 507, 257–264 (1998).
Angulo,M. C., Staiger,J. F., Rossier,J. & Audinat,E. Developmental synaptic changes increase the range of integrative capabilities of an identified excitatory neocortical connection. J. Neurosci. 19, 1566–1576 (1999).
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.
About this article
Cite this article
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
Journal of Comparative Physiology A (2018)
Complicating connectomes: Electrical coupling creates parallel pathways and degenerate circuit mechanisms
Developmental Neurobiology (2017)
Role of Ih in differentiating the dynamics of the gastric and pyloric neurons in the stomatogastric ganglion of the lobster, Homarus americanus
Journal of Neurophysiology (2016)
Current Opinion in Neurobiology (2014)
Mass Spectral Charting of Neuropeptidomic Expression in the Stomatogastric Ganglion at Multiple Developmental Stages of the LobsterHomarus americanus
ACS Chemical Neuroscience (2012)