Development of rhythmic pattern generators

Current Opinion in Neurobiology

Volumn 8, Issue 6, 1998, Pages 705-709

  Fénelon, Valérie S ^a   Casasnovas, Béatrice ^a   Simmers, John ^a   Meyrand, Pierre ^a  

^a CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ION CHANNEL;

MOTOR DEVELOPMENT; NERVE CELL NETWORK; NEUROMODULATION; NONHUMAN; PATTERN GENERATOR; PRIORITY JOURNAL; REVIEW;

EID: 0345627976     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-4388(98)80111-6     Document Type: Article

References (47)

1. Stein P, Stuart D, Selverston A, Grillner S. Neurons, Networks and Motor Behavior. 1997;MIT Press, Cambridge, Massachusetts.
2. Marder E, Calabrese RL. Principles of rhythmic motor pattern generation. Physiol Rev. 76:1996;687-717.
3. Arshavsky YI, Deliagina TG, Orlovsky GN. Pattern generation. Curr Opin Neurobiol. 7:1997;781-789.
4. Dale N, Kuenzi F. Ionic currents, transmitters and models of motor pattern generators. Curr Opin Neurobiol. 7:1997;790-796.
5. Bentley DR, Hoy RR. Postembryonic development of adult motor patterns in crickets: a neural analysis. Science. 170:1970;1409-1411.
6. Stevenson PA, Kutsch W. Demonstration of functional connectivity of the flight motor system in all stages of the locust. J Comp Physiol [A]. 162:1988;247-259.
7. Kammer AE, Rheuben MB. Adult motor patterns produced by moth pupae during development. J Exp Biol. 65:1976;65-84.
8. Cohen AH, Dobrov TA, Li G, Kiemel T, Baker MT. The development of the lamprey pattern generator for locomotion. J Neurobiol. 21:1990;958-969.
9. Kahn JA, Roberts A. The central nervous origin of the swimming motor pattern in embryos of Xenopus laevis. J Exp Biol. 99:1982;185-196.
10. Landmesser LT, O'Donovan MJ. Activation patterns of embryonic chick hind limb muscles recorded in ovo and in an isolated spinal cord preparation. J Physiol (Lond). 347:1984;189-204.
11. Cazalets JR, Sqalli-Houssaini Y, Clarac F. Activation of the central pattern generators for locomotion by serotonin and excitatory amino acids in neonatal rat. J Physiol (Lond). 455:1992;187-204.
12. Forssberg H, Hirschfeld H, Stokes VP. Development of human locomotor mechanisms. Armstrong DM, Bush BMH. Locomotor Neural Mechanisms in Arthropods and Vertebrates. 1991;313-331 Manchester University Press, Manchester.
13. Weeks JC, Truman JW. Neural organization of peptide-activated ecdysis behaviors during the metamorphosis of Manduca sexta. I. Conservation of the peristalsis motor pattern at the larval-pupal transformation. J Comp Physiol [A]. 155:1984;407-422.
14. Bekoff A. Neuroethological approaches to the study of motor development in chicks: achievements and challenges. J Neurobiol. 23:1992;1486-1505.
15. Champagnat J, Fortin G. Primordial respiratory-like rhythm generation in the vertebrate embryo. of outstanding interest Trends Neurosci. 20:1997;119-124 An important review on respiratory motor pattern generation in the embryonic hindbrain. Using a combination of genetic and electrophysiological approaches, the authors show that the primordial central pattern generator for respiration is active by the end of the transient segmentation period and is located in each successive pair of rhobomeres. Genes controlling hind-brain segmentation specify respiratory patterns, and it is proposed that they are responsible for the early specification of cell properties involved in rhythm generation. The authors also suggest that the early redundant embryonic rhythmogenic circuits are reconfigured by a regressive scheme.
16. Fortin G, Kato F, Lumsden A, Champagnat J. Rhythm generation in the segmented hindbrain of chick embryos. J Physiol (Lond). 486:1995;735-744.
17. Jacquin TD, Borday V, Schneider-Maunoury S, Topilko P, Ghilini G, Kato F, Charnay P, Champagnat J. Reorganization of pontine rhythmogenic neuronal networks in Krox-20 knockout mice. Neuron. 17:1996;747-758.
18. Fenelon VS, Casasnovas B, Faumont S, Meyrand P. Ontogenetic alteration in peptidergic expression within a stable neuronal population in lobster stomatogastric nervous system. of special interest J Comp Neurol. 399:1998;289-305 By neuronal counts and use of a marker of dividing cells, these authors demonstrate that a quantitatively stable neuronal population, organized in a single embryonic central pattern generator [19] is able, throughout development, to give rise to two adult motor pattern-generating networks. This study sets the stage for a future investigation of the developmental processes involved in this partitioning - the authors propose that neuromodulatory inputs are good candidates.
19. Casasnovas B, Meyrand P. Functional differentiation of multiple neural circuits from a single embryonic network. J Neurosci. 15:1995;5703-5718.
20. Sillar K. Synaptic specificity: development of locomotor rhythmicity. Curr Opin Neurobiol. 4:1994;101-107.
21. Nishimaru H, Iizuka M, Ozaki S, Kudo N. Spontaneous motoneuronal activity mediated by glycine and GABA in the spinal cord of rat fetuses in vitro. J Physiol. 497:1996;131-143.
22. Kudo N, Furukawa F, Okado N. Development of descending fibers to the rat embryonic spinal cord. Neurosci Res. 16:1993;131-141.
23. Spitzer NC. A developmental handshake: neuronal control of ionic currents and their control of neuronal differentiation. J Neurobiol. 22:1991;659-673.
24. Gleason EL, Spitzer NC. AMPA and NMDA receptors expressed by differentiating Xenopus spinal neurons. J Neurophysiol. 79:1998;2986-2998.
25. Ziskind-Conhaim L. Electrical properties of motoneurons in the spinal cord of rat embryos. Dev Biol. 128:1988;21-29.
26. Mandler RN, Schaffner AE, Novotny EA, Lange GD, Smith SV, Barker JL. Electrical and chemical excitability appear one week before birth in the embryonic rat spinal cord. Brain Res. 522:1990;46-54.
27. Bayliss DA, Viana F, Bellingham MC, Berger AJ. Characteristics and postnatal development of a hyperpolarization-activated inward current in rat hypoglossal motoneurons in vitro. J Neurophysiol. 71:1994;119-128.
28. Desarmenien MG, Clendening B, Spitzer NC. In vivo development of voltage-dependent ionic currents in embryonic Xenopus spinal neurons. J Neurosci. 13:1993;2575-2581.
29. Ziskind-Conhaim L, Seebach BS, Gao B-X. Changes in serotonin-induced potentials during spinal cord development. J Neurophysiol. 69:1993;1338-1349.
30. Scrymgeour-Wedderburn JF, Reith CA, Sillar KT. Voltage oscillations in Xenopus spinal cord neurons: developmental onset and dependence on co-activation of NMDA and 5HT receptors. of special interest Eur J Neurosci. 9:1997;1473-1482 This electrophysiological study demonstrates that tetrodotoxin (TTX)-resistant, NMDA-receptor-mediated voltage oscillations are acquired during the first day of larval life in Xenopus motor neurons and that they depend on 5HT or their activation. Because of the causal relationship between the development of descending 5HT fibers and the acquisition of a more complex locomotor pattern [35-37], the authors suggest that the increasing occurrence of 5HT-dependent membrane bistability in motor neurons contributes to the growing flexibility of the larval swimming pattern.
31. van Mier P, Joosten HWJ, van Rheden R, ten Donkelaar HJ. The development of serotoninergic raphespinal projections in Xenopus laevis. Int J Dev Neurosci. 4:1986;465-475.
32. Rajaofetra N, Sandillon F, Geffard M, Privat A. Pre- and post-natal ontogeny of serotonergic projections to the rat spinal cord. J Neurosci Res. 22:1989;305-321.
33. Okado N, Sako H, Homma S, Ishikawa K. Development of serotoninergic system in the brain and spinal cord of the chick. Prog Neurobiol. 38:1992;93-123.
34. Mesce KA, Truman JW. Metamorphosis of the ecdysis motor pattern in the hawkmoth, Manduca sexta. J Comp Physiol [A]. 163:1988;287-299.
35. Sillar KT, Wedderburn JF, Simmers AJ. Modulation of swimming rhythmicity by 5-hydroxytryptamine during post-embryonic development in Xenopus laevis. Proc R Soc Lond [Biol]. 250:1992;107-114.
36. Sillar KT, Simmers JA, 5HT induces NMDA receptor-mediated intrinsic oscillations in embryonic amphibian spinal neurons.
37. Sillar KT, Woolston AM, Wedderburn JF. Involvement of brainstem serotonergic interneurons in the development of a vertebrate spinal locomotor circuit. Proc R Soc Lond [Biol]. 259:1995;65-70.
38. Sun Q-Q, Dale N. Developmental changes in expression of ion currents accompany maturation of locomotor pattern in frog tadpoles. of outstanding interest J Physiol (Lond). 507:1998;257-264 This electrophysiological study reveals that changes in expression of outward current in embryonic versus larval Xenopus spinal neurons closely correlate with the known maturation of the motor pattern during development. At a time when the motor pattern has a need for a burst-terminating mechanism, larval spinal neurons express a channel with properties appropriate for such a role. However, it remains to be seen whether embryonic spinal neurons are able to express this channel if they are put in specific environmental conditions.
39. O'Dowd DK, Ribera AB, Spitzer NC. Development of voltage-dependent calcium, sodium, and potassium currents in Xenopus spinal neurons. J Neurosci. 8:1988;792-805.
40. Martinou JC, Merlie JP. Nerve-dependent modulation of acetylcholine receptor epsilon-subunit gene expression. J Neurosci. 11:1991;1291-1299.
41. Hyatt-Sachs H, Schreiber RC, Bennet TA, Zigmong RE. Phenotypic plasticity in adult sympathetic ganglia in vivo: effects of deafferentation and axotomy on the expression of vasoactive intestinal peptide. J Neurosci. 13:1993;1642-1653.
42. Kirsch J, Betz H. Glycine-receptor activation is required for receptor clustering in spinal neurons. Nature. 392:1998;717-720.
43. Traynor P, Dryden WF, Smith PA. Trophic regulation of action potential in bullfrog sympathetic neurons. Can J Physiol Pharmacol. 70:1992;826-834.
44. Thoby-Brisson M, Simmers JA. Neuromodulatory inputs maintain expression of a lobster motor pattern-generating network in a modulation-dependent state: evidence from long-term decentralization in vitro. of outstanding interest J Neurosci. 18:1998;2212-2225 These authors demonstrate that neuromodulatory inputs play a role in the long-term maintenance of adult neuronal network phenotype. By suppressing inputs to an invertebrate ganglion containing a well-described central pattern generator and by maintaining this ganglion in organotypic culture, they show that the CPG neurons, after falling silent, recover an inherent rhythmogenic capability that is normally maintained in a strictly conditional state when the neuromodulatory influences are present. This study is consistent with the hypothesis that neuromodulatory inputs play an important but hitherto underestimated role not only in the developmental elaboration of rhythmic motor pattern generator, but also in their long-term regulation in the mature nervous system.
45. Erickson GT, Conover JC, Borday V, Champagnat J, Barbacid M, Yancopoulos G, Katz DM. Mice lacking brain-derived neurotrophic factor exhibit visceral sensory neuron losses distinct from mice lacking NT4 and display a severe developmental deficit in control of breathing. J Neurosci. 16:1996;5361-5371.
46. Granato M, van Eeden FJ, Schach U, Trowe T, Brand M, Furutani-Seiki M, Haffter P, Hammerschmidt M, Heisenberg CP, Jiang YJ, Kane DA, et al. Genes controlling and mediating locomotion behavior of the zebrafish embryo and larva. Development. 123:1996;399-413.
47. + current, la) in individually identified CPG neurons and used in conjunction with standard electrophysiological techniques to investigate the role of differential Shaker family gene expression in creating neuronal la current diversity. This technique should allow assessment of developmental mechanisms involved in the maturational processes of intrin-.