Development of motor behaviour

Current Opinion in Neurobiology

Volumn 9, Issue 6, 1999, Pages 670-675

  Bate, Michael ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHICK EMBRYO; EMBRYO DEVELOPMENT; GENETIC REGULATION; LOCOMOTION; NERVE CELL DIFFERENTIATION; NERVE FIBER; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; REVIEW; SWIMMING; ZEBRA FISH;

EID: 0032763547     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-4388(99)00031-8     Document Type: Review

References (50)

1. Wilson D.M., Inherent asymmetry reflex modulation of the locust flight motor pattern J Exp Biol. 48:1968;631-641.
2. Bate M. Making sense of behavior. Int J Dev Biol. 42:1998;507-509.
3. Coghill G.E. Anatomy and the Problem of Behaviour. 1929;Cambridge University Press, London.
4. Reynolds S.A., French K.A., Baader A., Kristan W.B. Jr. Development of spontaneous and evoked behaviors in the medicinal leech. J Comp Neurol. 402:1998;168-180.
5. Saint-Amant L., Drapeau P. Time course of the development of motor behaviors in the zebrafish embryo. J Neurobiol. 37:1998;622-632. The authors used video microscopy to make a detailed description and quantitation of developing motor behaviour in zebrafish embryos. From spontaneous coiling through touch-induced coiling to swimming, each behaviour appears on a precise schedule during 10 hours of development. Anaesthesia during this period delays but does not prevent the onset of swimming. Lesions suggest that the hindbrain is essential for touch-induced coiling and swimming but not for spontaneous coiling. This paper represents an essential first step towards analysis of the development of underlying circuitry.
6. Bradley N.S. Transformations in embryonic motility in chick: kinematic correlates of type I and II motility at E9 and E12. J Neurophysiol. 81:1999;1486-1494.
7. Decker J.D. Motility of the turtle embryo, Chelydra serpentina (Linne). Science. 157:1967;952-954.
8. Narayanan C.H., Fox M.W., Hamburger V. Prenatal development of spontaneous and evoked activity in the rat (Rattus norvegicus albinus). Behaviour. 40:1971;100-134.
9. Suzue T. Movements of mouse fetuses in early stages of neural development studied in vitro. Neurosci Lett. 218:1996;131-134.
10. Dale N. Role of ionic currents in the operation of motor circuits in the Xenopus embryo. Stein P.S.G., Grillner S., Selverston A.I., Stuart D.G. Neurons, Networks and Behavior. 1997;91-96 MIT Press, Cambridge, Massachusetts.
11. Granato M., van Eeden F.J., Schach U., Trowe T., Brand M., Furutani-Seiki M., Haffter P., Hammerschmidt M., Heisenberg C.P., Jiang Y.J.et al. Genes controlling and mediating locomotion behavior of the zebrafish embryo and larva. Development. 123:1996;399-413.
12. Grillner S., Parker D., El Manira A. Vertebrate locomotion - a lamprey perspective. Ann NY Acad Sci. 860:1998;1-18.
13. Roberts A., Soffe S.R., Wolf E.S., Yoshida M., Zhao F.Y. Central circuits controlling locomotion in young frog tadpoles. Ann NY Acad Sci. 860:1998;19-34.
14. Kimmel C.B., Ballard W.W., Kimmel S.R., Ullmann B., Schilling T.F. Stages of embryonic development of the zebrafish. Dev Dyn. 203:1995;253-310.
15. Drapeau P., Ali D.W., Buss R.R., Saint-Amant L. In vivo recording from identifiable neurons of the locomotor network in the developing zebrafish. J Neurosci Methods. 88:1999;1-13. The authors describe an exposed hindbrain/spinal-cord preparation of the zebrafish embryo and larva that they used to label and make whole-cell patch-clamp recordings from identified motor neurons, sensory neurons and interneurons. They were able to make recordings from neurons at early stages of spontaneous movement up to the swimming larval stage. This work offers the exciting prospect of defining the developing characteristics of individual elements of motor circuitry as they differentiate in wild-type and mutant embryos.
16. Fetcho J.R., Cox K.J., O'Malley D.M. Monitoring activity in neuronal populations with single-cell resolution in a behaving vertebrate. Histochem J. 30:1998;153-167.
17. Fetcho J.R., Liu K.S. Zebrafish as a model system for studying neuronal circuits and behavior. Ann NY Acad Sci. 860:1998;333-345.
18. Liu K.S., Fetcho J.R. Laser ablations reveal functional relationships of segmental hindbrain neurons in zebrafish. Neuron. 23:1999;325-335.
19. Nguyen P.V., Aniksztejn L., Catarsi S., Drapeau P. Maturation of neuromuscular transmission during early development in zebrafish. J Neurophysiol. 81:1999;2852-2861.
20. van Mier P., Armstrong J., Roberts A. Development of early swimming in Xenopus laevis embryos: myotomal musculature, its innervation and activation. Neuroscience. 32:1989;113-126.
21. Sillar K.T., Reith C.A., McDearmid J.R. Development and aminergic neuromodulation of a spinal locomotor network controlling swimming in Xenopus larvae. Ann NY Acad Sci. 860:1998;318-332.
22. Foster R.G.A., Roberts A. The pineal eye in Xenopus laevis: a photoreceptor with a direct excitatory effect on behaviour. J Comp Physiol. 145:1982;413-419.
23. Boothby K.M., Roberts A. The stopping response of Xenopus laevis embryos: behaviour, development and physiology. J Comp Physiol. 170:1992;171-180.
24. Sillar K.T., Wedderburn J.F., Simmers A.J. The development of swimming rhythmicity in post-embryonic Xenopus laevis. Proc R Soc Lond [Biol]. 246:1991;147-153.
25. Sillar K.T., Woolston A.M., Wedderburn J.F. Involvement of brainstem serotonergic interneurons in the development of a vertebrate spinal locomotor circuit. Proc R Soc Lond [Biol]. 259:1995;65-70.
26. Moody W.J. The development of voltage-gated ion channels and its relation to activity-dependent development events. Curr Top Dev Biol. 39:1998;159-185. A really outstanding review and critique of ion channel development in excitable cells, particularly in the context of spontaneous activity as a prelude to the development of functional circuitry. Moody considers a variety of systems and emphasises the importance of developmental constraints in dictating particular constellations of ion channels that are required for spontaneous activity during early stages in the maturation of embryonic cells. Such specialised channel properties are probably incompatible with the mature functional properties of these cells, necessitating an orderly transition from one state to the other. As many of these changes will themselves be activity dependent, there is the potential for regulatory loops that control the actual mix of ion channels that develops.
27. + current. The authors conclude that the maturation of the motor pattern from embryo to larva is closely correlated with changes in the expression of ion channels.
28. + current and the overshoot to develop. These findings emphasise the power of mutant analysis and the requirement for an orderly maturation of channel properties for normal development of behaviour.
29. Katz L.C., Shatz C.J. Synaptic activity and the construction of cortical circuits. Science. 274:1996;1133-1138.
30. Sillar K.T. Synaptic specificity: development of locomotor rhythmicity. Curr Opin Neurobiol. 4:1994;101-107.
31. Cohen A.H. Evolution of the vertebrate central pattern generator for locomotion. Cohen A.H., Rossignol S., Grillner S. Neural Control of Rhythmic Movements in Vertebrates. 1988;129-166 Wiley-Interscience, New York.
32. Hamburger V., Oppenheim R. Prehatching motility and hatching behavior in the chick. J Exp Zool. 166:1967;171-203.
33. Bekoff A. Ontogeny of leg motor output in the chick embryo: a neural analysis. Brain Res. 106:1976;271-291.
34. O'Donovan M.J., Landmesser L. The development of hindlimb motor activity studied in the isolated spinal cord of the chick embryo. J Neurosci. 7:1987;3256-3264.
35. O'Donovan M., Sernagor E., Sholomenko G., Ho S., Antal M., Yee W. Development of spinal motor networks in the chick embryo. J Exp Zool. 261:1992;261-273.
36. Milner L.D., Landmesser L.T. Cholinergic and GABAergic inputs drive patterned spontaneous motoneuron activity before target contact. J Neurosci. 19:1999;3007-3022. This outstandingly interesting paper investigates the physiology and pharmacology of early spontaneous activity in lumbosacral motor neurons of the chick embryo. It demonstrates several key points. First, spontaneous activity is detectable as axons leave the glial plexus and before they reach their targets. Second, the distinction between flexor and extensor motor neurons is already established at this early stage. Third, the primary transmitter driving activity is acetylcholine, not glutamate as at later stages. Fourth, rhythmogenesis is plastic, being driven by GABAergic inputs in the presence of cholinergic blockers. Finally, gap junctional communication probably plays a role in early spontaneous activity. These findings represent a major advance in the description and analysis of the developing motor system, and they emphasise the apparent similarities with spontaneously active sensory systems.
37. Lin J.H., Saito T., Anderson D.J., Lance-Jones C., Jessell T.M., Arber S. Functionally related motor neuron pool and muscle sensory afferent subtypes defined by coordinate ETS gene expression. Cell. 95:1998;393-407.
38. Sernagor E., Chub N., Ritter A., O'Donovan M.J. Pharmacological characterization of the rhythmic synaptic drive onto lumbosacral motoneurons in the chick embryo spinal cord. J Neurosci. 15:1995;7452-7464.
39. 2+ transients and their transmission in the developing chick retina. Curr Biol. 8:1998;283-286.
40. Wong W.T., Sanes J.R., Wong R.O. Developmentally regulated spontaneous activity in the embryonic chick retina. J Neurosci. 18:1998;8839-8852.
41. Kudo N., Nishimaru H. Reorganization of locomotor activity during development in the prenatal rat. Ann NY Acad Sci. 860:1998;306-317.
42. Nakayama K., Nishimaru H., Iizuka M., Ozaki S., Kudo N. Rostrocaudal progression in the development of periodic spontaneous activity in fetal rat spinal motor circuits in vitro. J Neurophysiol. 81:1999;2592-2595.
43. Chub N., O'Donovan M.J. Blockade and recovery of spontaneous rhythmic activity after application of neurotransmitter antagonists to spinal networks of the chick embryo. J Neurosci. 18:1998;294-306. This important paper demonstrates a resilient capacity for spinal circuitry to generate rhythmic spontaneous activity in the presence of transmission blockers. Activity recovers and persists after blockade of either glutamatergic and cholinergic connections or after blocking GABAergic and glycinergic connections. This finding indicates that the detailed connectivity of the developing network may not be critical to the genesis of rhythmic activity. The authors suggest that such rhythmic activity may be a common feature of many developing spinal networks.
44. O'Donovan M.J. The origin of spontaneous activity in developing networks of the vertebrate nervous system. Curr Opin Neurobiol. 9:1999;94-104.
45. Fortin G., Champagnat J., Lumsden A. Onset and maturation of branchio-motor activities in the chick hindbrain. Neuroreport. 5:1994;1149-1152.
46. Champagnat J., Fortin G. Primordial respiratory-like rhythm generation in the vertebrate embryo. Trends Neurosci. 20:1997;119-124.
47. Lumsden A., Krumlauf R. Patterning the vertebrate neuraxis. Science. 274:1996;1109-1115.
48. Hughes S.M., Salinas P.C. Control of muscle fibre and motoneuron diversification. Curr Opin Neurobiol. 9:1999;54-64.
49. Baines R.A., Bate M. Electrophysiological development of central neurons in the Drosophila embryo. J Neurosci. 18:1998;4673-4683. The authors describe the development of electrical properties of central neurons in the Drosophila embryo, using whole-cell patch clamp on a dissected embryo with a semi-intact nervous system. This paper is important because it opens up the possibility of studying the acquisition of electrical excitability in identified central neurons in vivo, using the array of genetic and molecular methods that are available in Drosophila. In addition, it may be possible to relate the differentiation of central neurons to the progressive acquisition of motor behaviour in the developing embryo.
50. Siekhaus D.E., Fuller R.S. A role for amontillado, the Drosophila homolog of the neuropeptide precursor processing protease PC2, in triggering hatching behavior. J Neurosci. 19:1999;6942-6954. The authors identify amontillado, the Drosophila homologue of the mammalian neuropeptide precursor processing protease PC2. They use in situ hybridisation to show that expression of amontillado is largely restricted to late embryogenesis, in cells of the anterior sensory system and some cells in the CNS. Embryos deficient for amontillado show aberrant hatching behaviour, which is rescued by the wild-type gene product. The authors suggest that amontillado may be an important element in the regulation of this late embryonic pattern of motor behaviour.