Inhibition and motor control in the developing zebrafish spinal cord

Current Opinion in Neurobiology

Volumn 26, Issue , 2014, Pages 103-109

  Fidelin, Kevin ^a,b,c,d   Wyart, Claire ^a,b,c,d  

^a PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^b INSERM   (France)

^c INSTITUT DU CERVEAU ET DE LA MOELLE ÉPINIÈRE   (France)

^d SORBONNE UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCINE RECEPTOR;

DEVELOPMENTAL STAGE; DOWN REGULATION; GABAERGIC TRANSMISSION; GENE ACTIVATION; GENE TARGETING; GENETIC ANALYSIS; INTERNEURON; LARVAL STAGE; LATENT PERIOD; LOCOMOTION; MOTOR CONTROL; NERVE CELL INHIBITION; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SPINAL CORD; SPINAL CORD NERVE CELL; ZEBRA FISH; ANIMAL; CYTOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; MOTOR ACTIVITY; PHYSIOLOGY;

ANIMALS; INTERNEURONS; MOTOR ACTIVITY; NEURAL INHIBITION; SPINAL CORD; ZEBRAFISH;

EID: 84892468304     PISSN: 09594388     EISSN: 18736882     Source Type: Journal    
DOI: 10.1016/j.conb.2013.12.016     Document Type: Review

References (72)

1. Falgairolle M., et al. Metachronal propagation of motor activity. Front Biosci (Landmark Ed) 2013, 18:820-837.
2. Cappellini G., et al. Migration of motor pool activity in the spinal cord reflects body mechanics in human locomotion. J Neurophysiol 2010, 104:3064-3073.
3. Jankowska E. Spinal interneuronal networks in the cat: elementary components. Brain Res Rev 2008, 57:46-55.
4. Kiehn O. Development and functional organization of spinal locomotor circuits. Curr Opin Neurobiol 2011, 21:100-109.
5. Grillner S. Biological pattern generation: the cellular and computational logic of networks in motion. Neuron 2006, 52:751-766.
6. Roberts A., Li W.C., Soffe S.R. Roles for inhibition: studies on networks controlling swimming in young frog tadpoles. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 2008, 194:185-193.
7. Grillner S., Jessell T.M. Measured motion: searching for simplicity in spinal locomotor networks. Curr Opin Neurobiol 2009, 19:572-586.
8. Goulding M. Circuits controlling vertebrate locomotion: moving in a new direction. Nat Rev Neurosci 2009, 10:507-518.
9. Budick S.A., O'Malley D.M. Locomotor repertoire of the larval zebrafish: swimming, turning and prey capture. J Exp Biol 2000, 203:2565-2579.
10. Mirat O., et al. ZebraZoom: an automated program for high-throughput behavioral analysis and categorization. Front Neural Circuits 2013, 7:107.
11. McLean D.L., Fetcho J.R. Movement, technology and discovery in the zebrafish. Curr Opin Neurobiol 2011, 21:110-115.
12. Legendre P. The glycinergic inhibitory synapse. Cell Mol Life Sci 2001, 58:760-793.
13. Hirata H., et al. Defective glycinergic synaptic transmission in zebrafish motility mutants. Front Mol Neurosci 2009, 2:26.
14. Hirata H., et al. The biological role of the glycinergic synapse in early zebrafish motility. Neurosci Res 2011, 71:1-11.
15. Hirata H., et al. Defective escape behavior in DEAH-box RNA helicase mutants improved by restoring glycine receptor expression. J Neurosci 2013, 33:14638-14644.
16. Gosgnach S., et al. V1 spinal neurons regulate the speed of vertebrate locomotor outputs. Nature 2006, 440:215-219.
17. Higashijima S., et al. Engrailed-1 expression marks a primitive class of inhibitory spinal interneuron. J Neurosci 2004, 24:5827-5839.
18. Liao J.C., Fetcho J.R. Shared versus specialized glycinergic spinal interneurons in axial motor circuits of larval zebrafish. J Neurosci 2008, 28:12982-12992.
19. Briggman K.L., Kristan W.B. Multifunctional pattern-generating circuits. Annu Rev Neurosci 2008, 31:271-294.
20. Fetcho J.R. Spinal network of the Mauthner cell. Brain Behav Evol 1991, 37:298-316.
21. Kohashi T., Nakata N., Oda Y. Effective sensory modality activating an escape triggering neuron switches during early development in zebrafish. J Neurosci 2012, 32:5810-5820.
22. Fetcho J.R. Morphological variability, segmental relationships, and functional role of a class of commissural interneurons in the spinal cord of goldfish. J Comp Neurol 1990, 299:283-298.
23. Satou C., et al. Functional role of a specialized class of spinal commissural inhibitory neurons during fast escapes in zebrafish. J Neurosci 2009, 29:6780-6793.
24. Moly P.K., Hatta K. Early glycinergic axon contact with the Mauthner neuron during zebrafish development. Neurosci Res 2011, 70:251-259.
25. Kinkhabwala A., et al. A structural and functional ground plan for neurons in the hindbrain of zebrafish. Proc Natl Acad Sci U S A 2011, 108:1164-1169.
26. Koyama M., et al. Mapping a sensory-motor network onto a structural and functional ground plan in the hindbrain. Proc Natl Acad Sci U S A 2011, 108:1170-1175.
27. Sibilla S., Ballerini L. GABAergic and glycinergic interneuron expression during spinal cord development: dynamic interplay between inhibition and excitation in the control of ventral network outputs. Prog Neurobiol 2009, 89:46-60.
28. Allain A.E., et al. Maturation of the GABAergic transmission in normal and pathologic motoneurons. Neural Plast 2011, 2011:905624.
29. Schmitt D.E., Hill R.H., Grillner S. The spinal GABAergic system is a strong modulator of burst frequency in the lamprey locomotor network. J Neurophysiol 2004, 92:2357-2367.
30. Ziskind-Conhaim L. Neuronal correlates of the dominant role of GABAergic transmission in the developing mouse locomotor circuitry. Ann N Y Acad Sci 2013, 1279:43-53.
31. Satou C., Kimura Y., Higashijima S. Generation of multiple classes of V0 neurons in zebrafish spinal cord: progenitor heterogeneity and temporal control of neuronal diversity. J Neurosci 2012, 32:1771-1783.
32. Talpalar A.E., et al. Dual-mode operation of neuronal networks involved in left-right alternation. Nature 2013, 500:85-88.
33. Batista M.F., Jacobstein J., Lewis K.E. Zebrafish V2 cells develop into excitatory CiD and Notch signalling dependent inhibitory VeLD interneurons. Dev Biol 2008, 322:263-275.
34. Saint-Amant L., Drapeau P. Synchronization of an embryonic network of identified spinal interneurons solely by electrical coupling. Neuron 2001, 31:1035-1046.
35. Higashijima S., Schaefer M., Fetcho J.R. Neurotransmitter properties of spinal interneurons in embryonic and larval zebrafish. J Comp Neurol 2004, 480:19-37.
36. Yang L., Rastegar S., Strähle U. Regulatory interactions specifying Kolmer-Agduhr interneurons. Development 2010, 137:2713-2722.
37. Huang P., et al. Attenuation of Notch and Hedgehog signaling is required for fate specification in the spinal cord. PLoS Genet 2012, 8:e1002762.
38. Wyart C., et al. Optogenetic dissection of a behavioural module in the vertebrate spinal cord. Nature 2009, 461:407-410.
39. Ulloa F., Briscoe J. Morphogens and the control of cell proliferation and patterning in the spinal cord. Cell Cycle 2007, 6:2640-2649.
40. Alaynick W.A., Jessell T.M., Pfaff S.L. SnapShot: spinal cord development. Cell 2011, 146. 178-178.e1.
41. McDearmid J.R., Liao M., Drapeau P. Glycine receptors regulate interneuron differentiation during spinal network development. Proc Natl Acad Sci U S A 2006, 103:9679-9684.
42. CÔté S., Drapeau P. Regulation of spinal interneuron differentiation by the paracrine action of glycine. Dev Neurobiol 2012, 72:208-214.
43. Brustein E., et al. Spontaneous glycine-induced calcium transients in spinal cord progenitors promote neurogenesis. Dev Neurobiol 2013, 73:168-175.
44. Blankenship A.G., Feller M.B. Mechanisms underlying spontaneous patterned activity in developing neural circuits. Nat Rev Neurosci 2010, 11:18-29.
45. Ben-Ari Y. The Yin and Yen of GABA in brain development and operation in health and disease. Front Cell Neurosci 2012, 6:45.
46. Drapeau P., et al. Development of the locomotor network in zebrafish. Prog Neurobiol 2002, 68:85-111.
47. Reali C., et al. GABAergic signalling in a neurogenic niche of the turtle spinal cord. J Physiol 2011, 589:5633-5647.
48. Higashijima S., Mandel G., Fetcho J.R. Distribution of prospective glutamatergic, glycinergic, and GABAergic neurons in embryonic and larval zebrafish. J Comp Neurol 2004, 480:1-18.
49. Hale M.E., Ritter D.A., Fetcho J.R. A confocal study of spinal interneurons in living larval zebrafish. J Comp Neurol 2001, 437:1-16.
50. Abe G., Suster M.L., Kawakami K. Tol2-mediated transgenesis, gene trapping, enhancer trapping, and the Gal4-UAS system. Methods Cell Biol 2011, 104:23-49.
51. Suster M.L., et al. Transposon-mediated BAC transgenesis in zebrafish. Nat Protoc 2011, 6:1998-2021.
52. Satou C., et al. Transgenic tools to characterize neuronal properties of discrete populations of zebrafish neurons. Development 2013, 140:3927-3931.
53. Naumann E.A., et al. Monitoring neural activity with bioluminescence during natural behavior. Nat Neurosci 2010, 13:513-520.
54. Looger L.L., Griesbeck O. Genetically encoded neural activity indicators. Curr Opin Neurobiol 2012, 22:18-23.
55. Ahrens M.B., et al. Brain-wide neuronal dynamics during motor adaptation in zebrafish. Nature 2012, 485:471-477.
56. Akerboom J., et al. Optimization of a GCaMP calcium indicator for neural activity imaging. J Neurosci 2012, 32:13819-13840.
57. Chen T.W., et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 2013, 499:295-300.
58. Hinckley C.A., Pfaff S.L. Imaging spinal neuron ensembles active during locomotion with genetically encoded calcium indicators. Ann N Y Acad Sci 2013, 1279:71-79.
59. Nishimaru H., Restrepo C.E., Kiehn O. Activity of Renshaw cells during locomotor-like rhythmic activity in the isolated spinal cord of neonatal mice. J Neurosci 2006, 26:5320-5328.
60. McCrea D.A., Pratt C.A., Jordan L.M. Renshaw cell activity and recurrent effects on motoneurons during fictive locomotion. J Neurophysiol 1980, 44:475-488.
61. Kimura Y., et al. Hindbrain V2a neurons in the excitation of spinal locomotor circuits during zebrafish swimming. Curr Biol 2013, 23:843-849.
62. Hägglund M., et al. Activation of groups of excitatory neurons in the mammalian spinal cord or hindbrain evokes locomotion. Nat Neurosci 2010, 13:246-252.
63. Hägglund M., et al. Optogenetic dissection reveals multiple rhythmogenic modules underlying locomotion. Proc Natl Acad Sci U S A 2013, 110:11589-11594.
64. Moult P.R., Cottrell G.A., Li W.C. Fast silencing reveals a lost role for reciprocal inhibition in locomotion. Neuron 2013, 77:129-140.
65. Portugues R., et al. Optogenetics in a transparent animal: circuit function in the larval zebrafish. Curr Opin Neurobiol 2013, 23:119-126.
66. McLean D.L., et al. A topographic map of recruitment in spinal cord. Nature 2007, 446:71-75.
67. Ausborn J., Mahmood R., El Manira A. Decoding the rules of recruitment of excitatory interneurons in the adult zebrafish locomotor network. Proc Natl Acad Sci U S A 2012, 109:E3631-E3639.
68. Gabriel J.P., et al. Principles governing recruitment of motoneurons during swimming in zebrafish. Nat Neurosci 2011, 14:93-99.
69. Westphal R.E., O'Malley D.M. Fusion of locomotor maneuvers, and improving sensory capabilities, give rise to the flexible homing strikes of juvenile zebrafish. Front Neural Circuits 2013, 7:108.
70. Kyriakatos A., et al. Initiation of locomotion in adult zebrafish. J Neurosci 2011, 31:8422-8431.
71. Schmidt R., Strähle U., Scholpp S. Neurogenesis in zebrafish-from embryo to adult. Neural Dev 2013, 8:3.
72. Barreiro-Iglesias A., et al. Distribution of glycinergic neurons in the brain of glycine transporter-2 transgenic Tg(glyt2:Gfp) adult zebrafish: relationship to brain-spinal descending systems. J Comp Neurol 2013, 521:389-425.