Initiation of locomotion in adult Zebrafish

Journal of Neuroscience

Volumn 31, Issue 23, 2011, Pages 8422-8431

  Kyriakatos, Alexandros ^a   Mahmood, Riyadh ^a   Ausborn, Jessica ^a   Porres, Christian P ^b   Büschges, Ansgar ^b   Manira, Abdeljabbar El ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UNIVERSITY OF COLOGNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCINE RECEPTOR; IONOTROPIC RECEPTOR; N METHYL DEXTRO ASPARTIC ACID;

ACTION POTENTIAL; ANIMAL TISSUE; ARTICLE; BRAIN STEM; CELL ACTIVITY; CELL INTERACTION; CELL SHAPE; CONTROLLED STUDY; ELECTROSTIMULATION; ENZYME ACTIVATION; IN VITRO STUDY; LOCOMOTION; MOTONEURON; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; SENSORY STIMULATION; SPINAL CORD; SWIMMING; SYNAPSE; ZEBRA FISH;

ACTION POTENTIALS; ANIMALS; BRAIN STEM; EFFERENT PATHWAYS; ELECTROPHYSIOLOGY; EXCITATORY AMINO ACID AGONISTS; LOCOMOTION; MOTOR ACTIVITY; MOTOR NEURONS; N-METHYLASPARTATE; SPINAL CORD; SYNAPSES; ZEBRAFISH;

EID: 79958253706     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1012-11.2011     Document Type: Article

References (61)

1. Berkowitz A, Roberts A, Soffe SR (2010) Roles for multifunctional and specialized spinal interneurons during motor pattern generation in tadpoles, zebrafish larvae, and turtles. Front Behav Neurosci 4:36.
2. Budick SA, O'Malley DM (2000) Locomotor repertoire of the larval ze-brafish: swimming, turning and prey capture. J Exp Biol 203:2565-2579.
3. Cabelguen JM, Bourcier-Lucas C, Dubuc R (2003) Bimodal locomotion elicited by electrical stimulation of the midbrain in the salamander No-tophthalmus viridescens. J Neurosci 23:2434-2439.
4. Cazalets JR, Sqalli-Houssaini Y, Clarac F (1992) Activation of the central pattern generators for locomotion by serotonin and excitatory amino acids in neonatal rat. J Physiol 455:187-204.
5. Chong M, Drapeau P (2007) Interaction between hindbrain and spinal networks during the developmentof locomotioninzebrafish. Dev Neurobiol 67:933-947.
6. Clarac F, Pearlstein E, Pflieger JF, Vinay L (2004) The in vitro neonatal rat spinal cord preparation: a new insight into mammalian locomotor mechanisms. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 190:343-357.
7. Cowley KC, Zaporozhets E, Maclean JN, Schmidt BJ (2005) Is NMDA receptor activation essential for the productionof locomotor-like activity in the neonatal rat spinal cord? J Neurophysiol 94:3805-3814.
8. Deliagina TG, Zelenin PV, Orlovsky GN (2002) Encoding and decoding of reticulospinal commands. Brain Res Rev 40:166-177.
9. Drapeau P, Saint-Amant L, Buss RR, Chong M, McDearmid JR, Brustein E (2002) Development of the locomotor network in zebrafish. Prog Neu-robiol 68:85-111.
10. Dubuc R, Brocard F, Antri M, Fénelon K, Gariépy JF, Smetana R, Méard A, Le Ray D,Viana Di Prisco G, Pearlstein E, Sirota MG, Derjean D, St-Pierre M, Zielinski B, Auclair F, Veilleux D (2008) Initiation of locomotion in lampreys. Brain Res Rev 57:172-182.
11. El-Manira A, Clarac F (1994) Presynaptic inhibition is mediated by hista-mine and GABA in the crustacean escape reaction. J Neurophysiol 71:1088-1095.
12. El-Manira A, Grillner S (2008) Switching gears in the spinal cord. Nat Neurosci 11:1367-1368.
13. El-Manira A, Kyriakatos A (2010) The role of endocannabinoid signaling in motor control. Physiology 25:230-238.
14. El-Manira A, Pombal MA, Grillner S (1997) Diencephalic projection to reticulospinal neurons involved in the initiation of locomotion in adult lampreys Lampetra fluviatilis. J Comp Neurol 389:603-616.
15. Fetcho JR, McLean DL (2010) Some principles of organization of spinal neurons underlying locomotion in zebrafish and their implications. Ann N Y Acad Sci 1198:94-104.
16. Fetcho JR, Svoboda KR (1993) Fictive swimming elicited by electrical stimulation of the midbrain in goldfish. J Neurophysiol 70:765-780.
17. Fetcho JR, Higashijima S, McLean DL (2008) Zebrafish and motor control over the last decade. Brain Res Rev 57:86-93.
18. Gabriel JP, Mahmood R, Walter AM, Kyriakatos A, Hauptmann G, Calabrese RL, El-Manira A (2008) Locomotor pattern in the adult zebrafish spinal cord in vitro. J Neurophysiol 99:37-48.
19. Gabriel JP, Mahmood R, Kyriakatos A, Söll I, Hauptmann G, Calabrese RL, El-Manira A (2009) Serotonergic modulation of locomotion in zebrafish: endogenous release and synaptic mechanisms. J Neurosci 29: 10387-10395.
20. Gabriel JP, Ausborn J, Ampatzis K, Mahmood R, Eklöf-Ljunggren E, El-Manira A (2011) Principles governing recruitment of motoneurons during swimming in zebrafish. Nat Neurosci 14:93-99.
21. Gahtan E, Sankrithi N, Campos JB, O'Malley DM (2002) Evidence for a widespread brain stem escape network in larval zebrafish. J Neurophysiol 87:608-614.
22. Goulding M (2009) Circuits controlling vertebrate locomotion: moving ina new direction. Nat Rev Neurosci 10:507-518.
23. Grillner S (2003) The motor infrastructure: from ion channels to neuronal networks. Nat Rev Neurosci 4:573-586.
24. Grillner S (2006) Biological pattern generation: the cellular and computational logic of networks in motion. Neuron 52:751-766.
25. Grillner S, Jessell TM (2009) Measured motion: searching for simplicity in spinal locomotor networks. Curr Opin Neurobiol 19:572-586.
26. Hultborn H, Conway BA, Gossard JP, Brownstone R, Fedirchuk B, Schom-burg ED, Enríquez-Denton M, Perreault MC (1998) How do we approach the locomotor network in the mammalian spinal cord? Ann N Y Acad Sci 860:70-82.
27. Issberner JP, Sillar KT (2007) The contribution of the NMDA receptor gly-cine site to rhythm generation during fictive swimming in Xenopus laevis tadpoles. Eur J Neurosci 26:2556-2564.
28. Jordan LM, Brownstone RM, Noga BR (1992) Controloffunctional systems in the brainstem and spinal cord. Curr Opin Neurobiol 2:794-801.
29. Jordan LM, Liu J, Hedlund PB, Akay T, Pearson KG (2008) Descending command systems for the initiation of locomotion in mammals. Brain Res Rev 57:183-191.
30. Kettunen P, Kyriakatos A, Hallén K, El-Manira A (2005) Neuromodulation via conditional release of endocannabinoids in the spinal locomotor network. Neuron 45:95-104.
31. Kiehn O (2006) Locomotor circuits in the mammalian spinal cord. Annu Rev Neurosci 29:279-306.
32. Kimura Y, Okamura Y, Higashijima S (2006) alx, a zebrafish homolog of Chx10, marks ipsilateral descending excitatory interneurons that participate in the regulation of spinal locomotor circuits. J Neurosci 26: 5684-5697.
33. Kyriakatos A, El-Manira A (2007) Long-term plasticity of the spinal loco-motor circuitry mediated by endocannabinoid and nitric oxide signaling. J Neurosci 27:12664-12674.
34. LeBeau FE, El-Manira A, Griller S (2005) Tuning the network: modulation of neuronal microcircuits in the spinal cord and hippocampus. Trends Neurosci 28:552-561.
35. Liao JC, Fetcho JR (2008) Shared versus specialized glycinergic spinal in-terneurons in axial motor circuits of larval zebrafish. J Neurosci 28:12982-12992.
36. Li WC, Soffe SR, Wolf E, Roberts A (2006) Persistent responses to brief stimuli: feedback excitation among brainstem neurons. J Neurosci 26:4026-4035.
37. Li WC, Roberts A, Soffe SR (2010) Specific brainstem neurons switch each other into pacemaker mode to drive movement by activating NMDA receptors. J Neurosci 30:16609-16620.
38. Liu DW, Westerfield M (1988) Function of identified motoneurones and co-ordination of primary and secondary motor systems during zebra fish swimming. J Physiol 403:73-89.
39. Marder E, Bucher D, Schulz DJ, Taylor AL (2005) Invertebrate central pattern generation moves along. Curr Biol 15:R685-R699.
40. McDearmid JR, Drapeau P (2006) Rhythmic motor activity evoked by NMDA in the spinal zebrafish larva. J Neurophysiol 95:401-417.
41. McLean DL, Fetcho JR (2009) Spinal interneurons differentiate sequentially from those driving the fastest swimming movements in larval zebrafish to those driving the slowest ones. J Neurosci 29:13566-13577.
42. McLean DL, Fan J, Higashijima S, Hale ME, Fetcho JR (2007) Atopographic map of recruitment in spinal cord. Nature 446:71-75.
43. McLean DL, Masino MA, Koh IY, Lindquist WB, Fetcho JR (2008) Continuous shifts in the active set of spinal interneurons during changes in locomotor speed. Nat Neurosci 11:1419-1429.
44. Mentel T, Krause A, Pabst M, El-Manira A, Büschges A (2006) Activity of dorsal fin muscles and motoneurons during locomotor activity in lamprey in vivo and in vitro. Eur J Neurosci 23:2012-2026.
45. Muller UK, van Leeuwen JL (2004) Swimming of larval zebrafish: ontogeny of body waves and implications for locomotory development. J Exp Biol 207:853-868.
46. Muller UK, Stamhuis EJ, Videler JJ (2000) Hydrodynamics of unsteady fish swimming and the effects of body size: comparing the flow fields of fish larvae and adults. J Exp Biol 203:193-206.
47. Roberts A, Li WC, Soffe SR, Wolf E (2008) Origin of excitatory drive to a spinal locomotor network. Brain Res Rev 57:22-28.
48. Roberts A, Li WC, Soffe SR (2010) How neurons generate behavior in a hatchling amphibian tadpole: an outline. Front Behav Neurosci 4:16.
49. Rossignol S, Dubuc R, Gossard JP (2006) Dynamic sensorimotor interactions in locomotion. Physiol Rev 86:89-154.
50. Satou C, Kimura Y, Kohashi T, Horikawa K, Takeda H, Oda Y, Higashijima S (2009) Functional role of a specialized class of spinal commissural inhib itory neurons during fast escapes in zebrafish. J Neurosci 29:6780-6793.
51. Schmidt BJ, Hochman S, MacLean JN (1998) NMDA receptor-mediated oscillatory properties: potential role in rhythm generation in the mammalian spinal cord. Ann N Y Acad Sci 860:189-202.
52. Shaw AC, Jackson AW, Holmes T, Thurman S, Davis GR, McClellan AD (2010) Descending brain neurons in larval lamprey: spinal projection patterns and initiation of locomotion. Exp Neurol 224:527-541.
53. Sirota MG, Di Prisco GV, Dubuc R (2000) Stimulation ofthe mesencephalic locomotor region elicits controlled swimming in semi-intact lampreys. Eur J Neurosci 12:4081-4092.
54. Soffe SR, Roberts A, Li WC (2009) Defining the excitatory neurons that drive the locomotor rhythmin a simple vertebrate: insights into the origin of reticulospinal control. J Physiol 587:4829-4844.
55. Svoboda KR, Fetcho JR (1996) Interactions between the neural networks for escape and swimming in goldfish. J Neurosci 16:843-852.
56. Taccola G, Nistri A (2006) Oscillatory circuits underlying locomotor networks in the rat spinal cord. Crit Rev Neurobiol 18:25-36.
57. Talpalar AE, Kiehn O (2010) Glutamatergic mechanisms for speed control and network operation in the rodent locomotor CpG. Front Neural Circuits 4:pii:19.
58. Thorsen DH, Cassidy JJ, Hale ME (2004) Swimming of larval zebrafish: fin-axis coordination and implications for function and neural control. J Exp Biol 207:4175-4183.
59. van Raamsdonk W, van't Veer L, Veeken K, Heyting C, Pool CW (1982) Differentiation of muscle fiber types in the teleost Brachydanio rerio, the zebrafish. Posthatching development. Anat Embryol (Berl) 164:51-62.
60. van Raamsdonk W, Mos W, Smit-Onel MJ, van der Laarse WJ, Fehres R (1983) The development of the spinal motor column in relation to the myotomal muscle fibers in the zebrafish (Brachydanio rerio). I. Post-hatching development. Anat Embryol (Berl) 167:125-139.
61. Zhang W, Pombal MA, El-Manira A, Grillner S (1996) Rostrocaudal distribution of 5-HT innervation in the lamprey spinal cord and differential effects of 5-HT on fictive locomotion. J Comp Neurol 374:278-290.