Separate Microcircuit Modules of Distinct V2a Interneurons and Motoneurons Control the Speed of Locomotion

Neuron

Volumn 83, Issue 4, 2014, Pages 934-943

  Ampatzis, Konstantinos ^a   Song, Jianren ^a   Ausborn, Jessica ^a   ElManira, Abdeljabbar ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ACTION POTENTIAL; ARTICLE; BRAIN STEM; CONNECTOME; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; INTERNEURON; LOCOMOTION; MOTONEURON; NERVE CELL NETWORK; NERVE CELL STIMULATION; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; STIMULUS RESPONSE; SWIMMING; ZEBRA FISH; ACCELERATION; ANIMAL; CYTOLOGY; PHYSIOLOGY; SPINAL CORD;

ACCELERATION; ACTION POTENTIALS; ANIMALS; INTERNEURONS; LOCOMOTION; MOTOR NEURONS; NERVE NET; SPINAL CORD; ZEBRAFISH;

EID: 84907597053     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2014.07.018     Document Type: Article

References (48)

1. Ampatzis K., Song J., Ausborn J., El Manira A. Pattern of innervation and recruitment of different classes of motoneurons in adult zebrafish. J.Neurosci. 2013, 33:10875-10886.
2. Arber S. Motor circuits in action: specification, connectivity, and function. Neuron 2012, 74:975-989.
3. 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. USA 2012, 109:E3631-E3639.
4. Bernhardt R.R., Chitnis A.B., Lindamer L., Kuwada J.Y. Identification of spinal neurons in the embryonic and larval zebrafish. J.Comp. Neurol. 1990, 302:603-616.
5. Buchanan J.T., Grillner S. Newly identified 'glutamate interneurons' and their role in locomotion in the lamprey spinal cord. Science 1987, 236:312-314.
6. Buchanan J.T., Grillner S., Cullheim S., Risling M. Identification of excitatory interneurons contributing to generation of locomotion in lamprey: structure, pharmacology, and function. J.Neurophysiol. 1989, 62:59-69.
7. Burke R.E. Motor units: anatomy, physiology, and functional organization. Comprehensive Physiology 2011, 345-422. 10.1002/cphy.cp010210.
8. Büschges A., Scholz H., El Manira A. New moves in motor control. Curr. Biol. 2011, 21:R513-R524.
9. Cope T.C., Pinter M.J. The Size Principle: Still Working After All These Years. News Physiol. Sci. 1995, 10:280-286.
10. Crone S.A., Quinlan K.A., Zagoraiou L., Droho S., Restrepo C.E., Lundfald L., Endo T., Setlak J., Jessell T.M., Kiehn O., Sharma K. Genetic ablation of V2a ipsilateral interneurons disrupts left-right locomotor coordination in mammalian spinal cord. Neuron 2008, 60:70-83.
11. Crone S.A., Zhong G., Harris-Warrick R., Sharma K. In mice lacking V2a interneurons, gait depends on speed of locomotion. J.Neurosci. 2009, 29:7098-7109.
12. Dale N., Roberts A. Dual-component amino-acid-mediated synaptic potentials: excitatory drive for swimming in Xenopus embryos. J.Physiol. 1985, 363:35-59.
13. Dasen J.S., Jessell T.M. Hox networks and the origins of motor neuron diversity. Curr. Top. Dev. Biol. 2009, 88:169-200.
14. Devoto S.H., Melançon E., Eisen J.S., Westerfield M. Identification of separate slow and fast muscle precursor cells invivo, prior to somite formation. Development 1996, 122:3371-3380.
15. Dougherty K.J., Kiehn O. Functional organization of V2a-related locomotor circuits in the rodent spinal cord. Ann. N Y Acad. Sci. 2010, 1198:85-93.
16. Drapeau P., Saint-Amant L., Buss R.R., Chong M., McDearmid J.R., Brustein E. Development of the locomotor network in zebrafish. Prog. Neurobiol. 2002, 68:85-111.
17. Eklöf-Ljunggren E., Haupt S., Ausborn J., Dehnisch I., Uhlén P., Higashijima S.I., El Manira A. Origin of excitation underlying locomotion in the spinal circuit of zebrafish. Proc. Natl. Acad. Sci. USA 2012, 109:5511-5516.
18. Gabriel J.P., Mahmood R., Walter A.M., Kyriakatos A., Hauptmann G., Calabrese R.L., El Manira A. Locomotor pattern in the adult zebrafish spinal cord invitro. J.Neurophysiol. 2008, 99:37-48.
19. Gabriel J.P., Ausborn J., Ampatzis K., Mahmood R., Eklöf-Ljunggren E., El Manira A. Principles governing recruitment of motoneurons during swimming in zebrafish. Nat. Neurosci. 2011, 14:93-99.
20. Goulding M. Circuits controlling vertebrate locomotion: moving in a new direction. Nat. Rev. Neurosci. 2009, 10:507-518.
21. Grillner S. The motor infrastructure: from ion channels to neuronal networks. Nat. Rev. Neurosci. 2003, 4:573-586.
22. Grillner S., Jessell T.M. Measured motion: searching for simplicity in spinal locomotor networks. Curr. Opin. Neurobiol. 2009, 19:572-586.
23. Gustafsson B., Pinter M.J. An investigation of threshold properties among cat spinal alpha-motoneurones. J.Physiol. 1984, 357:453-483.
24. 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.
25. Henneman E. Relation between size of neurons and their susceptibility to discharge. Science 1957, 126:1345-1347.
26. Henneman E., Mendell L.M. Functional organization of motoneuron pool and its inputs. Handbook of Physiology 1981, Volume 2:423-507. American Physiological Society, Bethesda, MD.
27. Hoffer J.A., Sugano N., Loeb G.E., Marks W.B., O'Donovan M.J., Pratt C.A. Cat hindlimb motoneurons during locomotion. II. Normal activity patterns. J.Neurophysiol. 1987, 57:530-553.
28. Kiehn O. Locomotor circuits in the mammalian spinal cord. Ann. Rev. Neurosci. 2006, 29:279-306.
29. Kimura Y., Okamura Y., Higashijima S. alx, a zebrafish homolog of Chx10, marks ipsilateral descending excitatory interneurons that participate in the regulation of spinal locomotor circuits. J.Neurosci. 2006, 26:5684-5697.
30. Kimura Y., Satou C., Fujioka S., Shoji W., Umeda K., Ishizuka T., Yawo H., Higashijima S. Hindbrain V2a neurons in the excitation of spinal locomotor circuits during zebrafish swimming. Curr. Biol. 2013, 23:843-849.
31. Kyriakatos A., Mahmood R., Ausborn J., Porres C.P., Büschges A., El Manira A. Initiation of locomotion in adult zebrafish. J.Neurosci. 2011, 31:8422-8431.
32. Lewis K.E., Eisen J.S. From cells to circuits: development of the zebrafish spinal cord. Prog. Neurobiol. 2003, 69:419-449.
33. Liddell E.G.T., Sherrington C.S. Recruitment and some other factors of reflex inhibition. Proc. R. Soc. Lond., B 1925, 97:488-518.
34. Ljunggren E.E., Haupt S., Ausborn J., Ampatzis K., El Manira A. Optogenetic activation of excitatory premotor interneurons is sufficient to generate coordinated locomotor activity in larval zebrafish. J.Neurosci. 2014, 34:134-139.
35. Masino M.A., Fetcho J.R. Fictive swimming motor patterns in wild type and mutant larval zebrafish. J.Neurophysiol. 2005, 93:3177-3188.
36. McLean D.L., Fetcho J.R. Spinal interneurons differentiate sequentially from those driving the fastest swimming movements in larval zebrafish to those driving the slowest ones. J.Neurosci. 2009, 29:13566-13577.
37. McLean D.L., Fan J., Higashijima S., Hale M.E., Fetcho J.R. A topographic map of recruitment in spinal cord. Nature 2007, 446:71-75.
38. McLean D.L., Masino M.A., Koh I.Y., Lindquist W.B., Fetcho J.R. Continuous shifts in the active set of spinal interneurons during changes in locomotor speed. Nat. Neurosci. 2008, 11:1419-1429.
39. Roberts A., Li W.C., Soffe S.R. How neurons generate behavior in a hatchling amphibian tadpole: an outline. Front. Behav. Neurosci. 2010, 4:16.
40. Roberts A., Li W.C., Soffe S.R. A functional scaffold of CNS neurons for the vertebrates: the developing Xenopus laevis spinal cord. Dev. Neurobiol. 2012, 72:575-584.
41. Romanes G.J. The Motor Pools of the Spinal Cord. Prog. Brain Res. 1964, 11:93-119.
42. 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.
43. Stepien A.E., Tripodi M., Arber S. Monosynaptic rabies virus reveals premotor network organization and synaptic specificity of cholinergic partition cells. Neuron 2010, 68:456-472.
44. Tripodi M., Stepien A.E., Arber S. Motor antagonism exposed by spatial segregation and timing of neurogenesis. Nature 2011, 479:61-66.
45. van Raamsdonk W., van't Veer L., Veeken K., Heyting C., Pool C.W. Differentiation of muscle fiber types in the teleost Brachydanio rerio, the zebrafish. Posthatching development. Anat. Embryol. (Berl.) 1982, 164:51-62.
46. Zampieri N., Jessell T.M., Murray A.J. Mapping sensory circuits by anterograde transsynaptic transfer of recombinant rabies virus. Neuron 2014, 81:766-778.
47. Zhang H.Y., Issberner J., Sillar K.T. Development of a spinal locomotor rheostat. Proc. Natl. Acad. Sci. USA 2011, 108:11674-11679.
48. Zhong G., Droho S., Crone S.A., Dietz S., Kwan A.C., Webb W.W., Sharma K., Harris-Warrick R.M. Electrophysiological characterization of V2a interneurons and their locomotor-related activity in the neonatal mouse spinal cord. J.Neurosci. 2010, 30:170-182.