Spinal interneurons providing input to the final common path during locomotion

Progress in Brain Research

Volumn 187, Issue C, 2010, Pages 81-95

  Brownstone, Robert M ^a   Bui, Tuan V ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Central pattern generators; Last order interneurons; Microcircuits; Motoneurons; Spinal cord

Indexed keywords

ANATOMY; BOOK; CAT; EXCITATORY POSTSYNAPTIC POTENTIAL; INTERNEURON; LOCOMOTION; MOTONEURON; MOTOR ACTIVITY; NERVE CELL NETWORK; NONHUMAN; PHYSIOLOGY; PRIORITY JOURNAL; RENSHAW CELL; SPINAL CORD;

EID: 78649490837     PISSN: 00796123     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-444-53613-6.00006-X     Document Type: Chapter

References (120)

1. Al-Mosawie A., Wilson J.M., Brownstone R.M. Heterogeneity of V2-derived interneurons in the adult mouse spinal cord. The European Journal of Neuroscience 2007, 26:3003-3015.
2. Alvarez F.J., Fyffe R.E. The continuing case for the Renshaw cell. The Journal of Physiology 2007, 584:31-45.
3. Alvarez F.J., Jonas P.C., Sapir T., Hartley R., Berrocal M.C., Geiman E.J., et al. Postnatal phenotype and localization of spinal cord V1 derived interneurons. The Journal of Comparative Neurology 2005, 493:177-192.
4. Angel M.J., Jankowska E., Mccrea D.A. Candidate interneurones mediating group I disynaptic EPSPs in extensor motoneurones during fictive locomotion in the cat. The Journal of Physiology 2005, 563:597-610.
5. Arya T., Bajwa S., Edgley S.A. Crossed reflex actions from group II muscle afferents in the lumbar spinal cord of the anaesthetized cat. The Journal of Physiology 1991, 444:117-131.
6. Bannatyne B.A., Liu T.T., Hammar I., Stecina K., Jankowska E., Maxwell D.J. Excitatory and inhibitory intermediate zone interneurons in pathways from feline group I and II afferents: Differences in axonal projections and input. The Journal of Physiology 2009, 587:379-399.
7. Barber R.P., Phelps P.E., Houser C.R., Crawford G.D., Salvaterra P.M., Vaughn J.E. The morphology and distribution of neurons containing choline acetyltransferase in the adult rat spinal cord: An immunocytochemical study. The Journal of Comparative Neurology 1984, 229:329-346.
8. Brink E., Jankowska E., Mccrea D.A., Skoog B. Inhibitory interactions between interneurones in reflex pathways from group Ia and group Ib afferents in the cat. The Journal of Physiology 1983, 343:361-373.
9. Brown T. The intrinsic factors in the act of progression in the mammal. Proceedings of the Royal Society of London. Series B 1911, 84:308-319.
10. Brown T.G. On the nature of the fundamental activity of the nervous centres; together with an analysis of the conditioning of rhythmic activity in progression, and a theory of the evolution of function in the nervous system. The Journal of Physiology 1914, 48:18-46.
11. Brownstone R.M., Jordan L.M., Kriellaars D.J., Noga B.R., Shefchyk S.J. On the regulation of repetitive firing in lumbar motoneurones during fictive locomotion in the cat. Experimental Brain Research 1992, 90:441-455.
12. Brownstone R.M., Noga B.R., Jordan L.M. Convergence of excitatory Ib and descending locomotor pathways in the cat. Society for Neuroscience Abstracts 1992, 18:315. Abstract.
13. Brownstone R.M., Wilson J.M. Strategies for delineating spinal locomotor rhythm-generating networks and the possible role of Hb9 interneurones in rhythmogenesis. Brain Research Reviews 2008, 57:64-76.
14. Bui T.V., Grande G., Rose P.K. Multiple modes of amplification of synaptic inhibition to motoneurons by persistent inward currents. Journal of Neurophysiology 2008, 99:571-582.
15. Burke R.E., Degtyarenko A.M., Simon E.S. Patterns of locomotor drive to motoneurons and last-order interneurons: Clues to the structure of the CPG. Journal of Neurophysiology 2001, 86:447-462.
16. Carr P.A., Pearson J.C., Fyffe R.E. Distribution of 5-hydroxytryptamine-immunoreactive boutons on immunohistochemically-identified Renshaw cells in cat and rat lumbar spinal cord. Brain Research 1999, 823:198-201.
17. Cavallari P., Edgley S.A., Jankowska E. Post-synaptic actions of midlumbar interneurones on motoneurones of hind-limb muscles in the cat. The Journal of Physiology 1987, 389:675-689.
18. Chalfie M., Tu Y., Euskirchen G., Ward W.W., Prasher D.C. Green fluorescent protein as a marker for gene expression. Science 1994, 263:802-805.
19. Cowley K.C., Schmidt B.J. Effects of inhibitory amino acid antagonists on reciprocal inhibitory interactions during rhythmic motor activity in the in vitro neonatal rat spinal cord. Journal of Neurophysiology 1995, 74:1109-1117.
20. Cowley K.C., Zaporozhets E., Joundi R.A., Schmidt B.J. Contribution of commissural projections to bulbospinal activation of locomotion in the in vitro neonatal rat spinal cord. Journal of Neurophysiology 2009, 101:1171-1178.
21. Creed R.S., Denny-Brown D., Eccles J.C., Liddell E.G.T., Sherrington C.S. Reflex Activity of the Spinal Cord 1932, Oxford University Press, Oxford.
22. Crone S.A., Quinlan K.A., Zagoraiou L., Droho S., Restrepo C.E., Lundfald L., et al. Genetic ablation of V2a ipsilateral interneurons disrupts left-right locomotor coordination in mammalian spinal cord. Neuron 2008, 60:70-83.
23. Crone S.A., Zhong G., Harris-Warrick R., Sharma K. In mice lacking V2a interneurons, gait depends on speed of locomotion. The Journal of Neuroscience 2009, 29:7098-7109.
24. Davies H.E., Edgley S.A. Inputs to group II-activated midlumbar interneurones from descending motor pathways in the cat. The Journal of Physiology 1994, 479(Pt 3):463-473.
25. Duenas S.H., Rudomin P. Excitability changes of ankle extensor group Ia and Ib fibers during fictive locomotion in the cat. Experimental Brain Research 1988, 70:15-25.
26. Dyck J., Gosgnach S. Whole cell recordings from visualized neurons in the inner laminae of the functionally intact spinal cord. Journal of Neurophysiology 2009, 102:590-597.
27. Eccles J., Fatt P., Koketsu K. Cholinergic and inhibitory synapses in a pathway from motor-axon collaterals to motoneurones. The Journal of Physiology 1954, 126:524-562.
28. Eccles R.M., Lundberg A. Integrative pattern of Ia synaptic actions on motoneurones of hip and knee muscles. The Journal of Physiology 1958, 144:271-298.
29. Edgley S.A., Jankowska E. An interneuronal relay for group I and II muscle afferents in the midlumbar segments of the cat spinal cord. The Journal of Physiology 1987, 389:647-674.
30. Edgley S.A., Jankowska E., Shefchyk S. Evidence that mid-lumbar neurones in reflex pathways from group II afferents are involved in locomotion in the cat. The Journal of Physiology 1988, 403:57-71.
31. Engberg I., Lundberg A., Ryall R.W. Reticulospinal inhibition of transmission in reflex pathways. The Journal of Physiology 1968, 194:201-223.
32. Feldman A.G., Orlovsky G.N. Activity of interneurons mediating reciprocal 1a inhibition during locomotion. Brain Research 1975, 84:181-194.
33. Friedman W.A., Sypert G.W., Munson J.B., Fleshman J.W. Recurrent inhibition in type-identified motoneurons. Journal of Neurophysiology 1981, 46:1349-1359.
34. Geiman E.J., Zheng W., Fritschy J.M., Alvarez F.J. Glycine and GABA(A) receptor subunits on Renshaw cells: Relationship with presynaptic neurotransmitters and postsynaptic gephyrin clusters. The Journal of Comparative Neurology 2002, 444:275-289.
35. Gosgnach S., Lanuza G.M., Butt S.J., Saueressig H., Zhang Y., Velasquez T., et al. V1 spinal neurons regulate the speed of vertebrate locomotor outputs. Nature 2006, 440:215-219.
36. Gossard J.P. Control of transmission in muscle group IA afferents during fictive locomotion in the cat. Journal of Neurophysiology 1996, 76:4104-4112.
37. Gossard J.P., Brownstone R.M., Barajon I., Hultborn H. Transmission in a locomotor-related group Ib pathway from hindlimb extensor muscles in the cat. Experimental Brain Research 1994, 98:213-228.
38. Gossard J.P., Cabelguen J.M., Rossignol S. Intra-axonal recordings of cutaneous primary afferents during fictive locomotion in the cat. Journal of Neurophysiology 1989, 62:1177-1188.
39. Goulding M. Circuits controlling vertebrate locomotion: Moving in a new direction. Nature Reviews. Neuroscience 2009, 10:507-518.
40. Grillner S. Biological pattern generation: The cellular and computational logic of networks in motion. Neuron 2006, 52:751-766.
41. Grillner S., Wallen P., Saitoh K., Kozlov A., Robertson B. Neural bases of goal-directed locomotion in vertebrates-an overview. Brain Research Reviews 2008, 57:2-12.
42. Heckman C.J., Hyngstrom A.S., Johnson M.D. Active properties of motoneurone dendrites: Diffuse descending neuromodulation, focused local inhibition. The Journal of Physiology 2008, 586:1225-1231.
43. Hultborn H. Spinal reflexes, mechanisms and concepts: From Eccles to Lundberg and beyond. Progress in Neurobiology 2006, 78:215-232.
44. Hultborn H., Brownstone R.B., Toth T.I., Gossard J.P. Key mechanisms for setting the input-output gain across the motoneuron pool. Progress in Brain Research 2004, 143:77-95.
45. Hultborn H., Denton M.E., Wienecke J., Nielsen J.B. Variable amplification of synaptic input to cat spinal motoneurones by dendritic persistent inward current. The Journal of Physiology 2003, 552:945-952.
46. Hultborn H., Illert M., Santini M. Convergence on interneurones mediating the reciprocal Ia inhibition of motoneurones. I. Disynaptic Ia inhibition of Ia inhibitory interneurones. Acta Physiologica Scandinavica 1976, 96:193-201.
47. Hultborn H., Illert M., Santini M. Convergence on interneurones mediating the reciprocal Ia inhibition of motoneurones. II. Effects from segmental flexor reflex pathways. Acta Physiologica Scandinavica 1976, 96:351-367.
48. Hultborn H., Illert M., Santini M. Convergence on interneurones mediating the reciprocal Ia inhibition of motoneurones. III. Effects from supraspinal pathways. Acta Physiologica Scandinavica 1976, 96:368-391.
49. Hultborn H., Jankowska E., Lindstrom S. Recurrent inhibition from motor axon collaterals of transmission in the Ia inhibitory pathway to motoneurones. The Journal of Physiology 1971, 215:591-612.
50. Hultborn H., Nielsen J.B. Spinal control of locomotion-from cat to man. Acta Physiologica (Oxford) 2007, 189:111-121.
51. Hultborn H., Pierrot-Deseilligny E. Input-output relations in the pathway of recurrent inhibition to motoneurones in the cat. The Journal of Physiology 1979, 297:267-287.
52. Hyngstrom A.S., Johnson M.D., Miller J.F., Heckman C.J. Intrinsic electrical properties of spinal motoneurons vary with joint angle. Nature Neuroscience 2007, 10:363-369.
53. Hyngstrom A., Johnson M., Schuster J., Heckman C.J. Movement-related receptive fields of spinal motoneurones with active dendrites. The Journal of Physiology 2008, 586:1581-1593.
54. Jankowska E. Interneuronal relay in spinal pathways from proprioceptors. Progress in Neurobiology 1992, 38:335-378.
55. Jankowska E. Spinal interneuronal networks in the cat: elementary components. Brain Research Reviews 2008, 57:46-55.
56. Jankowska E., Bannatyne B.A., Stecina K., Hammar I., Cabaj A., Maxwell D.J. Commissural interneurons with input from group I and II muscle afferents in feline lumbar segments: Neurotransmitters, projections and target cells. The Journal of Physiology 2009, 587:401-418.
57. Jankowska E., Hammar I., Slawinska U., Maleszak K., Edgley S.A. Neuronal basis of crossed actions from the reticular formation on feline hindlimb motoneurons. The Journal of Neuroscience 2003, 23:1867-1878.
58. Jankowska E., Jukes M.G., Lund S., Lundberg A. The effect of DOPA on the spinal cord. 5. Reciprocal organization of pathways transmitting excitatory action to alpha motoneurones of flexors and extensors. Acta Physiologica Scandinavica 1967, 70:369-388.
59. Jankowska E., Mccrea D., Mackel R. Pattern of 'non-reciprocal' inhibition of motoneurones by impulses in group Ia muscle spindle afferents in the cat. The Journal of Physiology 1981, 316:393-409.
60. Jankowska E., Roberts W.J. An electrophysiological demonstration of the axonal projections of single spinal interneurones in the cat. The Journal of Physiology 1972, 222:597-622.
61. Jessell T.M. Neuronal specification in the spinal cord: Inductive signals and transcriptional codes. Nature Reviews. Genetics 2000, 1:20-29.
62. Jiang Z., Carlin K.P., Brownstone R.M. An in vitro functionally mature mouse spinal cord preparation for the study of spinal motor networks. Brain Research 1999, 816:493-499.
63. Jordan L.M. Factors determining motoneuron rhythmicity during fictive locomotion. Symposia of the Society for Experimental Biology 1983, 37:423-444.
64. Joshi K., Lee S., Lee B., Lee J.W., Lee S.K. LMO4 controls the balance between excitatory and inhibitory spinal V2 interneurons. Neuron 2009, 61:839-851.
65. Kiehn O. Locomotor circuits in the mammalian spinal cord. Annual Review of Neuroscience 2006, 29:279-306.
66. Kiehn O., Quinlan K.A., Restrepo C.E., Lundfald L., Borgius L., Talpalar A.E., Endo T. Excitatory components of the mammalian locomotor CPG. Brain Research Review 2008, 57:56-63.
67. Krutki P., Jankowska E., Edgley S.A. Are crossed actions of reticulospinal and vestibulospinal neurons on feline motoneurons mediated by the same or separate commissural neurons?. The Journal of Neuroscience 2003, 23:8041-8050.
68. Kuo J.J., Lee R.H., Johnson M.D., Heckman H.M., Heckman C.J. Active dendritic integration of inhibitory synaptic inputs in vivo. Journal of Neurophysiology 2003, 90:3617-3624.
69. Labella L.A., Niechaj A., Rossignol S. Low-threshold, short-latency cutaneous reflexes during fictive locomotion in the "semi-chronic" spinal cat. Experimental Brain Research 1992, 91:236-248.
70. Lamotte D'incamps B., Ascher P. Four excitatory postsynaptic ionotropic receptors coactivated at the motoneuron-Renshaw cell synapse. The Journal of Neuroscience 2008, 28:14121-14131.
71. Lanuza G.M., Gosgnach S., Pierani A., Jessell T.M., Goulding M. Genetic identification of spinal interneurons that coordinate left-right locomotor activity necessary for walking movements. Neuron 2004, 42:375-386.
72. Laporte Y., Lloyd D.P. Nature and significance of the reflex connections established by large afferent fibers of muscular origin. The American Journal of Physiology 1952, 169:609-621.
73. Lundberg A., Malmgren K., Schomburg E.D. Comments on reflex actions evoked by electrical stimulation of group II muscle afferents. Brain Research 1977, 122:551-555.
74. Lundberg A., Malmgren K., Schomburg E.D. Reflex pathways from group II muscle afferents. 1. Distribution and linkage of reflex actions to alpha-motoneurones. Experimental Brain Research 1987, 65:271-281.
75. Lundfald L., Restrepo C.E., Butt S.J., Peng C.Y., Droho S., Endo T., et al. Phenotype of V2-derived interneurons and their relationship to the axon guidance molecule EphA4 in the developing mouse spinal cord. The European Journal of Neuroscience 2007, 26:2989-3002.
76. Luscher H.R., Ruenzel P., Fetz E., Henneman E. Postsynaptic population potentials recorded from ventral roots perfused with isotonic sucrose: Connections of groups Ia and II spindle afferent fibers with large populations of motoneurons. Journal of Neurophysiology 1979, 42:1146-1164.
77. Maltenfort M.G., Heckman C.J., Rymer W.Z. Decorrelating actions of Renshaw interneurons on the firing of spinal motoneurons within a motor nucleus: A simulation study. Journal of Neurophysiology 1998, 80:309-323.
78. Manuel M., Iglesias C., Donnet M., Leroy F., Heckman C.J., Zytnicki D. Fast kinetics, high-frequency oscillations, and subprimary firing range in adult mouse spinal motoneurons. The Journal of Neuroscience 2009, 29:11246-11256.
79. Marder E., Bucher D. Understanding circuit dynamics using the stomatogastric nervous system of lobsters and crabs. Annual Review of Physiology 2007, 69:291-316.
80. Matsuyama K., Nakajima K., Mori F., Aoki M., Mori S. Lumbar commissural interneurons with reticulospinal inputs in the cat: Morphology and discharge patterns during fictive locomotion. The Journal of Comparative Neurology 2004, 474:546-561.
81. Mccrea D.A., Pratt C.A., Jordan L.M. Renshaw cell activity and recurrent effects on motoneurons during fictive locomotion. Journal of Neurophysiology 1980, 44:475-488.
82. Mccrea D.A., Shefchyk S.J., Stephens M.J., Pearson K.G. Disynaptic group I excitation of synergist ankle extensor motoneurones during fictive locomotion in the cat. The Journal of Physiology 1995, 487(Pt 2):527-539.
83. Mccurdy M.L., Hamm T.M. Topography of recurrent inhibitory postsynaptic potentials between individual motoneurons in the cat. Journal of Neurophysiology 1994, 72:214-226.
84. Mentis G.Z., Siembab V.C., Zerda R., O'donovan M.J., Alvarez F.J. Primary afferent synapses on developing and adult Renshaw cells. The Journal of Neuroscience 2006, 26:13297-13310.
85. Miles G.B., Hartley R., Todd A.J., Brownstone R.M. Spinal cholinergic interneurons regulate the excitability of motoneurons during locomotion. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:2448-2453.
86. Moschovakis A.K., Sholomenko G.N., Burke R.E. Differential control of short latency cutaneous excitation in cat FDL motoneurons during fictive locomotion. Experimental Brain Research 1991, 83:489-501.
87. Naka K.I. Electrophysiology of the fetal spinal cord. Ii. interaction among peripheral inputs and recurrent inhibition. The Journal of General Physiology 1964, 47:1023-1038.
88. Nishimaru H., Koganezawa T., Kakizaki M., Ebihara T., Yanagawa Y. Inhibitory Synaptic Modulation of Renshaw Cell Activity in the Lumbar Spinal Cord of Neonatal Mice. The Journal of Neurophysiology 2010, 103:3437-3447.
89. Nishimaru H., Restrepo C.E., Kiehn O. Activity of Renshaw cells during locomotor-like rhythmic activity in the isolated spinal cord of neonatal mice. The Journal of Neuroscience 2006, 26:5320-5328.
90. Noga B.R., Kriellaars D.J., Brownstone R.M., Jordan L.M. Mechanism for activation of locomotor centers in the spinal cord by stimulation of the mesencephalic locomotor region. Journal of Neurophysiology 2003, 90:1464-1478.
91. Noga B.R., Shefchyk S.J., Jamal J., Jordan L.M. The role of Renshaw cells in locomotion: Antagonism of their excitation from motor axon collaterals with intravenous mecamylamine. Experimental Brain Research 1987, 66:99-105.
92. Perreault M.C., Shefchyk S.J., Jimenez I., Mccrea D.A. Depression of muscle and cutaneous afferent-evoked monosynaptic field potentials during fictive locomotion in the cat. The Journal Of Physiology 1999, 521(Pt 3):691-703.
93. Perret C. Centrally generated pattern of motoneuron activity during locomotion in the cat. Symposia of the Society for Experimental Biology 1983, 37:405-422.
94. Perrier J.F., D'incamps B.L., Kouchtir-Devanne N., Jami L., Zytnicki D. Cooperation of muscle and cutaneous afferents in the feedback of contraction to peroneal motoneurons. Journal of Neurophysiology 2000, 83:3201-3208.
95. Pratt C.A., Jordan L.M. Ia inhibitory interneurons and Renshaw cells as contributors to the spinal mechanisms of fictive locomotion. Journal of Neurophysiology 1987, 57:56-71.
96. Quevedo J., Stecina K., Gosgnach S., Mccrea D.A. Stumbling corrective reaction during fictive locomotion in the cat. Journal of Neurophysiology 2005, 94:2045-2052.
97. Quinlan K.A., Kiehn O. Segmental, synaptic actions of commissural interneurons in the mouse spinal cord. The Journal of Neuroscience 2007, 27:6521-6530.
98. Renshaw B. Influence of discharge of motoneurons upon excitation of neighbouring motoneurons. Journal of Neurophysiology 1941, 4:167-183.
99. Renshaw B. Central effects of centripetal impulses in axons of spinal ventral roots. Journal of Neurophysiology 1946, 9:191-204.
100. Riddell J.S., Hadian M. Interneurones in pathways from group II muscle afferents in the lower-lumbar segments of the feline spinal cord. The Journal Of Physiology 2000, 522(Pt 1):109-123.
101. Ryall R.W. Renshaw cell mediated inhibition of Renshaw cells: Patterns of excitation and inhibition from impulses in motor axon collaterals. Journal of Neurophysiology 1970, 33:257-270.
102. Sapir T., Geiman E.J., Wang Z., Velasquez T., Mitsui S., Yoshihara Y., et al. Pax6 and engrailed 1 regulate two distinct aspects of Renshaw cell development. The Journal of Neuroscience 2004, 24:1255-1264.
103. Schneider S.P., Fyffe R.E. Involvement of GABA and glycine in recurrent inhibition of spinal motoneurons. Journal of Neurophysiology 1992, 68:397-406.
104. Shefchyk S.J., Jordan L.M. Excitatory and inhibitory postsynaptic potentials in alpha-motoneurons produced during fictive locomotion by stimulation of the mesencephalic locomotor region. Journal of Neurophysiology 1985, 53:1345-1355.
105. Shefchyk S., Mccrea D., Kriellaars D., Fortier P., Jordan L. Activity of interneurons within the L4 spinal segment of the cat during brainstem-evoked fictive locomotion. Experimental Brain Research 1990, 80:290-295.
106. Stauffer E.K., Watt D.G., Taylor A., Reinking R.M., Stuart D.G. Analysis of muscle receptor connections by spike-triggered averaging. 2. Spindle group II afferents. Journal of Neurophysiology 1976, 39:1393-1402.
107. Stuart D.G. Integration of posture and movement: Contributions of Sherrington, Hess, and Bernstein. Human Movement Science 2005, 24:621-643.
108. Trank T.V., Turkin V.V., Hamm T.M. Organization of recurrent inhibition and facilitation in motoneuron pools innervating dorsiflexors of the cat hindlimb. Experimental Brain Research 1999, 125:344-352.
109. Wang Z., Li L., Goulding M., Frank E. Early postnatal development of reciprocal Ia inhibition in the murine spinal cord. Journal of Neurophysiology 2008, 100:185-196.
110. Weber I., Puskar Z., Kozak N., Antal M. Projections of primary afferent fibers to last-order premotor interneurons in the lumbar spinal cord of rats. Brain Research Bulletin 2007, 71:337-343.
111. Westberg K.G., Kolta A., Clavelou P., Sandstrom G., Lund J.P. Evidence for functional compartmentalization of trigeminal muscle spindle afferents during fictive mastication in the rabbit. The European Journal of Neuroscience 2000, 12:1145-1154.
112. Wilson J.M., Blagovechtchenski E., Brownstone R.M. Genetically defined inhibitory neurons in the mouse spinal cord dorsal horn: A possible source of rhythmic inhibition of motoneurons during fictive locomotion. The Journal of Neuroscience 2010, 30:1137-1148.
113. Wilson J.M., Dombeck D.A., Diaz-Rios M., Harris-Warrick R.M., Brownstone R.M. Two-photon calcium imaging of network activity in XFP-expressing neurons in the mouse. Journal of Neurophysiology 2007, 97:3118-3125.
114. Windhorst U. On the role of recurrent inhibitory feedback in motor control. Progress in Neurobiology 1996, 49:517-587.
115. Zacharias D.A., Baird G.S., Tsien R.Y. Recent advances in technology for measuring and manipulating cell signals. Current Opinion in Neurobiology 2000, 10:416-421.
116. Zagoraiou L., Akay T., Martin J.F., Brownstone R.M., Jessell T.M., Miles G.B. A cluster of cholinergic premotor interneurons modulates mouse locomotor activity. Neuron 2009, 64:645-662.
117. Zhang F., Aravanis A.M., Adamantidis A., De Lecea L., Deisseroth K. Circuit-breakers: Optical technologies for probing neural signals and systems. Nature Reviews. Neuroscience 2007, 8:577-581.
118. Zhang Y., Narayan S., Geiman E., Lanuza G.M., Velasquez T., Shanks B., et al. V3 spinal neurons establish a robust and balanced locomotor rhythm during walking. Neuron 2008, 60:84-96.
119. Zhong G., Diaz-Rios M., Harris-Warrick R.M. Intrinsic and functional differences among commissural interneurons during fictive locomotion and serotonergic modulation in the neonatal mouse. The Journal of Neuroscience 2006, 26:6509-6517.
120. Zhou Y., Yamamoto M., Engel J.D. GATA2 is required for the generation of V2 interneurons. Development 2000, 127:3829-3838.