Specific brainstem neurons switch each other into pacemaker mode to drive movement by activating NMDA receptors

Journal of Neuroscience

Volumn 30, Issue 49, 2010, Pages 16609-16620

  Li, Wen Chang ^a,b   Roberts, Alan ^b   Soffe, Stephen R ^b  

^a UNIVERSITY OF ST ANDREWS   (United Kingdom)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMIC ACID; MAGNESIUM ION; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL EXPERIMENT; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; DEPOLARIZATION; FORCED SWIMMING TEST; HATCHING; NEUROTRANSMISSION; NONHUMAN; OSCILLATION; PACEMAKER NERVE CELL; PRIORITY JOURNAL; RHOMBENCEPHALON; SPINAL CORD NERVE CELL; TADPOLE; XENOPUS LAEVIS;

2-AMINO-5-PHOSPHONOVALERATE; ACTION POTENTIALS; ANIMALS; BIOLOGICAL CLOCKS; BRAIN STEM; CADMIUM CHLORIDE; DIHYDRO-BETA-ERYTHROIDINE; ELECTRIC STIMULATION; EXCITATORY AMINO ACID ANTAGONISTS; GABA ANTAGONISTS; GLUTAMIC ACID; GLYCYRRHETINIC ACID; HUMANS; LARVA; MODELS, BIOLOGICAL; MOVEMENT; N-METHYLASPARTATE; NEURONS; PATCH-CLAMP TECHNIQUES; PERIODICITY; PYRIDAZINES; QUINOXALINES; RECEPTORS, N-METHYL-D-ASPARTATE; SWIMMING; XENOPUS;

EID: 78650070468     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3695-10.2010     Document Type: Article

References (69)

1. Aiken SP, Kuenzi FM, Dale N (2003) Xenopus embryonic spinal neurons recorded in situ with patch-clamp electrodes - conditional oscillators after all? Eur J Neurosci 18:333-343.
2. Arshavsky YI (2003) Cellular and network properties in the functioning of the nervous system: from central pattern generators to cognition. Brain Res Brain Res Rev 41:229-267.
3. Arshavsky YuI, Gelfand IM, Orlovsky GN, Pavlova GA, Popova LB (1984) Origin of signals conveyed by the ventral spino-cerebellar tract and spino-reticulo- cerebellar pathway. Exp Brain Res 54:426-431.
4. Arshavsky YuI, Orlovsky GN, Panchin Yu V, Roberts A, Soffe SR (1993) Neuronal control of swimming locomotion: analysis of the pteropod mollusc Clione and embryos of the amphibian Xenopus. Trends Neurosci 16:227-233. (Pubitemid 23139187)
5. Atsuta Y, Garcia-Rill E, Skinner RD (1990) Characteristics of electrically induced locomotion in rat in vitro brain stem-spinal cord preparation. J Neurophysiol 64:727-735.
6. Brocard F, Tazerart S, Vinay L (2010) Do pacemakers drive the central pattern generator for locomotion in mammals? Neuroscientist 16:139-155.
7. Brownstone RM, Wilson JM (2008) Strategies for delineating spinal locomotor rhythm-generating networks and the possible role of Hb9 interneurones in rhythmogenesis. Brain Res Rev 57:64-76.
8. Buzsáki G, Draguhn A (2004) Neuronal oscillations in cortical networks. Science 304:1926-1929.
9. Cangiano L, Grillner S (2003) Fast and slow locomotor burst generation in the hemispinal cord of the lamprey. J Neurophysiol 89:2931-2942.
10. Cangiano L, Grillner S (2005) Mechanisms of rhythm generation in a spinal locomotor network deprived of crossed connections: the lamprey hemicord. J Neurosci 25:923-935.
11. Chapman RJ, Issberner JP, Sillar KT (2008) Group I mGluRs increase locomotor network excitability in Xenopus tadpoles via presynaptic inhibition of glycinergic neurotransmission. Eur J Neurosci 28:903-913.
12. Connors BW, Long MA (2004) Electrical synapses in the mammalian brain. Annu Rev Neurosci 27:393-418.
13. Cowley KC, Schmidt BJ (1995) Effects of inhibitory amino acid antagonists on reciprocal inhibitory interactions during rhythmic motor activity in the in vitro neonatal rat spinal cord. J Neurophysiol 74:1109-1117.
14. Cowley KC, Zaporozhets E, Maclean JN, Schmidt BJ (2005) Is NMDA receptor activation essential for the production of locomotor-like activity in the neonatal rat spinal cord? J Neurophysiol 94:3805-3814.
15. Cui WW, Saint-Amant L, Kuwada JY (2004) shocked gene is required for the function of a premotor network in the zebrafish CNS. J Neurophysiol 92:2898-2908.
16. Cui WW, Low SE, Hirata H, Saint-Amant L, Geisler R, Hume RI, Kuwada JY (2005) The zebrafish shocked gene encodes a glycine transporter and is essential for the function of early neural circuits in the CNS. J Neurosci 25:6610-6620.
17. Deister CA, Teagarden MA, Wilson CJ, Paladini CA (2009) An intrinsic neuronal oscillator underlies dopaminergic neuron bursting. J Neurosci 29:15888-15897.
18. Droge MH, Tao Y (1993) Glycine effects on in vitro motor pattern generation in mouse spinal cord. Neurosci Lett 158:139-142.
19. El Manira A, Kettunen P, Hess D, Krieger P (2002) Metabotropic glutamate receptors provide intrinsic modulation of the lamprey locomotor network. Brain Res Brain Res Rev 40:9-18. (Pubitemid 36183154)
20. Feldman JL, Del Negro CA (2006) Looking for inspiration: new perspectives on respiratory rhythm. Nat Rev Neurosci 7:232-242.
21. Ganong AH, Cotman CW (1986) Kynurenic acid and quinolinic acid act at N-methyl-D-aspartate receptors in the rat hippocampus. J Pharmacol Exp Ther 236:293-299.
22. Getting PA (1989) Emerging principles governing the operation of neural networks. Annu Rev Neurosci 12:185-204.
23. Grillner S (2003) The motor infrastructure: from ion channels to neuronal networks. Nat Rev Neurosci 4:573-586.
24. Grillner S, Wallén P (1985) The ionic mechanisms underlying N-methyl-Daspartate receptor-induced, tetrodotoxin-resistant membrane potential oscillations in lamprey neurons active during locomotion. Neurosci Lett 60:289-294.
25. Guertin PA (2009) The mammalian central pattern generator for locomotion. Brain Res Rev 62:45-56.
26. Guertin PA, Hounsgaard J (1998) NMDA-induced intrinsic voltage oscillations depend on L-type calcium channels in spinal motoneurons of adult turtles. J Neurophysiol 80:3380-3382.
27. Harris-Warrick RM (2002) Voltage-sensitive ion channels in rhythmic motor systems. Curr Opin Neurobiol 12:646-651.
28. Hochman S, Jordan LM, MacDonald JF (1994a) N-Methyl-D-aspartate receptor-mediated voltage oscillations in neurons surrounding the central canal in slices of rat spinal cord. J Neurophysiol 72:565-577.
29. Hochman S, Jordan LM, Schmidt BJ (1994b) TTX-resistant NMDA receptor-mediated voltage oscillations in mammalian lumbar motoneurons. J Neurophysiol 72:2559-2562. (Pubitemid 24362650)
30. Kahn JA, Roberts A (1982) Experiments on the central pattern generator for swimming in amphibian embryos. Philos Trans R Soc Lond B Biol Sci 296:229-243.
31. Kahn JA, Roberts A, Kashin SM (1982) The neuromuscular basis of swimming movements in embryos of the amphibian Xenopus laevis. J Exp Biol 99:175-184.
32. Katz PS, Frost WN (1996) Intrinsic neuromodulation: altering neuronal circuits from within. Trends Neurosci 19:54-61.
33. Kiehn O, Tresch MC (2002) Gap junctions and motor behavior. Trends Neurosci 25:108-115.
34. Kremer E, Lev-Tov A (1997) Localization of the spinal network associated with generation of hindlimb locomotion in the neonatal rat and organization of its transverse coupling system. J Neurophysiol 77:1155-1170.
35. 2+ in rat phaeochromocytoma cells. J Physiol 466:683-706.
36. Kwan AC, Dietz SB, Webb WW, Harris-Warrick RM (2009) Activity of Hb9 interneurons during fictive locomotion in mouse spinal cord. J Neurosci 29:11601-11613.
37. Li WC, Soffe SR, Roberts A (2002) Spinal inhibitory neurons that modulate cutaneous sensory pathways during locomotion in a simple vertebrate. J Neurosci 22:10924-10934.
38. Li WC, Soffe SR, Roberts A (2004) Glutamate and acetylcholine corelease at developing synapses. Proc Natl Acad Sci U S A 101:15488-15493.
39. Li WC, Soffe SR, Wolf E, Roberts A (2006) Persistent responses to brief stimuli: feedback excitation among brainstem neurons. J Neurosci 26:4026-4035.
40. Li WC, Roberts A, Soffe SR (2009) Locomotor rhythm maintenance: electrical coupling among premotor excitatory interneurons in the brainstem and spinal cord of young Xenopus tadpoles. J Physiol 587:1677-1693.
41. Lieske SP, Ramirez JM (2006) Pattern-specific synaptic mechanisms in a multifunctional network. II. Intrinsic modulation by metabotropic glutamate receptors. J Neurophysiol 95:1334-1344.
42. MacLean JN, Schmidt BJ, Hochman S (1997) NMDA receptor activation triggers voltage oscillations, plateau potentials and bursting in neonatal rat lumbar motoneurons in vitro. Eur J Neurosci 9:2702-2711.
43. Marder E, Bucher D (2007) Understanding circuit dynamics using the stomatogastric nervous system of lobsters and crabs. Annu Rev Physiol 69:291-316.
44. Marder E, Bucher D, Schulz DJ, Taylor AL (2005) Invertebrate central pattern generation moves along. Curr Biol 15:R685-R699.
45. 2+ of NMDA responses in spinal cord neurones. Nature 309:261-263.
46. Nieuwkoop PD, Faber J (1956) Normal tables of Xenopus laevis (Daudin). Amsterdam: North Holland.
47. Noga BR, Kriellaars DJ, Jordan LM (1991) The effect of selective brainstem or spinal cord lesions on treadmill locomotion evoked by stimulation of the mesencephalic or pontomedullary locomotor regions. J Neurosci 11:1691-1700.
48. Ozaki S, Yamada T, Iizuka M, Nishimaru H, Kudo N (1996) Development of locomotor activity induced by NMDA receptor activation in the lumbar spinal cord of the rat fetus studied in vitro. Brain Res Dev Brain Res 97:118-125.
49. Prime L, Pichon Y, Moore LE (1999) N-Methyl-D-aspartate-induced oscillations in whole cell clamped neurons from the isolated spinal cord of Xenopus laevis embryos. J Neurophysiol 82:1069-1073.
50. Ramirez JM, Tryba AK, Peña F (2004) Pacemaker neurons and neuronal networks: an integrative view. Curr Opin Neurobiol 14:665-674.
51. Reith CA, Sillar KT (1998) A role for slow NMDA receptor-mediated, intrinsic neuronal oscillations in the control of fast fictive swimming in Xenopus laevis larvae. Eur J Neurosci 10:1329-1340.
52. Rioult-Pedotti MS (1997) Intrinsic NMDA-induced oscillations in motoneurons of an adult vertebrate spinal cord are masked by inhibition. J Neurophysiol 77:717-730.
53. Roberts A, Li WC, Soffe SR, Wolf E (2008) Origin of excitatory drive to a spinal locomotor network. Brain Res Rev 57:22-28.
54. Sakurai A, Katz PS (2003) Spike timing-dependent serotonergic neuromodulation of synaptic strength intrinsic to a central pattern generator circuit. J Neurosci 23:10745-10755. (Pubitemid 37499680)
55. Samara RF, Currie SN (2008) Electrically evoked locomotor activity in the turtle spinal cord hemi-enlargement preparation. Neurosci Lett 441:105-109.
56. Sautois B, Soffe SR, Li WC, Roberts A (2007) Role of type-specific neuron properties in a spinal cord motor network. J Comput Neurosci 23:59-77.
57. Sillar KT, Simmers AJ (1994) Electrical coupling and intrinsic neuronal oscillations in Rana temporaria spinal cord. Eur J Morphol 32:293-298.
58. Soffe SR (1989) Roles of glycinergic inhibition and N-methyl-D-aspartate receptor mediated excitation in the locomotor rhythmicity of one half of the Xenopus embryo central nervous system. Eur J Neurosci 1:561-571.
59. Soffe SR, Roberts A (1989) The influence of magnesium ions on the NMDA mediated responses of ventral rhythmic neurons in the spinal cord of Xenopus embryos. Eur J Neurosci 1:507-515.
60. Soffe SR, Roberts A, Li WC (2009) Defining the excitatory neurons that drive the locomotor rhythm in a simple vertebrate: insights into the origin of reticulospinal control. J Physiol 587:4829-4844.
61. Soto-Treviño C, Rabbah P, Marder E, Nadim F (2005) Computational model of electrically coupled, intrinsically distinct pacemaker neurons. J Neurophysiol 94:590-604.
62. Stein PS, McCullough ML, Currie SN (1998) Reconstruction of flexor/extensor alternation during fictive rostral scratching by two-site stimulation in the spinal turtle with a transverse spinal hemisection. J Neurosci 18:467-479.
63. Tazerart S, Vinay L, Brocard F (2008) The persistent sodium current generates pacemaker activities in the central pattern generator for locomotion and regulates the locomotor rhythm. J Neurosci 28:8577-8589.
64. Thörn Pérez C, Hill RH, El Manira A, Grillner S (2009) Endocannabinoids mediate tachykinin-induced effects in the lamprey locomotor network. J Neurophysiol 102:1358-1365.
65. Tresch MC, Kiehn O (2000) Motor coordination without action potentials in the mammalian spinal cord. Nat Neurosci 3:593-599.
66. Wallén P, Grillner S (1985) The effect of current passage on N-methyl-Daspartate-induced, tetrodotoxin-resistant membrane potential oscillations in lamprey neurons active during locomotion. Neurosci Lett 56:87-93.
67. Wallén P, Grillner S (1987) N-Methyl-D-aspartate receptor-induced, inherent oscillatory activity in neurons active during fictive locomotion in the lamprey. J Neurosci 7:2745-2755.
68. Wilson JM, Hartley R, Maxwell DJ, Todd AJ, Lieberam I, Kaltschmidt JA, Yoshida Y, Jessell TM, Brownstone RM (2005) Conditional rhythmicity of ventral spinal interneurons defined by expression of the Hb9 homeodomain protein. J Neurosci 25:5710-5719.
69. Ziskind-Conhaim L, Wu L, Wiesner EP (2008) Persistent sodium current contributes to induced voltage oscillations in locomotor-related hb9 interneurons in the mouse spinal cord. J Neurophysiol 100:2254-2264.