The persistent sodium current generates pacemaker activities in the central pattern generator for locomotion and regulates the locomotor rhythm

Journal of Neuroscience

Volumn 28, Issue 34, 2008, Pages 8577-8589

  Tazerart, Sabrina ^a   Vinay, Laurent ^a   Brocard, Frédéric ^a,b  

^a AIX MARSEILLE UNIVERSITY   (France)

^b CNRS   (France)

Author keywords

Central pattern generator; Locomotion; Neonatal rat; Rhythm; Riluzole; Spinal cord

Indexed keywords

RILUZOLE; VERATRIDINE; CALCIUM; ENHANCED GREEN FLUORESCENT PROTEIN; FLUORESCENT DYE; GREEN FLUORESCENT PROTEIN; HOMEODOMAIN PROTEIN; SODIUM CHANNEL;

ANIMAL TISSUE; ARTICLE; CELL BURSTING; CELL DAMAGE; CONTROLLED STUDY; EXTRACELLULAR CALCIUM; INTERNEURON; ISOLATED ORGAN; LOCOMOTION; MOUSE; NERVE CELL NETWORK; NEWBORN; NONHUMAN; PACEMAKER; PACEMAKER NERVE CELL; PRIORITY JOURNAL; RAT; SODIUM CURRENT; SPINAL CORD; SYNAPSE; ANIMAL; BIOLOGICAL RHYTHM; CYTOLOGY; DRUG EFFECT; ELECTROPHYSIOLOGY; EXTRACELLULAR SPACE; GENETICS; IN VITRO STUDY; METABOLISM; PERIODICITY; PHYSIOLOGY; TRANSGENIC MOUSE; WISTAR RAT;

ANIMALS; ANIMALS, NEWBORN; BIOLOGICAL CLOCKS; CALCIUM; ELECTROPHYSIOLOGY; EXTRACELLULAR SPACE; FLUORESCENT DYES; GREEN FLUORESCENT PROTEINS; HOMEODOMAIN PROTEINS; INTERNEURONS; LOCOMOTION; MICE; MICE, TRANSGENIC; PERIODICITY; RATS; RATS, WISTAR; SODIUM CHANNELS; SPINAL CORD; VERATRIDINE;

EID: 51649091712     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1437-08.2008     Document Type: Article

References (79)

1. Alkadhi KA, Tian LM (1996) Veratridine-enhanced persistent sodium current induces bursting in CA1 pyramidal neurons. Neuroscience 71:625-632.
2. Amzica F, Massimini M, Manfridi A (2002) Spatial buffering during slow and paroxysmal sleep oscillations in cortical networks of glial cells in vivo. J Neurosci 22:1042-1053.
3. Arshavsky YI (2003) Cellular and network properties in the functioning of the nervous system: from central pattern generators to cognition. Brain Res Rev 41:229-267.
4. Azouz R, Alroy G, Yaari Y (1997) Modulation of endogenous firing patterns by osmolarity in rat hippocampal neurones. J Physiol 502:175-187.
5. Ballerini L, Bracci E, Nistri A (1997) Pharmacological block of the electrogenic sodium pump disrupts rhythmic bursting induced by strychnine and bicuculline in the neonatal rat spinal cord. J Neurophysiol 77:17-23.
6. Barrière G, Mellen N, Cazalets JR (2004) Neuromodulation of the locomotor network by dopamine in the isolated spinal cord of newborn rat. Eur J Neurosci 19:1325-1335.
7. Bennett MV, Zukin RS (2004) Electrical coupling and neuronal synchronization in the mammalian brain. Neuron 41:495-511.
8. Bertil Hille (2001) Ion channels of excitable membranes. Sunderland, MA: Sinauer.
9. 2+ model of epilepti-form activity. J Neurophysiol 82:2262-2270.
10. Brocard F, Vinay L, Clarac F (1999) Gradual development of the ventral funiculus input to lumbar motoneurons in the neonatal rat. Neuroscience 90:1543-1554.
11. Brocard F, Verdier D, Arsenault I, Lund JP, Kolta A (2006) Emergence of intrinsic bursting in trigeminal sensory neurons parallels the acquisition of mastication in weanling rats. J Neurophysiol 96:2410-2424.
12. 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.
13. Butera RJ Jr, Rinzel J, Smith JC (1999) Models of respiratory rhythm generation in the pre-Botzinger complex. I. Bursting pacemaker neurons. J Neurophysiol 82:382-397.
14. Butt SJ, Kiehn O (2003) Functional identification of interneurons responsible for left-right coordination of hindlimbs in mammals. Neuron 38:953-963.
15. Carlin KP, Dai Y, Jordan LM (2006) Cholinergic and serotonergic excitation of ascending commissural neurons in the thoraco-lumbar spinal cord of the neonatal mouse. J Neurophysiol 95:1278-1284.
16. Cazalets JR, Borde M, Clarac F (1995) Localization and organization of the central pattern generator for hindlimb locomotion in newborn rat. J Neurosci 15:4943-4951.
17. Cazalets JR, Sqalli-Houssaini Y, Magoul R (1999) Differential effects of potassium channel blockers on the activity of the locomotor network in neonatal rat. Brain Res 827:185-197.
18. + channel expression and function in rat Purkinje neurons. J Neurosci 22:4456-4467.
19. Crill WE (1996) Persistent sodium current in mammalian central neurons. Annu Rev Physiol 58:349-362.
20. Darbon P, Tscherter A, Yvon C, Streit J (2003) Role of the electrogenic Na/K pump in disinhibition-induced bursting in cultured spinal networks. J Neurophysiol 90:3119-3129.
21. NaP underlies intrinsic spiking and rhythm generation in networks of cultured rat spinal cord neurons. Eur J Neurosci 20:976-988.
22. Del Negro CA, Koshiya N, Butera RJ Jr, Smith JC (2002) Persistent sodium current, membrane properties and bursting behavior of pre-Botzinger complex inspiratory neurons in vitro. J Neurophysiol 88:2242-2250.
23. Del Negro CA, Morgado-Valle C, Hayes JA, Mackay DD, Pace RW, Crowder EA, Feldman JL (2005) Sodium and calcium current-mediated pacemaker neurons and respiratory rhythm generation. J Neurosci 25:446-453.
24. Gao BX, Stricker C, Ziskind-Conhaim L (2001) Transition from GABAergic to glycinergic synaptic transmission in newly formed spinal networks. J Neurophysiol 86:492-502.
25. Gorelova NA, Yang CR (2000) Dopamine D1/D5 receptor activation modulates a persistent sodium current in rat prefrontal cortical neurons in vitro. J Neurophysiol 84:75-87.
26. Grillner S (2006) Biological pattern generation: the cellular and computational logic of networks in motion. Neuron 52:751-766.
27. Han P, Nakanishi ST, Tran MA, Whelan PJ (2007) Dopaminergic modulation of spinal neuronal excitability. J Neurosci 27:13192-13204.
28. Harvey PJ, Li X, Li Y, Bennett DJ (2006) 5-HT2 receptor activation facilitates a persistent sodium current and repetitive firing in spinal motoneurons of rats with and without chronic spinal cord injury. J Neurophysiol 96:1158-1170.
29. Hinckley CA, Ziskind-Conhaim L (2006) Electrical coupling between locomotor-related excitatory interneurons in the mammalian spinal cord. J Neurosci 26:8477-8483.
30. Hinckley CA, Hartley R, Wu L, Todd A, Ziskind-Conhaim L (2005) Locomotor-like rhythms in a genetically distinct cluster of interneurons in the mammalian spinal cord. J Neurophysiol 93:1439-1449.
31. Hochman S, Jordan LM, MacDonald JF (1994) 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.
32. Hsiao CF, Del Negro CA, Trueblood PR, Chandler SH (1998) Ionic basis for serotonin-induced bistable membrane properties in guinea pig trigeminal motoneurons. J Neurophysiol 79:2847-2856.
33. Jones HC, Keep RF (1988) Brain fluid calcium concentration and response to acute hypercalcaemia during development in the rat. J Physiol 402:579-593.
34. Kiehn O (2006) Locomotor circuits in the mammalian spinal cord. Annu Rev Neurosci 29:279-306.
35. Kiehn O, Kjaerulff O (1996) Spatiotemporal characteristics of 5-HT and dopamine-induced rhythmic hindlimb activity in the in vitro neonatal rat. J Neurophysiol 75:1472-1482.
36. Kiehn O, Johnson BR, Raastad M (1996) Plateau properties in mammalian spinal interneurons during transmitter-induced locomotor activity. Neuroscience 75:263-273.
37. Kjaerulff O, Kiehn O (1996) Distribution of networks generating and coordinating locomotor activity in the neonatal rat spinal cord in vitro: a lesion study. J Neurosci 16:5777-5794.
38. +-dominated leak currents contribute to respiratory rhythm generation in the pre-Botzinger complex in vitro. J Neurosci 28:1773-1785.
39. Kozlov AK, Lansner A, Grillner S, Kotaleski JH (2007) A hemicord locomotor network of excitatory interneurons: a simulation study. Biol Cybern 96:229-243.
40. Lee RH, Heckman CJ (1998) Bistability in spinal motoneurons in vivo: systematic variations in persistent inward currents. J Neurophysiol 80:583-593.
41. Leibowitz MD, Sutro JB, Hille B (1986) Voltage-dependent gating of veratridine-modified Na channels. J Gen Physiol 87:25-46.
42. 2+ and gap junctions. J Physiol 496:379-394.
43. 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.
44. Madriaga MA, McPhee LC, Chersa T, Christie KJ, Whelan PJ (2004) Modulation of locomotor activity by multiple 5-HT and dopaminergic receptor subtypes in the neonatal mouse spinal cord. J Neurophysiol 92:1566-1576.
45. McCrea DA, Rybak IA (2007) Modeling the mammalian locomotor CPG: insights from mistakes and perturbations. In: Progress in brain research computational neuroscience: theoretical insights into brain function (Cisek P, Drew T, Kalaska JF, eds), pp 235-253. Amsterdam: Elsevier.
46. Pape HC (1996) Queer current and pacemaker: the hyperpolarization- activated cation current in neurons. Annu Rev Physiol 58:299-327.
47. Pearlstein E, Mabrouk FB, Pflieger JF, Vinay L (2005) Serotonin refines the locomotor-related alternations in the in vitro neonatal rat spinal cord. Eur J Neurosci 21:1338-1346.
48. Peña F, Parkis MA, Tryba AK, Ramirez JM (2004) Differential contribution of pacemaker properties to the generation of respiratory rhythms during normoxia and hypoxia. Neuron 43:105-117.
49. Perez-Velazquez JL, Valiante TA, Carlen PL (1994) Modulation of gap junctional mechanisms during calcium-free induced field burst activity: a possible role for electrotonic coupling in epileptogenesis. J Neurosci 14:4308-4317.
50. Pumain R, Heinemann U (1981) Extracellular calcium and potassium changes in mammalian neocortex. Adv Biochem Psychopharmacol 29:53-58.
51. Purvis LK, Smith JC, Koizumi H, Butera RJ (2007) Intrinsic bursters increase the robustness of rhythm generation in an excitatory network. J Neurophysiol 97:1515-1526.
52. Ramirez JM, Tryba AK, Peña F (2004) Pacemaker neurons and neuronal networks: an integrative view. Curr Opin Neurobiol 14:665-674.
53. Rybak IA, Shevtsova NA, Lafreniere-Roula M, McCrea DA (2006) Modelling spinal circuitry involved in locomotor pattern generation: insights from deletions during fictive locomotion. J Physiol 577:617-639.
54. 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.
55. Schwindt PC, Spain WJ, Crill WE (1989) Long-lasting reduction of excitability by a sodium-dependent potassium current in cat neocortical neurons. J Neurophysiol 61:233-244.
56. Skinner FK, Zhang L, Velazquez JL, Carlen PL (1999) Bursting in inhibitory interneuronal networks: a role for gap-junctional coupling. J Neurophysiol 81:1274-1283.
57. Smolen P, Rinzel J, Sherman A (1993) Why pancreatic islets burst but single beta cells do not. The heterogeneity hypothesis. Biophys J 64:1668-1680.
58. Sqalli-Houssaini Y, Cazalets JR, Clarac F (1993) Oscillatory properties of the central pattern generator for locomotion in neonatal rats. J Neurophysiol 70:803-813.
59. Su H, Alroy G, Kirson ED, Yaari Y (2001) Extracellular calcium modulates persistent sodium current-dependent burst-firing in hippocampal pyramidal neurons. J Neurosci 21:4173-4182.
60. Svirskis G, Hounsgaard J (1998) Transmitter regulation of plateau properties in turtle motoneurons. J Neurophysiol 79:45-50.
61. Taccola G, Nistri A (2007) Differential modulation by tetraethyl-ammonium of the processes underlying network bursting in the neonatal rat spinal cord in vitro. Neuroscience 146:1906-1917.
62. Tazerart S, Vinay L, Brocard F (2007a) Persistent sodium current-dependent pacemaker properties in the central pattern generator for locomotion in rodents. Soc Neurosci Abstr 33:406.3.
63. Tazerart S, Viemari JC, Darbon P, Vinay L, Brocard F (2007b) Contribution of persistent sodium current to locomotor pattern generation in neonatal rats. J Neurophysiol 98:613-628.
64. Theiss RD, Heckman CJ (2005) Systematic variation in effects of serotonin and norepinephrine on repetitive firing properties of ventral horn neurons. Neuroscience 134:803-815.
65. Theiss RD, Kuo JJ, Heckman CJ (2007) Persistent inward currents in rat ventral horn neurones. J Physiol 580:507-522.
66. Thoby-Brisson M, Ramirez JM (2001) Identification of two types of inspiratory pacemaker neurons in the isolated respiratory neural network of mice. J Neurophysiol 86:104-112.
67. Tresch MC, Kiehn O (2000) Motor coordination without action potentials in the mammalian spinal cord. Nat Neurosci 3:593-599.
68. van Drongelen W, Koch H, Elsen FP, Lee HC, Mrejeru A, Doren E, Marcuccilli CJ, Hereld M, Stevens RL, Ramirez JM (2006) Role of persistent sodium current in bursting activity of mouse neocortical networks in vitro. J Neurophysiol 96:2564-2577.
69. Wichterle H, Lieberam I, Porter JA, Jessell TM (2002) Directed differentiation of embryonic stem cells into motor neurons. Cell 110:385-397.
70. 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.
71. Wilson JM, Cowan AI, Brownstone RM (2007) Heterogeneous electrotonic coupling and synchronization of rhythmic bursting activity in mouse Hb9 interneurons. J Neurophysiol 98:2370-2381.
72. Wilson JM, Cowan AI, Brownstone RM (2008) Hb9 interneurons: reply to Ziskind-Conhaim and Hinckley. J Neurophysiol 99:1047-1049.
73. Xiong Z, Lu W, MacDonald JF (1997) Extracellular calcium sensed by a novel cation channel in hippocampal neurons. Proc Natl Acad Sci U S A 94:7012-7017.
74. Yue C, Yaari Y (2004) KCNQ/M channels control spike afterdepolarization and burst generation in hippocampal neurons. J Neurosci 24:4614-4624.
75. + channels drive spike afterdepolarizations and associated bursting in adult CA1 pyramidal cells. J Neurosci 25:9704 -9720.
76. Zhong G, Díaz-Ríos M, Harris-Warrick RM (2006a) Serotonin modulates the properties of ascending commissural interneurons in the neonatal mouse spinal cord. J Neurophysiol 95:1545-1555.
77. Zhong G, Díaz-Ríos M, Harris-Warrick RM (2006b) Intrinsic and functional differences among commissural interneurons during fictive locomotion and serotonergic modulation in the neonatal mouse. J Neurosci 26:6509-6517.
78. Zhong G, Masino MA, Harris-Warrick RM (2007) Persistent sodium currents participate in fictive locomotion generation in neonatal mouse spinal cord. J Neurosci 27:4507-4518.
79. Ziskind-Conhaim L, Hinckley CA (2008) Hb9 versus type 2 interneurons. J Neurophysiol 99:1044-1046.