Modulation of intrinsic spiking in spinal cord neurons

Journal of Neurophysiology

Volumn 102, Issue 4, 2009, Pages 2441-2452

  Czarnecki, Antonny ^a   Magloire, Vincent ^a   Streit, Jürg ^a  

^a UNIVERSITY OF BERN   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; GLUTAMIC ACID; GLYCINE; MUSCARINE; PHOSPHOLIPASE C; SEROTONIN; SEROTONIN 2 RECEPTOR;

ACTION POTENTIAL; ANIMAL TISSUE; ARTICLE; CELL LEVEL; CONTROLLED STUDY; EMBRYO; INHIBITION KINETICS; NERVE CELL NETWORK; NEUROTRANSMISSION; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; SODIUM CURRENT; SPIKE WAVE; SPINAL CORD; SPINAL CORD NERVE CELL; WHOLE CELL;

ACTION POTENTIALS; ANIMALS; CELLS, CULTURED; MICROELECTRODES; MUSCARINE; MUSCARINIC AGONISTS; NEURONAL PLASTICITY; NEURONS; PATCH-CLAMP TECHNIQUES; RATS; RECEPTORS, SEROTONIN, 5-HT2; SEROTONIN; SIGNAL TRANSDUCTION; SODIUM; SPINAL CORD; SYNAPSES; SYNAPTIC TRANSMISSION; TIME FACTORS; TYPE C PHOSPHOLIPASES;

EID: 70350322440     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00244.2009     Document Type: Article

References (76)

1. +-dependent theta-like rhythmicity in stellate cells of entorhinal cortex layer II. Nature 342: 175-177, 1989.
2. Antri M, Barthe JY, Mouffle C, Orsal D. Long-lasting recovery of locomotor function in chronic spinal rat following chronic combined pharmacological stimulation of serotonergic receptors with 8-OHDPAT and quipazine. Neurosci Lett 384: 162-167, 2005. (Pubitemid 40826637)
3. Aracri P, Colombo E, Mantegazza M, Scalmani P, Curia G, Avanzini G, Franceschetti S. Layer-specific properties of the persistent sodium current in sensorimotor cortex. J Neurophysiol 95: 3460-3468, 2006. (Pubitemid 43846155)
4. Arshavsky YuI. Cellular and network properties in the functioning of the nervous system: from central pattern generators to cognition. Brain Res 41: 229-267, 2003.
5. Arshavsky YuI, Beloozerova IN, Orlovsky GN, Panchin YuV, Pavlova GA. Control of locomotion in marine mollusc Clione limacina. I. Efferent activity during actual and fictitious swimming. Exp Brain Res 58: 255-262, 1985. (Pubitemid 15114562)
6. Ballion B, Branchereau P, Chapron J, Viala D. Ontogeny of descending serotonergic innervation and evidence for intraspinal 5-HT neurons in the mouse spinal cord. Brain Res 137: 81-88, 2002. (Pubitemid 34786639)
7. Beato M, Nistri A. Serotonin-induced inhibition of locomotor rhythm of the rat isolated spinal cord is mediated by the 5-HT1 receptor class. Proc Biol Sci 265: 2073-2080, 1998. (Pubitemid 28502543)
8. (NaP)] underlies single-spike activity in rat subthalamic neurons. J Neurophysiol 83: 1951-1957, 2000.
9. Britt SG, Gonias SL, Sanders JM, Vandenberg SR. Agonist and antagonist activities of arylpiperazines at human platelet serotonin2 receptors. J Pharmacol Exp Ther 247: 965-970, 1988. (Pubitemid 19022102)
10. Butt SJ, Lundfald L, Kiehn O. EphA4 defines a class of excitatory locomotor- related interneurons. Proc Natl Acad Sci USA 102: 14098-14103, 2005. (Pubitemid 41377709)
11. Carr DB, Cooper DC, Ulrich SL, Spruston N, Surmeier DJ. Serotonin receptor activation inhibits sodium current and dendritic excitability in prefrontal cortex via a protein kinase C-dependent mechanism. J Neurosci 22: 6846-6855, 2002. (Pubitemid 35379142)
12. Cazalets JR, Sqalli-Houssaini Y, Clarac F. Activation of the central pattern generators for locomotion by serotonin and excitatory amino acids in neonatal rat. J Physiol 455: 187-204, 1992.
13. Chevallier S, Nagy F, Cabelguen JM. Cholinergic control of excitability of spinal motoneurones in the salamander. J Physiol 570: 525-540, 2006.
14. Cramer NP, Li Y, Keller A. The whisking rhythm generator: a novel mammalian network for the generation of movement. J Neurophysiol 97: 2148-2158, 2007. (Pubitemid 46411150)
15. Crill WE. Persistent sodium current in mammalian central neurons. Annu Rev Physiol 58: 349-362, 1996. (Pubitemid 26106725)
16. Czarnecki A, Magloire V, Streit J. Local oscillations of spiking activity in organotypic spinal cord slice cultures. Eur J Neurosci 27: 2076-2088, 2008.
17. Dai Y, Jordan LM, Fedirchuk B. Modulation of transient and persistent inward currents by activation of protein kinase C in spinal ventral neurons of the neonatal rat. J Neurophysiol 101: 112-128, 2009.
18. Darbon P, Scicluna L, Tscherter A, Streit J. Mechanisms controlling bursting activity induced by disinhibition in spinal cord networks. Eur J Neurosci 15: 671-683, 2002. (Pubitemid 35471936)
19. Darbon P, Yvon C, Legrand JC, Streit J. INaP underlies intrinsic spiking and rhythm generation in networks of cultured rat spinal cord neurons. Eur J Neurosci 20: 976-988, 2004. (Pubitemid 39144406)
20. Del Negro CA, Koshiya N, Butera RJ Jr, Smith JC. Persistent sodium current, membrane properties, and bursting behavior of pre-Bötzinger complex inspiratory neurons in vitro. J Neurophysiol 88: 2242-2250, 2002. (Pubitemid 35346030)
21. Del Negro CA, Morgado-Valle C, Hayes JA, Mackay DD, Pace RW, Crowder EA, Feldman JL. Sodium and calcium current-mediated pacemaker neurons and respiratory rhythm generation. J Neurosci 25: 446-453, 2005. (Pubitemid 40105615)
22. Diaz-Rios M, Dombeck DA, Webb WW, Harris-Warrick RM. Serotonin modulates dendritic calcium influx in commissural interneurons in the mouse spinal locomotor network. J Neurophysiol 98: 2157-2167, 2007. (Pubitemid 47584401)
23. Do MT, Bean BP. Subthreshold sodium currents and pacemaking of subthalamic neurons: modulation by slow inactivation. Neuron 39: 109-120, 2003.
24. Fong AJ, Cai LL, Otoshi CK, Reinkensmeyer DJ, Burdick JW, Roy RR, Edgerton VR. Spinal cord-transected mice learn to step in response to quipazine treatment and robotic training. J Neurosci 25: 11738-11747, 2005.
25. Grillner S. The motor infrastructure: from ion channels to neuronal networks. Nat Rev 4: 573-586, 2003. (Pubitemid 37279129)
26. Grillner S, Ekeberg, El Manira A, Lansner A, Parker D, Tegner J, Wallén P. Intrinsic function of a neuronal network: a vertebrate central pattern generator. Brain Res 26: 184-197, 1998. (Pubitemid 28318075)
27. Grudt TJ, Williams JT, Travagli RA. Inhibition by 5-hydroxytryptamine and noradrenaline in substantia gelatinosa of guinea-pig spinal trigeminal nucleus. J Neurophysiol 485: 113-120, 1995.
28. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch 391: 85-100, 1981. (Pubitemid 11012976)
29. Harvey PJ, Li X, Li Y, Bennett DJ. 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, 2006. (Pubitemid 44371511)
30. Hattox A, Li Y, Keller A. Serotonin regulates rhythmic whisking. Neuron 39: 343-352, 2003.
31. Hinckley CA, Hartley R, Wu L, Todd A, Ziskind-Conhaim L. Locomotorlike rhythms in a genetically distinct cluster of interneurons in the mammalian spinal cord. J Neurophysiol 93: 1439-1449, 2005. (Pubitemid 40283732)
32. Hochman S, Jordan LM, Schmidt BJ. TTX-resistant NMDA receptormediated voltage oscillations in mammalian lumbar motoneurons. J Neurophysiol 72: 2559-2562, 1994. (Pubitemid 24362650)
33. Hori Y, Endo K, Takahashi T. Long-lasting synaptic facilitation induced by serotonin in superficial dorsal horn neurones of the rat spinal cord. J Physiol 492: 867-876, 1996. (Pubitemid 26154370)
34. Hounsgaard J, Kiehn O. Serotonin-induced bistability of turtle motoneurones caused by a nifedipine-sensitive calcium plateau potential. J Physiol 414: 265-282, 1989. (Pubitemid 19177302)
35. Hoyer D, Clarke DE, Fozard JR, Hartig PR, Martin GR, Mylecharane EJ, Saxena PR, Humphrey PP. International Union of Pharmacology classification of receptors for 5-hydroxytryptamine (serotonin). Pharmacol Rev 46: 157-203, 1994. (Pubitemid 24185150)
36. Jinno S, Ishizuka S, Kosaka T. Ionic currents underlying rhythmic bursting of ventral mossy cells in the developing mouse dentate gyrus. Eur J Neurosci 17: 1338-1354, 2003. (Pubitemid 36560834)
37. Kay AR, Sugimori M, Llinás R. Kinetic and stochastic properties of a persistent sodium current in mature guinea pig cerebellar Purkinje cells. J Neurophysiol 80: 1167-1179, 1998. (Pubitemid 28495718)
38. Kiehn O, Johnson BR, Raastad M. Plateau properties in mammalian spinal interneurons during transmitter-induced locomotor activity. Neuroscience 75: 263-273, 1996. (Pubitemid 26344619)
39. Kim D, Adipudi V, Shibayama M, Giszter S, Tessler A, Murray M, Simansky KJ. Direct agonists for serotonin receptors enhance locomotor function in rats that received neural transplants after neonatal spinal transection. J Neurosci 19: 6213-6224, 1999. (Pubitemid 29327953)
40. Kim TW, Koh SD, Ordog T, Ward SM, Sanders KM. Muscarinic regulation of pacemaker frequency in murine gastric interstitial cells of Cajal. J Physiol 546: 415-425, 2003. (Pubitemid 36175977)
41. Kuo JJ, Lee RH, Zhang L, Heckman CJ. Essential role of the persistent sodium current in spike initiation during slowly rising inputs in mouse spinal neurones. J Physiol 574: 819-834, 2006. (Pubitemid 44089073)
42. Landry ES, Guertin PA. Differential effects of 5-HT1 and 5-HT2 receptor agonists on hindlimb movements in paraplegic mice. Prog Neuropsychopharmacol 28: 1053-1060, 2004.
43. Lape R, Nistri A. Current- and voltage-clamp studies of the spike medium afterhyperpolarization of hypoglossal motoneurons in a rat brain stem slice preparation. J Neurophysiol 83: 2987-2995, 2000. (Pubitemid 30321487)
44. Le Bon-Jego M, Yuste R. Persistently active, pacemaker-like neurons in neocortex. Front Neurosci 1: 123-129, 2007.
45. Li X, Murray K, Harvey PJ, Ballou EW, Bennett DJ. Serotonin facilitates a persistent calcium current in motoneurons of rats with and without chronic spinal cord injury. J Neurophysiol 97: 1236-1246, 2007. (Pubitemid 46239501)
46. Madriaga MA, McPhee LC, Chersa T, Christie KJ, Whelan PJ. Modulation of locomotor activity by multiple 5-HT and dopaminergic receptor subtypes in the neonatal mouse spinal cord. J Neurophysiol 92: 1566-1576, 2004. (Pubitemid 39100655)
47. McEwen ML, Van Hartesveldt C, Stehouwer DJ. L-DOPA and quipazine elicit air-stepping in neonatal rats with spinal cord transections. Behav Neurosci 111: 825-833, 1997.
48. Miles GB, Hartley R, Todd AJ, Brownstone RM. Spinal cholinergic interneurons regulate the excitability of motoneurons during locomotion. Proc Natl Acad Sci USA 104: 2448-2453, 2007. (Pubitemid 46391417)
49. Miller JF, Paul KD, Lee RH, Rymer WZ, Heckman CJ. Restoration of extensor excitability in the acute spinal cat by the 5-HT2 agonist DOI. J Neurophysiol 75: 620-628, 1996. (Pubitemid 26073460)
50. + current in rat neocortical pyramidal neurons. J Neurophysiol 79: 1579-1582, 1998.
51. Myers CP, Lewcock JW, Hanson MG, Gosgnach S, Aimone JB, Gage FH, Lee KF, Landmesser LT, Pfaff SL. Cholinergic input is required during embryonic development to mediate proper assembly of spinal locomotor circuits. Neuron 46: 37-49, 2005. (Pubitemid 40488310)
52. Newton BW, Maley BE, Hamill RW. Immunohistochemical demonstration of serotonin neurons in autonomic regions of the rat spinal cord. Brain Res 376: 155-163, 1986.
53. Pace RW, Mackay DD, Feldman JL, Del Negro CA. Role of persistent sodium current in mouse pre-Bötzinger complex neurons and respiratory rhythm generation. J Physiol 580: 485-496, 2007. (Pubitemid 46564177)
54. Panchin YuV, Arshavsky YuI, Deliagina TG, Orlovsky GN, Popova LB, Selverston AI. Control of locomotion in the marine mollusc Clione limacina. XI. Effects of serotonin. Exp Brain Res 109: 361-365, 1996. (Pubitemid 26142153)
55. Perrier JF, Cotel F. Serotonin differentially modulates the intrinsic properties of spinal motoneurons from the adult turtle. J Physiol 586: 1233-1238, 2008. (Pubitemid 351321263)
56. Rajaofetra N, Sandillon F, Geffard M, Privat A. Pre- and post-natal ontogeny of serotonergic projections to the rat spinal cord. J Neurosci Res 22: 305-321, 1989. (Pubitemid 19112427)
57. Raymond JR, Mukhin YV, Gelasco A, Turner J, Collinsworth G, Gettys TW, Grewal JS, Garnovskaya MN. Multiplicity of mechanisms of serotonin receptor signal transduction. Pharmacol Ther 92: 179-212, 2001. (Pubitemid 34251133)
58. Roth BL, Willins DL, Kristiansen K, Kroeze WK. 5-Hydroxytryptamine2- family receptors (5-hydroxytryptamine2A, 5-hydroxytryptamine2B, 5-hydroxytryptamine2C): where structure meets function. Pharmacol Ther 79: 231-257, 1998. (Pubitemid 28393877)
59. Selverston AI, Moulins M. Oscillatory neural networks. Annu Rev Physiol 47: 29-48, 1985.
60. Shao XM, Feldman JL. Acetylcholine modulates respiratory pattern: effects mediated by M3-like receptors in pre-Bötzinger complex inspiratory neurons. J Neurophysiol 83: 1243-1252, 2000.
61. Shay BL, Sawchuk M, Machacek DW, Hochman S. Serotonin 5-HT2 receptors induce a long-lasting facilitation of spinal reflexes independent of ionotropic receptor activity. J Neurophysiol 94: 2867-2877, 2005. (Pubitemid 41324702)
62. Streit J, Tscherter A, Heuschkel MO, Renaud P. The generation of rhythmic activity in dissociated cultures of rat spinal cord. Eur J Neurosci 14: 191-202, 2001. (Pubitemid 32777627)
63. Stuart G, Sakmann B. Amplification of EPSPs by axosomatic sodium channels in neocortical pyramidal neurons. Neuron 15: 1065-1076, 1995.
64. Tanaka S, Chandler SH. Serotonergic modulation of persistent sodium currents and membrane excitability via cyclic AMP-protein kinase A cascade in mesencephalic V neurons. J Neurosci Res 83: 1362-1372, 2006. (Pubitemid 43668019)
65. Tazerart S, Viemari JC, Darbon P, Vinay L, Brocard F. Contribution of persistent sodium current to locomotor pattern generation in neonatal rats. J Neurophysiol 98: 613-628, 2007. (Pubitemid 47236019)
66. Tazerart S, Vinay L, Brocard F. The persistent sodium current generates pacemaker activities in the central pattern generator for locomotion and regulates the locomotor rhythm. J Neurosci 28: 8577-8589, 2008.
67. Theiss RD, Kuo JJ, Heckman CJ. Persistent inward currents in rat ventral horn neurones. J Physiol 580: 507-522, 2007.
68. Tscherter A, Heuschkel MO, Renaud P, Streit J. Spatiotemporal characterization of rhythmic activity in rat spinal cord slice cultures. Eur J Neurosci 14: 179-190, 2001. (Pubitemid 32777626)
69. Ung RV, Landry ES, Rouleau P, Lapointe NP, Rouillard C, Guertin PA. Role of spinal 5-HT2 receptor subtypes in quipazine-induced hindlimb movements after a low-thoracic spinal cord transection. Eur J Neurosci 28: 2231-2242, 2008.
70. van Drongelen W, Koch H, Elsen FP, Lee HC, Mrejeru A, Doren E, Marcuccilli CJ, Hereld M, Stevens RL, Ramirez JM. Role of persistent sodium current in bursting activity of mouse neocortical networks in vitro. J Neurophysiol 96: 2564-2577, 2006. (Pubitemid 44785906)
71. Yamazaki J, Fukuda H, Nagao T, Ono H. 5-HT2/5-HT1C receptor-mediated facilitatory action on unit activity of ventral horn cells in rat spinal cord slices. Eur J Pharmacol 220: 237-242, 1992.
72. Yoshimura M, Furue H. Mechanisms for the anti-nociceptive actions of the descending noradrenergic and serotonergic systems in the spinal cord. J Pharmacol Sci 101: 107-117, 2006. (Pubitemid 43938761)
73. Yvon C, Czarnecki A, Streit J. Riluzole-induced oscillations in spinal networks. J Neurophysiol 97: 3607-3620, 2007.
74. Zhong G, Diaz-Rios M, Harris-Warrick RM. Intrinsic and functional differences among commissural interneurons during fictive locomotion and serotonergic modulation in the neonatal mouse. J Neurosci 26: 6509-6517, 2006. (Pubitemid 44318331)
75. Zhong G, Masino MA, Harris-Warrick RM. Persistent sodium currents participate in fictive locomotion generation in neonatal mouse spinal cord. J Neurosci 27: 4507-4518, 2007. (Pubitemid 46663577)
76. Ziskind-Conhaim L, Wu L, Wiesner EP. Persistent sodium current contributes to induced voltage oscillations in locomotor-related Hb9 interneurons in the mouse spinal cord. J Neurophysiol 100: 2254-2264, 2008.