NMDA induces persistent inward and outward currents that cause rhythmic bursting in adult rodent motoneurons

Journal of Neurophysiology

Volumn 108, Issue 11, 2012, Pages 2991-2998

  Manuel, Marin ^a   Li, Yaqing ^b   ElBasiouny, Sherif M ^a   Murray, Katie ^b   Griener, Anna ^b   Heckman, C J ^a   Bennett, David J ^b  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Fictive locomotion; Persistent inward current; Persistent outward current; Spinal cord

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; MEMBRANE POTENTIAL; MOTONEURON; MOUSE; NERVE CELL MEMBRANE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; RAT; SPINAL CORD; SWIMMING; VENTRAL ROOT;

ACTION POTENTIALS; ANIMALS; EXCITATORY AMINO ACID AGONISTS; LOCOMOTION; MICE; MOTOR NEURONS; N-METHYLASPARTATE; POTASSIUM CHANNEL BLOCKERS; RATS; SPINAL CORD; SPINAL NERVE ROOTS; TAIL; TETRODOTOXIN;

EID: 84870487196     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00518.2012     Document Type: Article

References (73)

1. Bennett DJ, Hultborn H, Fedirchuk B, Gorassini M. Synaptic activation of plateaus in hindlimb motoneurons of decerebrate cats. J Neurophysiol 80: 2023-2037, 1998.
2. Bennett DJ, Li Y, Siu M. Plateau potentials in sacrocaudal motoneurons of chronic spinal rats, recorded in vitro. J Neurophysiol 86: 1955-1971, 2001.
3. Binder MD. Integration of synaptic and intrinsic dendritic currents in cat spinal motoneurons. Brain Res Brain Res Rev 40: 1-8, 2002.
4. Binder MD, Heckman CJ, Powers RK. The physiological control of motoneuron activity. In: Handbook of Physiology. Exercise: Regulation and Integration of Multiple Systems. Bethesda, MD: Am. Physiol. Soc., 1996.
5. Brink EE, Pfaff DW. Vertebral muscles of the back and tail of the albino rat (Rattus norvegicus albinus). Brain Behav Evol 17: 1-47, 1980.
6. Brownstone RM, Gossard JP, Hultborn H. Voltage-dependent excitation of motoneurones from spinal locomotor centres in the cat. Exp Brain Res 102: 34-44, 1994.
7. Burke RE, Degtyarenko AM, Simon ES. Patterns of locomotor drive to motoneurons and last-order interneurons: clues to the structure of the CPG. J Neurophysiol 86: 447-462, 2001.
8. Chang Q, Gonzalez M, Pinter MJ, Balice-Gordon RJ. Gap junctional coupling and patterns of connexin expression among neonatal rat lumbar spinal motor neurons. J Neurosci 19: 10813-10828, 1999.
9. del Negro CA, Hsiao CF, Chandler SH. Outward currents influencing bursting dynamics in guinea pig trigeminal motoneurons. J Neurophysiol 81: 1478-1485, 1999.
10. Delvolve I, Gabbay H, Lev-Tov A. The motor output and behavior produced by rhythmogenic sacrocaudal networks in spinal cords of neonatal rats. J Neurophysiol 85: 2100-2110, 2001.
11. Durand J. NMDA actions on rat abducens motoneurons. Eur J Neurosci 3: 621-633, 1991.
12. Durand J. Synaptic excitation triggers oscillations during NMDA receptor activation in rat abducens motoneurons. Eur J Neurosci 5: 1389-1397, 1993.
13. el Manira A, Tegner J, Grillner S. Calcium-dependent potassium channels play a critical role for burst termination in the locomotor network in lamprey. J Neurophysiol 72: 1852-1861, 1994.
14. Engberg I, Tarnawa I, Durand J, Ouardouz M. An analysis of synaptic transmission to motoneurones in the cat spinal cord using a new selective receptor blocker. Acta Physiol Scand 148: 97-100, 1993.
15. Enríquez Denton M, Wienecke J, Zhang M, Hultborn H, Kirkwood PA. Voltage-dependent amplification of synaptic inputs in respiratory motoneurones. J Physiol 590: 3067-3090, 2012.
16. Flatman JA, Schwindt PC, Crill WE, Stafstrom CE. Multiple actions of N-methyl-D-aspartate on cat neocortical neurons in vitro. Brain Res 266: 169-173, 1983.
17. Goulding M, Lanuza G, Sapir T, Narayan S. The formation of sensorimotor circuits. Curr Opin Neurobiol 12: 508-515, 2002.
18. Grillner S, Wallen P. The ionic mechanisms underlying N-methyl-D-aspartate receptor-induced, tetrodotoxin-resistant membrane potential oscillations in lamprey neurons active during locomotion. Neurosci Lett 60: 289-294, 1985.
19. Grossman ML, Basbaum AI, Fields HL. Afferent and efferent connections of the rat tail flick reflex (a model used to analyze pain control mechanisms). J Comp Neurol 206: 9-16, 1982
20. Guertin PA, Hounsgaard J. NMDA-induced intrinsic voltage oscillations depend on L-type calcium channels in spinal motoneurons of adult turtles. J Neurophysiol 80: 3380-3382, 1998.
21. Harvey PJ, Li Y, Li X, Bennett DJ. Persistent sodium currents and repetitive firing in motoneurons of the sacrocaudal spinal cord of adult rats. J Neurophysiol 96: 1141-1157, 2006.
22. Heckman CJ, Hyngstrom AS, Johnson MD. Active properties of motoneurone dendrites: diffuse descending neuromodulation, focused local inhibition. J Physiol 586: 1225-1231, 2008a.
23. Heckman CJ, Johnson M, Mottram C, Schuster J. Persistent inward currents in spinal motoneurons and their influence on human motoneuron firing patterns. Neuroscientist 14: 264-275, 2008b.
24. Heckman CJ, Mottram C, Quinlan K, Theiss R, Schuster J. Motoneuron excitability: the importance of neuromodulatory inputs. Clin Neurophysiol 120: 2040-2054, 2009.
25. Heckmann CJ, Gorassini MA, Bennett DJ. Persistent inward currents in motoneuron dendrites: implications for motor output. Muscle Nerve 31: 135-156, 2005.
26. Holstege JC, Kuypers HG. Brainstem projections to spinal motoneurons: an update. Neuroscience 23: 809-821, 1987.
27. Hornby TG, McDonagh JC, Reinking RM, Stuart DG. Motoneurons: a preferred firing range across vertebrate species? Muscle Nerve 25: 632-648, 2002.
28. Hounsgaard J, Hultborn H, Jespersen B, Kiehn O. Bistability of alphamotoneurones in the decerebrate cat and in the acute spinal cat after intravenous 5-hydroxytryptophan. J Physiol 405: 345-367, 1988.
29. Hounsgaard J, Kiehn O. Serotonin-induced bistability of turtle motoneurones caused by a nifedipine-sensitive calcium plateau potential. J Physiol 414: 265-282, 1989.
30. Hsiao CF, Wu N, Levine MS, Chandler SH. Development and serotonergic modulation of NMDA bursting in rat trigeminal motoneurons. J Neurophysiol 87: 1318-1328, 2002.
31. Hultborn H, Brownstone RB, Toth TI, Gossard JP. Key mechanisms for setting the input-output gain across the motoneuron pool. Prog Brain Res 143: 77-95, 2004.
32. Hultborn H, Denton ME, Wienecke J, Nielsen JB. Variable amplification of synaptic input to cat spinal motoneurones by dendritic persistent inward current. J Physiol 552: 945-952, 2003.
33. Hyngstrom AS, Johnson MD, Miller JF, Heckman CJ. Intrinsic electrical properties of spinal motoneurons vary with joint angle. Nat Neurosci 10: 363-369, 2007.
34. Jessell TM. Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat Rev Genet 1: 20-29, 2000.
35. Jiang MC, Heckman CJ. In vitro sacral cord preparation and motoneuron recording from adult mice. J Neurosci Methods 156: 31-36, 2006.
36. Johnson MD, Hyngstrom AS, Manuel M, Heckman CJ. Push-pull control of motor output. J Neurosci 32: 4592-4599, 2012.
37. Kalb RG, Lidow MS, Halsted MJ, Hockfield S. N-methyl-D-aspartate receptors are transiently expressed in the developing spinal cord ventral horn. Proc Natl Acad Sci USA 89: 8502-8506, 1992.
38. Kandler K, Katz LC. Neuronal coupling and uncoupling in the developing nervous system. Curr Opin Neurobiol 5: 98-105, 1995.
39. Kiehn O, Butt SJ. Physiological, anatomical and genetic identification of CPG neurons in the developing mammalian spinal cord. Prog Neurobiol 70: 347-361, 2003.
40. Kiehn O, Kjaerulff O, Tresch MC, Harris-Warrick RM. Contributions of intrinsic motor neuron properties to the production of rhythmic motor output in the mammalian spinal cord. Brain Res Bull 53: 649-659, 2000.
41. Kim YI, Chandler SH. NMDA-induced burst discharge in guinea pig trigeminal motoneurons in vitro. J Neurophysiol 74: 334-346, 1995.
42. Lanuza GM, Gosgnach S, Pierani A, Jessell TM, Goulding M. Genetic identification of spinal interneurons that coordinate left-right locomotor activity necessary for walking movements. Neuron 42: 375-386, 2004.
43. Lee RH, Heckman CJ. Adjustable amplification of synaptic input in the dendrites of spinal motoneurons in vivo. J Neurosci 20: 6734-6740, 2000.
44. Li Y, Bennett DJ. Persistent sodium and calcium currents cause plateau potentials in motoneurons of chronic spinal rats. J Neurophysiol 90: 857-869, 2003.
45. Li Y, Li X, Harvey PJ, Bennett DJ. Effects of baclofen on spinal reflexes and persistent inward currents in motoneurons of chronic spinal rats with spasticity. J Neurophysiol 92: 2694-2703, 2004.
46. MacDonald JF, Porietis AV, Wojtowicz JM. L-Aspartic acid induces a region of negative slope conductance in the current-voltage relationship of cultured spinal cord neurons. Brain Res 237: 248-253, 1982
47. MacLean JN, Schmidt BJ, Hochman S. NMDA receptor activation triggers voltage oscillations, plateau potentials and burstinq in neonatal rat lumbar motoneurons in vitro. Eur J Neurosci 9: 2702-2711, 1997.
48. Masson RL Jr, Sparkes ML, Ritz LA. Descending projections to the rat sacrocaudal spinal cord. J Comp Neurol 307: 120-130, 1991.
49. 2+ of NMDA responses in spinal cord neurones. Nature 309: 261-263, 1984.
50. McCrea DA, Rybak IA. Organization of mammalian locomotor rhythm and pattern generation. Brain Res Rev 57: 134-146, 2008.
51. McQuiston AR, Madison DV. Muscarinic receptor activity induces an afterdepolarization in a subpopulation of hippocampal CA1 interneurons. J Neurosci 19: 5703-5710, 1999.
52. 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.
53. Monyer H, Burnashev N, Laurie DJ, Sakmann B, Seeburg PH. Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12: 529-540, 1994.
54. Murray KC, Nakae A, Stephens MJ, Rank M, D'Amico J, Harvey PJ, Li X, Harris RL, Ballou EW, Anelli R, Heckman CJ, Mashimo T, Vavrek R, Sanelli L, Gorassini MA, Bennett DJ, Fouad K. Recovery of motoneuron and locomotor function after spinal cord injury depends on constitutive activity in 5-HT2C receptors. Nat Med 16: 694-700, 2010.
55. Murray KC, Stephens MJ, Ballou EW, Heckman CJ, Bennett DJ. Motoneuron excitability and muscle spasms are regulated by 5-HT2B and 5-HT2C receptor activity. J Neurophysiol 105: 731-748, 2011.
56. Nowak L, Bregestovski P, Ascher P, Herbet A, Prochiantz A. Magnesium gates glutamate-activated channels in mouse central neurones. Nature 307: 462-465, 1984.
57. Palecek JI, Abdrachmanova G, Vlachova V, Vyklick L Jr. Properties of NMDA receptors in rat spinal cord motoneurons. Eur J Neurosci 11: 827-836, 1999.
58. Piehl F, Tabar G, Cullheim S. Expression of NMDA receptor mRNAs in rat motoneurons is down-regulated after axotomy. Eur J Neurosci 7: 2101-2110, 1995.
59. Power KE, McCrea DA, Fedirchuk B. Intraspinally mediated state-dependent enhancement of motoneurone excitability during fictive scratch in the adult decerebrate cat. J Physiol 588: 2839-2857, 2010.
60. Powers RK, Binder MD. Input-output functions of mammalian motoneurons. Rev Physiol Biochem Pharmacol 143: 137-263, 2001.
61. Rank MM, Murray KC, Stephens MJ, D'Amico J, Gorassini MA, Bennett DJ. Adrenergic receptors modulate motoneuron excitability, sensory synaptic transmission and muscle spasms after chronic spinal cord injury. J Neurophysiol 105: 410-422, 2011.
62. Rioult-Pedotti MS. Intrinsic NMDA-induced oscillations in motoneurons of an adult vertebrate spinal cord are masked by inhibition. J Neurophysiol 77: 717-730, 1997.
63. Rossignol S. Neural control of stereotypic limb movements. In: Handbook of Physiology. Exercise: Regulation and Integration of Multiple Systems. Bethesda, MD: Am. Physiol. Soc., 1996, p. 173-216.
64. Schmidt BJ, Hochman S, MacLean JN. NMDA receptor-mediated oscillatory properties: potential role in rhythm generation in the mammalian spinal cord. Ann NY Acad Sci 860: 189-202, 1998.
65. Schwindt P, Crill WE. A persistent negative resistance in cat lumbar motoneurons. Brain Res 120: 173-178, 1977.
66. Svirskis G, Hounsgaard J. Transmitter regulation of plateau properties in turtle motoneurons. J Neurophysiol 79: 45-50, 1998.
67. Tolle TR, Berthele A, Zieglgansberger W, Seeburg PH, Wisden W. The differential expression of 16 NMDA and non-NMDA receptor subunits in the rat spinal cord and in periaqueductal gray. J Neurosci 13: 5009-5028, 1993.
68. Wallen P, Grillner S. The effect of current passage on N-methyl-D-aspartateinduced, tetrodotoxin-resistant membrane potential oscillations in lamprey neurons active during locomotion. Neurosci Lett 56: 87-93, 1985.
69. Wallen P, Grillner S. N-methyl-D-aspartate receptor-induced, inherent oscillatory activity in neurons active during fictive locomotion in the lamprey. J Neurosci 7: 2745-2755, 1987.
70. Walton KD, Navarrete R. Postnatal changes in motoneurone electrotonic coupling studied in the in vitro rat lumbar spinal cord. J Physiol 433: 283-305, 1991.
71. Wee KS, Zhang Y, Khanna S, Low CM. Immunolocalization of NMDA receptor subunit NR3B in selected structures in the rat forebrain, cerebellum, and lumbar spinal cord. J Comp Neurol 509: 118-135, 2008.
72. Wenner P, O'Donovan MJ, Matise MP. Topographical and physiological characterization of interneurons that express engrailed-1 in the embryonic chick spinal cord. J Neurophysiol 84: 2651-2657, 2000.
73. Zagoraiou L, Akay T, Martin JF, Brownstone RM, Jessell TM, Miles GB. A cluster of cholinergic premotor interneurons modulates mouse locomotor activity. Neuron 64: 645-662, 2009.