Sodium-mediated plateau potentials in lumbar motoneurons of neonatal rats

Journal of Neuroscience

Volumn 33, Issue 39, 2013, Pages 15626-15641

  Bouhadfane, Mouloud ^a   Tazerart, Sabrina ^a   Moqrich, Aziz ^b   Vinay, Laurent ^a   Brocard, Frédéric ^a  

^a AIX MARSEILLE UNIVERSITÉ   (France)

^b AIX MARSEILLE UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

SODIUM CALCIUM EXCHANGE PROTEIN; VANILLOID RECEPTOR; VOLTAGE GATED CALCIUM CHANNEL;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CONTROLLED STUDY; ELECTROPHYSIOLOGY; ION CONDUCTANCE; ION TRANSPORT; MOTONEURON; NERVE CELL MEMBRANE STEADY POTENTIAL; NEWBORN; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; RAT; RECEPTOR POTENTIAL; RECEPTOR UPREGULATION; SPIKE WAVE; TRICEPS SURAE MUSCLE;

ACTION POTENTIALS; ANIMALS; BORON COMPOUNDS; CALCIUM; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS, L-TYPE; FLUFENAMIC ACID; HOT TEMPERATURE; MOTOR NEURONS; PROBENECID; RATS; RATS, WISTAR; SODIUM; SPINAL CORD; TRPV CATION CHANNELS;

EID: 84884539375     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1483-13.2013     Document Type: Article

References (108)

1. Altman J, Sudarshan K (1975) Postnatal development of locomotion in the laboratory rat. Anim Behav 23:896-920. CrossRef Medline
2. Angstadt JD, Choo JJ (1996) Sodium-dependent plateau potentials in cultured Retzius cells of the medicinal leech. J Neurophysiol 76:1491-1502. Medline
3. Bang S, Kim KY, Yoo S, Lee SH, Hwang SW (2007) Transient receptor potential V2 expressed in sensory neurons is activated by probenecid. Neurosci Lett 425:120-125. CrossRef Medline
4. Bang S, Yoo S, Yang TJ, Cho H, Hwang SW (2011) Isopentenyl pyrophosphate is a novel antinociceptive substance that inhibits TRPV3 and TRPA1 ion channels. Pain 152:1156-1164. CrossRef Medline
5. Benham CD, Gunthorpe MJ, Davis JB (2003) TRPV channels as temperature sensors. Cell Calcium 33:479-487. CrossRef Medline
6. Bennett DJ, Hultborn H, Fedirchuk B, Gorassini M (1998) Short-term plasticity in hindlimb motoneurons of decerebrate cats. J Neurophysiol 80: 2038-2045. Medline
7. Beurrier C, Bioulac B, Hammond C (2000) Slowly inactivating sodium current (INaP) underlies single-spike activity in rat subthalamic neurons. J Neurophysiol 83:1951-1957. Medline
8. Booth V, Rinzel J (1995) A minimal, compartmental model for a dendritic origin of bistability of motoneuron firing patterns. J Comput Neurosci 2:299-312. CrossRef Medline
9. Bregman BS (1987) Development of serotonin immunoreactivity in the rat spinal cord and its plasticity after neonatal spinal cord lesions. Brain Res 431:245-263. Medline
10. Brocard F, Vinay L, Clarac F (1999) Development of hindlimb postural control during the first postnatal week in the rat. Brain Res Dev Brain Res 117:81-89. CrossRef Medline
11. + reveal pacemakers in the spinal locomotor-related network. Neuron 77:1047-1054. CrossRef Medline
12. Brownstone RM (2006) Beginning at the end: repetitive firing properties in the final common pathway. Prog Neurobiol 78:156-172. CrossRef Medline
13. 2+ channels in motoneurons based on variable threshold of activation of persistent inward currents. J Neurophysiol 95:225-241. CrossRef Medline
14. Carlin KP, Jiang Z, Brownstone RM (2000a) Characterization of calcium currents in functionally mature mouse spinal motoneurons. Eur J Neurosci 12:1624-1634. CrossRef Medline
15. Carlin KP, Jones KE, Jiang Z, Jordan LM, Brownstone RM (2000b) Dendritic L-type calcium currents in mouse spinal motoneurons: implications for bistability. Eur J Neurosci 12:1635-1646. CrossRef Medline
16. Carlin KP, Bui TV, Dai Y, Brownstone RM (2009) Staircase currents in motoneurons: insight into the spatial arrangement of calcium channels in the dendritic tree. J Neurosci 29:5343-5353. CrossRef Medline
17. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389:816-824. CrossRef Medline
18. Cattaert D, Araque A, Buno W, Clarac F (1994) Motor neurons of the crayfish walking system possess TEA-revealed regenerative electrical properties. J Exp Biol 188:339-345. Medline
19. Cazalets JR, Menard I, Crémieux J, Clarac F (1990) Variability as a characteristic of immature motor systems: an electromyographic study of swimming in the newborn rat. Behav Brain Res 40:215-225. CrossRef Medline
20. Chang SY, Kim U (2004) Ionic mechanism of long-lasting discharges of action potentials triggered by membrane hyperpolarization in the medial lateral habenula. J Neurosci 24:2172-2181. CrossRef Medline
21. Clarac F, Brocard F, Vinay L (2004) The maturation of locomotor networks. Prog Brain Res 143:57-66. CrossRef Medline
22. Collins DF, Burke D, Gandevia SC (2001) Large involuntary forces consistent with plateau-like behavior of human motoneurons. J Neurosci 21: 4059-4065. Medline
23. Conway BA, Hultborn H, Kiehn O, Mintz I (1988) Plateau potentials in alpha-motoneurones induced by intravenous injection of L-dopa and clonidine in the spinal cat. J Physiol 405:369-384. Medline
24. Crone C, Hultborn H, Kiehn O, Mazieres L, Wigström H (1988) Maintained changes in motoneuronal excitability by short-lasting synaptic inputs in the decerebrate cat. J Physiol 405:321-343. Medline
25. 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. CrossRef Medline
26. Derjean D, Bertrand S, Nagy F, Shefchyk SJ (2005) Plateau potentials and membrane oscillations in parasympathetic preganglionic neurones and intermediolateral neurones in the rat lumbosacral spinal cord. J Physiol 563:583-596. CrossRef Medline
27. Di Prisco GV, Pearlstein E, Robitaille R, Dubuc R (1997) Role of sensory-evokedNMDAplateau potentials in the initiation of locomotion. Science 278:1122-1125. CrossRef Medline
28. Di Prisco GV, Pearlstein E, Le Ray D, Robitaille R, Dubuc R (2000) Acellular mechanism for the transformation of a sensory input into a motor command. J Neurosci 20:8169-8176. Medline
29. Eken T, Hultborn H, Kiehn O (1989) Possible functions of transmittercontrolled plateau potentials in alpha motoneurones. Prog Brain Res 80: 257-267; discussion 239-242. CrossRef Medline
30. Facer P, Casula MA, Smith GD, Benham CD, Chessell IP, Bountra C, Sinisi M, Birch R, Anand P (2007) Differential expression of the capsaicin receptor TRPV1 and related novel receptors TRPV3, TRPV4 and TRPM8 in normal human tissues and changes in traumatic and diabetic neuropathy. BMC Neurol 7:11. CrossRef Medline
31. Fady JC, Jamon M, Clarac F (1998) Early olfactory-induced rhythmic limb activity in the newborn rat. Brain Res Dev Brain Res 108:111-123. CrossRef Medline
32. Fowler SJ, Kellogg C (1975) Ontogeny of thermoregulatory mechanisms in the rat. J Comp Physiol Psychol 89:738-746. CrossRef Medline
33. Fraser DD, MacVicar BA (1996) Cholinergic-dependent plateau potential in hippocampal CA1 pyramidal neurons. J Neurosci 16:4113-4128. Medline
34. Friedman A, Arens J, Heinemann U, Gutnick MJ (1992) Slow depolarizing afterpotentials in neocortical neurons are sodium and calciumdependent. Neurosci Lett 135:13-17. CrossRef Medline
35. Gao BX, Ziskind-Conhaim L (1998) Development of ionic currents underlying changes in action potential waveforms in rat spinal motoneurons. J Neurophysiol 80:3047-3061. Medline
36. Gorassini MA, Bennett DJ, Yang JF (1998) Self-sustained firing of human motor units. Neurosci Lett 247:13-16. CrossRef Medline
37. Gorassini M, Bennett DJ, Kiehn O, Eken T, Hultborn H (1999) Activation patterns of hindlimb motor units in the awake rat and their relation to motoneuron intrinsic properties. J Neurophysiol 82:709-717. Medline
38. Grillner S, Zangger P (1975) How detailed is the central pattern generation for locomotion? Brain Res 88:367-371. CrossRef Medline
39. Guinamard R, Simard C, Del Negro C (2013) Flufenamic acid as an ion channel modulator. Pharmacol Ther 138:272-284. CrossRef Medline
40. Harteneck C, Gollasch M (2011) Pharmacological modulation of diacylglycerol-sensitive TRPC3/6/7 channels. Curr Pharm Biotechnol 12: 35-41. CrossRef Medline
41. 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. CrossRef Medline
42. Hasuo H, Phelan KD, Twery MJ, Gallagher JP (1990) A calcium-dependent slow afterdepolarization recorded in rat dorsolateral septal nucleus neurons in vitro. J Neurophysiol 64:1838-1846. Medline
43. Heckman CJ, Lee RH, Brownstone RM (2003) Hyperexcitable dendrites in motoneurons and their neuromodulatory control during motor behavior. Trends Neurosci 26:688-695. CrossRef Medline
44. Heckman CJ, Hyngstrom AS, Johnson MD (2008a) Active properties of motoneurone dendrites: diffuse descending neuromodulation, focused local inhibition. J Physiol 586:1225-1231. CrossRef Medline
45. Heckman CJ, Johnson M, Mottram C, Schuster J (2008b) Persistent inward currents in spinal motoneurons and their influence on human motoneuron firing patterns. Neuroscientist 14:264-275. CrossRef Medline
46. Hisanaga E, Nagasawa M, Ueki K, Kulkarni RN, Mori M, Kojima I (2009) Regulation of calcium-permeable TRPV2 channel by insulin in pancreatic beta-cells. Diabetes 58:174-184. CrossRef Medline
47. Hounsgaard J, Kiehn O (1989) Serotonin-induced bistability of turtle motoneurones caused by a nifedipine-sensitive calcium plateau potential. J Physiol 414:265-282. Medline
48. Hounsgaard J, Kiehn O (1993) Calcium spikes and calcium plateaux evoked by differential polarization in dendrites of turtle motoneurones in vitro. J Physiol 468:245-259. Medline
49. Hounsgaard J, Mintz I (1988) Calcium conductance and firing properties of spinal motoneurones in the turtle. J Physiol 398:591-603. Medline
50. Hounsgaard J, Hultborn H, Jespersen B, Kiehn O (1984) Intrinsic membrane properties causing a bistable behaviour of alpha-motoneurones. Exp Brain Res 55:391-394. Medline
51. Hounsgaard J, Hultborn H, Jespersen B, Kiehn O (1988) Bistability of alpha-motoneurones in the decerebrate cat and in the acute spinal cat after intravenous 5-hydroxytryptophan. J Physiol 405:345-367. Medline
52. 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. Medline
53. Hu HZ, Gu Q, Wang C, Colton CK, Tang J, Kinoshita-Kawada M, Lee LY, Wood JD, Zhu MX (2004) 2-aminoethoxydiphenyl borate is a common activator of TRPV1, TRPV2, and TRPV3. J Biol Chem 279:35741-35748. CrossRef Medline
54. Hultborn H, Wigström H, Wangberg B (1975) Prolonged activation of soleus motoneurones following a conditioning train in soleus Ia afferents: a case for a reverberating loop? Neurosci Lett 1:147-152. CrossRef Medline
55. Jasinski PE, Molkov YI, Shevtsova NA, Smith JC, Rybak IA (2013) Sodium and calcium mechanisms of rhythmic bursting in excitatory neural networks of the pre-Bötzinger complex: a computational modelling study. Eur J Neurosci 37:212-230. CrossRef Medline
56. Jiang Z, Rempel J, Li J, Sawchuk MA, Carlin KP, Brownstone RM (1999) Development of L-type calcium channels and a nifedipine-sensitive motor activity in the postnatal mouse spinal cord. Eur J Neurosci 11:3481-3487. CrossRef Medline
57. Jones HC, Keep RF (1988) Brain fluid calcium concentration and response to acute hypercalcaemia during development in the rat. J Physiol 402: 579-593. Medline
58. Kiehn O, Eken T (1997) Prolonged firing in motor units: evidence of plateau potentials in human motoneurons? J Neurophysiol 78:3061-3068. Medline
59. Kiehn O, Eken T (1998) Functional role of plateau potentials in vertebrate motor neurons. Curr Opin Neurobiol 8:746-752. CrossRef Medline
60. Kiehn O, Harris-Warrick RM (1992) Serotonergic stretch receptors induce plateau properties in a crustacean motor neuron by a dual-conductance mechanism. J Neurophysiol 68:485-495. Medline
61. Kuo JJ, Lee RH, Zhang L, Heckman CJ (2006) Essential role of the persistent sodium current in spike initiation during slowly rising inputs in mouse spinal neurones. J Physiol 574:819-834. CrossRef Medline
62. Lee CR, Tepper JM (2007) A calcium-activated nonselective cation conductance underlies the plateau potential in rat substantia nigra GABAergic neurons. J Neurosci 27:6531-6541. CrossRef Medline
63. Lee RH, Heckman CJ (1998) Bistability in spinal motoneurons in vivo: systematic variations in persistent inward currents. J Neurophysiol 80:583-593. Medline
64. Lee RH, Heckman CJ (2001) Essential role of a fast persistent inward current in action potential initiation and control of rhythmic firing. J Neurophysiol 85:472-475. Medline
65. Leffler A, Linte RM, Nau C, Reeh P, Babes A (2007) A high-threshold heatactivated channel in cultured rat dorsal root ganglion neurons resembles TRPV2 and is blocked by gadolinium. Eur J Neurosci 26:12-22. CrossRef Medline
66. Lewinter RD, Skinner K, Julius D, Basbaum AI (2004) Immunoreactive TRPV-2 (VRL-1), a capsaicin receptor homolog, in the spinal cord of the rat. J Comp Neurol 470:400-408. CrossRef Medline
67. Li Y, Bennett DJ (2003) Persistent sodium and calcium currents cause plateau potentials in motoneurons of chronic spinal rats. J Neurophysiol 90:857-869. CrossRef Medline
68. Li Y, Gorassini MA, Bennett DJ (2004) Role of persistent sodium and calcium currents in motoneuron firing and spasticity in chronic spinal rats. J Neurophysiol 91:767-783. CrossRef Medline
69. Ma W, Hui H, Pelegrin P, Surprenant A (2009) Pharmacological characterization of pannexin-1 currents expressed in mammalian cells. J Pharmacol Exp Ther 328:409-418. CrossRef Medline
70. Mandadi S, Nakanishi ST, Takashima Y, Dhaka A, Patapoutian A, McKemy DD, Whelan PJ (2009) Locomotor networks are targets of modulation by sensory transient receptor potential vanilloid 1 and transient receptor potential melastatin 8 channels. Neuroscience 162:1377-1397. CrossRef Medline
71. Mejia-Gervacio S, Hounsgaard J, Diaz-Munoz M (2004) Roles of ryanodine and inositol triphosphate receptors in regulation of plateau potentials in turtle spinal motoneurons. Neuroscience 123:123-130. CrossRef Medline
72. Montell C (2005) The TRP superfamily of cation channels. Sci STKE 2005: re3. CrossRef Medline
73. Moqrich A, Hwang SW, Earley TJ, Petrus MJ, Murray AN, Spencer KS, Andahazy M, Story GM, Patapoutian A (2005) Impaired thermosensation in mice lacking TRPV3, a heat and camphor sensor in the skin. Science 307:1468-1472. CrossRef Medline
74. Moran MM, Xu H, Clapham DE (2004) TRP ion channels in the nervous system. Curr Opin Neurobiol 14:362-369. CrossRef Medline
75. Morisset V, Nagy F (1999) Ionic basis for plateau potentials in deep dorsal horn neurons of the rat spinal cord. J Neurosci 19:7309-7316. Medline
76. Mrejeru A, Wei A, Ramirez JM (2011) Calcium-activated nonselective cation currents are involved in generation of tonic and bursting activity in dopamine neurons of the substantia nigra pars compacta. J Physiol 589: 2497-2514. CrossRef Medline
77. Nicholson C, Bruggencate GT, Steinberg R, Stöckle H (1977) Calcium modulation in brain extracellular microenvironment demonstrated with ionselective micropipette. Proc Natl Acad Sci U S A 74:1287-1290. CrossRef Medline
78. Nishimura Y, Schwindt PC, Crill WE (1989) Electrical properties of facial motoneurons in brainstem slices from guinea pig. Brain Res 502:127-142. CrossRef Medline
79. Pambo-Pambo A, Durand J, Gueritaud JP (2009) Early excitability changes in lumbar motoneurons of transgenic SOD1G85R and SOD1G(93A-low) mice. J Neurophysiol 102:3627-3642. CrossRef Medline
80. Partridge LD, Swandulla D (1988) Calcium-activated nonspecific cation channels. Trends Neurosci 11:69-72. CrossRef Medline
81. Perrier JF, Delgado-Lezama R (2005) Synaptic release of serotonin induced by stimulation of the raphe nucleus promotes plateau potentials in spinal motoneurons of the adult turtle. J Neurosci 25:7993-7999. CrossRef Medline
82. Perrier JF, Hounsgaard J (1999) Ca(2+)-activated nonselective cationic current (I(CAN)) in turtle motoneurons. J Neurophysiol 82:730-735. Medline
83. Perrier JF, Hounsgaard J (2000) Development and regulation of response properties in spinal cord motoneurons. Brain Res Bull 53:529-535. CrossRef Medline
84. Perrier JF, Tresch MC (2005) Recruitment of motor neuronal persistent inward currents shapes withdrawal reflexes in the frog. J Physiol 562:507-520. CrossRef Medline
85. Powers RK, Binder MD (2003) Persistent sodium and calcium currents in rat hypoglossal motoneurons. J Neurophysiol 89:615-624. Medline
86. Raggenbass M, Pierson P, Metzger D, Alberi S (1997) Action of a metabotropic glutamate receptor agonist in rat lateral septum: induction of a sodium-dependent inward aftercurrent. Brain Res 776:75-87. CrossRef Medline
87. Rajaofetra N, Sandillon F, Geffard M, Privat A (1989) Pre- and post-natal ontogeny of serotonergic projections to the rat spinal cord. J Neurosci Res 22:305-321. CrossRef Medline
88. Rajaofetra N, Poulat P, Marlier L, Geffard M, Privat A (1992) Pre- and postnatal development of noradrenergic projections to the rat spinal cord: an immunocytochemical study. Brain Res Dev Brain Res 67:237-246. CrossRef Medline
89. Reichling DB, MacDermott AB (1991) Lanthanum actions on excitatory amino acid-gated currents and voltage-gated calcium currents in rat dorsal horn neurons. J Physiol 441:199-218. Medline
90. Rekling JC and Feldman JL (1997) Calcium-dependent plateau potentials in rostral ambiguus neurons in the newborn mouse brain stem in vitro. J Neurophysiol 78:2483-2492.
91. 2+ exchanger in presynaptic boutons of hippocampal cells in culture. Neuron 15:1077-1084. CrossRef Medline
92. Russo RE, Hounsgaard J (1996) Plateau-generating neurones in the dorsal horn in an in vitro preparation of the turtle spinal cord. J Physiol 493:39-54. Medline
93. Sadlaoud K, Tazerart S, Brocard C, Jean-Xavier C, Portalier P, Brocard F, Vinay L, Bras H (2010) Differential plasticity of the GABAergic and glycinergic synaptic transmission to rat lumbar motoneurons after spinal cord injury. J Neurosci 30:3358-3369. CrossRef Medline
94. Schwindt PC, Crill WE (1980) Properties of a persistent inward current in normal and TEA-injected motoneurons. J Neurophysiol 43:1700-1724. Medline
95. Tazerart S, Viemari JC, Darbon P, Vinay L, Brocard F (2007) Contribution of persistent sodium current to locomotor pattern generation in neonatal rats. J Neurophysiol 98:613-628. CrossRef Medline
96. 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. CrossRef Medline
97. 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. Medline
98. Tsuruyama K, Hsiao CF, Chandler SH (2013) Participation of a persistent sodium current and calcium-activated non-specific cationic current to burst generation in trigeminal principal sensory neurons. J Neurophysiol, in press. CrossRef Medline
99. Vinay L, Brocard F, Clarac F (2000a) Differential maturation of motoneurons innervating ankle flexor and extensor muscles in the neonatal rat. Eur J Neurosci 12:4562-4566. CrossRef Medline
100. Vinay L, Brocard F, Pflieger JF, Simeoni-Alias J, Clarac F (2000b) Perinatal development of lumbar motoneurons and their inputs in the rat. Brain Res Bull 53:635-647. CrossRef Medline
101. Vinay L, Brocard F, Clarac F, Norreel JC, Pearlstein E, Pflieger JF (2002) Development of posture and locomotion: an interplay of endogenously generated activities and neurotrophic actions by descending pathways. Brain Res Rev 40:118-129. CrossRef Medline
102. Vincent F, Acevedo A, Nguyen MT, Dourado M, DeFalco J, Gustafson A, Spiro P, Emerling DE, Kelly MG, Duncton MA (2009) Identification and characterization of novel TRPV4 modulators. Biochem Biophys Res Commun 389:490-494. CrossRef Medline
103. Watanabe H, Davis JB, Smart D, Jerman JC, Smith GD, Hayes P, Vriens J, Cairns W, Wissenbach U, Prenen J, Flockerzi V, Droogmans G, Benham CD, Nilius B (2002) Activation of TRPV4 channels (hVRL-2/mTRP12) by phorbol derivatives. J Biol Chem 277:13569-13577. CrossRef Medline
104. Westerga J, Gramsbergen A (1990) The development of locomotion in the rat. Brain Res Dev Brain Res 57:163-174. CrossRef Medline
105. Wu LJ, Sweet TB, Clapham DE (2010) International union of basic and clinical pharmacology: LXXVI. Current progress in the mammalian TRP ion channel family. Pharmacol Rev 62:381-404. CrossRef Medline
106. 2+-activated nonselective cation channels in neuroblastoma. Nature 296:357-359. CrossRef Medline
107. Zhang B, Wootton JF, Harris-Warrick RM (1995) Calcium-dependent plateau potentials in a crab stomatogastric ganglion motor neuron: II. Calcium-activated slow inward current. J Neurophysiol 74:1938-1946. Medline
108. Zhu ZT, Munhall A, Shen KZ, Johnson SW (2004) Calcium-dependent subthreshold oscillations determine bursting activity induced by N-methyl-D-aspartate in rat subthalamic neurons in vitro. Eur J Neurosci 19:1296-1304. CrossRef Medline