Participation of a persistent sodium current and calcium-activated nonspecific cationic current to burst generation in trigeminal principal sensory neurons

Journal of Neurophysiology

Volumn 110, Issue 8, 2013, Pages 1903-1914

  Tsuruyama, Kentaro ^a   Hsiao, Chie Fang ^a   Chandler, Scott H ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Bursting; CPG; In vitro; Mastication; Patch clamp

Indexed keywords

RILUZOLE; VERATRIDINE;

ACTION POTENTIAL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; BRAIN STEM; CALCIUM ACTIVATED NONSPECIFIC CATIONIC CURRENT; CALCIUM CELL LEVEL; CELL MEMBRANE DEPOLARIZATION; CEREBROSPINAL FLUID; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; EXTRACELLULAR CALCIUM; ION CURRENT; NERVE CELL MEMBRANE POTENTIAL; NONHUMAN; PATCH CLAMP; PRINCIPAL SENSORY NUCLEUS; PRIORITY JOURNAL; RAT; SENSORY NERVE CELL; SLOW WAVE SLEEP; SODIUM CURRENT; SPIKE; SPINAL CORD MOTONEURON; TRIGEMINAL MOTOR NUCLEUS; VOLTAGE CLAMP; WHOLE CELL;

BURSTING; CPG; IN VITRO; MASTICATION; PATCH CLAMP;

ACTION POTENTIALS; ANIMALS; CALCIUM; CALCIUM SIGNALING; ENDOPLASMIC RETICULUM; MEMBRANE POTENTIALS; RATS; RATS, SPRAGUE-DAWLEY; RILUZOLE; SENSORY RECEPTOR CELLS; SODIUM; TRIGEMINAL NUCLEI; VERATRIDINE;

EID: 84884578390     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00410.2013     Document Type: Article

References (61)

1. Amzica F, Massimini M, Manfridi A. Spatial buffering during slow and paroxysmal sleep oscillations in cortical networks of glial cells in vivo. J Neurosci 22: 1042-1053, 2002.
2. Athanassiadis T, Olsson KA, Kolta A, Westberg KG. Identification of c-Fos immunoreactive brainstem neurons activated during fictive mastication in the rabbit. Exp Brain Res 165: 478-489, 2005.
3. Brocard F, Verdier D, Arsenault I, Lund JP, Kolta A. Emergence of intrinsic bursting in trigeminal sensory neurons parallels the acquisition of mastication in weanling rats. J Neurophysiol 96: 2410-2424, 2006.
4. Brownstone RM, Wilson JM. Strategies for delineating spinal locomotor rhythm-generating networks and the possible role of Hb9 interneurones in rhythmogenesis. Brain Res Rev 57: 64, 2008.
5. Del Negro CA, Chandler SH. Regulation of intrinsic and synaptic properties of neonatal rat trigeminal motoneurons by metabotropic glutamate receptors. J Neurosci 18: 9216-9226, 1998.
6. Del Negro CA, Hsiao CF, Chandler SH. Outward currents influencing bursting dynamics in guinea pig trigeminal motoneurons. J Neurophysiol 81: 1478-1485, 1999.
7. Del Negro CA, Hsiao CF, Chandler SH, Garfinkel A. Evidence for a novel bursting mechanism in rodent trigeminal neurons. Biophys J 75: 174-182, 1998.
8. Del Negro CA, Koshiya N, Butera RJ Jr, Smith JC. Persistent sodium current, membrane properties and bursting behavior of pre-Botzinger complex inspiratory neurons in vitro. J Neurophysiol 88: 2242-2250, 2002a.
9. Del Negro CA, Morgado-Valle C, Feldman JL. Respiratory rhythm: an emergent network property? Neuron 34: 821-830, 2002b.
10. 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.
11. 2+-dependent nonselective cation currents and rhythmic bursting in main olfactory bulb external tufted cells. J Neurosci 29: 11943-11953, 2009.
12. Enomoto A, Han JM, Hsiao CF, Chandler SH. Sodium currents in mesencephalic trigeminal neurons from Nav1.6 null mice. J Neurophysiol 98: 710-719, 2007.
13. Feldman JL, Del Negro CA. Looking for inspiration: new perspectives on respiratory rhythm. Nat Rev Neurosci 7: 232-242, 2006.
14. 2+ can affect the pattern of discharge in rat thalamic neurons. J Physiol 535: 33-45, 2001.
15. Frankenhaeuser B, Hodgkin AL. The action of calcium on the electrical properties of squid axons. J Physiol 137: 218-244, 1957.
16. Gafni J, Munsch JA, Lam TH, Catlin MC, Costa LG, Molinski TF, Pessah IN. Xestospongins: potent membrane permeable blockers of the inositol 1,4,5-trisphosphate receptor. Neuron 19: 723-733, 1997.
17. Gogelein H, Dahlem D, Englert HC, Lang HJ. Flufenamic acid, mefenamic acid and niflumic acid inhibit single nonselective cation channels in the rat exocrine pancreas. FEBS Lett 268: 79-82, 1990.
18. 2+ activate a transient inward current in chick dorsal root ganglion cells. Biophys J 50: 753-757, 1986.
19. Harks EG, de Roos AD, Peters PH, de Haan LH, Brouwer A, Ypey DL, van Zoelen EJ, Theuvenet AP. Fenamates: a novel class of reversible gap junction blockers. J Pharmacol Exp Ther 298: 1033-1041, 2001.
20. Harris-Warrick RM. General principles of rhythmogenesis in central pattern generator networks. Prog Brain Res 187: 213-222, 2010.
21. Heinemann U, Lux HD, Gutnick MJ. Extracellular free calcium and potassium during paroxysmal activity in the cerebral cortex of the cat. Exp Brain Res 27: 237-243, 1977.
22. Hille B. Ion Channels of Excitable Membranes. Sunderland, MA: Sinauer, 2001.
23. Hsiao CF, Gougar K, Asai J, Chandler SH. Intrinsic membrane properties and morphological characteristics of interneurons in the rat supratrigeminal region. J Neurosci Res 85: 3673-3686, 2007.
24. Hsiao CF, Kaur G, Vong A, Bawa H, Chandler SH. Participation of Kv1 channels in control of membrane excitability and burst generation in mesencephalic V neurons. J Neurophysiol 101: 1407-1418, 2009.
25. 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.
26. Kadiri LR, Kwan AC, Webb WW, Harris-Warrick RM. Dopamineinduced oscillations of the pyloric pacemaker neuron rely on release of calcium from intracellular stores. J Neurophysiol 106: 1288-1298, 2011.
27. Kiehn O, Dougherty KJ, Hägglund M, Borgius L, Talpalar A, Restrepo CE. Probing spinal circuits controlling walking in mammals. Biochem Biophys Res Commun 396: 11, 2010.
28. Kiehn O, Johnson BR, Raastad M. Plateau properties in mammalian spinal interneurons during transmitter-induced locomotor activity. Neuroscience 75: 263-273, 1996.
29. + channels by flufenamic acid. Membr Cell Biol 14: 285-298, 2000.
30. Kogo M, Tanaka S, Chandler SH, Matsuya T. Examination of the relationships between jaw opener and closer rhythmical muscle activity in an in vitro brainstem jaw-attached preparation. Somatosens Mot Res 15: 200-210, 1998.
31. Kolta A, Brocard F, Verdier D, Lund JP. A review of burst generation by trigeminal main sensory neurons. Arch Oral Biol 52: 325-328, 2007.
32. Kolta A, Westberg KG, Lund JP. Identification of brainstem interneurons projecting to the trigeminal motor nucleus and adjacent structures in the rabbit. J Chem Neuroanat 19: 175-195, 2000.
33. Kramer RH, Zucker RS. Calcium-dependent inward current in Aplysia bursting pace-maker neurones. J Physiol 362: 107-130, 1985.
34. 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.
35. Li J, Baccei ML. Pacemaker neurons within newborn spinal pain circuits. J Neurosci 31: 9010-9022, 2011.
36. Li Z, Hatton GI. Oscillatory bursting of phasically firing rat supraoptic neurones in low-Ca2+ medium: Na+ influx, cytosolic Ca2+ and gap junctions. J Physiol 496: 379-394, 1996.
37. Lu B, Zhang Q, Wang H, Wang Y, Nakayama M, Ren D. Extracellular calcium controls background current and neuronal excitability via an UNC79-UNC80-NALCN cation channel complex. Neuron 68: 488-499, 2010.
38. Morquette P, Lavoie R, Fhima MD, Lamoureux X, Verdier D, Kolta A. Generation of the masticatory central pattern and its modulation by sensory feedback. Prog Neurobiol 96: 340-355, 2012.
39. Ottolia M, Toro L. Potentiation of large conductance KCa channels by niflumic, flufenamic, and mefenamic acids. Biophys J 67: 2272-2279, 1994.
40. Pace RW, Mackay DD, Feldman JL, Del Negro CA. Inspiratory bursts in the preBotzinger complex depend on a calcium-activated non-specific cation current linked to glutamate receptors in neonatal mice. J Physiol 582: 113-125, 2007.
41. Pena F, Parkis MA, Tryba AK, Ramirez JM. Differential contribution of pacemaker properties to the generation of respiratory rhythms during normoxia and hypoxia. Neuron 43: 105, 2004a.
42. Pena F, Parkis MA, Tryba AK, Ramirez JM. Differential contribution of pacemaker properties to the generation of respiratory rhythms during normoxia and hypoxia. Neuron 43: 105-117, 2004b.
43. Pumain R, Heinemann U. Extracellular calcium and potassium changes in mammalian neocortex. Adv Biochem Psychopharmacol 29: 53-58, 1981.
44. Purvis LK, Smith JC, Koizumi H, Butera RJ. Intrinsic bursters increase the robustness of rhythm generation in an excitatory network. J Neurophysiol 97: 1515-1526, 2007.
45. Rubin JE, Hayes JA, Mendenhall JL, Del Negro CA. Calcium-activated nonspecific cation current and synaptic depression promote network-dependent burst oscillations. Proc Natl Acad Sci USA 106: 2939-2944, 2009.
46. Sakmann B, Neher E. Single Channel Recording. New York: Plenum, 1995.
47. Sandler VM, Puil E, Schwarz DW. Intrinsic response properties of bursting neurons in the nucleus principalis trigemini of the gerbil. Neuroscience 83: 891-904, 1998.
48. Shigenaga Y, Okamoto T, Nishimori T, Suemune S, Nasution ID, Chen IC, Tsuru K, Yoshida A, Tabuchi K, Hosoi M, Tsuru H. Oral and facial representation in the trigeminal principal and rostral spinal nuclei of the cat. J Comp Neurol 244: 1-18, 1986.
49. Smith SM, Bergsman JB, Harata NC, Scheller RH, Tsien RW. Recordings from single neocortical nerve terminals reveal a nonselective cation channel activated by decreases in extracellular calcium. Neuron 41: 243-256, 2004.
50. Su H, Alroy G, Kirson ED, Yaari Y. Extracellular calcium modulates persistent sodium current-dependent burst-firing in hippocampal pyramidal neurons. J Neurosci 21: 4173-4182, 2001.
51. Tanaka S, Kogo M, Chandler SH, Matsuya T. Localization of oral-motor rhythmogenic circuits in the isolated rat brainstem preparation. Brain Res 821: 190-199, 1999.
52. 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.
53. Tsuboi A, Kolta A, Chen CC, Lund JP. Neurons of the trigeminal main sensory nucleus participate in the generation of rhythmic motor patterns. Eur J Neurosci 17: 229-238, 2003.
54. Turman J Jr, Chandler SH. Immunohistochemical evidence for GABA and glycine-containing trigeminal premotoneurons in the guinea pig. Synapse 18: 7-20, 1994a.
55. Turman JE Jr, Chandler SH. Immunohistochemical localization of glutamate and glutaminase in guinea pig trigeminal premotoneurons. Brain Res 634: 49-61, 1994b.
56. Urbani A, Belluzzi O. Riluzole inhibits the persistent sodium current in mammalian CNS neurons. Eur J Neurosci 12: 3567-3574, 2000.
57. Westneat MW, Hall WG. Ontogeny of feeding motor patterns in infant rats: an electromyographic analysis of suckling and chewing. Behav Neurosci 106: 539-554, 1992.
58. Wilson JM, Blagovechtchenski E, Brownstone RM. Genetically defined inhibitory neurons in the mouse spinal cord dorsal horn: a possible source of rhythmic inhibition of motoneurons during fictive locomotion. J Neurosci 30: 1137-1148, 2010.
59. Wu N, Enomoto A, Tanaka S, Hsiao CF, Nykamp DQ, Izhikevich E, Chandler SH. Persistent sodium currents in mesencephalic v neurons participate in burst generation and control of membrane excitability. J Neurophysiol 93: 2710-2722, 2005.
60. Wu N, Hsiao CF, Chandler SH. Membrane resonance and subthreshold membrane oscillations in mesencephalic V neurons: participants in burst generation. J Neurosci 21: 3729-3739, 2001.
61. Yoshida A, Hiraga T, Moritani M, Chen K, Takatsuki Y, Hirose Y, Bae YC, Shigenaga Y. Morphologic characteristics of physiologically defined neurons in the cat trigeminal nucleus principalis. J Comp Neurol 401: 308-328, 1998.