Importance of chloride homeostasis in the operation of rhythmic motor networks

Progress in Brain Research

Volumn 188, Issue , 2011, Pages 3-14

  Viemari, Jean Charles ^a   Bos, Rémi ^a   Boulenguez, Pascale ^a   Brocard, Cécile ^a   Brocard, Frédéric ^a   Bras, Hélène ^a   Coulon, Patrice ^a   Liabeuf, Sylvie ^a   Pearlstein, Edouard ^a   Sadlaoud, Karina ^a   Stil, Aurélie ^a   Tazerart, Sabrina ^a   Vinay, Laurent ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

Author keywords

Activity; Chloride; Inhibition; KCC2; Networks

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; CHLORIDE ION; POTASSIUM ION; SODIUM ION; CHLORIDE; GLYCINE;

BOOK; CHLORIDE TRANSPORT; CPG ISLAND; HOMEOSTASIS; HUMAN; LOCOMOTION; MOTONEURON; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE POTENTIAL; NEUROMUSCULAR SYNAPSE; POLARIZATION AND DEPOLARIZATION; POSTSYNAPTIC INHIBITION; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; SENSORY NERVE; SPINAL CORD INJURY; ANIMAL; CELL MEMBRANE POTENTIAL; CYTOLOGY; METABOLISM; NERVE CELL; NERVE CELL NETWORK; PATHOPHYSIOLOGY; PERIODICITY; PHYSIOLOGY; REVIEW; SPINAL CORD; SPINAL GANGLION;

ANIMALS; CHLORIDES; GAMMA-AMINOBUTYRIC ACID; GANGLIA, SPINAL; GLYCINE; HOMEOSTASIS; LOCOMOTION; MEMBRANE POTENTIALS; NERVE NET; NEURONS; PERIODICITY; SPINAL CORD; SPINAL CORD INJURIES;

EID: 79951620270     PISSN: 00796123     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-444-53825-3.00006-1     Document Type: Chapter

References (75)

1. Abdul-Razzak R., Bagust J., Kerkut G.A. Postnatal changes in the dorsal root reflex in the isolated spinal cord of the hamster Mesocricetus auratus. Comparative Biochemistry and Physiology 1994, 107C:195-204.
2. Alvarez F.J. Anatomical basis for presynaptic inhibition of primary sensory fibers. Presynaptic inhibition and neural control 1998, 13-49. Oxford University Press, Oxford. P. Rudomin, L.M. Romo, S. Mendell (Eds.).
3. Alvarez-Leefmans F.J., Nani A., Marquez S. Chloride transport, osmotic balance, and presynaptic inhibition. Presynaptic inhibition and neural control 1998, 50-79. Oxford University Press, Oxford. P. Rudomin, R. Romo, L.M. Mendell (Eds.).
4. Bagust J., Kerkut G.A., Rakkah N.I.A. The dorsal root reflex in isolated mammalian spinal cord. Comparative Biochemistry and Physiology 1989, 93A:151-160.
5. Barron D.H., Matthews B.H.C. Dorsal root reflexes. Journal of Physiology (London) 1938, 94:26P-27P.
6. Beloozerova I., Rossignol S. Antidromic discharges in dorsal roots of decerebrate cats. I: Studies at rest and during fictive locomotion. Brain Research 1999, 846:87-105.
7. Beloozerova I.N., Rossignol S. Antidromic discharges in dorsal roots of decerebrate cats. II: Studies during treadmill locomotion. Brain Research 2004, 996:227-236.
8. Boorman G.I., Lee R.G., Becker W.J., Windhorst U.R. Impaired "natural reciprocal inhibition" in patients with spasticity due to incomplete spinal cord injury. Electroencephalography and Clinical Neurophysiology 1996, 101:84-92.
9. Boulenguez P., Liabeuf S., Bos R., Bras H., Jean-Xavier C., Brocard C., et al. Down-regulation of the potassium-chloride cotransporter KCC2 contributes to spasticity after spinal cord injury. Nature Medicine 2010, 16:302-307.
10. Brocard F., Vinay L., Clarac F. Gradual development of the ventral funiculus input to lumbar motoneurons in the neonatal rat. Neuroscience 1999, 90:1543-1554.
11. Busselberg D., Bischoff A.M., Becker K., Becker C.M., Richter D.W. The respiratory rhythm in mutant oscillator mice. Neuroscience Letters 2001, 316:99-102.
12. Busselberg D., Bischoff A.M., Paton J.F., Richter D.W. Reorganisation of respiratory network activity after loss of glycinergic inhibition. Pflügers Archiv 2001, 441:444-449.
13. Chen Y., Bagust J., Kerkut G.A., Tyler A.W. Correlation between spontaneous bursts of activity recorded from the dorsal roots in an isolated hamster spinal cord. Experimental Physiology 1993, 78:811-824.
14. Chub N., O'Donovan M.J. Post-episode depression of GABAergic transmission in spinal neurons of the chick embryo. Journal of Neurophysiology 2001, 85:2166-2176.
15. Curtis D.R., Lodge D. The depolarization of feline ventral horn group Ia spinal afferent terminations by GABA. Experimental Brain Research 1982, 46:215-233.
16. Delpire E., Mount D.B. Human and murine phenotypes associated with defects in cation-chloride cotransport. Annual Review of Physiology 2002, 64:803-843.
17. Delpy A., Allain A.E., Meyrand P., Branchereau P. NKCC1 cotransporter inactivation underlies embryonic development of chloride-mediated inhibition in mouse spinal motoneuron. Journal of Physiology 2008, 586:1059-1075.
18. Dubuc R., Cabelguen J.M., Rossignol S. Rhythmic antidromic discharges of single primary afferents recorded in cut dorsal root filaments during locomotion in the cat. Brain Research 1985, 359:375-378.
19. Dubuc R., Cabelguen J.-M., Rossignol S. Rhythmic fluctuations of dorsal root potentials and antidromic discharges of primary afferents during fictive locomotion in the cat. Journal of Neurophysiology 1988, 60:2014-2036.
20. Duenas S.H., Loeb G.E., Marks W.B. Monosynaptic and dorsal root reflexes during locomotion in normal and thalamic cats. Journal of Neurophysiology 1990, 63:1467-1476.
21. Dzhala V.I., Talos D.M., Sdrulla D.A., Brumback A.C., Mathews G.C., Benke T.A., et al. NKCC1 transporter facilitates seizures in the developing brain. Nature Medicine 2005, 11:1205-1213.
22. Eccles J.C., Schmidt R.F., Willis W.D. Pharmacological studies on presynaptic inhibition. Journal of Physiology (London) 1963, 168:500-530.
23. Fellippa-Marques S., Vinay L., Clarac F. Spontaneous and locomotor-related GABAergic input onto primary afferents in the neonatal rat. European Journal of Neuroscience 2000, 12:155-164.
24. Gao X.B., Chen G., van den Pol A.N. GABA-dependent firing of glutamate-evoked action potentials at AMPA/kainate receptors in developing hypothalamic neurons. Journal of Neurophysiology 1998, 79:716-726.
25. Gao B.X., Stricker C., Ziskind-Conhaim L. Transition from GABAergic to glycinergic synaptic transmission in newly formed spinal networks. Journal of Neurophysiology 2001, 86:492-502.
26. Gao B.-X., Ziskind-Conhaim L. Development of glycine- and GABA-gated currents in rat spinal motoneurons. Journal of Neurophysiology 1995, 74:113-121.
27. Gonzalez-Islas C.E., Chub N.L., Wenner P. NKCC1 and AE3 appear to accumulate chloride in embryonic motoneurons. Journal of Neurophysiology 2009, 101:507-518.
28. Gossard J.P., Cabelguen J.-M., Rossignol S. An intracellular study of muscle primary afferents during fictive locomotion in the cat. Journal of Neurophysiology 1991, 65:914-926.
29. Gulledge A.T., Stuart G.J. Excitatory actions of GABA in the cortex. Neuron 2003, 37:299-309.
30. Hanson M.G., Landmesser L.T. Characterization of the circuits that generate spontaneous episodes of activity in the early embryonic mouse spinal cord. Journal of Neuroscience 2003, 23:587-600.
31. Hübner C.A., Stein V., Hermans-Borgmeyer I., Meyer T., Ballanyi K., Jentsch T.J. Disruption of KCC2 reveals an essential role of K-Cl cotransport already in early synaptic inhibition. Neuron 2001, 30:515-524.
32. Iizuka M., Kiehn O., Kudo N. Development in neonatal rats of the sensory resetting of the locomotor rhythm induced by NMDA and 5-HT. Experimental Brain Research 1997, 114:193-204.
33. Ikeda M., Toyoda H., Yamada J., Okabe A., Sato K., Hotta Y., et al. Differential development of cation-chloride cotransporters and Cl- homeostasis contributes to differential GABAergic actions between developing rat visual cortex and dorsal lateral geniculate nucleus. Brain Research 2003, 984:149-159.
34. Jean-Xavier C., Mentis G.Z., O'Donovan M., Cattaert D., Vinay L. Dual personality of GABA/glycine-mediated depolarizations in the immature spinal cord. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:11477-11482.
35. Jean-Xavier C., Pflieger J.-F., Liabeuf S., Vinay L. Inhibitory post-synaptic potentials in lumbar motoneurons remain depolarizing after neonatal spinal cord transection in the rat. Journal of Neurophysiology 2006, 96:2274-2281.
36. Kerkut G.A., Bagust J. The isolated mammalian spinal cord. Progress in Neurobiology 1995, 46:1-48.
37. Kolta A., Lund J.P., Westberg K.G., Clavelou P. Do muscle-spindle afferents act as interneurons during mastication? (letter; comment). Trends in Neurosciences 1995, 18:441.
38. Kremer E., Lev-Tov A. GABA-Receptor-independent dorsal root afferents depolarization in the neonatal rat spinal cord. Journal of Neurophysiology 1998, 79:2581-2592.
39. Levy R.A. The effect of intravenously administered gamma-aminobutyric acid on afferent fiber polarization. Brain Research 1975, 92:21-34.
40. Marchetti C., Tabak J., Chub N., O'Donovan M.J., Rinzel J. Modeling spontaneous activity in the developing spinal cord using activity-dependent variations of intracellular chloride. Journal of Neuroscience 2005, 25:3601-3612.
41. Mazzocchio R., Rossi A. Involvement of spinal recurrent inhibition in spasticity. Further insight into the regulation of Renshaw cell activity. Brain 1997, 120(Pt 6):991-1003.
42. Morita H., Crone C., Christenhuis D., Petersen N.T., Nielsen J.B. Modulation of presynaptic inhibition and disynaptic reciprocal Ia inhibition during voluntary movement in spasticity. Brain 2001, 124:826-837.
43. Myers C.P., Lewcock J.W., Hanson M.G., Gosgnach S., Aimone J.B., Gage F.H., et al. Cholinergic input is required during embryonic development to mediate proper assembly of spinal locomotor circuits. Neuron 2005, 46:37-49.
44. Nishimaru H., Iizuka M., Ozaki S., Kudo N. Spontaneous motoneuronal activity mediated by glycine and GABA in the spinal cord of rat fetuses in vitro. Journal of Physiology 1996, 497:131-143.
45. Nishimaru H., Kudo N. Formation of the central pattern generator for locomotion in the rat and mouse. Brain Research Bulletin 2000, 53:661-669.
46. Norreel J.-C., Pflieger J.-F., Pearlstein E., Simeoni-Alias J., Clarac F., Vinay L. Reversible disorganization of the locomotor pattern after neonatal spinal cord transection in the rat. Journal of Neuroscience 2003, 23:1924-1932.
47. Payne J.A., Rivera C., Voipio J., Kaila K. Cation-chloride co-transporters in neuronal communication, development and trauma. Trends in Neurosciences 2003, 26:199-206.
48. Pilyavskii A.I., Yakhnitsa V.A., Bulgakova N.V. Antidromic dorsal root impulses during naturally occurring locomotion in rats. Neurophysiology 1988, 20:417-422.
49. Plotkin M.D., Snyder E.Y., Hebert S.C., Delpire E. Expression of the Na-K-2Cl cotransporter is developmentally regulated in postnatal rat brains: A possible mechanism underlying GABA's excitatory role in immature brain. Journal of Neurobiology 1997, 33:781-795.
50. Ramirez J.M., Telgkamp P., Elsen F.P., Quellmalz U.J., Richter D.W. Respiratory rhythm generation in mammals: Synaptic and membrane properties. Respiratory Physiology 1997, 110:71-85.
51. Ren J., Greer J.J. Ontogeny of rhythmic motor patterns generated in the embryonic rat spinal cord. Journal of Neurophysiology 2003, 89:1187-1195.
52. Ren J., Greer J.J. Modulation of respiratory rhythmogenesis by chloride-mediated conductances during the perinatal period. Journal of Neuroscience 2006, 26:3721-3730.
53. Rivera C., Voipio J., Kaila K. Two developmental switches in GABAergic signalling: The K-Cl cotransporter KCC2, and carbonic anhydrase CAVII. Journal of Physiology 2004, 562:27-36.
54. Rivera C., Voipio J., Payne J.A., Ruusuvuori E., Lahtinen H., Lamsa K., et al. The K+/Cl- co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 1999, 397:251-255.
55. Rossignol S., Beloozerova I.N., Gossard J.P., Dubuc R. Presynaptic mechanisms during locomotion. Presynaptic inhibition and neural control 1998, 385-397. Oxford University Press, Oxford. P. Rudomin, R. Romo, L.M. Mendell (Eds.).
56. Rudomin P. Presynaptic inhibition of muscle spindle and tendon organ afferents in the mammalian spinal cord. Trends in Neurosciences 1990, 13:499-505.
57. Rudomin P., Engberg I., Jimenez I. Mechanisms involved in presynaptic depolarization of group I and rubrospinal fibers in cat spinal cord. Journal of Neurophysiology 1981, 46:532-548.
58. Rudomin P., Quevedo J., Eguibar J.R. Presynaptic modulation of spinal reflexes. Current Opinion in Neurobiology 1993, 3:997-1004.
59. Sadlaoud K., Tazerart S., Brocard C., Jean-Xavier C., Portalier P., Brocard F., et al. Differential plasticity of the GABAergic and glycinergic synaptic transmission to rat lumbar motoneurons after spinal cord injury. Journal of Neuroscience 2010, 30:3358-3369.
60. Shao X.M., Feldman J.L. Respiratory rhythm generation and synaptic inhibition of expiratory neurons in pre-Botzinger complex: Differential roles of glycinergic and GABAergic neural transmission. Journal of Neurophysiology 1997, 77:1853-1860.
61. Stein V., Hermans-Borgmeyer I., Jentsch T.J., Hubner C.A. Expression of the KCl cotransporter KCC2 parallels neuronal maturation and the emergence of low intracellular chloride. Journal of Comparative Neurology 2004, 468:57-64.
62. Stil A., Liabeuf S., Jean-Xavier C., Brocard C., Viemari J.C., Vinay L. Developmental up-regulation of the potassium-chloride cotransporter type 2 in the rat lumbar spinal cord. Neuroscience 2009, 164:809-821.
63. Sun D., Murali S.G. Na+-K+-2Cl- cotransporter in immature cortical neurons: A role in intracellular Cl- regulation. Journal of Neurophysiology 1999, 81:1939-1948.
64. Sung K.W., Kirby M., McDonald M.P., Lovinger D.M., Delpire E. Abnormal GABAA receptor-mediated currents in dorsal root ganglion neurons isolated from Na-K-2Cl cotransporter null mice. Journal of Neuroscience 2000, 20:7531-7538.
65. Takahashi T. Inhibitory miniature synaptic potentials in rat motoneurons. Proceedings of Royal Society of London B Biological Sciences 1984, 221:103-109.
66. Toennies J.F. Reflex discharge from the spinal cord over the dorsal roots. Journal of Neurophysiology 1938, 1:378-390.
67. Vardi N., Zhang L.L., Payne J.A., Sterling P. Evidence that different cation chloride cotransporters in retinal neurons allow opposite responses to GABA. Journal of Neuroscience 2000, 20:7657-7663.
68. Verdier D., Lund J.P., Kolta A. GABAergic control of action potential propagation along axonal branches of mammalian sensory neurons. Journal of Neuroscience 2003, 23:2002-2007.
69. Vinay L., Brocard F., Clarac F., Norreel J.C., Pearlstein E., Pflieger J.F. Development of posture and locomotion: An interplay of endogenously generated activities and neurotrophic actions by descending pathways. Brain Research Review 2002, 40:118-129.
70. Vinay L., Brocard F., Fellippa-Marques S., Clarac F. Antidromic discharges of dorsal root afferents in the neonatal rat. Journal of Physiology Paris 1999, 93:359-367.
71. Vinay L., Brocard F., Pflieger J.F., Simeoni-Alias J., Clarac F. Perinatal development of lumbar motoneurons and their inputs in the rat. Brain Research Bulletin 2000, 53:635-647.
72. Vinay L., Clarac F. Antidromic discharges of dorsal root afferents and inhibition of the lumbar monosynaptic reflex in the neonatal rat. Neuroscience 1999, 90:165-176.
73. Vinay L., Jean-Xavier C. Plasticity of spinal cord locomotor networks and contribution of cation-chloride cotransporters. Brain Research Review 2008, 57:103-110.
74. Wu W.-L., Ziskind-Conhaim L., Sweet M.A. Early development of glycine- and GABA-mediated synapses in rat spinal cord. Journal of Neuroscience 1992, 12:3935-3945.
75. Ziskind-Conhaim L. Physiological functions of GABA-induced depolarizations in the developing rat spinal cord. Perspectives on Developemental Neurobiology 1998, 5:279-287.