Multiple monoaminergic modulation of posturo-locomotor network activity in the newborn rat spinal cord

Frontiers in Neural Circuits

Volumn 8, Issue AUG, 2014, Pages

  Beliez, Lauriane ^a   Barrière, Gregory ^a   Bertrand, Sandrine S ^a   Cazalets, Jean René ^a  

^a UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

Dopamine; Locomotion; Neuromodulation; Noradrenaline; Posture; Serotonin; Spinal cord

Indexed keywords

DOPAMINE; EXCITATORY AMINO ACID; EXCITATORY AMINO ACID RECEPTOR; NEUROTRANSMITTER; NORADRENALIN; SEROTONIN; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; BIOGENIC AMINE;

ANIMAL TISSUE; ARTICLE; BODY POSTURE; CONTROLLED STUDY; HINDLIMB; IN VITRO STUDY; INTRACELLULAR RECORDING; LOCOMOTION; LUMBAR SPINE; MONOAMINERGIC SYSTEM; MOTOR COORDINATION; MOTOR PERFORMANCE; NERVE CELL NETWORK; NEUROMODULATION; NEWBORN; NONHUMAN; RAT; RECEPTOR UPREGULATION; SACRAL SPINAL CORD; SPINAL CORD; VENTRAL ROOT; ACTION POTENTIAL; AGE; ANALYSIS OF VARIANCE; ANIMAL; CYTOLOGY; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NERVE CELL; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ACTION POTENTIALS; AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BIOGENIC MONOAMINES; IN VITRO TECHNIQUES; LOCOMOTION; NERVE NET; NEURONS; NEUROTRANSMITTER AGENTS; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD;

EID: 84923306126     PISSN: 16625110     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncir.2014.00099     Document Type: Article

References (83)

1. Akazawa, K., Aldridge, J. W., Steeves, J. D., and Stein, R. B. (1982). Modulation of stretch reflexes during locomotion in the mesencephalic cat.J. Physiol. 329, 553-567.
2. Ballion, B., Morin, D., and Viala, D. (2001). Forelimb locomotor generators and quadrupedal locomotion in the neonatal rat. Eur. J. Neurosci.14, 1727-1738. doi: 10.1046/j.0953-816x.2001.01794.x
3. Barriere, G., Mellen, N., and Cazalets, J.-R. (2004). Neuromodulation of the locomotor network by dopamine in the isolated spinal cord of newborn rat. Eur. J. Neurosci.19, 1325-1335. doi: 10.1111/j.1460-9568.2004.03210.x
4. Bartos, M., Manor, Y., Nadim, F., Marder, E., and Nusbaum, M. P. (1999). Coordination of fast and slow rhythmic neuronal circuits.J. Neurosci. 19, 6650-6660.
5. Beato, M., Bracci, E., and Nistri, A. (1997). Contribution of NMDA and non-NMDA glutamate receptors to locomotor pattern generation in the neonatal rat spinal cord. Proc. Biol. Sci.264, 877-884. doi: 10.1098/rspb.1997.0122
6. Beato, M., and Nistri, A. (1998). 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. doi: 10.1098/rspb.1998.0542
7. Berens, P. (2009). CircStat: a MATLAB toolbox for circular statistics.J. Stat. Softw. 31, 1-21.
8. Berger, A. J., and Takahashi, T. (1990). Serotonin enhances a low-voltage-activated calcium current in rat spinal motoneurons.J. Neurosci.10, 1922-1928.
9. Beyeler, A., Metais, C., Combes, D., Simmers, J., and Le Ray, D. (2008). Metamorphosis-induced changes in the coupling of spinal thoraco-lumbar motor outputs during swimming inXenopus laevis.J. Neurophysiol.100, 1372-1383. doi: 10.1152/jn.00023.2008
10. Cang, J., and Friesen, W. O. (2002). Model for intersegmental coordination of leech swimming: central and sensory mechanisms.J. Neurophysiol.87, 2760-2769.
11. Cattaert, D., and Clarac, F. (1983). Influence of walking on swimmeret beating in the lobster Homarus gammarus. J. Neurobiol. 14, 421-439. doi: 10.1002/neu.480140603
12. Cazalets, J. R. (2000). "Organization of the spinal locomotor network in neonatal rat, " inNeurobiology of Spinal Cord Injury, eds R. Kalb, and S. M. Stritmatter (Totowa, NJ: Humana Press Inc.), 89-111. doi: 10.1007/978-1-59259-200-5_4
13. Cazalets, J. R., Grillner, P., Menard, I., Cremieux, J., and Clarac, F. (1990). Two types of motor rhythm induced by NMDA and amines in an in vitro spinal cord preparation of neonatal rat. Neurosci. Lett.111, 116-121. doi: 10.1016/0304-3940(90)90354-C
14. Cazalets, J. R., Sqalli-Houssaini, Y., and Clarac, F. (1992). Activation of the central pattern generators for locomotion by serotonin and excitatory amino acids in neonatal rat.J. Physiol.455, 187-204.
15. Cazalets, J. R., Sqalli-Houssaini, Y., and Magoul, R. (1999). Differential effects of potassium channel blockers on the activity of the locomotor network in neonatal rat. Brain Res.827, 185-197. doi: 10.1016/S0006-8993(99)01342-6
16. Chrachri, A., and Neil, D. M. (1993). Interaction and synchronization between two abdominal motor systems in crayfish.J. Neurophysiol.69, 1373-1383.
17. Clemens, S., Belin-Rauscent, A., Simmers, J., and Combes, D. (2012). Opposing modulatory effects of D1-and D2-like receptor activation on a spinal central pattern generator. J. Neurophysiol. 107, 2250-2259. doi: 10.1152/jn.00366. 2011
18. Combes, D., Sillar, K. T., and Simmers, J. (2012). A switch in aminergic modulation of locomotor CPG output during amphibian metamorphosis. Front. Biosci. (Schol. Ed.)4:1364-1374.
19. Delvolve, I., Bem, T., and Cabelguen, J. M. (1997). Epaxial and limb muscle activity during swimming and terrestrial stepping in the adult newt, Pleurodeles waltl. J. Neurophysiol.78, 638-650.
20. De Sèze, M., Falgairolle, M., Viel, S., Assaiante, C., and Cazalets, J.-R. (2008). Sequential activation of axial muscles during different forms of rhythmic behavior in man. Exp. Brain Res.185, 237-247. doi: 10.1007/s00221-007-1146-2
21. Dietz, V. (2002). Do human bipeds use quadrupedal coordination?Trends Neurosci. 25, 462-467. doi: 10.1016/S0166-2236(02)02229-4
22. Duenas, S. H., Loeb, G. E., and Marks, W. B. (1990). Monosynaptic and dorsal root reflexes during locomotion in normal and thalamic cats.J. Neurophysiol.63, 1467-1476.
23. Duysens, J., and Van de Crommert, H. W. (1998). Neural control of locomotion: the central pattern generator from cats to humans. Gait Posture7, 131-141. doi: 10.1016/S0966-6362(97)00042-8
24. El Manira, A., Tegner, J., and Grillner, S. (1994). Calcium-dependent potassium channels play a critical role for burst termination in the locomotor network in lamprey.J. Neurophysiol.72, 1852-1861.
25. Falgairolle, M., and Cazalets, J. R. (2007). Metachronal coupling between spinal neuronal networks during locomotor activity in newborn rat.J. Physiol. 580, 87-102. doi: 10.1113/jphysiol.2006.115709
26. Falgairolle, M., Ceccato, J.-C., Seze, M. D., Herbin, M., and Cazalets, J.-R. (2013). Metachronal propagation of motor activity. Front. Biosci. (Landmark Ed.)18:820-837.
27. Falgairolle, M., De Seze, M., Juvin, L., Morin, D., and Cazalets, J. R. (2006). Coordinated network functioning in the spinal cord: an evolutionary perspective.J. Physiol. Paris 100, 304-316. doi: 10.1016/j.jphysparis.2007. 05.003
28. Faumont, S., Combes, D., Meyrand, P., and Simmers, J. (2005). Reconfiguration of multiple motor networks by short-and long-term actions of an identified modulatory neuron. Eur. J. Neurosci. 22, 2489-2502. doi: 10.1111/j.1460-9568.2005.04442.x
29. Gabbay, H., Delvolvé, I., and Lev-Tov, A. (2002). Pattern generation in caudal-lumbar and sacrococcygeal segments of the neonatal rat spinal cord. J. Neurophysiol.88, 732-739.
30. Gabbay, H., and Lev-Tov, A. (2004). Alpha-1 adrenoceptor agonists generate a "fast" NMDA receptor-independent motor rhythm in the neonatal rat spinal cord.J. Neurophysiol.92, 997-1010. doi: 10.1152/jn.00205.2004
31. Gestreau, C., Grelot, L., and Bianchi, A. L. (2000). Activity of respiratory laryngeal motoneurons during fictive coughing and swallowing. Exp. Brain Res.130, 27-34. doi: 10.1007/s002210050003
32. Gordon, I. T., and Whelan, P. J. (2006). Monoaminergic control of cauda-equinaevoked locomotion in the neonatal mouse spinal cord.J. Neurophysiol.96, 3122-3129. doi: 10.1152/jn.00606.2006
33. Gramsbergen, A., Geisler, H. C., Taekema, H., and Van Eykern, L. A. (1999). The activation of back muscles during locomotion in the developing rat. Brain Res. Dev. Brain Res.112, 217-228. doi: 10.1016/S0165-3806(98)00184-9
34. Grinsted, A., Moore, J. C., and Jevrejeva, S. (2004). NPG-Abstract-application of the cross wavelet transform and wavelet coherence to geophysical time series. Nonlinear Process. Geophys. 11, 561-566. doi: 10.5194/npg-11-561-2004
35. Guertin, P. A. (2009). Recovery of locomotor function with combinatory drug treatments designed to synergistically activate specific neuronal networks. Curr. Med. Chem.16, 1366-1371. doi: 10.2174/092986709787846541
36. Han, P., Nakanishi, S. T., Tran, M. A., and Whelan, P. J. (2007). Dopaminergic modulation of spinal neuronal excitability.J. Neurosci. 27, 13192-13204. doi: 10.1523/JNEUROSCI.1279-07.2007
37. Hao, Z. Z., Spardy, L. E., Nguyen, E. B., Rubin, J. E., and Berkowitz, A. (2011). Strong interactions between spinal cord networks for locomotion and scratching. J. Neurophysiol.106, 1766-1781. doi: 10.1152/jn.00460.2011
38. Harris-Warrick, R. M. (2011). Neuromodulation and flexibility in central pattern generator networks. Curr. Opin. Neurobiol. 21, 685-692. doi: 10.1016/j.conb.2011.05.011
39. Islam, S. S., Zelenin, P. V., Orlovsky, G. N., Grillner, S., and Deliagina, T. G. (2006). Pattern of motor coordination underlying backward swimming in the lamprey. J. Neurophysiol.96, 451-460. doi: 10.1152/jn.01277.2005
40. Jamon, M., and Clarac, F. (1998). Early walking in the neonatal rat: a kinematic study. Behav. Neurosci.112, 1218-1228. doi: 10.1037/0735-7044.112.5.1218
41. Jiang, Z., Carlin, K. P., and Brownstone, R. M. (1999). An in vitro functionally mature mouse spinal cord preparation for the study of spinal motor networks. Brain Res.816, 493-499. doi: 10.1016/S0006-8993(98)01199-8
42. Juvin, L., Simmers, J., and Morin, D. (2005). Propriospinal circuitry underlying interlimb coordination in mammalian quadrupedal locomotion.J. Neurosci.25, 6025-6035. doi: 10.1523/JNEUROSCI.0696-05.2005
43. Kawahara, K., Nakazono, Y., Yamauchi, Y., and Miyamoto, Y. (1989). Coupling between respiratory and locomotor rhythms during fictive locomotion in decerebrate cats. Neurosci. Lett.103, 326-330. doi: 10.1016/0304-3940(89)90121-3
44. Kiehn, O., and Kjaerulff, O. (1996). Spatiotemporal characteristics of 5-HT and dopamine-induced rhythmic hindlimb activity in the in vitro neonatal rat. J. Neurophysiol.75, 1472-1482.
45. Kiehn, O., Sillar, K. T., Kjaerulff, O., and Mcdearmid, J. R. (1999). Effects of noradrenaline on locomotor rhythm-generating networks in the isolated neonatal rat spinal cord.J. Neurophysiol.82, 741-746.
46. Kjaerulff, O., and Kiehn, O. (2001). 5-HT modulation of multiple inward rectifiers in motoneurons in intact preparations of the neonatal rat spinal cord. J. Neurophysiol.85, 580-593.
47. Koehler, W. J., Schomburg, E. D., and Steffens, H. (1984). Phasic modulation of trunk muscle efferents during fictive spinal locomotion in cats. J. Physiol. 353, 187-197.
48. Krenz, W. D., Parker, A. R., Rodgers, E. W., and Baro, D. J. (2014). Dopaminergic tone persistently regulates voltage-gated ion current densities through the D1RPKA axis, RNA polymerase II transcription, RNAi, mTORC1, and translation. Front. Cell. Neurosci.8:39. doi: 10.3389/fncel.2014.00039
49. Kudo, N., and Yamada, T. (1987). N-methyl-D, L-aspartate-induced locomotor activity in a spinal cord-hindlimb muscles preparation of the newborn rat studied in vitro. Neurosci. Lett.75, 43-48. doi: 10.1016/0304-3940(87)90072-3
50. Landry, E. S., Lapointe, N. P., Rouillard, C., Levesque, D., Hedlund, P. B., and Guertin, P. A. (2006). Contribution of spinal 5-HT1A and 5-HT7 receptors to locomotor-like movement induced by 8-OH-DPAT in spinal cord-transected mice. Eur. J. Neurosci.24, 535-546. doi: 10.1111/j.1460-9568.2006.04917.x
51. Lapointe, N. P., and Guertin, P. A. (2008). Synergistic effects of D1/5 and 5-HT1A/7 receptor agonists on locomotor movement induction in complete spinal cordtransected mice.J. Neurophysiol.100, 160-168. doi: 10.1152/jn.90339.2008
52. Lapointe, N. P., Rouleau, P., Ung, R. V., and Guertin, P. A. (2009). Specific role of dopamine D1 receptors in spinal network activation and rhythmic movement induction in vertebrates.J. Physiol. 587, 1499-1511. doi: 10.1113/jphysiol.2008.166314
53. Lapointe, N. P., Ung, R. V., Rouleau, P., and Guertin, P. A. (2008). Effects of spinal alpha(2)-adrenoceptor and I(1)-imidazoline receptor activation on hindlimb movement induction in spinal cord-injured mice.J. Pharmacol. Exp. Ther.325, 994-1006. doi: 10.1124/jpet.107.134874
54. Leblond, H., L'esperance, M., Orsal, D., and Rossignol, S. (2003). Treadmill locomotion in the intact and spinal mouse.J. Neurosci.23, 11411-11419.
55. Liu, J., Akay, T., Hedlund, P. B., Pearson, K. G., and Jordan, L. M. (2009). Spinal 5-HT7 receptors are critical for alternating activity during locomotion: invitro neonatal and in vivo adult studies using 5-HT7 receptor knockout mice. J. Neurophysiol.102, 337-348. doi: 10.1152/jn.91239.2008
56. Maclellan, M. J., Ivanenko, Y. P., Cappellini, G., Sylos Labini, F., and Lacquaniti, F. (2011). Features of hand-foot crawling behavior in human adults.J. Neurophysiol. 107, 114-125. doi: 10.1152/jn.00693.2011
57. Madriaga, M. A., Mcphee, L. C., Chersa, T., Christie, K. J., and Whelan, P. J. (2004). Modulation of locomotor activity by multiple 5-HT and dopaminergic receptor subtypes in the neonatal mouse spinal cord.J. Neurophysiol.92, 1566-1576. doi: 10.1152/jn.01181.2003
58. Miles, G. B., and Sillar, K. T. (2011). Neuromodulation of vertebrate locomotor control networks. Physiology (Bethesda)26, 393-411. doi: 10.1152/physiol.00013.2011
59. Mor, Y., and Lev-Tov, A. (2007). Analysis of rhythmic patterns produced by spinal neural networks.J. Neurophysiol.98, 2807-2817. doi: 10.1152/jn.00740.2007
60. Morin, D., and Viala, D. (2002). Coordinations of locomotor and respiratory rhythms in vitro are critically dependent on hindlimb sensory inputs.J. Neurosci. 22, 4756-4765.
61. Nakajima, T., Mezzarane, R. A., Klarner, T., Barss, T. S., Hundza, S. R., Komiyama, T., et al. (2013). Neural mechanisms influencing interlimb coordination during locomotion in humans: presynaptic modulation of forearm H-reflexes during leg cycling. PLoS ONE8:e76313. doi: 10.1371/journal.pone. 0076313
62. Pearlstein, E., Ben Mabrouk, F., Pflieger, J. F., and Vinay, L. (2005). Serotonin refines the locomotor-related alternations in the in vitro neonatal rat spinal cord. Eur. J. Neurosci.21, 1338-1346. doi: 10.1111/j.1460-9568.2005.03971.x
63. Rauscent, A., Einum, J., Le Ray, D., Simmers, J., and Combes, D. (2009). Opposing aminergic modulation of distinct spinallocomotor circuits and their functional coupling during amphibian metamorphosis. J. Neurosci. 29, 1163-1174. doi: 10.1523/JNEUROSCI.5255-08.2009
64. Rodgers, E. W., Krenz, W. D., and Baro, D. J. (2011). Tonic dopamine induces persistent changes in the transient potassium current through translational regulation. J. Neurosci. 31, 13046-13056. doi: 10.1523/JNEUROSCI.2194-11.2011
65. Rossignol, S. (1996). "Neural control of stereotypic limb movements, " inHandbook of Physiology, Section 12. Exercise: Regulation and Integration of Multiple Systems, eds B. Rowell and J. T. Sheperd (Bethesda, MD: American Physiological Society), 173-216.
66. Schwartz, E. J., Gerachshenko, T., and Alford, S. (2005). 5-HT prolongs ventral root bursting via presynaptic inhibition of synaptic activity during fictive locomotion in lamprey.J. Neurophysiol.93, 980-988. doi: 10.1152/jn.00669.2004
67. Smarandache, C., Hall, W. M., and Mulloney, B. (2009). Coordination of rhythmic motor activity by gradients of synaptic strength in a neural circuit that couples modular neural oscillators. J. Neurosci. 29, 9351-9360. doi: 10.1523/JNEUROSCI.1744-09.2009
68. Smith, J. C., and Feldman, J. L. (1987). In vitro brainstem-spinal cord preparations for study of motor systems for mammalian respiration and locomotion. J. Neurosci. Methods21, 321-333. doi: 10.1016/0165-0270(87)90126-9
69. Somjen, G. G. (1979). Extracellular potassium in the mammalian central nervous system. Annu. Rev. Physiol.41, 159-177. doi: 10.1146/annurev.ph.41.030179. 001111
70. Sqalli-Houssaini, Y., and Cazalets, J. R. (2000). Noradrenergic control of locomotor networks in the in vitro spinal cord of the neonatal rat. Brain Res.852, 100-109. doi: 10.1016/S0006-8993(99)02219-2
71. Sqalli-Houssaini, Y., Cazalets, J. R., and Clarac, F. (1993). Oscillatory properties of the central pattern generator for locomotion in neonatal rats.J. Neurophysiol.70, 803-813.
72. Sqalli-Houssaini, Y., Cazalets, J. R., Fabre, J. C., and Clarac, F. (1991). A cooling/heating system for use with in vitro preparations: study of temperature effects on newborn rat rhythmic activities. J. Neurosci. Methods 39, 131-139. doi: 10.1016/0165-0270(91)90079-F
73. Talpalar, A. E., and Kiehn, O. (2010). Glutamatergic mechanisms for speed control and network operation in the rodent locomotor CPG. Front. Neural Circuits4:19. doi: 10.3389/fncir.2010.00019
74. Thorstensson, A., Carlson, H., Zomlefer, M. R., and Nilsson, J. (1982). Lumbar back muscle activity in relation to trunk movements during locomotion in man. Acta Physiol. Scand.116, 13-20. doi: 10.1111/j.1748-1716.1982.tb10593.x
75. Torrence, C., and Compo, G. P. (2010). A practical guide to wavelet analysis. Bull. Am. Meteorol. Soc. 79, 61-78. doi: 10.1175/1520-0477(1998)0790061:APGTWA2.0.CO;2
76. Wallen, P., Christenson, J., Brodin, L., Hill, R., Lansner, A., and Grillner, S. (1989). Mechanisms underlying the serotonergic modulation of the spinal circuitry for locomotion in lamprey. Prog. Brain Res.80, 321-327; discussion 315-329. doi: 10.1016/S0079-6123(08)62227-X
77. Wannier, T., Bastiaanse, C., Colombo, G., and Dietz, V. (2001). Arm to leg coordination in humans during walking, creeping and swimming activities. Exp. Brain Res.141, 375-379. doi: 10.1007/s002210100875
78. Whelan, P., Bonnot, A., and O'donovan, M. J. (2000). Properties of rhythmic activity generated by the isolated spinal cord of the neonatal mouse.J. Neurophysiol.84, 2821-2833.
79. Zehr, E. P., and Duysens, J. (2004). Regulation of arm and leg movement during human locomotion. Neuroscientist10, 347-361. doi: 10.1177/107385840 4264680
80. Zhong, G., Diaz-Rios, M., and Harris-Warrick, R. M. (2006a). Intrinsic and functional differences among commissural interneurons during fictive locomotion and serotonergic modulation in the neonatal mouse.J. Neurosci.26, 6509-6517. doi: 10.1523/JNEUROSCI.1410-06.2006
81. Zhong, G., Diaz-Rios, M., and Harris-Warrick, R. M. (2006b). Serotonin modulates the properties of ascending commissural interneurons in the neonatal mouse spinal cord.J. Neurophysiol.95, 1545-1555. doi: 10.1152/jn.01103.2005
82. Zhong, G., Masino, M. A., and Harris-Warrick, R. M. (2007). Persistent sodium currents participate in fictive locomotion generation in neonatal mouse spinal cord.J. Neurosci.27, 4507-4518. doi: 10.1523/JNEUROSCI.0124-07.2007
83. Zomlefer, M. R., Provencher, J., Blanchette, G., and Rossignol, S. (1984). Electromyographic study of lumbar back muscles during locomotion in acute high decerebrate and in low spinal cats. Brain Res. 290, 249-260. doi: 10.1016/0006-8993(84)90942-9