Inhibitory synaptic modulation of renshaw cell activity in the lumbar spinal cord of neonatal mice

Journal of Neurophysiology

Volumn 103, Issue 6, 2010, Pages 3437-3447

  Nishimaru, Hiroshi ^a   Koganezawa, Tadachika ^a   Kakizaki, Miyo ^a   Ebihara, Tatsuhiko ^b   Yanagawa, Yuchio ^c,d  

^a UNIVERSITY OF TSUKUBA   (Japan)

^b NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^c GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMATE DECARBOXYLASE 67; GLYCINE; GREEN FLUORESCENT PROTEIN; MECAMYLAMINE;

ANIMAL EXPERIMENT; ARTICLE; CELL ACTIVITY; LUMBAR SPINAL CORD; MOTONEURON; MOUSE; NONHUMAN; PRIORITY JOURNAL; RENSHAW CELL; SYNAPSE; VENTRAL ROOT; VOLTAGE CLAMP;

ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; ELECTRIC STIMULATION; GLUTAMATE DECARBOXYLASE; GREEN FLUORESCENT PROTEINS; INTERNEURONS; LUMBOSACRAL REGION; MECAMYLAMINE; MICE; MICE, TRANSGENIC; MOTOR NEURONS; NEURAL INHIBITION; NEURAL PATHWAYS; NICOTINIC ANTAGONISTS; PATCH-CLAMP TECHNIQUES; SPINAL CORD; SYNAPTIC TRANSMISSION;

EID: 77953524837     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00100.2010     Document Type: Article

References (48)

1. Alvarez FJ, Dewey DE, Harrington DA, Fyffe RE. Cell-type specific organization of glycine receptor clusters in the mammalian spinal cord. J Comp Neurol 379: 150-170, 1997.
2. Alvarez FJ, Fyffe RE. The continuing case for the Renshaw cell. J Physiol 584: 31-45, 2007.
3. Baldissera F, Hultborn H, Illert M. Integration in spinal neuronal systems. In: Handbook of Physiology. The Nervous System. Motor Control, Bethesda: American Physiological Society, 1981, sect. 1, vol. II, part 1, chapt. 10, p. 509-595.
4. Bonnot A, Morin D, Viala D. Genesis of spontaneous rhythmic motor patterns in the lumbosacral spinal cord of neonate mouse. Brain Res Dev Brain Res 108: 89-99, 1998. (Pubitemid 28332822)
5. Bui TV, Dewey DE, Fyffe RE, Rose PK. Comparison of the inhibition of Renshaw cells during subthreshold and suprathreshold conditions using anatomically and physiologically realistic models. J Neurophysiol 94: 1688-1698, 2005.
6. Delpy A, Allain AE, Meyrand P, Branchereau P. NKCC1 cotransporter inactivation underlies embryonic development of chloride-mediated inhibition in mouse spinal motoneuron. J Physiol 586: 1059-1075, 2008.
7. Eccles JC, Fatt P, Koketsu K. Cholinergic and inhibitory synapses in a pathway from motor-axon collaterals to motoneurones. J Physiol 126: 524-562, 1954.
8. Geiman EJ, Knox MC, Alvarez FJ. Postnatal maturation of gephyrin/glycine receptor clusters on developing Renshaw cells. J Comp Neurol 426: 130-142, 2000.
9. Gonzalez-Forero D, Alvarez FJ. Differential postnatal maturation of GABAA, glycine receptor, and mixed synaptic currents in Renshaw cells and ventral spinal interneurons. J Neurosci 25: 2010-2023, 2005.
10. Gonzalez-Forero D, Pastor AM, Geiman EJ, Benitez-Temino B, Alvarez FJ. Regulation of gephyrin cluster size and inhibitory synaptic currents on Renshaw cells by motor axon excitatory inputs. J Neurosci 25: 417-429, 2005.
11. Goulding M. Circuits controlling vertebrate locomotion: moving in a new direction. Nat Rev Neurosci 10: 507-518, 2009.
12. Haase J, van der Meullen J. Effects of supraspinal stimulation on Renshaw cells belonging to extensor motoneurones. J Neurophysiol 24: 510-520, 1961.
13. Hinckley CA, Hartley R, Wu L, Todd A, Ziskind-Conhaim L. Locomotor-like rhythms in a genetically distinct cluster of interneurons in the mammalian spinal cord. J Neurophysiol 93: 1439-1449, 2005. (Pubitemid 40283732)
14. 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. (Pubitemid 37442983)
15. Hultborn H, Lindstrom S, Wigstrom H. On the function of recurrent inhibition in the spinal cord. Exp Brain Res 37: 399-403, 1979. (Pubitemid 10243992)
16. Hultborn H, Pierrot-Deseilligny E. Changes in recurrent inhibition during voluntary soleus contractions in man studied by an H-reflex technique. J Physiol 297: 229-251, 1979. (Pubitemid 10166917)
17. Jiang Z, Rempel J, Li J, Sawchuk MA, Carlin KP, Brownstone RM. Development of L-type calcium channels and a nifedipine-sensitive motor activity in the postnatal mouse spinal cord. Eur J Neurosci 11: 3481-3487, 1999.
18. Kiehn O. Locomotor circuits in the mammalian spinal cord. Annu Rev Neurosci 29: 279-306, 2006.
19. Kudo N, Yamada T. Development of the monosynaptic stretch reflex in the rat: an in vitro study. J Physiol 369: 127-144, 1985. (Pubitemid 16176869)
20. Lamotte d'Incamps B, Ascher P. Four excitatory postsynaptic ionotropic receptors coactivated at the motoneuron-Renshaw cell synapse. J Neurosci 28: 14121-14131, 2008.
21. MacLean JB, Leffman H. Supraspinal control of Renshaw cells. Exp Neurol 18: 94-104, 1967.
22. Marchetti C, Taccola G, Nistri A. Activation of group I metabotropic glutamate receptors depresses recurrent inhibition of motoneurons in the neonatal rat spinal cord in vitro. Exp Brain Res 164: 406-410, 2005.
23. McCrea DA, Pratt CA, Jordan LM. Renshaw cell activity and recurrent effects on motoneurons during fictive locomotion. J Neurophysiol 44: 475-488, 1980.
24. Mentis GZ, Alvarez FJ, Bonnot A, Richards DS, Gonzalez-Forero D, Zerda R, O'Donovan MJ. Noncholinergic excitatory actions of motoneurons in the neonatal mammalian spinal cord. Proc Natl Acad Sci USA 102: 7344-7349, 2005.
25. Nakayama K, Nishimaru H, Kudo N. Basis of changes in left-right coordination of rhythmic motor activity during development in the rat spinal cord. J Neurosci 22: 10388-10398, 2002. (Pubitemid 35416876)
26. Nishimaru H, Kakizaki M. The role of inhibitory neurotransmission in locomotor circuits of the developing mammalian spinal cord. Acta Physiol (Oxf) 197: 83-97, 2009.
27. Nishimaru H, Kudo N. Formation of the central pattern generator for locomotion in the rat and mouse. Brain Res Bull 53: 661-669, 2000.
28. Nishimaru H, Restrepo CE, Kiehn O. Activity of Renshaw cells during locomotor-like rhythmic activity in the isolated spinal cord of neonatal mice. J Neurosci 26: 5320-5328, 2006.
29. Nishimaru H, Restrepo CE, Ryge J, Yanagawa Y, Kiehn O. Mammalian motor neurons corelease glutamate and acetylcholine at central synapses. Proc Natl Acad Sci USA 102: 5245-5249, 2005.
30. Noga BR, Kriellaars DJ, Brownstone RM, Jordan LM. Mechanism for activation of locomotor centers in the spinal cord by stimulation of the mesencephalic locomotor region. J Neurophysiol 90: 1464-1478, 2003.
31. Noga BR, Shefchyk SJ, Jamal J, Jordan LM. The role of Renshaw cells in locomotion: antagonism of their excitation from motor axon collaterals with intravenous mecamylamine. Exp Brain Res 66: 99-105, 1987. (Pubitemid 17039277)
32. Pierrot-Deseilligny E, Morin C, Katz R, Bussel B. Influence of voluntary movement and posture on recurrent inhibition in human subjects. Brain Res 124: 427-436, 1977.
33. Pratt CA, Jordan LM. Recurrent inhibition of motoneurons in decerebrate cats during controlled treadmill locomotion. J Neurophysiol 44: 489-500, 1980.
34. Pratt CA, Jordan LM. Ia inhibitory interneurons and Renshaw cells as contributors to the spinal mechanisms of fictive locomotion. J Neurophysiol 57: 56-71, 1987.
35. Renshaw B. Central effects of centripetal impulses in axons of spinal ventral roots. J Neurophysiol 9: 191-204, 1946.
36. Ryall RW. Patterns of recurrent excitation and mutual inhibition of cat Renshaw cells. J Physiol 316: 439-452, 1981.
37. Ryall RW, Piercey MF, Polosa C. Intersegmental and intrasegmental distribution of mutual inhibition of Renshaw cells. J Neurophysiol 34: 700-707, 1971.
38. Sapir T, Geiman EJ, Wang Z, Velasquez T, Mitsui S, Yoshihara Y, Frank E, Alvarez FJ, Goulding M. Pax6 and engrailed 1 regulate two distinct aspects of renshaw cell development. J Neurosci 24: 1255-1264, 2004.
39. Shefchyk SJ, Jordan LM. Excitatory and inhibitory postsynaptic potentials in alpha-motoneurons produced during fictive locomotion by stimulation of the mesencephalic locomotor region. J Neurophysiol 53: 1345-1355, 1985. (Pubitemid 15067222)
40. Song ZM, Hu J, Rudy B, Redman SJ. Developmental changes in the expression of calbindin and potassium-channel subunits Kv3.1b and Kv3.2 in mouse Renshaw cells. Neuroscience 139: 531-538, 2006.
41. Tamamaki N, Yanagawa Y, Tomioka R, Miyazaki J, Obata K, Kaneko T. Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J Comp Neurol 467: 60-79, 2003.
42. Wang Z, Li LY, Goulding M, Frank E. Early postnatal development of reciprocal Ia inhibition in the murine spinal cord. J Neurophysiol 100: 185-196, 2008.
43. Whelan P, Bonnot A, O'Donovan MJ. Properties of rhythmic activity generated by the isolated spinal cord of the neonatal mouse. J Neurophysiol 84: 2821-2833, 2000.
44. Wilson JM, Hartley R, Maxwell DJ, Todd AJ, Lieberam I, Kaltschmidt JA, Yoshida Y, Jessell TM, Brownstone RM. Conditional rhythmicity of ventral spinal interneurons defined by expression of the Hb9 homeodomain protein. J Neurosci 25: 5710-5719, 2005.
45. Wilson JM, Rempel J, Brownstone RM. Postnatal development of cholinergic synapses on mouse spinal motoneurons. J Comp Neurol 474: 13-23, 2004.
46. Wilson VJ, Talbot WH, Kato M. Inhibitory convergence upon Renshaw cells. J Neurophysiol 27: 1063-1079, 1964.
47. Windhorst U. On the role of recurrent inhibitory feedback in motor control. Prog Neurobiol 49: 517-587, 1996.
48. 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.