The continuing case for the Renshaw cell

Journal of Physiology

Volumn 584, Issue 1, 2007, Pages 31-45

  Alvarez, Francisco J ^a   Fyffe, Robert E W ^a  

^a WRIGHT STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; ACETYLCHOLINE; AMPA RECEPTOR; CALCIUM BINDING PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANATOMICAL VARIATION; CELL LABELING; CELL STRUCTURE; DORSAL ROOT; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; IMMUNOCYTOCHEMISTRY; INHIBITORY POSTSYNAPTIC POTENTIAL; MOTONEURON; MOTOR PERFORMANCE; NERVE CELL DIFFERENTIATION; NEUROMODULATION; NEUROTRANSMISSION; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RENSHAW CELL; REVIEW; SPINAL CORD NERVE CELL; SYNAPTIC MEMBRANE; CELL FUNCTION; CELL MANIPULATION; CELL MATURATION; CELLULAR DISTRIBUTION; INTERNEURON; LOCOMOTION; MOTOR CONTROL; MUSCLE SPINDLE AFFERENT NERVE; NERVE CELL INHIBITION; NERVE CELL STIMULATION; NERVE FIBER; NEUROANATOMY; NEUROPHYSIOLOGY; ONTOGENY; POSTNATAL DEVELOPMENT; RECURRENT INHIBITION; SYNAPSE; SYNAPTIC TRANSMISSION;

ANIMALS; CALCIUM-BINDING PROTEINS; INTERNEURONS; SYNAPSES;

EID: 34848922166     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2007.136200     Document Type: Review

References (96)

1. Alvarez FJ, Dewey DE, Harrington DA & Fyffe RE (1997). Cell-type specific organization of glycine receptor clusters in the mammalian spinal cord. J Comp Neurol 379, 150-170.
2. Alvarez FJ, Dewey DE, McMillin P & Fyffe RE (1999). Distribution of cholinergic contacts on Renshaw cells in the rat spinal cord: A light microscopic study. J Physiol 515, 787-797.
3. Alvarez FJ & Gonzalez-Forero D (2006). Maturation of GABA A synapses on Renshaw cells. Abstr Soc Neurosci 716. -717.
4. Alvarez FJ, Jonas PC, Sapir T, Hartley R, Berrocal MC, Geiman EJ, Todd AJ & Goulding M (2005). Postnatal phenotype and localization of spinal cord V1 derived interneurons. J Comp Neurol 493, 177-192.
5. Arvidsson U, Ulfhake B, Cullheim S, Ramirez V, Shupliakov O & Hokfelt T (1992). Distribution of calbindin D28k-like immunoreactivity (LI) in the monkey ventral horn: Do Renshaw cells contain calbindin D28k-LI? J Neurosci 12, 718-728.
6. Ascoli GA (2006). Mobilizing the base of neuroscience data: The case of neuronal morphologies. Nat Rev Neurosci 7, 318-324.
7. Baldissera F, Hultborn H & Illert M (1981). Integration in spinal neural systems. In Handbook of Physiology, section 1, The Nervous System, Vol. II, Motor Control, Part I, ed. Brooks VB, pp. 509-595. American Physiological Society, Bethesda, MD, USA.
8. Bui TV, Cushing S, Dewey D, Fyffe RE & Rose PK (2003). Comparison of the morphological and electrotonic properties of Renshaw cells, Ia inhibitory interneurons, and motoneurons in the cat. J Neurophysiol 90, 2900-2918.
9. Bui TV, Dewey DE, Fyffe RE & Rose PK (2005). Comparison of the inhibition of Renshaw cells during subthreshold and suprathreshold conditions using anatomically and physiologically realistic models. J Neurophysiol 94, 1688-1698.
10. Burke RE (2006). John Eccles' pioneering role in understanding central synaptic transmission. Prog Neurobiol 78, 173-188.
11. Carr PA, Alvarez FJ, Leman EA & Fyffe RE (1998). Calbindin D28k expression in immunohistochemically identified Renshaw cells. Neuroreport 9, 2657-2661.
12. Carr PA, Pearson JC & Fyffe RE (1999). Distribution of 5-hydroxytryptamine-immunoreactive boutons on immunohistochemically-identified Renshaw cells in cat and rat lumbar spinal cord. Brain Res 823, 198-201.
13. Cullheim S & Kellerth JO (1981). Two kinds of recurrent inhibition of cat spinal α-motoneurones as differentiated pharmacologically. J Physiol 312, 209-224.
14. Curtis DR & Andersen P (2001). Sir John Carew Eccles, A.C. Biogr Mem Fellows R Soc 47, 159-187.
15. Curtis DR, Phillis JW & Watkins JC (1960). The chemical excitation of spinal neurones by certain acidic amino acids. J Physiol 150, 656-682.
16. Curtis DR & Ryall RW (1966 a). The acetylcholine receptors of Renshaw cells. Exp Brain Res 2, 66-80.
17. Curtis DR & Ryall RW (1966 b). The synaptic excitation of Renshaw cells. Exp Brain Res 2, 81-96.
18. Dourado M & Sargent PB (2002). Properties of nicotinic receptors underlying Renshaw cell excitation by α-motor neurons in neonatal rat spinal cord. J Neurophysiol 87, 3117-3125.
19. Eccles JC, Eccles RM, Iggo A & Ito M (1961). Distribution of recurrent inhibition among motoneurones. J Physiol 159, 479-499.
20. Eccles JC, Fatt P & Koketsu K (1954). Cholinergic and inhibitory synapses in a pathway from motor-axon collaterals to motoneurones. J Physiol 126, 524-562.
21. Fatt P & Katz B (1952). The electric activity of the motor end-plate. Proc R Soc Lond B Biol Sci 140, 183-186.
22. Fetcho JR (2001). Optical and genetic approaches towards understanding spinal circuits. In Motor Neurobiology of the Spinal Cord, ed. Cope TC, pp. 3-20. CRC Press, Boca de Raton, FL, USA.
23. FitzSimons E, Van Zundert B, Constaine-Paton M, Brown RH Jr & Alvarez FJ (2006). Alterations in the Renshaw cell recurrent inhibitory circuit in the G93A SOD1 mouse model ALS. Abstr Soc Neurosci 678. -679.
24. Frank K & Fuortes MG (1956). Unitary activity of spinal interneurones of cats. J Physiol 131, 424-435.
25. Fyffe RE (1990). Evidence for separate morphological classes of Renshaw cells in the cat's spinal cord. Brain Res 536, 301-304.
26. Fyffe RE (1991 a). Glycine-like immunoreactivity in synaptic boutons of identified inhibitory interneurons in the mammalian spinal cord. Brain Res 547, 175-179.
27. Fyffe RE (1991 b). Spatial distribution of recurrent inhibitory synapses on spinal motoneurons in the cat. J Neurophysiol 65, 1134-1149.
28. Geiman EJ, Knox MC & Alvarez FJ (2000). Postnatal maturation of gephyrin/glycine receptor clusters on developing Renshaw cells. J Comp Neurol 426, 130-142.
29. Geiman EJ, Narayan S & Goulding M (2004). Synaptic inputs from ventral horn interneurons to Renshaw cells. Abstr Soc Neurosci 838-845.
30. Geiman EJ, Zheng W, Fritschy JM & Alvarez FJ (2002). Glycine and GABA A receptor subunits on Renshaw cells: Relationship with presynaptic neurotransmitters and postsynaptic gephyrin clusters. J Comp Neurol 444, 275-289.
31. Gingrich KJ, Roberts WA & Kass RS (1995). Dependence of the GABA A receptor gating kinetics on the α-subunit isoform: Implications for structure-function relations and synaptic transmission. J Physiol 489, 529-543.
32. Gonzalez-Forero D & Alvarez FJ (2005). Differential postnatal maturation of GABA A, glycine receptor, and mixed synaptic currents in Renshaw cells and ventral spinal interneurons. J Neurosci 25, 2010-2023.
33. Gonzalez-Forero D, Pastor AM, Geiman EJ, Benitez-Temino B & Alvarez FJ (2005). Regulation of gephyrin cluster size and inhibitory synaptic currents on Renshaw cells by motor axon excitatory inputs. J Neurosci 25, 417-429.
34. Gosgnach S, Lanuza GM, Butt SJ, Saueressig H, Zhang Y, Velasquez T, Riethmacher D, Callaway EM, Kiehn O & Goulding M (2006). V1 spinal neurons regulate the speed of vertebrate locomotor outputs. Nature 440, 215-219.
35. Goulding M, Lanuza G, Sapir T & Narayan S (2002). The formation of sensorimotor circuits. Curr Opin Neurobiol 12, 508-515.
36. Hamm TM (1990). Recurrent inhibition to and from motoneurons innervating the flexor digitorum and flexor hallucis longus muscles of the cat. J Neurophysiol 63, 395-403.
37. Hanson MG & Landmesser LT (2003). Characterization of the circuits that generate spontaneous episodes of activity in the early embryonic mouse spinal cord. J Neurosci 23, 587-600.
38. Herzog E, Landry M, Buhler E, Bouali-Benazzouz R, Legay C, Henderson CE, Nagy F, Dreyfus P, Giros B & El Mestikawy S (2004). Expression of vesicular glutamate transporters, VGLUT1 and VGLUT2, in cholinergic spinal motoneurons. Eur J Neurosci 20, 1752-1760.
39. Higashijima S, Masino MA, Mandel G & Fetcho JR (2004). Engrailed-1 expression marks a primitive class of inhibitory spinal interneuron. J Neurosci 24, 5827-5839.
40. Hultborn H, Lindstrom S & Wigstrom H (1979). On the function of recurrent inhibition in the spinal cord. Exp Brain Res 37, 399-403.
41. Isaac JT (2003). Postsynaptic silent synapses: Evidence and mechanisms. Neuropharmacology 45, 450-460.
42. Ishii K, Wong JK & Sumikawa K (2005). Comparison of α2 nicotinic acetylcholine receptor subunit mRNA expression in the central nervous system of rats and mice. J Comp Neurol 493, 241-260.
43. Jankowska E (1992). Interneuronal relay in spinal pathways from proprioceptors. Prog Neurobiol 38, 335-378.
44. Jankowska E, Krutki P & Matsuyama K (2005). Relative contribution of Ia inhibitory interneurones to inhibition of feline contralateral motoneurones evoked via commissural interneurones. J Physiol 568, 617-628.
45. Jankowska E & Lindstrom S (1971). Morphological identification of Renshaw cells. Acta Physiol Scand 81, 428-430.
46. Jessell TM (2000). Neuronal specification in the spinal cord: Inductive signals and transcriptional codes. Nat Rev Genet 1, 20-29.
47. Kiehn O (2006). Locomotor circuits in the mammalian spinal cord. Annu Rev Neurosci 29, 279-306.
48. Lagerback PA (1983). An ultrastructural study of serially sectioned Renshaw cells. III. Quantitative distribution of synaptic boutons. Brain Res 264, 215-223.
49. Lagerback PA & Kellerth JO (1985 a). Light microscopic observations on cat Renshaw cells after intracellular staining with horseradish peroxidase. I. The axonal systems. J Comp Neurol 240, 359-367.
50. Lagerback PA & Kellerth JO (1985 b). Light microscopic observations on cat Renshaw cells after intracellular staining with horseradish peroxidase. II. The cell bodies and dendrites. J Comp Neurol 240, 368-376.
51. Lagerback PA & Ronnevi LO (1982 a). An ultrastructural study of serially sectioned Renshaw cells. I. Architecture of the cell body, axon hillock, initial axon segment and proximal dendrites. Brain Res 235, 1-15.
52. Lagerback PA & Ronnevi LO (1982 b). An ultrastructural study of serially sectioned Renshaw cells. II. Synaptic types. Brain Res 246, 181-192.
53. Lee SK & Pfaff SL (2001). Transcriptional networks regulating neuronal identity in the developing spinal cord. Nat Neurosci 4, 1183-1191.
54. Li WC, Higashijima S, Parry DM, Roberts A & Soffe SR (2004). Primitive roles for inhibitory interneurons in developing frog spinal cord. J Neurosci 24, 5840-5848.
55. Lim R, Alvarez FJ & Walmsley B (1999). Quantal size is correlated with receptor cluster area at glycinergic synapses in the rat brainstem. J Physiol 516, 505-512.
56. McCurdy ML & Hamm TM (1994). Topography of recurrent inhibitory postsynaptic potentials between individual motoneurons in the cat. J Neurophysiol 72, 214-226.
57. Maltenfort MG, Heckman CJ & Rymer WZ (1998). Decorrelating actions of Renshaw interneurons on the firing of spinal motoneurons within a motor nucleus: A simulation study. J Neurophysiol 80, 309-323.
58. Mangin JM, Guyon A, Eugène D, Paupardin-Tritsch D, Legendre P (2002). Functional glycine receptor maturation in the absence of glycinergic input in dopaminergic neurones of the rat substantia nigra. J Physiol 542, 685-697.
59. Mattei B, Schmied A, Mazzocchio R, Decchi B, Rossi A & Vedel JP (2003). Pharmacologically induced enhancement of recurrent inhibition in humans: Effects on motoneurone discharge patterns. J Physiol 548, 615-629.
60. Meier J (2003). The enigma of transmitter-selective receptor accumulation at developing inhibitory synapses. Cell Tissue Res 311, 271-276.
61. Mentis GZ, Alvarez FJ, Bonnot A, Richards DS, Gonzalez-Forero D, Zerda R & O'Donovan MJ (2005). Noncholinergic excitatory actions of motoneurons in the neonatal mammalian spinal cord. Proc Natl Acad Sci U S A 102, 7344-7349.
62. Mentis GZ, Siembab VC, Zerda R, O'Donovan MJ & Alvarez FJ (2006). Primary afferent synapses on developing and adult Renshaw cells. J Neurosci 26, 13297-13310.
63. Myers CP, Lewcock JW, Hanson MG, Gosgnach S, Aimone JB, Gage FH, Lee KF, Landmesser LT & Pfaff SL (2005). Cholinergic input is required during embryonic development to mediate proper assembly of spinal locomotor circuits. Neuron 46, 37-49.
64. Naka KI (1964). Electrophysiology of the fetal spinal cord. II. Interaction among peripheral inputs and recurrent inhibition. J Gen Physiol 47, 1023-1038.
65. Nishimaru H, Restrepo CE & Kiehn O (2006). Activity of Renshaw cells during locomotor-like rhythmic activity in the isolated spinal cord of neonatal mice. J Neurosci 26, 5320-5328.
66. Nishimaru H, Restrepo CE, Ryge J, Yanagawa Y & Kiehn O (2005). Mammalian motor neurons corelease glutamate and acetylcholine at central synapses. Proc Natl Acad Sci U S A 102, 5245-5249.
67. Noga BR, Shefchyk SJ, Jamal J & Jordan LM (1987). The role of Renshaw cells in locomotion: Antagonism of their excitation from motor axon collaterals with intravenous mecamylamine. Exp Brain Res 66, 99-105.
68. Nusser Z, Cull-Candy S & Farrant M (1998). Differences in synaptic GABA A receptor number underlie variation in GABA mini amplitude. Neuron 19, 697-709.
69. O'Donovan MJ, Chub N & Wenner P (1998). Mechanisms of spontaneous activity in developing spinal networks. J Neurobiol 37, 131-145.
70. Oleskevich S, Alvarez FJ & Walmsley B (1999). Glycinergic miniature synaptic currents and receptor cluster sizes differ between spinal cord interneurons. J Neurophysiol 82, 312-319.
71. Pinard A, Levesque S, Vallee J & Robitaille R (2003). Glutamatergic modulation of synaptic plasticity at a PNS vertebrate cholinergic synapse. Eur J Neurosci 18, 3241-3250.
72. Price SR & Briscoe J (2004). The generation and diversification of spinal motor neurons: Signals and responses. Mech Dev 121, 1103-1115.
73. Renshaw B (1941). Influence of the discharge of motoneurons upon exciation of neighboring motoneurons. J Neurophysiol 4, 167-183.
74. Renshaw B (1946). Central effects of centripetal impulses in axons of spinal ventral roots. J Neurophysiol 9, 191-204.
75. Ryall RW & Piercey MF (1971). Excitation and inhibition of Renshaw cells by impulses in peripheral afferent nerve fibers. J Neurophysiol 34, 242-251.
76. Rybak IA, Shevtsova NA, Lafreniere-Roula M & McCrea DA (2006 a). Modelling spinal circuitry involved in locomotor pattern generation: insights from deletions during fictive locomotion. J Physiol 577, 617-639.
77. Rybak IA, Stecina K, Shevtsova NA & McCrea DA (2006 b). Modelling spinal circuitry involved in locomotor pattern generation: Insights from the effects of affeent stimulation. J Physiol 577, 641-658.
78. Sapir T, Geiman EJ, Wang Z, Velasquez T, Mitsui S, Yoshihara Y, Frank E, Alvarez FJ & Goulding M (2004). Pax6 and engrailed 1 regulate two distinct aspects of Renshaw cell development. J Neurosci 24, 1255-1264.
79. Saueressig H, Burrill J & Goulding M (1999). Engrailed-1 and netrin-1 regulate axon pathfinding by association interneurons that project to motor neurons. Development 126, 4201-4212.
80. Schneider SP & Fyffe RE (1992). Involvement of GABA and glycine in recurrent inhibition of spinal motoneurons. J Neurophysiol 68, 397-406.
81. Shirasaki R & Pfaff SL (2002). Transcriptional codes and the control of neuronal identity. Annu Rev Neurosci 25, 251-281.
82. Shupliakov O, Ornung G, Brodin L, Ulfhake B, Ottersen OP, Storm-Mathisen J & Cullheim S (1993). Immunocytochemical localization of amino acid neurotransmitter candidates in the ventral horn of the cat spinal cord: a light microscopic study. Exp Brain Res 96, 404-418.
83. Smith C, Siembab VC, Berrocal MC, Goulding M & Alvarez F (2005). Postnatal diversification of V1-derived interneurons. Abstr Soc Neurosci 603. -615.
84. Thomas RC & Wilson VJ (1965). Precise localization of Renshaw cells with a new marking technique. Nature 206, 211-213.
85. Turkin VV, Monroe KS & Hamm TM (1998). Organization of recurrent inhibition and facilitation in motor nuclei innervating ankle muscles of the cat. J Neurophysiol 79, 778-790.
86. Van Keulen LC (1979). Axon trajectories of Renshaw cells in the lumbar spinal cord of the cat, as reconstructed after intracellular staining with horseradish peroxidase. Brain Res 167, 157-162.
87. Van Keulen L (1981). Autogenetic recurrent inhibition of individual spinal motoneurones of the cat. Neurosci Lett 21, 297-300.
88. Voronin LL & Cherubini E (2004). "Deaf, mute and whispering" silent synapses: Their role in synaptic plasticity. J Physiol 557, 3-12.
89. Waerhaug O & Ottersen OP (1993). Demonstration of glutamate-like immunoreactivity at rat neuromuscular junctions by quantitative electron microscopic immunocytochemistry. Anat Embryol (Berl) 188, 501-513.
90. Walmsley B & Tracey DJ (1981). An intracellular study of Renshaw cells. Brain Res 223, 170-175.
91. Wenner P & O'Donovan MJ (1999). Identification of an interneuronal population that mediates recurrent inhibition of motoneurons in the developing chick spinal cord. J Neurosci 19, 7557-7567.
92. Wenner P & O'Donovan MJ (2001). Mechanisms that initiate spontaneous network activity in the developing chick spinal cord. J Neurophysiol 86, 1481-1498.
93. Wenner P, O'Donovan MJ & Matise MP (2000). Topographical and physiological characterization of interneurons that express engrailed-1 in the embryonic chick spinal cord. J Neurophysiol 84, 2651-2657.
94. Willis WD (1971). The case for the Renshaw cell. Brain Behav Evol 4, 5-52.
95. Windhorst U (1990). Activation of Renshaw cells. Prog Neurobiol 35, 135-179.
96. Zhang JH, Morita Y, Hironaka T, Emson PC & Tohyama M (1990). Ontological study of calbindin-D28k-like and parvalbumin-like immunoreactivities in rat spinal cord and dorsal root ganglia. J Comp Neurol 302, 715-728.