Early postnatal development of reciprocal Ia inhibition in the murine spinal cord

Journal of Neurophysiology

Volumn 100, Issue 1, 2008, Pages 185-196

  Wang, Zhi ^a   Li, Ngying ^a   Goulding, Martyn ^b   Frank, Eric ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCINE; STRYCHNINE; TRANSCRIPTION FACTOR PAX6; 4 AMINOBUTYRIC ACID RECEPTOR BLOCKING AGENT; AMINO ACID RECEPTOR AFFECTING AGENT; BICUCULLINE; EYE PROTEIN; HOMEODOMAIN PROTEIN; PAIRED BOX TRANSCRIPTION FACTOR; REPRESSOR PROTEIN;

AFFERENT NERVE GROUP 1; ARTICLE; BICEPS BRACHII MUSCLE; CONTROLLED STUDY; INTERNEURON; MOTONEURON; MOUSE; NERVE FIBER; NERVE STIMULATION; NEWBORN; NONHUMAN; PERINATAL DEVELOPMENT; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; SEMITENDINOUS MUSCLE; SPINAL CORD; SYNAPTIC POTENTIAL; AGE; ANIMAL; C57BL MOUSE; CYTOLOGY; DRUG EFFECT; GENETICS; GROWTH, DEVELOPMENT AND AGING; IN VITRO STUDY; INNERVATION; MONOSYNAPTIC REFLEX; MOUSE MUTANT; MUSCLE; NERVE CELL INHIBITION; NERVE CONDUCTION; PHYSIOLOGY; RADIATION EXPOSURE; RADIATION RESPONSE; REACTION TIME; STIMULATION;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BICUCULLINE; DOSE-RESPONSE RELATIONSHIP, RADIATION; EYE PROTEINS; GABA ANTAGONISTS; GLYCINE AGENTS; HOMEODOMAIN PROTEINS; INTERNEURONS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOTOR NEURONS; MUSCLES; NEURAL CONDUCTION; NEURAL INHIBITION; PAIRED BOX TRANSCRIPTION FACTORS; PHYSICAL STIMULATION; REACTION TIME; REFLEX, MONOSYNAPTIC; REPRESSOR PROTEINS; SPINAL CORD; STRYCHNINE;

EID: 55249085812     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.90354.2008     Document Type: Article

References (53)

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, Jonas PC, Sapir T, Hartley R, Berrocal MC, Geiman EJ, Todd AJ, Goulding M. Postnatal phenotype and localization of spinal cord V1 derived interneurons. J Comp Neurol 493: 177-192, 2005.
3. Araki T, Eccles JC, Ito M. Correlation of the inhibitory post-synaptic potential of motoneurons with the latency and time course of inhibition of monosynaptic reflexes. J Physiol 154: 354-377, 1960.
4. Arber S, Ladle DR, Lin JH, Frank E, Jessell TM. ETS gene Er81 controls the formation of functional connections between group Ia sensory afferents and motor neurons. Cell 101: 485-498, 2000.
5. Baccei ML, Fitzgerald M. Development of GABAergic and glycinergic transmission in the neonatal rat dorsal horn. J Neurosci 24: 4749-4757, 2004.
6. Berry M, Pentreath VW. Criteria for distinguishing between monosynaptic and polysynaptic transmission. Brain Res 105: 1-20, 1976.
7. Burrill JD, Moran L, Goulding MD, Saueressig H. PAX2 is expressed in multiple spinal cord interneurons, including a population of EN1 + interneurons that require PAX6 for their development. Development 124: 4493-4503, 1997.
8. Chen HH, Hippenmeyer S, Arber S, Frank E. Development of the monosynaptic stretch reflex circuit. Curr Opin Neurobiol 13: 96-102, 2003.
9. Chen HH, Tourtellotte WG, Frank E. Muscle spindle-derived neurotrophin 3 regulates synaptic connectivity between muscle sensory and motor neurons. J Neurosci 22: 3512-3519, 2002.
10. Curtis DR. Pharmacological investigations upon inhibition of spinal motoneurons. J Physiol 145: 175-192, 1959.
11. Curtis DR, Hosli L, Johnston GA. A pharmacological study of the depression of spinal neurones by glycine and related amino acids. Exp Brain Res 6: 1-18, 1968a.
12. Curtis DR, Hosli L, Johnston GA, Johnston IH. The hyperpolarization of spinal motoneurones by glycine and related amino acids. Exp Brain Res 5: 235-258, 1968b.
13. 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.
14. Eccles JC, Eccles RM, Lundberg A. Synaptic actions on motoneurons caused by impulses in Golgi tendon organ afferents. J Physiol 138: 227-252, 1957.
15. Eccles JC, Fatt P, Koketsu K. Cholinergic and inhibitory synapses in a pathway from motor-axon collaterals to motoneurons. J Physiol 126: 524-562, 1954.
16. Eccles JC, Fatt P, Landgren S. Central pathway for direct inhibitory action of impulses in largest afferent nerve fibers to muscle. J Neurophysiol 19: 75-98, 1956.
17. Eccles RM, Lundberg A. Integrative pattern of Ia synaptic actions on motoneurones of hip and knee muscles. J Physiol 144: 271-298, 1958.
18. Ericson J, Rashbass P, Schedl A, Brenner-Morton S, Kawakami A, van Heyningen V, Jessell TM, Briscoe J. Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling. Cell 90: 169-180, 1997.
19. Frank E, Westerfield M. Development of sensory-motor synapses in the spinal cord of the frog. J Physiol 343: 593-610, 1983.
20. Gao BX, Stricker C, Ziskind-Conhaim L. Transition from GABAergic to glycinergic synaptic transmission in newly formed spinal networks. J Neurophysiol 86: 492-502, 2001.
21. Glover JC. Development of specific connectivity between premotor neurons and motoneurons in the brain stem and spinal cord. Physiol Rev 80: 615-647, 2000.
22. 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.
23. Gosgnach S, Lanuza GM, Butt SJ, Saueressig H, Zhang Y, Velasquez T, Riethmacher D, Callaway EM, Kiehn O, Goulding M. V1 spinal neurons regulate the speed of vertebrate locomotor outputs. Nature 440: 215-219, 2006.
24. Hippenmeyer S, Huber RM, Ladle DR, Murphy K, Arber S. ETS transcription factor Erm controls subsynaptic gene expression in skeletal muscles. Neuron 55: 726-740, 2007.
25. Hultborn H, Jankowska E, Lindstrom S. Recurrent inhibition from motor axon collaterals of transmission in the Ia inhibitory pathway to motoneurons. J Physiol 215: 591-612, 1971a.
26. Hultborn H, Jankowska E, Lindstrom S. Recurrent inhibition of interneurons monosynaptically activated from group Ia afferents. J Physiol 215: 613-636, 1971b.
27. Hultborn H, Jankowska E, Lindstrom S. Relative contribution from different nerves to recurrent depression of Ia IPSPs in motoneurons. J Physiol 215: 637-664, 1971c.
28. Hultborn H, Udo M. Convergence of large muscle spindle (Ia) afferents at interneuronal level in the reciprocal Ia inhibitory pathway to motoneurons. Acta Physiol Scand 84: 493-499, 1972.
29. Jankowska E. Interneuronal relay in spinal pathways from proprioceptors. Prog Neurobiol 38: 335-378, 1992.
30. Jankowska E. Spinal interneuronal systems: identification, multifunctional character and reconfigurations in mammals. J Physiol 533: 31-40, 2001.
31. Jonas P, Bischofberger J, Sandkuhler J. Corelease of two fast neurotransmitters at a central synapse. Science 281: 419-424, 1998.
32. Kudo N, Yamada T. Development of the monosynaptic stretch reflex in the rat: an in vitro study. J Physiol 369: 127-144, 1985.
33. Lee MT, O'Donovan MJ. Organization of hindlimb muscle afferent projections to lumbosacral motoneurons in the chick embryo. J Neurosci 11: 2564-2573, 1991.
34. Lichtman JW, Frank E. Physiological evidence for specificity of synaptic connections between individual sensory and motor neurons in the brachial spinal cord of the bullfrog. J Neurosci 4: 1745-1753, 1984.
35. Lloyd DPC. A direct central inhibitory action of dromically conducted inpulses. J Neurophysiol 4: 184-190, 1941.
36. Lloyd DPC. Facilitation and inhibition of spinal motoneurons. J Neurophysiol 9: 421-438, 1946.
37. Martini FH, Timmons MJ, Mckinley MP, Ober WC, Garrison CW, Welch K, Hutchings RT. The muscle system: the appendicular musculature. In: Human Anatomy, Upper Saddle River, NJ: Prentice Hall, 2000, p. 286-319.
38. Mc Donough SM, Clowry GJ, Miller S, Eyre JA. Reciprocal and Renshaw (recurrent) inhibition are functional in man at birth. Brain Res 899: 66-81, 2001.
39. Mears SC, Frank E. Formation of specific monosynaptic connections between muscle spindle afferents and motoneurons in the mouse. J Neurosci 17: 3128-3135, 1997.
40. Mendelson B, Frank E. Specific monosynaptic sensory-motor connections in the chick embryonic spinal cord form in the absence of patterned neural activity and motoneuronal cell death. J Neurosci 11: 1390-1403, 1991.
41. Mentis GZ, Siembab VC, Zerda R, O'Donovan MJ, Alvarez FJ. Primary afferent synapses on developing and adult Renshaw cells. J Neurosci 26: 13297-13310, 2006.
42. 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.
43. Renshaw B. influence of discharge of motoneurons upon excitation of neighboring motoneurons. J Neurophysiol 4: 167-183, 1941.
44. 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.
45. Schneider SP, Fyffe REW. Involvement of GABA and glycine in recurrent inhibition of spinal motor neurons. J Neurophysiol 68: 397-406, 1992.
46. Seebach BS, Ziskind-Conhaim L. Formation of transient inappropriate sensorimotor synapses in developing rat spinal cords. J Neurosci 14: 4520-4528, 1994.
47. Stein V, Hermans-Borgmeyer I, Jentsch TJ, Hubner CA. Expression of the KCl cotransporter KCC2 parallels neuronal maturation and the emergence of low intracellular chloride. J Comp Neurol 468: 57-64, 2004.
48. Stuart GJ, Redman SJ. Voltage dependence of Ia reciprocal inhibitory currents in cat spinal motoneurons. J Physiol 420: 111-125, 1990.
49. Wang Z, Li LY, Taylor MD, Wright DE, Frank E. Prenatal exposure to elevated NT3 disrupts synaptic selectivity in the spinal cord. J Neurosci 27: 3686-3694, 2007.
50. Wenner P, O'Donovan MJ. Identification of an interneuronal population that mediates recurrent inhibition of motoneurons in the developing chick spinal cord. J Neurosci 19: 7557-7567, 1999.
51. Wenner P, O'Donovan MJ, Matise MP. Topographical and physiological characterization of interneurons that express engrailed-1 in the embryonic chick spinal cord. J Neurophysiol 84: 2651-2657, 2000.
52. Xu H, Clement A, Wright TM, Wenner P. Developmental reorganization of the output of a GABAergic interneuronal circuit. J Neurophysiol 97: 2769-2779, 2007.
53. Xu H, Whelan PJ, Wenner P. Development of an inhibitory interneuronal circuit in the embryonic spinal cord. J Neurophysiol 93: 2922-2933, 2005.