Segmental, synaptic actions of commissural interneurons in the mouse spinal cord

Journal of Neuroscience

Volumn 27, Issue 24, 2007, Pages 6521-6530

  Quinlan, Katharina A ^a   Kiehn, Ole ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Commissural interneurons; CPG; GABA; Glutamate; Glycine; Locomotion; Motor neurons; Spinal cord

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; GLUTAMATE RECEPTOR; GLYCINE RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN COMMISSURE; BRAIN DEPTH STIMULATION; CELL COUNT; COORDINATION; IN VITRO STUDY; INTERNEURON; LOCOMOTION; MOTONEURON; MOUSE; NERVE CELL; NERVE FIBER; NERVE PROJECTION; NERVOUS SYSTEM; NEWBORN; NONHUMAN; PRIORITY JOURNAL; SPINAL CORD; SYNAPSE; SYNAPTIC EFFICACY;

ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, RADIATION; ELECTRIC STIMULATION; EXCITATORY AMINO ACID ANTAGONISTS; FUNCTIONAL LATERALITY; INTERNEURONS; LOCOMOTION; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MOTOR NEURONS; SPINAL CORD; SYNAPSES;

EID: 34250359446     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1618-07.2007     Document Type: Article

References (62)

1. Angel MJ, Jankowska E, McCrea DA (2005) Candidate interneurons mediating group I disynaptic EPSPs in extensor motoneurones during fictive locomotion in the cat. J Physiol (Lond) 563:597-610.
2. Antonio-Green DM, Cheng J, Magnuson DS (2002) Neurons labeled from locomotor-related ventrolateral funiculus stimulus sites in the neonatal rat spinal cord. J Comp Neurol 442:226-238.
3. Bannatyne BA, Edgley SA, Hammar I, Jankowska E, Maxwell DJ (2003) Networks of inhibitory and excitatory commissural interneurons mediating crossed reticulospinal actions. Eur J Neurosci 18:2273-2284.
4. Birinyi A, Viszokay K, Weber I, Kiehn O, Antal M (2003) Synaptic targets of commissural interneurons in the lumbar spinal cord of neonatal rats. J Comp Neurol 461:429-440.
5. Brink E, Jankowska E, McCrea DA, Skoog B (1983) Inhibitory interactions between interneurones in reflex pathways from group Ia and group Ib afferents in the cat. J Physiol (Lond) 343:361-373.
6. Buchanan JT (1982) Identification of interneurons with contralateral, caudal axons in the lamprey spinal cord: synaptic interactions and morphology. J Neurophys 47:961-975.
7. Buchanan JT (2001) Contributions of identifiable neurons and neuron classes to lamprey vertebrate neurobiology. Prog Neurbiol 63:441-466.
8. Butt SJ, Kiehn O (2003) Functional identification of interneurons responsible for left-right coordination of hindlimbs in mammals. Neuron 38:953-963.
9. Butt SJ, Harris-Warrick RM, Kiehn O (2002) Firing properties of identified interneuron populations in the mammalian hindlimb central pattern generator. J Neurosci 15:9961-9971.
10. Butt SJ, Lundfald L, Kiehn O (2005) EphA4 defines a class of excitatory locomotor-related interneurons. Proc Natl Acad Sci USA 102:14098-14103.
11. Carlin KP, Dai Y, Jordan LM (2006) Cholinergic and serotonergic excitation of ascending commissural neurons in the thoraco-lumbar spinal cord of the neonatal mouse. J Neurophyiol 95:1278-1284.
12. Dale N (1985) Reciprocal inhibitory interneurones in the Xenopus embryo spinal cord. J Physiol (Lond) 363:61-70.
13. Edgley SA, Jankowska E, Hammar I (2004) Ipsilateral actions of feline corticospinal tract neurons on limb motoneurons. J Neurosci 24:7804-7813.
14. Eide AL, Glover J, Kjaerulff O, Kiehn O (1999) Characterization of commissural interneurons in the lumbar region of the neonatal rat. J Comp Neurol 403:332-345.
15. Farkas S, Tarnawa I, Berzsenyi P (1989) Effects of some centrally acting muscle relaxants on spinal root potentials: a comparative study. Neuropharmacology 28:161-173.
16. Gossard JP, Brownstone RM, Barajon I, Hultborn H (1994) Transmission in a locomotor-related group Ib pathway from hindlimb extensor muscles in the cat. Exp Brain Res 98:213-228.
17. Grillner S (2003) The motor infrastructure: from ion channels to neuronal networks. Nat Rev 4:573-586.
18. Hammar I, Bannatyne BA, Maxwell DJ, Edgley SA, Jankowska E (2004) The actions of monoamines and distribution of noradrenergic and serotoninergic contacts on different subpopulations of commissural interneurons in the cat spinal cord. Eur J Neurosci 19:1305-1316.
19. Hinckley C, Seebach B, Ziskind-Conhaim L (2005) Distinct roles of glycinergic and GABAergic inhibition in coordinating locomotor-like rhythms in the neonatal mouse spinal cord. Neuroscience 131:745-758.
20. Hinckley CA, Ziskind-Conhaim L (2006) Electrical coupling between locomotor-related excitatory interneurons in the mammalian spinal cord. J Neurosci 26:8477-8483.
21. Hoover JE, Durkovic RG (1992) Retrograde labeling of lumbosacral interneurons following injections of red and green fluorescent microspheres into hindlimb motor nuclei of the cat. Somatosens Mot Res 9:211-226.
22. Huang A, Noga BR, Carr PA, Fedirchuk B, Jordan LM (2000) Spinal cholinergic neurons activated during locomotion: localization and electrophysiological characterization. J Neurophysiol 83:3537-3547.
23. Jahr CE, Yoshioka K (1986) Ia afferent excitation of motoneurones in the in vitro new-born rat spinal cord is selectively antagonized by kynurenate. J Physiol (Lond) 370:515-530.
24. Jankowska E, Jukes MG, Lund S, Lundberg A (1967) The effect of DOPA on the spinal cord. 5. Reciprocal organization of pathways transmitting excitatory action to alpha motoneurones of flexors and extensors. Acta Physiol Scand 70:369-388.
25. Jankowska E, Hammar I, Slawinska U, Maleszak K, Edgley SA (2003) Neuronal basis of crossed actions from the reticular formation on feline hind-limb motoneurons. J Neurosci 23:1867-1878.
26. Jankowska E, Edgley SA, Krutki P, Hammar I (2005a) Functional differentiation and organization of feline midlumbar commissural interneurons. J Physiol (Lond) 565:645-658.
27. Jankowska E, Cabaj A, Pettersson LG (2005b) How to enhance ipsilateral actions of pyramidal tract neurons. J Neurosci 25:7401-7405.
28. Jankowska E, Krutki P, Matsuyama K (2005c) Relative contribution of Ia inhibitory interneurons to inhibition of feline contralateral motoneurones evoked via commissural interneurons. J Physiol (Lond) 568:617-628.
29. Juvin L, Simmers J, Morin D (2005) Propriospinal circuitry underlying interlimb coordination in mammalian quadrupedal locomotion. J Neurosci 25:6025-6035.
30. Kiehn O (2006) Locomotor circuits in the mammalian spinal cord. Annu Rev Neurosci 29:279-306.
31. Kiehn O, Kjaerulff O (1998) Distribution of central pattern generators for rhythmic motor outputs in the spinal cord of limbed vertebrates. Ann NY Acad Sci 860:110-129.
32. Kiehn O, Johnson BR, Raastad M (1996) Plateau properties in mammalian spinal interneurons during transmitter-induced locomotor activity. Neuroscience 75:263-273.
33. Kjaerulff O, Kiehn O (1996) Distribution of networks generating and coordinating locomotor activity in the neonatal rat spinal cord: a lesion study. J Neurosci 16:5777-5794.
34. Krutki P, Jankowska E, Edgley SA (2003) Are crossed actions of reticulospinal and vestibulospinal neurons on feline motoneurons mediated by the same or separate commissural neurons? J Neurosci 23:8041-8050.
35. Ma W, Behar T, Maric D, Maric I, Barker JL (1992a) Neuroepithelial cells in the rat spinal cord express glutamate decarboxylase immunoreactivity in vivo and in vitro. J Comp Neurol 325:257-270.
36. Ma W, Behar T, Barker JL (1992b) Transient expression of GABA immunoreactivity in the developing rat spinal cord. J Comp Neurol 325:271-290.
37. Matsuyama K, Jankowska E (2004) Coupling between feline cerebellum (fastigial neurons) and motoneurons innervating hindlimb muscles. J Neurophysiol 91:1183-1192.
38. Matsuyama K, Nakajima K, Mori F, Aoki M, Mori S (2004) Lumbar commissural interneurons with reticulospinal inputs in the cat: morphology and discharge patterns during fictive locomotion. J Comp Neurol 474:546-561.
39. Matsuyama K, Kobayashi S, Aoki M (2006) Projection patterns of lamina VIII commissural neurons in the lumbar spinal cord of the adult cat: an anterograde neural tracing study. Neuroscience 140:203-218.
40. McCrea DA (2001) Spinal circuitry of sensorimotor control of locomotion. J Physiol (Lond) 533:41-50.
41. McLean DA, Merrywest SD, Sillar KT (2000) The development of neuromodulatory systems and the maturation of motor patterns in amphibian tadpoles. Brain Res Bull 53:595-603.
42. Nakayama K, Nishimaru H, Kudo N (2002) Basis of changes in left-right coordination of rhythmic motor activity during development in the rat spinal cord. J Neurosci 22:10388-10398.
43. Nishimaru H, Kudo N (2000) Formation of the central pattern generator for locomotion in the rat and mouse. Brain Res Bull 53:661-669.
44. 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.
45. Nissen U, Mochida H, Glover JC (2005) Development of projection-specific interneurons and projection neurons in the embryonic mouse and rat spinal cord. J Comp Neurol 483:30-47.
46. Parker D (2006) Complexities and uncertainties of neuronal network function. Philos Trans R Soc Lond B Biol Sci 361:81-99.
47. Pflieger JF, Clarac F, Vinay L (2002) Picrotoxin and bicuculline have different effects on lumbar spinal networks and motoneurons in the neonatal rat. Brain Res 935:81-86.
48. Quinlan KA, Kiehn O (2005) Synaptic effects of intrasegmental commissural interneurons in the mouse spinal cord. Soc Neurosci Abstr 31:516.1.
49. Raastad M, Enriquez-Denton M, Kiehn O (1998) Synaptic signaling in an active central network only moderately changes passive membrane properties. Proc Natl Acad Sci USA 95:10251-10256.
50. Roberts A, Soffe SR, Wolf ES, Yoshida M, Zhao FY (1998) Central circuits controlling locomotion in young frog tadpoles. Ann NY Acad Sci 860:19-34.
51. Rudomin P, Solodkin M, Jiménez I (1987) Synaptic potentials of primary afferent fibers and motoneurons evoked by single intermediate nucleus interneurons in the cat spinal cord. J Neurophysiol 57:1288-1313.
52. Scheibel ME, Scheibel AB (1969) A structural analysis of spinal interneurons and Renshaw cells. UCLA Forum Med Sci 11:159-208.
53. Stokke MF, Nissen U, Glover JC, Kiehn O (2002) Projection patterns of commissural interneurons in the lumbar spinal cord of the neonatal rat. J Comp Neurol 446:349-359.
54. Tran TS, Alijani A, Phelps PE (2003) Unique developmental patterns of GABAergic neurons in rat spinal cord. J Comp Neurol 456:112-126.
55. Tran TS, Cohen-Cory S, Phelps PE (2004) Embryonic GABAergic spinal commissural neurons project rostrally to mesencephalic targets. J Comp Neurol 475:327-339.
56. Tresch MC, Kiehn O (1999) Coding of locomotor phase in populations of neurons in rostral and caudal segments of the neonatal rat lumbar spinal cord. J Neurophysiol 82:3563-3574.
57. Tyzio R, Cossart R, Khalilov I, Minlebaev M, Hübner CA, Represa A, Ben-Ari Y, Khazipov R (2006) Maternal oxytocin triggers a transient inhibitory switch in GABA signalling in the fetal brain during delivery. Science 314:1788-1792.
58. Vinay L, Cazalets JR, Clarac F (1995) Evidence for a functional polysynaptic pathway from trigeminal afferents to lumbar motoneurons in the neonatal rat. Eur J Neurosci 7:143-151.
59. 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.
60. Wilson JM, Hartley R, Maxwell DJ, Todd AJ, Lieberam I, Kaltschmidt JA, Yoshida Y, Jessell TM, Brownstone RM (2005) Conditional rhythmicity of ventral spinal interneurons defined by expression of the Hb9 homeodomain protein. J Neurosci 25:5710-5719.
61. Zhong G, Diaz-Rios M, Harris-Warrick RM (2006a) Serotonin modulates the properties of ascending commissural interneurons in the neonatal mouse spinal cord. J Neurophysiol 95:1545-1555.
62. Zhong G, Diaz-Rios M, Harris-Warrick RM (2006b) Intrinsic and functional differences among commissural interneurons during fictive locomotion and serotonergic modulation in the neonatal mouse. J Neurosci 26:6509-6517.