Inhibitory inputs to four types of spinocerebellar tract neurons in the cat spinal cord

Neuroscience

Volumn 226, Issue , 2012, Pages 253-269

  Shakya Shrestha, S ^a   Bannatyne, B A ^a   Jankowska, E ^b   Hammar, I ^b   Nilsson, E ^b   Maxwell, D J ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

Inhibition; Intracellular recording; Morphology; Motor control; Neuronal networks; Neurotransmitters

Indexed keywords

4 AMINOBUTYRIC ACID CARRIER; GLUTAMATE DECARBOXYLASE; GLYCINE; VESICULAR GLUTAMATE TRANSPORTER 1; VESICULAR GLUTAMATE TRANSPORTER 2;

AFFERENT NERVE GROUP 1; ANIMAL CELL; ARTICLE; CAT; CELL DENSITY; CELL LABELING; CELL POPULATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; GABAERGIC SYSTEM; IMMUNOHISTOCHEMISTRY; INHIBITORY POSTSYNAPTIC POTENTIAL; INTERNEURON; MOTONEURON; MOTOR CONTROL; NERVE CELL; NERVE ENDING; NEUROTRANSMISSION; NONHUMAN; PREMOTOR CORTEX; PRIORITY JOURNAL; SPINAL CORD DORSAL HORN; SPINAL CORD NERVE CELL; SPINOCEREBELLAR TRACT; SYNAPTIC TRANSMISSION;

ANIMALS; CATS; ELECTRIC STIMULATION; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; GLYCINE; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; MICROSCOPY, CONFOCAL; NERVE ENDINGS; NEURONS; PERIPHERAL NERVES; SPINAL CORD; SPINOCEREBELLAR TRACTS; VESICULAR GLUTAMATE TRANSPORT PROTEIN 1; VESICULAR GLUTAMATE TRANSPORT PROTEIN 2; VESICULAR INHIBITORY AMINO ACID TRANSPORT PROTEINS;

EID: 84867310439     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.09.015     Document Type: Article

References (65)

1. Abzug C., Maeda M., Peterson B.W., Wilson V.J. Cervical branching of lumbar vestibulospinal axons. J Physiol 1974, 243:499-522.
2. Alvarez F.J., Dewey D.E., Harrington D.A., Fyffe R.E. Cell-type specific organization of glycine receptor clusters in the mammalian spinal cord. J Comp Neurol 1997, 379:150-170.
3. Alvarez F.J., Fyffe R.E. The continuing case for the Renshaw cell. J Physiol 2007, 584:31-45.
4. Alvarez F.J., Villalba R.M., Zerda R., Schneider S.P. Vesicular glutamate transporters in the spinal cord, with special reference to sensory primary afferent synapses. J Comp Neurol 2004, 472:257-280.
5. Alvina K., Khodakhah K. The therapeutic mode of action of 4-aminopyridine in cerebellar ataxia. J Neurosci 2010, 30:7258-7268.
6. Alstermark B., Lundberg A., Sasaki S. Integration in descending motor pathways controlling the forelimb in the cat. 10. Inhibitory pathways to forelimb motoneurones via C3-C4 propriospinal neurones. Exp Brain Res 1984, 56:279-292.
7. Aubrey K.R., Rossi F.M., Ruivo R., Alboni S., Bellenchi G.C., Le Goff A., Gasnier B., Supplisson S. The transporters GlyT2 and VIAAT cooperate to determine the vesicular glycinergic phenotype. J Neurosci 2007, 27:6273-6281.
8. Baldissera F., Roberts W.J. Effects from the vestibulospinal tract on transmission from primary afferents to ventral spino-cerebellar tract neurones. Acta Physiol Scand 1976, 96:217-232.
9. Baldissera F., ten Bruggencate G. Rubrospinal effects on ventral spinocerebellar tract neurones. Acta Physiol Scand 1976, 96:233-249.
10. Bannatyne B.A., Edgley S.A., Hammar I., Jankowska E., Maxwell D.J. Networks of inhibitory and excitatory commissural interneurons mediating crossed reticulospinal actions. Eur J Neurosci 2003, 18:2273-2284.
11. Bannatyne B.A., Edgley S.A., Hammar I., Jankowska E., Maxwell D.J. Differential projections of excitatory and inhibitory dorsal horn interneurons relaying information from group II muscle afferents in the cat spinal cord. J Neurosci 2006, 26:2871-2880.
12. Bannatyne B.A., Liu T.T., Hammar I., Stecina K., Jankowska E., Maxwell D.J. Excitatory and inhibitory intermediate zone interneurons in pathways from feline group I and II afferents: differences in axonal projections and input. J Physiol 2009, 587:379-399.
13. Berger A.J., Dieudonné S., Ascher P. Glycine uptake governs glycine site occupancy at NMDA receptors of excitatory synapses. J Neurophysiol 1998, 80:3336-3340.
14. Bosco G., Poppele R.E. Proprioception from a spinocerebellar perspective. Physiol Rev 2001, 81:539-568.
15. Burger P.M., Hell J., Mehl E., Krasel C., Lottspeich F., Jahn R. GABA and glycine in synaptic vesicles: storage and transport characteristics. Neuron 1991, 7:287-293.
16. Burke R., Lundberg A., Weight F. Spinal border cell origin of the ventral spinocerebellar tract. Exp Brain Res 1971, 12:283-294.
17. Burke R.E., Fedina L., Lundberg A. Spatial synaptic distribution of recurrent and group Ia inhibitory systems in cat spinal motoneurones. J Physiol 1971, 214:305-326.
18. Chaudhry F.A., Reimer R.J., Bellocchio E.E., Danbolt N.C., Osen K.K., Edwards R.H., Storm-Mathisen J. The vesicular GABA transporter, VGAT, localizes to synaptic vesicles in sets of glycinergic as well as GABAergic neurons. J Neurosci 1998, 18:9733-9750.
19. Curtis D.R., Eccles J.C. The time courses of excitatory and inhibitory synaptic actions. J Physiol 1959, 145:529-546.
20. Destombes J., Horcholle-Bossavit G., Thiesson D. Distribution of glycinergic terminals on lumbar motoneurons of the adult cat: an ultrastructural study. Brain Res 1992, 599:353-360.
21. Du Beau A, Shakya Shrestha S, Bannatyne BA, Jalicy S, Linnen S, Maxwell DJ (2012) Neurotransmitter phenotypes of descending systems in the rat lumbar spinal cord. Neuroscience.
22. Eccles J.C., Hubbard J.I., Oscarsson O. Intracellular recording from cells of the ventral spinocerebellar tract. J Physiol 1961, 158:486-516.
23. Edgley S.A., Jankowska E. Field potentials generated by group II muscle afferents in the middle lumbar segments of the cat spinal cord. J Physiol 1987, 385:393-413.
24. Edgley S.A., Jankowska E. Information processed by dorsal horn spinocerebellar tract neurones in the cat. J Physiol 1988, 397:81-97.
25. Fetz E.E., Perlmutter S.I., Prut Y., Seki K., Votaw S. Roles of primate spinal interneurons in preparation and execution of voluntary hand movement. Brain Res Rev 2002, 40:53-65.
26. Fyffe R.E. Glycine-like immunoreactivity in synaptic boutons of identified inhibitory interneurons in the mammalian spinal cord. Brain Res 1991, 547:175-179.
27. Fyffe R.E. Spatial distribution of recurrent inhibitory synapses on spinal motoneurons in the cat. J Neurophysiol 1991, 65:1134-1149.
28. Hammar I., Chojnicka B., Jankowska E. Modulation of responses of feline ventral spinocerebellar tract neurons by monoamines. J Comp Neurol 2002, 443:298-309.
29. Hammar I., Krutki P., Drzymala-Celichowska H., Nilsson E., Jankowska E. A trans-spinal loop between neurones in the reticular formation and in the cerebellum. J Physiol 2011, 589:653-665.
30. Holstege J.C., Bongers C.M. A glycinergic projection from the ventromedial lower brainstem to spinal motoneurons. An ultrastructural double labeling study in rat. Brain Res 1991, 566:308-315.
31. Hongo T., Jankowska E., Ohno T., Sasaki S., Yamashita M., Yoshida K. The same interneurones mediate inhibition of dorsal spinocerebellar tract cells and lumbar motoneurones in the cat. J Physiol 1983, 342:161-180.
32. Hultborn H., Jankowska E., Lindstrom S. Recurrent inhibition from motor axon collaterals of transmission in the Ia inhibitory pathway to motoneurones. J Physiol 1971, 215:591-612.
33. Jankowska E., Krutki P., Hammar I. Collateral actions of premotor interneurons on ventral spinocerebellar tract neurons in the cat. J Neurophysiol 2010, 104:1872-1883.
34. Jankowska E., Nilsson E., Hammar I. Do spinocerebellar neurones forward information on spinal actions of neurones in the feline red nucleus?. J Physiol 2011, 589:5727-5739.
35. Jankowska E., Puczynska A. Interneuronal activity in reflex pathways from group II muscle afferents is monitored by dorsal spinocerebellar tract neurons in the cat. J Neurosci 2008, 28:3615-3622.
36. Kaufman D.L., Houser C.R., Tobin A.J. Two forms of the gamma-aminobutyric acid synthetic enzyme glutamate decarboxylase have distinct intraneuronal distributions and cofactor interactions. J Neuroch 1991, 56:720-723.
37. Klausberger T., Somogyi P. Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 2008, 321:53-57.
38. Korogod S.M., Kulagina I.B., Horcholle-Bossavit G., Gogan P., Tyc-Dumont S. Activity-dependent reconfiguration of the effective dendritic field of motoneurons. J Comp Neurol 2000, 422:18-34.
39. Krutki P., Jelen S., Jankowska E. Do premotor interneurons act in parallel on spinal motoneurons and on dorsal horn spinocerebellar and spinocervical tract neurons in the cat?. J Neurophysiol 2011, 105:1581-1593.
40. Lindstrom S., Schomburg E.D. Recurrent inhibition from motor axon collaterals of ventral spinocerebellar tract neurones. Acta Physiol Scand 1973, 88:505-515.
41. Lindstrom S., Schomburg E.D. Group I inhibition in Ib excited ventral spinocerebellar tract neurones. Acta Physiol Scand 1974, 90:166-185.
42. Liu T.T., Bannatyne B.A., Maxwell D.J. Organization and neurochemical properties of intersegmental interneurons in the lumbar enlargement of the adult rat. Neuroscience 2010, 171:461-484.
43. Lundberg A. Function of the ventral spinocerebellar tract. A new hypothesis. Exp Brain Res 1971, 12:317-330.
44. Lundberg A., Weight F. Functional organization of connexions to the ventral spinocerebellar tract. Exp Brain Res 1971, 12:295-316.
45. Mackie M., Hughes D.I., Maxwell D.J., Tillakaratne N.J., Todd A.J. Distribution and colocalisation of glutamate decarboxylase isoforms in the rat spinal cord. Neuroscience 2003, 119:461-472.
46. McIntire S.L., Reimer R.J., Schuske K., Edwards R.H., Jorgensen E.M. Identification and characterization of the vesicular GABA transporter. Nature 1997, 389:870-876.
47. Mitchell K., Spike R.C., Todd A.J. An immunocytochemical study of glycine receptor and GABA in laminae I-III of rat spinal dorsal horn. J Neurosci 1993, 13:2371-2381.
48. Ornung G., Ottersen O.P., Cullheim S., Ulfhake B. Distribution of glutamate-, glycine- and GABA-immunoreactive nerve terminals on dendrites in the cat spinal motor nucleus. Exp Brain Res 1998, 118:517-532.
49. Ornung G., Shupliakov O., Lindå H., Ottersen O.P., Storm-Mathisen J., Ulfhake B., Cullheim S. Qualitative and quantitative analysis of glycine- and GABA-immunoreactive nerve terminals on motoneuron cell bodies in the cat spinal cord: a postembedding electron microscopic study. J Comp Neurol 1996, 365:413-426.
50. Ornung G., Shupliakov O., Ottersen O.P., Storm-Mathisen J., Cullheim S. Immunohistochemical evidence for coexistence of glycine and GABA in nerve terminals on cat spinal motoneurones: an ultrastructural study. Neuroreport 1994, 5:889-892.
51. Oscarsson O. Functional organization of the spino- and cuneocerebellar tracts. Physiol Rev 1965, 45:495-522.
52. Rall W., Burke R.E., Smith T.G., Nelson P.G., Frank K. Dendritic location of synapses and possible mechanisms for the monosynaptic EPSP in motoneurons. J Neurophysiol 1967, 30:1169-1193.
53. Rexed B. A cytoarchitectonic atlas of the spinal cord in the cat. J Comp Neurol 1954, 100:297-379.
54. Schneider S.P., Fyffe R.E. Involvement of GABA and glycine in recurrent inhibition of spinal motoneurons. J Neurophysiol 1992, 68:397-406.
55. Shakya Shrestha S., Bannatyne B.A., Jankowska E., Hammar I., Nilsson E., Maxwell D.J. Excitatory inputs to four types of spinocerebellar tract neurons in the cat and the rat thoraco-lumbar spinal cord. J Physiol 2012, 590:1737-1755.
56. Soghomonian J.J., Martin D.L. Two isoforms of glutamate decarboxylase: why?. Trends Pharmacol Sci 1998, 19:500-505.
57. Takei T., Seki K. Spinal interneurons facilitate coactivation of hand muscles during a precision grip task in monkeys. J Neurosci 2010, 30:17041-17050.
58. Taal W., Holstege J.C. GABA and glycine frequently colocalize in terminals on cat spinal motoneurons. Neuroreport 1994, 5:2225-2228.
59. Todd A.J., Hughes D.I., Polgar E., Nagy G.G., Mackie M., Ottersen O.P., Maxwell D.J. The expression of vesicular glutamate transporters VGLUT1 and VGLUT2 in neurochemically defined axonal populations in the rat spinal cord with emphasis on the dorsal horn. Eur J Neurosci 2003, 17:13-27.
60. Todd A.J., Spike R.C., Chong D., Neilson M. The relationship between glycine and gephyrin in synapses of the rat spinal cord. Eur J Neurosci 1995, 7:1-11.
61. Todd A.J., Sullivan A.C. Light microscope study of the coexistence of GABA-like and glycine-like immunoreactivities in the spinal cord of the rat. J Comp Neurol 1990, 296:496-505.
62. Triller A., Cluzeaud F., Korn H. Gamma-aminobutyric acid-containing terminals can be apposed to glycine receptors at central synapses. J Cell Biol 1987, 104:947-956.
63. Varoqui H., Schafer M.K., Zhu H., Weihe E., Erickson J.D. Identification of the differentiation-associated Na+/PI transporter as a novel vesicular glutamate transporter expressed in a distinct set of glutamatergic synapses. J Neurosci 2002, 22:142-155.
64. Walmsley B., Wieniawa-Narkiewicz E., Nicol M.J. The ultrastructural basis for synaptic transmission between primary muscle afferents and neurons in Clarke's column of the cat. J Neurosci 1985, 5:2095-2106.
65. Wojcik S.M., Katsurabayashi S., Guillemin I., Friauf E., Rosenmund C., Brose N., Rhee J.S. A shared vesicular carrier allows synaptic corelease of GABA and glycine. Neuron 2006, 50:575-587.