Inhibitory synaptogenesis in the rat anteroventral cochlear nucleus

Neuroscience

Volumn 154, Issue 1, 2008, Pages 315-328

  Lujan R ^a   de Cabo, C ^a   Juiz, J M ^a  

^a University of Castilla La Mancha   (Spain)

Author keywords

auditory; cochlear nucleus; development; GABA; glycine; synaptogenesis

Indexed keywords

4 AMINOBUTYRIC ACID; GLYCINE; GLYCINE RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COCHLEAR NUCLEUS; CONTROLLED STUDY; GABAERGIC SYSTEM; GEOMETRY; IMMUNOCYTOCHEMISTRY; INHIBITORY POSTSYNAPTIC POTENTIAL; MALE; NERVE ENDING; NEUROTRANSMISSION; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RAT; REGULATORY MECHANISM; SYNAPTOGENESIS;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; COCHLEAR NUCLEUS; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLYCINE; MALE; MICROSCOPY, IMMUNOELECTRON; NEURAL INHIBITION; NEURONS; RATS; RATS, WISTAR; SYNAPSES;

EID: 44749085517     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2008.03.027     Document Type: Article

References (62)

1. Akerman C.J., and Cline H.T. Refining the roles of GABAergic signaling during neural circuit formation. Trends Neurosci 30 (2007) 382-389
2. Altschuler R.A., Juiz J.M., Shore S.E., Bledsoe S.C., Helfert R.H., and Wenthold R.J. Inhibitory amino acid synapse and pathways in the ventral cochlear nucleus. In: Merchan M.A., Juiz J.M., Godfrey D.A., and Mugnaini E. (Eds). The mammalian cochlear nuclei: organization and function (1993), Plenum, New York 211-224
3. Angulo A., Merchan J.A., and Merchan M.A. Morphology of the rat cochlear primary afferents during prenatal development: a Cajal's reduced silver and rapid Golgi study. J Anat 168 (1987) 241-255
4. Awatramani G.B., Turecek R., and Trussell L.O. Staggered development of GABAergic and glycinergic transmission in the MNTB. J Neurophysiol 93 (2005) 819-828
5. Ben-Ari Y., Gaiarsa J.L., Tyzio R., and Khazipov R. GABA: A pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol Rev 87 (2007) 1215-1284
6. Benson C.G., and Potashner S.J. Retrograde transport of [3H]glycine from the cochlear nucleus to the superior olive in the guinea pig. J Comp Neurol 296 (1990) 415-426
7. Blaesse P., Guillemin I., Schindler J., Schweizer M., Delpire E., Khiroug L., Friauf E., and Nothwang H.G. Oligomerization of KCC2 correlates with development of inhibitory neurotransmission. J Neurosci 26 (2006) 10407-10419
8. Brenowitz S., and Trussell L.O. Maturation of synaptic transmission at end-bulb synapses of the cochlear nucleus. J Neurosci 21 (2001) 9487-9498
9. Brunso-Bechtold J.K., Henkel C.K., and Linville C. Ultrastructural development of the medial superior olive (MSO) in the ferret. J Comp Neurol 324 (1992) 539-556
10. Campos M.L., de Cabo C., Wisden W., Juiz J.M., and Merlo D. Expression of GABA(A) receptor subunits in rat brainstem auditory pathways: cochlear nuclei, superior olivary complex and nucleus of the lateral lemniscus. Neuroscience 102 (2001) 625-638
11. Cant N.B., and Morest D.K. The bushy cells in the anteroventral cochlear nucleus of the cat. A study with the electron microscope. Neuroscience 4 (1979) 1925-1945
12. Cant N.B. Structural development of the mammalian auditory pathways. In: Rubel E.W., Popper A.N., and Fay R.N. (Eds). Development of the auditory system (1998), Springer-Verlag, New York 315-413
13. Caspary D.M., Backoff P.M., Finlayson P.G., and Palombi P.S. Inhibitory inputs modulate discharge rate within frequency receptive fields of anteroventral cochlear nucleus neurons. J Neurophysiol 72 (1994) 2124-2133
14. Code R.A., and Rubel E.W. Glycine-immunoreactivity in the auditory brain stem of the chick. Hear Res 40 (1989) 167-172
15. Code R.A., Burd G.D., and Rubel E.W. Development of GABA immunoreactivity in brainstem auditory nuclei of the chick: ontogeny of gradients in terminal staining. J Comp Neurol 284 (1989) 504-518
16. Code R.A., and Churchill L. GABAA receptors in auditory brainstem nuclei of the chick during development and after cochlea removal. Hear Res 54 (1991) 281-295
17. Friauf E. Developmental changes and cellular plasticity in the superior olivary complex. In: Parks T.N., Rubel E.W., Fay R.R., and Popper A.N. (Eds). Plasticity of the auditory system (2004), Springer, New York 49-95
18. Friauf E., Hammerschmidt B., and Kirsch J. Development of adult-type inhibitory glycine receptors in the central auditory system of rats. J Comp Neurol 385 (1997) 117-134
19. Gao X.B., and van den Pol A.N. GABA release from mouse axonal growth cones. J Physiol 523 Pt 3 (2000) 629-637
20. Gleich O., and Vater M. Postnatal development of GABA- and glycine-like immunoreactivity in the cochlear nucleus of the Mongolian gerbil (Meriones unguiculatus). Cell Tissue Res 293 (1998) 207-225
21. Green J.S., and Sanes D.H. Early appearance of inhibitory input to the MNTB supports binaural processing during development. J Neurophysiol 94 (2005) 3826-3835
22. Helfert R.H., Juiz J.M., Bledsoe S.C., Bonneau J.M., Wenthold R.J., and Altschuler R.A. Patterns of glutamate, glycine, and GABA immunolabeling in four synaptic terminal classes in the lateral superior olive of the guinea pig. J Comp Neurol 323 (1992) 305-325
23. Juiz J.M., Rubio M.E., Helfert R.H., and Altschuler R.A. Localizing putative excitatory endings in the cochlear nucleus by quantitative immunocytochemistry. In: Merchan M.A., Juiz J.M., Godfrey D.A., and Mugnaini E. (Eds). The mammalian cochlear nuclei: organization and function (1993), Plenum, New York 167-177
24. Juiz J.M., Helfert R.H., Bonneau J.M., Wenthold R.J., and Altschuler R.A. Three classes of inhibitory amino acid terminals in the cochlear nucleus of the guinea pig. J Comp Neurol 373 (1996) 11-26
25. Kandler K., and Friauf E. Pre- and postnatal development of efferent connections of the cochlear nucleus in the rat. J Comp Neurol 328 (1993) 161-184
26. Kandler K., and Friauf E. Development of glycinergic and glutamatergic synaptic transmission in the auditory brainstem of perinatal rats. J Neurosci 15 (1995) 6890-6904
27. Kandler K. Activity-dependent organization of inhibitory circuits: lessons from the auditory system. Curr Opin Neurobiol 14 (2004) 96-104
28. Kandler K., and Gillespie D.C. Developmental refinement of inhibitory sound-localization circuits. Trends Neurosci 28 (2005) 290-296
29. Kolston J., Osen K.K., Hackney C.M., Ottersen O.P., and Storm-Mathissen J. An atlas of glycine- and GABA-like immunoreactivity and colocalization in the cochlear nuclear complex of the guinea pig. Anat Embryol (Berl) 186 (1992) 443-465
30. Kopp-Scheinpflug C., Dehmel S., Dorrscheidt G.J., and Rubsamen R. Interaction of excitation and inhibition in anteroventral cochlear nucleus neurons that receive large endbulb synaptic endings. J Neurosci 22 (2002) 11004-11018
31. Kotak V.C., and Sanes D.H. Gain adjustment of inhibitory synapses in the auditory system. Biol Cybern 89 (2003) 363-370
32. Kullmann P.H., Ene F.A., and Kandler K. Glycinergic and GABAergic calcium responses in the developing lateral superior olive. Eur J Neurosci 15 (2002) 1093-1104
33. 2+ responses in neonatal lateral superior olive neurons elicited by glycinergic/GABAergic synapses and action potentials. Neuroscience 154 (2008) 338-345
34. Liu S., Wang J., Zhu D., Fu Y., Lukowiak K., and Lu Y.M. Generation of functional inhibitory neurons in the adult rat hippocampus. J Neurosci 23 (2003) 732-736
35. Lohrke S., Srinivasan G., Oberhofer M., Doncheva E., and Friauf E. Shift from depolarizing to hyperpolarizing glycine action occurs at different perinatal ages in superior olivary complex nuclei. Eur J Neurosci 22 (2005) 2708-2722
36. Mattox D.E., Neises G.R., and Gulley R.L. A freeze-fracture study of the maturation of synapses in the anteroventral cochlear nucleus of the developing rat. Anat Rec 204 (1982) 281-287
37. McAllister A.K. Dynamic aspects of CNS synapse formation. Annu Rev Neurosci 30 (2007) 425-450
38. Milenkovic I., Witte M., Turecek R., Heinrich M., Reinert T., and Rubsamen R. Development of chloride-mediated inhibition in neurons of the anteroventral cochlear nucleus of gerbil (Meriones unguiculatus). J Neurophysiol 98 (2007) 1634-1644
39. Morest D.K. The cellular basis for signal processing in the mammalian cochlear nuclei. In: Merchan M.A., Juiz J.M., Godfrey D.A., and Mugnaini E. (Eds). The mammalian cochlear nuclei: organization and function (1993), Plenum, New York 1-18
40. Neises G.R., Mattox D.E., and Gulley R.L. The maturation of the end bulb of Held in the rat anteroventral cochlear nucleus. Anat Rec 204 (1982) 271-279
41. Oertel D. Synaptic responses and electrical properties of cells in brain slices of the mouse anteroventral cochlear nucleus. J Neurosci 3 (1983) 2043-2053
42. Osen K.K. Cytoarchitecture of the cochlear nuclei in the cat. J Comp Neurol 136 (1969) 453-484
43. Ottersen O.P. Postembedding light- and electron microscopic immunocytochemistry of amino acids: description of a new model system allowing identical conditions for specificity testing and tissue processing. Exp Brain Res 69 (1987) 167-174
44. Ottersen O.P., Storm-Mathisen J., and Somogyi P. Colocalization of glycine-like and GABA-like immunoreactivities in Golgi cell terminals in the rat cerebellum: a postembedding light and electron microscopic study. Brain Res 450 (1988) 342-353
45. Peters A., Palay S.L., and Webster H.F. The fine structure of the nervous system. Neurons and their supporting cells. 3rd ed. (1991), Oxford University Press, New York
46. Piechotta K., Weth F., Harvey R.J., and Friauf E. Localization of rat glycine receptor alpha1 and alpha2 subunit transcripts in the developing auditory brainstem. J Comp Neurol 438 (2001) 336-352
47. Potashner S.J., Benson C.G., Ostapoff E.-M., Lindberg N., and Morest D.K. Glycine and GABA: transmitter candidates of projections descending to the cochlear nucleus. In: Merchan M.A., Juiz J.M., Godfrey D.A., and Mugnaini E. (Eds). The mammalian cochlear nuclei: organization and function (1993), Plenum Press, New York 195-210
48. Riggs G.H., Walsh E.J., and Schweitzer L. The development of glycine-like immunoreactivity in the dorsal cochlear nucleus. Hear Res 89 (1995) 172-180
49. Rubel E.W., Parks T.N., and Zirpel L. Assembling, connecting and maintaining the cochlear nucleus. In: Parks T.N., Rubel E.W., Fay R.R., and Popper A.N. (Eds). Plasticity of the auditory system (2004), Springer, New York 8-47
50. Sanes D.H., and Walsh E.J. The development of central auditory processing. In: Rubel E.W., Popper A.N., and Fay R.N. (Eds). Development of the auditory system (1998), Springer-Verlag, New York 271-314
51. Sato K., Kuriyama H., and Altschuler R.A. Expression of glycine receptor subunits in the cochlear nucleus and superior olivary complex using non-radioactive in-situ hybridization. Hear Res 91 (1995) 7-18
52. Sato K., Kuriyama H., and Altschuler R.A. Expression of glycine receptor subunit mRNAs in the rat cochlear nucleus. Hear Res 144 (2000) 47-52
53. Schweitzer L., Cecil T., and Walsh E.J. Development of GAD-immunoreactivity in the dorsal cochlear nucleus of the hamster and cat: light and electron microscopic observations. Hear Res 65 (1993) 240-252
54. Somogyi P., and Hodgson A.J. Antisera to gamma-amino butyric acid. III. Demonstration of GABA in Golgi-impregnated neurons and in conventional electron microscopic sections of cat striate cortex. J Histochem Cytochem 33 (1985) 249-257
55. Staatz-Benson C., and Potashner S.J. Uptake and release of glycine in the guinea pig cochlear nucleus after axotomy of afferent or centrifugal fibers. J Neurochem 51 (1988) 370-379
56. Tolbert L.P., and Morest D.K. The neuronal architecture of the anteroventral cochlear nucleus of the cat in the region of the cochlear nerve root: Electron microscopy. Neuroscience 7 (1982) 3053-3067
57. Uchizono K. Characteristic of excitatory and inhibitory synapses in the central nervous system of the cat. Nature 207 (1965) 642-643
58. - cotransporter KCC2 in the cochlear nucleus. Hear Res 206 (2005) 107-115
59. Waites C.L., Craig A.M., and Garner C.C. Mechanisms of vertebrate synaptogenesis. Annu Rev Neurosci 28 (2005) 251-274
60. Wenthold R.J., Huie D., Altschuler R.A., and Reeks K.A. Glycine immunoreactivity localized in the cochlear nucleus and superior olivary complex. Neuroscience 22 (1987) 897-912
61. Wu S.H., and Oertel D. Intracellular injection with horseradish peroxidase of physiologically characterized stellate and bushy cells in slices of mouse anteroventral cochlear nucleus. J Neurosci 4 (1984) 1577-1588
62. Wu S.H., and Oertel D. Inhibitory circuitry in the ventral cochlear nucleus is probably mediated by glycine. J Neurosci 6 (1986) 2691-2706