Distribution of glial cells in the auditory brainstem: Normal development and effects of unilateral lesion

Neuroscience

Volumn 278, Issue 1, 2014, Pages 237-252

  Dinh, M L ^a   Koppel, S J ^a   Korn, M J ^a   Cramer, K S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Astrocyte; Auditory system; Brainstem; Deafferentation; Microglia; Oligodendrocyte

Indexed keywords

ALDEHYDE DEHYDROGENASE 1 FAMILY MEMBER L1; ALDEHYDE DEHYDROGENASE ISOENZYME 1; CALCIUM BINDING PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; PROTEIN S100B; UNCLASSIFIED DRUG;

AFFINITY CHROMATOGRAPHY; ANIMAL TISSUE; ARTICLE; ASTROCYTE; AUDITORY SYSTEM; BRAIN STEM; CARBOXY TERMINAL SEQUENCE; CELL FUNCTION; CELL MATURATION; CELL MIGRATION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GLIA CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; ION EXCHANGE CHROMATOGRAPHY; MOUSE; NONHUMAN; OLIGODENDROGLIA; OXYGENATION; PERIKARYON; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SYNAPSE; VENTRAL COCHLEAR NUCLEUS; ANIMAL; CELL COUNT; COCHLEAR NUCLEUS; CYTOLOGY; GLIA; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NERVE TRACT; PHYSIOLOGY; TRAPEZOID BODY;

ANIMALS; CELL COUNT; COCHLEAR NUCLEUS; MICE; NEURAL PATHWAYS; NEUROGLIA; TRAPEZOID BODY;

EID: 84908160836     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2014.08.016     Document Type: Article

References (62)

1. Allen N.J., Bennett M.L., Foo L.C., Wang G.X., Chakraborty C., Smith S.J., Barres B.A. Astrocyte glypicans 4 and 6 promote formation of excitatory synapses via GluA1 AMPA receptors. Nature 2012, 486:410-414.
2. Borst J.G., Van Hoeve S.J. The calyx of held synapse: from model synapse to auditory relay. Annu Rev Physiol 2012, 74:199-224.
3. Cahoy J.D., Emery B., Kaushal A., Foo L.C., Zamanian J.L., Christopherson K.S., Xing Y., Lubischer J.L., Krieg P.A., Krupenko S.A., Thompson W.J., Barres B.A. A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J Neurosci 2008, 28:264-278.
4. Campos-Torres A., Touret M., Vidal P.P., Barnum S., de Waele C. The differential response of astrocytes within the vestibular and cochlear nuclei following unilateral labyrinthectomy or vestibular afferent activity blockade by transtympanic tetrodotoxin injection in the rat. Neuroscience 2005, 130:853-865.
5. Campos Torres A., Vidal P.P., de Waele C. Evidence for a microglial reaction within the vestibular and cochlear nuclei following inner ear lesion in the rat. Neuroscience 1999, 92:1475-1490.
6. Christopherson K.S., Ullian E.M., Stokes C.C., Mullowney C.E., Hell J.W., Agah A., Lawler J., Mosher D.F., Bornstein P., Barres B.A. Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis. Cell 2005, 120:421-433.
7. Chung W.S., Barres B.A. The role of glial cells in synapse elimination. Curr Opin Neurobiol 2012, 22:438-445.
8. Dalmau I., Finsen B., Tonder N., Zimmer J., Gonzalez B., Castellano B. Development of microglia in the prenatal rat hippocampus. J Comp Neurol 1997, 377:70-84.
9. Dalmau I., Finsen B., Zimmer J., Gonzalez B., Castellano B. Development of microglia in the postnatal rat hippocampus. Hippocampus 1998, 8:458-474.
10. de Waele C., Campos Torres A., Josset P., Vidal P.P. Evidence for reactive astrocytes in rat vestibular and cochlear nuclei following unilateral inner ear lesion. Eur J Neurosci 1996, 8:2006-2018.
11. Delassalle A., Zalc B., Lachapelle F., Raoul M., Collier P., Jacque C. Regional distribution of myelin basic protein in the central nervous system of quaking, jimpy, and normal mice during development and aging. J Neurosci Res 1981, 6:303-313.
12. Elezgarai I., Bilbao A., Mateos J.M., Azkue J.J., Benitez R., Osorio A., Diez J., Puente N., Donate-Oliver F., Grandes P. Group II metabotropic glutamate receptors are differentially expressed in the medial nucleus of the trapezoid body in the developing and adult rat. Neuroscience 2001, 104:487-498.
13. Foran D.R., Peterson A.C. Myelin acquisition in the central nervous system of the mouse revealed by an MBP-Lac Z transgene. J Neurosci 1992, 12:4890-4897.
14. Ford M.C., Grothe B., Klug A. Fenestration of the calyx of Held occurs sequentially along the tonotopic axis, is influenced by afferent activity, and facilitates glutamate clearance. J Comp Neurol 2009, 514:92-106.
15. Fuentes-Santamaria V., Alvarado J.C., Juiz J.M. Long-term interaction between microglial cells and cochlear nucleus neurons after bilateral cochlear ablation. J Comp Neurol 2012, 520:2974-2990.
16. Ghandour M.S., Vincendon G., Gombos G. Astrocyte and oligodendrocyte distribution in adult rat cerebellum: an immunohistological study. J Neurocytol 1980, 9:637-646.
17. Hajos F., Kalman M. Distribution of glial fibrillary acidic protein (GFAP)-immunoreactive astrocytes in the rat brain. II. Mesencephalon, rhombencephalon and spinal cord. Exp Brain Res 1989, 78:164-173.
18. Hashisaki G.T., Rubel E.W. Effects of unilateral cochlea removal on anteroventral cochlear nucleus neurons in developing gerbils. J Comp Neurol 1989, 283:5-73.
19. Hoffpauir B.K., Grimes J.L., Mathers P.H., Spirou G.A. Synaptogenesis of the calyx of Held: rapid onset of function and one-to-one morphological innervation. J Neurosci 2006, 26:5511-5523.
20. Holcomb P.S., Hoffpauir B.K., Hoyson M.C., Jackson D.R., Deerinck T.J., Marrs G.S., DehoffM., Wu J., Ellisman M.H., Spirou G.A. Synaptic inputs compete during rapid formation of the calyx of Held: a new model system for neural development. J Neurosci 2013, 33:12954-12969.
21. Hsieh C.Y., Cramer K.S. Deafferentation induces novel axonal projections in the auditory brainstem after hearing onset. J Comp Neurol 2006, 497:589-599.
22. Hsieh C.Y., Hong C.T., Cramer K.S. Deletion of EphA4 enhances deafferentation-induced ipsilateral sprouting in auditory brainstem projections. J Comp Neurol 2007, 504:508-518.
23. Hughes E.G., Elmariah S.B., Balice-Gordon R.J. Astrocyte secreted proteins selectively increase hippocampal GABAergic axon length, branching, and synaptogenesis. Mol Cell Neurosci 2010, 43:136-145.
24. Jackson H., Parks T.N. Functional synapse elimination in the developing avian cochlear nucleus with simultaneous reduction in cochlear nerve axon branching. J Neurosci 1982, 2:1736-1743.
25. Kandler K., Friauf E. Pre- and postnatal development of efferent connections of the cochlear nucleus in the rat. J Comp Neurol 1993, 328:161-184.
26. Karimi-Abdolrezaee S., Billakanti R. Reactive astrogliosis after spinal cord injury-beneficial and detrimental effects. Mol Neurobiol 2012, 46:251-264.
27. Kil J., Kageyama G.H., Semple M.N., Kitzes L.M. Development of ventral cochlear nucleus projections to the superior olivary complex in gerbil. J Comp Neurol 1995, 353:317-340.
28. Kitzes L.M., Kageyama G.H., Semple M.N., Kil J. Development of ectopic projections from the ventral cochlear nucleus to the superior olivary complex induced by neonatal ablation of the contralateral cochlea. J Comp Neurol 1995, 353:341-363.
29. Korn M.J., Cramer K.S. Distribution of glial-associated proteins in the developing chick auditory brainstem. Dev Neurobiol 2008, 68:1093-1106.
30. Korn M.J., Koppel S.J., Cramer K.S. Astrocyte-secreted factors modulate a gradient of primary dendritic arbors in nucleus laminaris of the avian auditory brainstem. PLoS One 2011, 6:e27383.
31. Korn M.J., Koppel S.J., Li L.H., Mehta D., Mehta S.B., Seidl A.H., Cramer K.S. Astrocyte-secreted factors modulate the developmental distribution of inhibitory synapses in nucleus laminaris of the avian auditory brainstem. J Comp Neurol 2012, 520:1262-1277.
32. Kucukdereli H., Allen N.J., Lee A.T., Feng A., Ozlu M.I., Conatser L.M., Chakraborty C., Workman G., Weaver M., Sage E.H., Barres B.A., Eroglu C. Control of excitatory CNS synaptogenesis by astrocyte-secreted proteins Hevin and SPARC. Proc Natl Acad Sci U S A 2011, 108:E440-E449.
33. Kuwabara N., DiCaprio R.A., Zook J.M. Afferents to the medial nucleus of the trapezoid body and their collateral projections. J Comp Neurol 1991, 314:684-706.
34. Kuwabara N., Zook J.M. Classification of the principal cells of the medial nucleus of the trapezoid body. J Comp Neurol 1991, 314:707-720.
35. Lawson L.J., Perry V.H., Dri P., Gordon S. Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain. Neuroscience 1990, 39:151-170.
36. Leao R.M., Kushmerick C., Pinaud R., Renden R., Li G.L., Taschenberger H., Spirou G., Levinson S.R., von GersdorffH. Presynaptic Na+ channels: locus, development, and recovery from inactivation at a high-fidelity synapse. J Neurosci 2005, 25:3724-3738.
37. Lurie D.I., Rubel E.W. Astrocyte proliferation in the chick auditory brainstem following cochlea removal. J Comp Neurol 1994, 346:276-288.
38. Mauch D.H., Nagler K., Schumacher S., Goritz C., Muller E.C., Otto A., Pfrieger F.W. CNS synaptogenesis promoted by glia-derived cholesterol. Science (New York, NY) 2001, 294:1354-1357.
39. Mikaelian D., Alford B.R., Ruben R.J. Cochlear potentials and 8 nerve action potentials in normal and genetically deaf mice. Ann Otol Rhinol Laryngol 1965, 74:146-157.
40. Miller R.H., RaffM.C. Fibrous and protoplasmic astrocytes are biochemically and developmentally distinct. J Neurosci 1984, 4:585-592.
41. Moore D.R., Kowalchuk N.E. Auditory brainstem of the ferret: effects of unilateral cochlear lesions on cochlear nucleus volume and projections to the inferior colliculus. J Comp Neurol 1988, 272:503-515.
42. Mostafapour S.P., Cochran S.L., Del Puerto N.M., Rubel E.W. Patterns of cell death in mouse anteroventral cochlear nucleus neurons after unilateral cochlea removal. J Comp Neurol 2000, 426:561-571.
43. Muller C.M. Astrocytes in cat visual cortex studied by GFAP and S-100 immunocytochemistry during postnatal development. J Comp Neurol 1992, 317:309-323.
44. Nakamura P.A., Cramer K.S. Formation and maturation of the calyx of Held. Hear Res 2011, 276:70-78.
45. Nakamura P.A., Cramer K.S. EphB2 signaling regulates lesion-induced axon sprouting but not critical period length in the postnatal auditory brainstem. Neural Dev 2013, 8:2.
46. Nakamura P.A., Hsieh C.Y., Cramer K.S. EphB signaling regulates target innervation in the developing and deafferented auditory brainstem. Dev Neurobiol 2012, 72:1243-1255.
47. Renden R., Taschenberger H., Puente N., Rusakov D.A., Duvoisin R., Wang L.Y., Lehre K.P., von GersdorffH. Glutamate transporter studies reveal the pruning of metabotropic glutamate receptors and absence of AMPA receptor desensitization at mature calyx of held synapses. J Neurosci 2005, 25:8482-8497.
48. Reyes-Haro D., Muller J., Boresch M., Pivneva T., Benedetti B., Scheller A., Nolte C., Kettenmann H. Neuron-astrocyte interactions in the medial nucleus of the trapezoid body. J Gen Physiol 2010, 135:583-594.
49. Richardson W.D., Kessaris N., Pringle N. Oligodendrocyte wars. Nat Rev Neurosci 2006, 7:11-18.
50. Rodriguez-Contreras A., van Hoeve J.S., Habets R.L., Locher H., Borst J.G. Dynamic development of the calyx of Held synapse. Proc Natl Acad Sci U S A 2008, 105:5603-5608.
51. Rubel E.W., MacDonald G.H. Rapid growth of astrocytic processes in N. magnocellularis following cochlea removal. J Comp Neurol 1992, 318:415-425.
52. Russell F.A., Moore D.R. Afferent reorganisation within the superior olivary complex of the gerbil: development and induction by neonatal, unilateral cochlear removal. J Comp Neurol 1995, 352:607-625.
53. Saliu A., Adise S., Xian S., Kudelska K., Rodriguez-Contreras A. Natural and lesion-induced decrease in cell proliferation in the medial nucleus of the trapezoid body during hearing development. J Comp Neurol 2014, 522:Spc1.
54. Saunders J.C., Coles R.B., Gates G.R. The development of auditory evoked responses in the cochlea and cochlear nuclei of the chick. Brain Res 1973, 63:59-74.
55. Schafer D.P., Lehrman E.K., Kautzman A.G., Koyama R., Mardinly A.R., Yamasaki R., RansohoffR.M., Greenberg M.E., Barres B.A., Stevens B. Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 2012, 74:691-705.
56. Sonntag M., Englitz B., Typlt M., Rubsamen R. The calyx of held develops adult-like dynamics and reliability by hearing onset in the mouse in vivo. J Neurosci 2011, 31:6699-6709.
57. Takebayashi H., Nabeshima Y., Yoshida S., Chisaka O., Ikenaka K. The basic helix-loop-helix factor olig2 is essential for the development of motoneuron and oligodendrocyte lineages. Curr Biol: CB 2002, 12:1157-1163.
58. Takebayashi H., Yoshida S., Sugimori M., Kosako H., Kominami R., Nakafuku M., Nabeshima Y. Dynamic expression of basic helix-loop-helix Olig family members: implication of Olig2 in neuron and oligodendrocyte differentiation and identification of a new member, Olig3. Mech Dev 2000, 99:143-148.
59. Taschenberger H., Leao R.M., Rowland K.C., Spirou G.A., von GersdorffH. Optimizing synaptic architecture and efficiency for high-frequency transmission. Neuron 2002, 36:1127-1143.
60. Trune D.R. Influence of neonatal cochlear removal on the development of mouse cochlear nucleus: I. Number, size, and density of its neurons. J Comp Neurol 1982, 209:409-424.
61. Wake H., Moorhouse A.J., Miyamoto A., Nabekura J. Microglia: actively surveying and shaping neuronal circuit structure and function. Trends Neurosci 2013, 36:209-217.
62. Young S.R., Rubel E.W. Embryogenesis of arborization pattern and topography of individual axons in N. laminaris of the chicken brain stem. J Comp Neurol 1986, 254:425-459.