Development of N-methyl-D-aspartate receptor subunits in avian auditory brainstem

Journal of Comparative Neurology

Volumn 502, Issue 3, 2007, Pages 400-413

  Tang, Ye Zhong ^a   Carr, Catherine E ^a  

^a Bldg 142   (United States)

Author keywords

Angularis; Cochlear nucleus; Laminaris; Magnocellularis; Tonotopic gradient

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2C; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2D; RECEPTOR SUBUNIT; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; AUDITORY NERVOUS SYSTEM; BRAIN DEVELOPMENT; BRAIN STEM; CHICK EMBRYO; EMBRYO; EMBRYO DEVELOPMENT; MAGNOCELLULAR NUCLEUS; NEUROCHEMISTRY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DETERMINATION; THALAMUS INTRALAMINAR NUCLEUS;

ANIMALS; CHICK EMBRYO; CHICKENS; EVOKED POTENTIALS, AUDITORY, BRAIN STEM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IN SITU HYBRIDIZATION; PROTEIN SUBUNITS; RECEPTORS, N-METHYL-D-ASPARTATE; RNA, MESSENGER;

EID: 34147139403     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21303     Document Type: Article

References (97)

1. Akazawa C, Shigemoto R, Bessho Y, Nakanishi S, Mizuno N. 1994. Differential expression of five N-methyl-D-aspartate receptor subunit mRNAs in the cerebellum of developing and adult rats. J Comp Neurol 347:150-160.
2. Alladi PA, Wadhwa S, Singh N. 2002. Effect of prenatal auditory enrichment on developmental expression of synaptophysin and syntaxin 1 in chick brainstem auditory nuclei. Neuroscience 114:577-590.
3. Basham ME, Sohrabji F, Singh TD, Nordeen EJ, Nordeen KW. 1999. Developmental regulation of NMDA receptor 2B subunit mRNA and ifenprodil binding in the zebra finch anterior forebrain. J Neurobiol 39:155-167.
4. Behe P, Stern P, Wyllie DJ, Nassar M, Schoepfer R, Colquhoun D. 1995. Determination of NMDA NR1 subunit copy number in recombinant NMDA receptors. Proc Biol Sci 262:205-213.
5. Bellingham MC, Lim R, Walmsley B. 1998. Developmental changes in EPSC quantal size and quantal content at a central glutamatergic synapse in rat. J Physiol 511:861-869.
6. Berardi N, Pizzorusso T, Maffei L. 2000. Critical periods during sensory development. Curr Opin Neurobiol 10:138-145.
7. Bilak MM, Bilak SR, Morest DK. 1996. Differential expression of N-methyl-D-aspartate receptor in the cochlear nucleus of the mouse. Neuroscience 75:1075-1097.
8. Blahos J 2nd, Wenthold RJ. 1996. Relationship between N-methyl-D-aspartate receptor NR1 splice variants and NR2 subunits. J Biol Chem 271:15669-15674.
9. Brenowitz S, Trussell LO. 2001. Maturation of synaptic transmission at end-bulb synapses of the cochlear nucleus. J Neurosci 21:9487-9498.
10. Caicedo A, Eybalin M. 1999. Glutamate receptor phenotypes in the auditory brainstem and mid-brain of the developing rat. Eur J Neurosci 11:51-74.
11. Carr CE, Konishi M. 1990. A circuit for detection of interaural time differences in the brain stem of the barn owl. J Neurosci 10:3227-3246.
12. Carr CE, Soares D. 2002. Evolutionary convergence and shared computational principles in the auditory system. Brain Behav Evol 59:294-311.
13. Chazot PL, Stephenson FA. 1997. Molecular dissection of native mammalian forebrain NMDA receptors containing the NR1 C2 exon: direct demonstration of NMDA receptors comprising NR1, NR2A, and NR2B subunits within the same complex. J Neurochem 69:2138-2144.
14. Chazot PL, Coleman SK, Cike M Stephenson FA. 1994. Molecular characterization of N-methyl-D-aspartate receptors expressed in mammalian cells yields evidence for the coexistence of three subunit types within a discrete receptor molecule. J Biol Chem 269:24403-24409.
15. Ciabarra AM, Sullivan JM, Gahn LG, Pecht G, Heinemann S, Sevarino KA. 1995. Cloning and characterization of x-1: a developmentally regulated member of a noval class of the ionotropic glutamate receptor family. J Neurosci 15:6498-6508.
16. Cull-Candy S, Brickley, S, Farrant M. 2001. NMDA receptor subunits: diversity, development and disease. Current Opinion in Neurobiology 11:327-335.
17. Ding L, Perkel DJ. 2004. Long-term potentiation in an avian basal ganglia nucleus essential for vocal learning. J Neurosci 24:488-494.
18. Dunah AW, Luo J, Wang YH, Yasuda RP, Wolfe BB. 1998. Subunit composition of N-methyl-D-aspartate receptors in the central nervous system that contain the NR2D subunit. Mol Pharmacol 53:429-437.
19. Esteban JA. 2003. AMPA receptor trafficking: a road map for synaptic plasticity. Mol Intervent 3:375-385.
20. Fu Z, Logan SM, Vicini S. 2005. Deletion of the NR2A subunit prevents developmental changes of NMDA-mEPSCs in cultured mouse cerebellar granule neurones. J Physiol 563:867-881.
21. Fukui I, Ohmori H. 2003. Developmental changes in membrane excitability and morphology of neurons in the nucleus angularis of the chicken. J Physiol 548:219-232.
22. Futai K, Okada M, Matsuyama K, Takahashi T. 2001. High-fidelity transmission acquired via a developmental decrease in NMDA receptor expression at an auditory synapse. J Neurosci 21:3342-3349.
23. Hawkins LM, Chazot PL, Stephenson FA. 1999. Biochemical evidence for the co-association of three N-methyl-D-aspartate (NMDA) R2 subunits in recombinant NMDA receptors. J Biol Chem 274:27211-27218.
24. Hoffpauir BK, Grimes JL, Mathers PH, Spirou GA. 2006. Synaptogenesis of the calyx of Held: rapid onset of function and one-to-one morphological innervation. J Neurosci 26:5511-5523.
25. Isaacson JS, Walmsley B. 1995. Receptors underlying excitatory synaptic transmission in slices of the rat anteroventral cochlear nucleus. J Neurophysiol 73:964-973.
26. Jackson H, Parks TN. 1982. Functional synapse elimination in the developing avian cochlear nucleus with simultaneous reduction in cochlear nerve axon branching. J Neurosci 2:1736-1743.
27. Jackson H, Rubel EW. 1978. Ontogeny of behavioral responsiveness to sound in the chick embryo as indicated by electrical recordings of motility. J Comp Physiol Psychol 92:682-696.
28. Jackson H, Hackett JT, Rubel EW. 1982. Organization and development of brain stem auditory nuclei in the chick: ontogeny of postsynaptic responses. J Comp Neurol 210:80-86.
29. Jhaveri S, Morest DK. 1982a. Sequential alterations of neuronal architecture in nucleus magnocellularis of the developing chicken: a Golgi study. Neuroscience 7:837-853.
30. Jhaveri S, Morest DK. 1982b. Neuronal architecture in nucleus magnocellularis of the chicken auditory system with observations on nucleus laminaris: a light and electron microscope study. Neuroscience 7:809-836.
31. Joelson D, Schwartz IR. 1998. Development of N-methyl-D-aspartate receptor subunit immunoreactivity in the neonatal gerbil cochlear nucleus. Microsc Res Techniq 41:246-262.
32. Joshi I, Wang LY. 2002. Developmental profiles of glutamate receptors and synaptic transmission at a single synapse in the mouse auditory brainstem. J Physiol 540:861-873.
33. Kempter R, Leibold C, Wagner H, van Hemmen JL. 2001. Formation of temporal-feature maps by axonal propagation of synaptic learning. Proc Natl Acad Sci U S A 98:4166-4171.
34. Kim MJ, Dunah AW, Wang YT, Sheng M. 2005. Differential roles of NR2A-and NR2B-containing NMDA receptors in Ras-ERK signaling and AMPA receptor trafficking. Neuron 46:745-760.
35. Koppl C, Carr CE. 2003. Computational diversity in the cochlear nucleus angularis of the barn owl. J Neurophysiol 89:2313-2329.
36. Kuba H, Koyano K, Ohmori H. 2002. Development of membrane conductance improves coincidence detection in the nucleus laminaris of the chicken. J Physiol 540:529-542.
37. Kubke MF, Carr CE. 1998. Development of AMPA-selective glutamate receptors in the auditory brainstem of the barn owl. Microsc Res Techniq 41:176-186.
38. Kubke MF, Carr CE. 2000. Development of the auditory brainstem of birds: comparison between barn owls and chickens. Hear Res 147:1-20.
39. Kutsuwada T, Kashiwabuchi N, Mori H, Sakimura K, Kushiya E, Araki K, Meguro H, Masaki H, Kumanishi T, Arakawa M, et al. 1992. Molecular diversity of the NMDA receptor channel. Nature 358:36-41.
40. Laube B, Kuhse J, Betz H. 1998. Evidence for a tetrameric structure of recombinant NMDA receptors. J Neurosci 18:2954-2961.
41. Leibold C, Kempter R, van Hemmen JL. 2001. Temporal map formation in the barn owl's brain. Phys Rev Lett 87:248101.
42. Lippe WR. 1995. Relationship between frequency of spontaneous bursting and tonotopic position in the developing avian auditory system. Brain Res 703:205-213.
43. Lisman J, Schulman H, Cline H. 2002. The molecular basis of CaMKII function in synaptic and behavioural memory. Nat Rev Neurosci 3:175-190.
44. Liu L, Wong TP, Pozza MF, Lingenhoehl K, Wang Y, Sheng M, Auberson YP, Wang YT. 2004. Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science 304:1021-1024.
45. Loftis JM, Janowsky A. 2003. The N-methyl-D-aspartate receptor subunit NR2B: localization, functional properties, regulation, and clinical implications. Pharmacol Ther 97:55-85.
46. Lu HC, Gonzalez E, Crair MC. 2001. Barrel cortex critical period plasticity is independent of changes in NMDA receptor subunit composition. Neuron 32:619-634.
47. Lu T, Trussell LO. 2002. The early development of glutamatergic synapses in nucleus magnocellularis. Program No. 146.1. 2002 Abstract viewer and itinerary planner. Washington, DC: Society for Neuroscience, 2002 [CD-ROM].
48. Luo J, Wang Y, Yasuda RP, Dunah AW, Wolfe BB. 1997. The majority of N-methyl-D-aspartate receptor complexes in adult rat cerebral cortex contain at least three different subunits (NR1/NR2A/NR2B). Mol Pharmacol 51:79-86.
49. MacLeod KM, Carr CE. 2005. Synaptic physiology in the cochlear nucleus angularis of the chick. J Neurophysiol 93:2520-2529.
50. Massey PV, Johnson BE, Moult PR, Auberson YP, Brown MW, Molnar E, Collingridge GL, Bashir ZI. 2004. Differential roles of NR2A and NR2B-containing NMDA receptors in cortical long-term potentiation and long-term depression. J Neurosci 24:7821-7828.
51. Munemoto Y, Kuriyama H, Doi T, Sato K, Matsumoto A, Sugatani J, Cho H, Komeda M, Altschuler RA, Kitajiri M, Mishina M, Yamashita T. 1998. Auditory pathway and auditory brainstem response in mice lacking NMDA receptor epsilon 1 and epsilon 4 subunits. Neurosci Lett 251:101-104.
52. Niedzielski AS, Wenthold RJ. 1995. Expression of AMPA, kainate, and NMDA receptor subunits in cochlear and vestibular ganglia. J Neurosci 15:2338-2353.
53. Nishi M, Hinds H, Lu HP, Kawata M, Hayashi Y. 2001. Motoneuron-specific expression of NR3B, a noval NMDA-type glutamate receptor subunit that works in a dominant-negative manner. J Neurosci 21:1-6.
54. Opella SJ, Marassi FM, Gesell JJ, Valente AP, Kim Y, Oblatt-Montal M, Montal M. 1999. Structures of the M2 channel-lining segments from nicotinic acetylcholine and NMDA receptors by NMR spectroscopy. Nat Struct Biol 6:374-379.
55. Overholt EM, Rubel EW, Hyson RL. 1992. A circuit for coding interaural time differences in the chick brainstem. J Neurosci 12:1698-1708.
56. Parks TN. 2000. The AMPA receptors of auditory neurons. Hear Res 147:77-91.
57. Parks TN, Jackson H. 1984. A developmental gradient of dendritic loss in the avian cochlear nucleus occurring independently of primary afferents. J Comp Neurol 227:459-466.
58. Parks TN, Rubel EW. 1975. Organization and development of brain stem auditory nuclei of the chicken: organization of projections from n. magnocellularis to n. laminaris. J Comp Neurol 164:435-448.
59. Parks TN, Gill SS, Jackson H. 1987. Experience-independent development of dendritic organization in the avian nucleus laminaris. J Comp Neurol 260:312-319.
60. Perez-Otano I, Ehlers MD. 2005. Homeostatic plasticity and NMDA receptor trafficking. Trends Neurosci 28:229-238.
61. Philpot BD, Sekhar AK, Shouval HZ, Bear MF. 2001. Visual experience and deprivation bidirectionally modify the composition and function of NMDA receptors in visual cortex. Neuron 29:157-169.
62. Premkumar LS, Auerbach A. 1997. Stoichiometry of recombinant N-methyl-D-aspartate receptor channels inferred from single-channel current patterns. J Gen Physiol 110:485-502.
63. Quinlan EM, Olstein DH, Bear MF. 1999a. Bidirectional, experience-dependent regulation of N-methyl-D-aspartate receptor subunit composition in the rat visual cortex during postnatal development. Proc Natl Acad Sci U S A 96:12876-12880.
64. Quinlan EM, Philpot BD, Huganir RL, Bear MF. 1999b. Rapid, experience-dependent expression of synaptic NMDA receptors in visual cortex in vivo. Nat Neurosci 2:352-357.
65. Rubel EW, Parks TN. 1975. Organization and development of brain stem auditory nuclei of the chicken: tonotopic organization of n. magnocellularis and n. laminaris. J Comp Neurol 164:411-433.
66. Rubel EW, Parks TN. 1988. Organization and development of the avian brain-stem auditory system. In: Edelman GM, Einar Gall W, Maxwell Cowan W, editors. Brain function. New York: John Wiley & Sons. p 3-92.
67. Rubel EW, Smith DJ, Miller LC. 1976. Organization and development of brain stem auditory nuclei of the chicken: ontogeny of n. magnocellularis and n. laminaris. J Comp Neurol 166:469-489.
68. Sato K, Momose-Sato Y. 2003. Optical detection of developmental origin of synaptic function in the embryonic chick vestibulocochlear nuclei. J Neurophysiol 89:3215-3224.
69. Sato K, Kuriyama H, Altschuler RA. 1998. Differential distribution of NMDA receptor subunit mRNA in the rat cochlear nucleus. Microsc Res Techniq 41:217-223.
70. Saunders JC, Coles RB, Gates GR. 1973. The development of auditory evoked responses in the cochlea and cochlear nuclei of the chick. Brain Res 63:59-74.
71. Schorge S, Colquhoun D. 2003. Studies of NMDA receptor function and stoichiometry with truncated and tandem subunits. J Neurosci 23: 1151-1158.
72. Sheng M, Lee SH. 2001. AMPA receptor trafficking and the control of synaptic transmission. Cell 105:825-828.
73. Sheng M, Cummings J, Roldan LA, Jan YN, Jan LY. 1994. Changing subunit composition of heteromeric NMDA receptors during development of rat cortex. Nature 368:144-147.
74. Singh TD, Basham ME, Nordeen EJ, Nordeen KW. 2000. Early sensory and hormonal experience modulate age-related changes in NR2B mRNA within a forebrain region controlling avian vocal learning. J Neurobiol 44:82-94.
75. 2+ flux during uncorrelated activity. Neuron 44:835-849.
76. Smith ZD. 1981. Organization and development of brain stem auditory nuclei of the chicken: dendritic development in n. laminaris. J Comp Neurol 203:309-333.
77. Soares D, Chitwood RA, Hyson RL, Carr CE. 2002. Intrinsic neuronal properties of the chick nucleus angularis. J Neurophysiol 88:152-162.
78. Song I, Huganir RL. 2002. Regulation of AMPA receptors during synaptic plasticity. Trends Neurosci 25:578-588.
79. Sprengel R, Seeburg PH. 1994. Ionotropic glutamate receptors. In: North RA, editor. Handbook of receptors and channels, vol 2: ligand and voltage-gated ion channels. Boca Raton, FL: CRC Press.
80. Stocca G, Vicini S. 1998. Increased contribution of NR2A subunit to synaptic NMDA receptors in developing rat cortical neurons. J Physiol 507:13-24.
81. Sucher NJ, Brose N, Deitcher DL, Awobuluyi M, Gasic GP, Bading H, Cepko CL, Greenberg ME, Jahn R, Heimemann SF. 1993. Expression of endogenous NMDAR1 transcripts without receptor protein suggests post-transcriptional control in PC12 cells. J Biol Chem 268:22299-22304.
82. Tang YP, Shimizu E, Dube GR, Rampon C, Kerchner GA, Zhuo M, Liu G, Tsien JZ. 1999. Genetic enhancement of learning and memory in mice. Nature 401:63-69.
83. Tang YZ, Carr CE. 2004. Development of NMDA R1 expression in chicken auditory brainstem. Hear Res 191:79-89.
84. Tang YZ, Piao YS, Zhuang LZ, Wang ZW. 2001. Expression of androgen receptor mRNA in the brain of Gekko gecko: implications for understanding the role of androgens in controlling auditory and vocal processes. J Comp Neurol 438:136-147.
85. Tang YZ, Yan K, Carr CE. 2004. Changes in NMDA receptor subunit 2A and 2B expression in chick cochlear nucleus during embryonic development. Program No. 304.3. Society for Neuroscience.
86. Taschenberger H, von Gersdorff H. 2000. Fine-tuning an auditory synapse for speed and fidelity: developmental changes in presynaptic waveform, EPSC kinetics, and synaptic plasticity. J Neurosci 20:9162-9173.
87. Wada K, Sakaguchi H, Jarvis ED, Hagiwara M. 2004. Differential expression of glutamate receptors in avian neural pathways for learned vocalization. J Comp Neurol 476:44-64.
88. Wafford KA, Bain CJ, Le Bourdelles B, Whiting PJ, Kemp JA. 1993. Preferential co-assembly of recombinant NMDA receptors composed of three different subunits. Neuroreport 4:1347-1349.
89. Warchol ME, Dallos P. 1990. Neural coding in the chick cochlear nucleus. J Comp Physiol A166:721-734.
90. Watanabe M, Inoue Y, Sakimura K, Mishina M. 1992. Developmental changes in distribution of NMDA receptor channel subunit mRNAs. Neuroreport 3:1138-1140.
91. Wenzel A, Fritschy JM, Mohler H, Benke D. 1997. NMDA receptor heterogeneity during postnatal development of the rat brain: differential expression of the NR2A, NR2B, and NR2C subunit proteins. J Neurochem 68:469-478.
92. Young SR, Rubel EW. 1986. Embryogenesis of arborization pattern and topography of individual axons in n. laminaris of the chicken brain stem. J Comp Neurol 254:425-459.
93. Youssoufian M, Oleskevich S, Walmsley B. 2005. Development of a robust central auditory synapse in congenital deafness. J Neurophysiol 94: 3168-3180.
94. Zarain-Herzberg A, Lee-Rivera I, Rodriguez G, Lopez-Colome AM. 2005. Cloning and characterization of the chick NMDA receptor subunit-1 gene. Brain Res Mol Brain Res 137:235-251.
95. Zhang S, Trussell LO. 1994a. A characterization of excitatory postsynaptic potentials in the avian nucleus magnocellularis. J Neurophysiol 72: 705-718.
96. Zhang S, Trussell LO. 1994b. Voltage clamp analysis of excitatory synaptic transmission in the avian nucleus magnocellularis. J Physiol 480:123-136.
97. Zhou N, Parks TN. 1992. Developmental changes in the effects of drugs acting at NMDA or non-NMDA receptors on synaptic transmission in the chick cochlear nucleus (nuc. magnocellularis). Brain Res Dev Brain Res 67:145-152.