Sensory activity differentially modulates N-methyl-d-aspartate receptor subunits 2A and 2B in cortical layers

Neuroscience

Volumn 163, Issue 3, 2009, Pages 920-932

  Corson, J ^a   Nahmani, M ^a   Lubarsky, K ^a   Badr, N ^a   Wright, C ^a   Erisir, A ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

ferret; glutamate receptors; immunoelectron microscopy; NMDAR; ocular dominance plasticity

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; RECEPTOR SUBUNIT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; ELECTRON MICROSCOPY; EYELID MOVEMENT; FERRET; LIGHT DARK CYCLE; NERVE CELL PLASTICITY; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; SENSORY CORTEX; SENSORY STIMULATION; SYNAPSE; VISION; VISUAL CORTEX;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; DARKNESS; DOWN-REGULATION; FERRETS; LIGHT; NEURONAL PLASTICITY; PHOTIC STIMULATION; PROTEIN SUBUNITS; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES; UP-REGULATION; VISUAL CORTEX;

EID: 70149101555     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2009.07.016     Document Type: Article

References (87)

1. Abraham W.C., and Bear M.F. Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci 19 4 (1996) 126-130
2. Albanese A., Albanese E., Brusco A., and Saavedra J.P. A quantitative study of visual cortex synapses during the postnatal development of dark-reared rats. J Neurobiol 14 1 (1983) 1-8
3. Baschong W., and Stierhof Y.D. Preparation, use, and enlargement of ultrasmall gold particles in immunoelectron microscopy. Microsc Res Tech 42 1 (1998) 66-79
4. Bear M.F. Bidirectional synaptic plasticity: from theory to reality. Philos Trans R Soc Lond B Biol Sci 358 1432 (2003) 649-655
5. Bear M.F., Kleinschmidt A., Gu Q.A., and Singer W. Disruption of experience-dependent synaptic modifications in striate cortex by infusion of an NMDA receptor antagonist. J Neurosci 10 3 (1990) 909-925
6. Bear M.F., and Rittenhouse C.D. Molecular basis for induction of ocular dominance plasticity. J Neurobiol 41 1 (1999) 83-91
7. Bellone C., and Nicoll R.A. Rapid bidirectional switching of synaptic NMDA receptors. Neuron 55 5 (2007) 779-785
8. Bienenstock E.L., Cooper L.N., and Munro P.W. Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J Neurosci 2 1 (1982) 32-48
9. Binzegger T., Douglas R.J., and Martin K.A. A quantitative map of the circuit of cat primary visual cortex. J Neurosci 24 39 (2004) 8441-8453
10. Bourgeois J.P., and Rakic P. Changes of synaptic density in the primary visual cortex of the macaque monkey from fetal to adult stage. J Neurosci 13 7 (1993) 2801-2820
11. Burkhalter A., Bernardo K.L., and Charles V. Development of local circuits in human visual cortex. J Neurosci 13 5 (1993) 1916-1931
12. Callaway E.M., and Katz L.C. Emergence and refinement of clustered horizontal connections in cat striate cortex. J Neurosci 10 4 (1990) 1134-1153
13. Callaway E.M., and Katz L.C. Development of axonal arbors of layer 4 spiny neurons in cat striate cortex. J Neurosci 12 2 (1992) 570-582
14. Cao Z., Liu L., Lickey M., Graves A., Pham T., and Gordon B. Virally mediated knock-down of NR2 subunits ipsilateral to the deprived eye blocks ocular dominance plasticity. Exp Brain Res 177 1 (2007) 64-77
15. Carmignoto G., and Vicini S. Activity-dependent decrease in NMDA receptor responses during development of the visual cortex. Science 258 5084 (1992) 1007-1011
16. Chan J., Aoki C., and Pickel V.M. Optimization of differential immunogold-silver and peroxidase labeling with maintenance of ultrastructure in brain sections before plastic embedding. J Neurosci Methods 33 2-3 (1990) 113-127
17. Chapman B., and Stryker M.P. Development of orientation selectivity in ferret visual cortex and effects of deprivation. J Neurosci 13 12 (1993) 5251-5262
18. Chapman B., Stryker M.P., and Bonhoeffer T. Development of orientation preference maps in ferret primary visual cortex. J Neurosci 16 20 (1996) 6443-6453
19. Chen W.S., and Bear M.F. Activity-dependent regulation of NR2B translation contributes to metaplasticity in mouse visual cortex. Neuropharmacology 52 1 (2007) 200-214
20. Colonnier M., and Beaulieu C. An empirical assessment of stereological formulae applied to the counting of synaptic disks in the cerebral cortex. J Comp Neurol 231 2 (1985) 175-179
21. Corlew R., Wang Y., Ghermazien H., Erisir A., and Philpot B.D. Developmental switch in the contribution of presynaptic and postsynaptic NMDA receptors to long-term depression. J Neurosci 27 37 (2007) 9835-9845
22. Cragg B.G. The development of synapses in kitten visual cortex during visual deprivation. Exp Neurol 46 3 (1975) 445-451
23. Crozier R.A., Wang Y., Liu C.H., and Bear M.F. Deprivation-induced synaptic depression by distinct mechanisms in different layers of mouse visual cortex. Proc Natl Acad Sci U S A 104 4 (2007) 1383-1388
24. Cynader M., and Mitchell D.E. Prolonged sensitivity to monocular deprivation in dark-reared cats. J Neurophysiol 43 4 (1980) 1026-1040
25. Daw N., Rao Y., Wang X.F., Fischer Q., and Yang Y. LTP and LTD vary with layer in rodent visual cortex. Vis Res 44 28 (2004) 3377-3380
26. Daw N.W. Mechanisms of plasticity in the visual cortex. The Friedenwald Lecture. Invest Ophthalmol Vis Sci 35 13 (1994) 4168-4179
27. Daw N.W., Fox K., Sato H., and Czepita D. Critical period for monocular deprivation in the cat visual cortex. J Neurophysiol 67 1 (1992) 197-202
28. Daw N.W., Reid S.N., Wang X.F., and Flavin H.J. Factors that are critical for plasticity in the visual cortex. Ciba Found Symp 193 (1995) 258-276 discussion: 258-276, 322-324
29. DeFelipe J., Marco P., Busturia I., and Merchan-Perez A. Estimation of the number of synapses in the cerebral cortex: methodological considerations. Cereb Cortex 9 7 (1999) 722-732
30. Desai N.S. Homeostatic plasticity in the CNS: synaptic and intrinsic forms. J Physiol Paris 97 4-6 (2003) 391-402
31. Douglas R.J., and Martin K.A. Neuronal circuits of the neocortex. Annu Rev Neurosci 27 (2004) 419-451
32. Dumas T.C. Developmental regulation of cognitive abilities: modified composition of a molecular switch turns on associative learning. Prog Neurobiol 76 3 (2005) 189-211
33. Durack J.C., and Katz L.C. Development of horizontal projections in layer 2/3 of ferret visual cortex. Cereb Cortex 6 2 (1996) 178-183
34. Erisir A., and Dreusicke M. Quantitative morphology and postsynaptic targets of thalamocortical axons in critical period and adult ferret visual cortex. J Comp Neurol 485 1 (2005) 11-31
35. Erisir A., and Harris J.L. Decline of the critical period of visual plasticity is concurrent with the reduction of NR2B subunit of the synaptic NMDA receptor in layer 4. J Neurosci 23 12 (2003) 5208-5218
36. Fagiolini M., Katagiri H., Miyamoto H., Mori H., Grant S.G., Mishina M., and Hensch T.K. Separable features of visual cortical plasticity revealed by N-methyl-D-aspartate receptor 2A signaling. Proc Natl Acad Sci U S A 100 5 (2003) 2854-2859
37. Fagiolini M., Pizzorusso T., Berardi N., Domenici L., and Maffei L. Functional postnatal development of the rat primary visual cortex and the role of visual experience: dark rearing and monocular deprivation. Vis Res 34 6 (1994) 709-720
38. Fox K., Daw N., Sato H., and Czepita D. The effect of visual experience on development of NMDA receptor synaptic transmission in kitten visual cortex. J Neurosci 12 7 (1992) 2672-2684
39. Fox K., Sato H., and Daw N. The location and function of NMDA receptors in cat and kitten visual cortex. J Neurosci 9 7 (1989) 2443-2454
40. Frenkel M.Y., and Bear M.F. How monocular deprivation shifts ocular dominance in visual cortex of young mice. Neuron 44 6 (2004) 917-923
41. Gabbott P.L., and Somogyi P. Quantitative distribution of GABA-immunoreactive neurons in the visual cortex (area 17) of the cat. Exp Brain Res 61 2 (1986) 323-331
42. Gilbert C.D. Microcircuitry of the visual cortex. Annu Rev Neurosci 6 (1983) 217-247
43. Goodman C.S., and Shatz C.J. Developmental mechanisms that generate precise patterns of neuronal connectivity. Cell 72 (1993) 77-98
44. Hagihara K., Tsumoto T., Sato H., and Hata Y. Actions of excitatory amino acid antagonists on geniculo-cortical transmission in the cat's visual cortex. Exp Brain Res 69 2 (1988) 407-416
45. He H.Y., Hodos W., and Quinlan E.M. Visual deprivation reactivates rapid ocular dominance plasticity in adult visual cortex. J Neurosci 26 11 (2006) 2951-2955
46. Hensch T.K., Fagiolini M., Mataga N., Stryker M.P., Baekkeskov S., and Kash S.F. Local GABA circuit control of experience-dependent plasticity in developing visual cortex. Science 282 5393 (1998) 1504-1508
47. Heynen A.J., Yoon B.J., Liu C.H., Chung H.J., Huganir R.L., and Bear M.F. Molecular mechanism for loss of visual cortical responsiveness following brief monocular deprivation. Nat Neurosci 6 8 (2003) 854-862
48. Hubel D.H., and Wiesel T.N. The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J Physiol (Lond) 206 2 (1970) 419-436
49. Hubel D.H., Wiesel T.N., and LeVay S. Plasticity of ocular dominance columns in monkey striate cortex. Philos Trans R Soc Lond B Biol Sci 278 961 (1977) 377-409
50. Iny K., Heynen A.J., Sklar E., and Bear M.F. Bidirectional modifications of visual acuity induced by monocular deprivation in juvenile and adult rats. J Neurosci 26 28 (2006) 7368-7374
51. Issa N.P., Trachtenberg J.T., Chapman B., Zahs K.R., and Stryker M.P. The critical period for ocular dominance plasticity in the ferret's visual cortex. J Neurosci 19 16 (1999) 6965-6978
52. Issa N.P., Trepel C., and Stryker M.P. Spatial frequency maps in cat visual cortex. J Neurosci 20 22 (2000) 8504-8514
53. Jiang B., Trevino M., and Kirkwood A. Sequential development of long-term potentiation and depression in different layers of the mouse visual cortex. J Neurosci 27 36 (2007) 9648-9652
54. Kleinschmidt A., Bear M.F., and Singer W. Blockade of "NMDA" receptors disrupts experience-dependent plasticity of kitten striate cortex. Science 238 4825 (1987) 355-358
55. Li Y., Fitzpatrick D., and White L.E. The development of direction selectivity in ferret visual cortex requires early visual experience. Nat Neurosci 9 5 (2006) 676-681
56. Liu X.B., Murray K.D., and Jones E.G. Switching of NMDA receptor 2A and 2B subunits at thalamic and cortical synapses during early postnatal development. J Neurosci 24 40 (2004) 8885-8895
57. Luhmann H.J., Singer W., and Martinez-Millan L. Horizontal interactions in cat striate cortex: I. Anatomical substrate and postnatal development. Eur J Neurosci 2 4 (1990) 344-357
58. Maffei A., Nataraj K., Nelson S.B., and Turrigiano G.G. Potentiation of cortical inhibition by visual deprivation. Nature 443 7107 (2006) 81-84
59. Malenka R.C., and Bear M.F. LTP and LTD: an embarrassment of riches. Neuron 44 1 (2004) 5-21
60. Mower G.D. The effect of dark rearing on the time course of the critical period in cat visual cortex. Brain Res Dev Brain Res 58 2 (1991) 151-158
61. Mower G.D., and Christen W.G. Role of visual experience in activating critical period in cat visual cortex. J Neurophysiol 53 2 (1985) 572-589
62. Mrsic-Flogel T.D., Hofer S.B., Ohki K., Reid R.C., Bonhoeffer T., and Hubener M. Homeostatic regulation of eye-specific responses in visual cortex during ocular dominance plasticity. Neuron 54 6 (2007) 961-972
63. Nahmani M., and Erisir A. VGluT2 immunocytochemistry identifies thalamocortical terminals in layer 4 of adult and developing visual cortex. J Comp Neurol 484 4 (2005) 458-473
64. Philpot B.D., Espinosa J.S., and Bear M.F. Evidence for altered NMDA receptor function as a basis for metaplasticity in visual cortex. J Neurosci 23 13 (2003) 5583-5588
65. Philpot B.D., Cho K.K., and Bear M.F. Obligatory role of NR2A for metaplasticity in visual cortex. Neuron 53 4 (2007) 495-502
66. Philpot B.D., Sekhar A.K., Shouval H.Z., and Bear M.F. Visual experience and deprivation bidirectionally modify the composition and function of NMDA receptors in visual cortex. Neuron 29 1 (2001) 157-169
67. Quinlan E.M., Olstein D.H., and Bear M.F. 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 22 (1999) 12876-12880
68. Quinlan E.M., Philpot B.D., Huganir R.L., and Bear M.F. Rapid, experience-dependent expression of synaptic NMDA receptors in visual cortex in vivo. Nat Neurosci 2 4 (1999) 352-357
69. Ramoa A.S., Mower A.F., Liao D., and Jafri S.I. Suppression of cortical NMDA receptor function prevents development of orientation selectivity in the primary visual cortex. J Neurosci 21 12 (2001) 4299-4309
70. Rampon C., and Tsien J.Z. Genetic analysis of learning and behavior-induced structural plasticity. Hippocampus 10 5 (2000) 605-609
71. Rao Y., and Daw N.W. Layer variations of long-term depression in rat visual cortex. J Neurophysiol 92 5 (2004) 2652-2658
72. Rittenhouse C.D., Shouval H.Z., Paradiso M.A., and Bear M.F. Monocular deprivation induces homosynaptic long-term depression in visual cortex. Nature 397 6717 (1999) 347-350
73. Rittenhouse C.D., Siegler B.A., Voelker C.C., Shouval H.Z., Paradiso M.A., and Bear M.F. Stimulus for rapid ocular dominance plasticity in visual cortex. J Neurophysiol 95 5 (2006) 2947-2950
74. Rivadulla C., Sharma J., and Sur M. Specific roles of NMDA and AMPA receptors in direction-selective and spatial phase-selective responses in visual cortex. J Neurosci 21 5 (2001) 1710-1719
75. Roberts E.B., Meredith M.A., and Ramoa A.S. Suppression of NMDA receptor function using antisense DNA block ocular dominance plasticity while preserving visual responses. J Neurophysiol 80 3 (1998) 1021-1032
76. Sawtell N.B., Frenkel M.Y., Philpot B.D., Nakazawa K., Tonegawa S., and Bear M.F. NMDA receptor-dependent ocular dominance plasticity in adult visual cortex. Neuron 38 6 (2003) 977-985
77. Scheetz A.J., and Contstantine-Paton M. Modulation of NMDA receptor function: implications for vertebrate neural development. FASEB J 8 10 (1994) 745-752
78. Smith G.B., Heynen A.J., and Bear M.F. Bidirectional synaptic mechanisms of ocular dominance plasticity in visual cortex. Philos Trans R Soc Lond B Biol Sci 364 1515 (2009) 357-364
79. Timney B., Mitchell D.E., and Cynader M. Behavioral evidence for prolonged sensitivity to effects of monocular deprivation in dark-reared cats. J Neurophysiol 43 4 (1980) 1041-1054
80. Trachtenberg J.T., Trepel C., and Stryker M.P. Rapid extragranular plasticity in the absence of thalamocortical plasticity in the developing primary visual cortex. Science 287 5460 (2000) 2029-2032
81. van Zundert B., Yoshii A., and Constantine-Paton M. Receptor compartmentalization and trafficking at glutamate synapses: a developmental proposal. Trends Neurosci 27 7 (2004) 428-437
82. White L.E., Coppola D.M., and Fitzpatrick D. The contribution of sensory experience to the maturation of orientation selectivity in ferret visual cortex. Nature 411 6841 (2001) 1049-1052
83. White L.E., and Fitzpatrick D. Vision and cortical map development. Neuron 56 2 (2007) 327-338
84. Wiesel T.N., and Gilbert C.D. The Sharpey-Schafer lecture. Morphological basis of visual cortical function. Q J Exp Physiol 68 4 (1983) 525-543
85. Yashiro K., and Philpot B.D. Regulation of NMDA receptor subunit expression and its implications for LTD, LTP, and metaplasticity. Neuropharmacology 55 (2008) 1081-1094
86. Yasuda H., Higashi H., Kudo Y., Inoue T., Hata Y., Mikoshiba K., and Tsumoto T. Imaging of calcineurin activated by long-term depression-inducing synaptic inputs in living neurons of rat visual cortex. Eur J Neurosci 17 2 (2003) 287-297
87. Yoshimura Y., Ohmura T., and Komatsu Y. Two forms of synaptic plasticity with distinct dependence on age, experience, and NMDA receptor subtype in rat visual cortex. J Neurosci 23 16 (2003) 6557-6566