NMDAR-regulated dynamics of layer 4 neuronal dendrites during thalamocortical reorganization in neonates

Neuron

Volumn 82, Issue 2, 2014, Pages 365-379

  Mizuno, Hidenobu ^a,b   Luo, Wenshu ^a,b   Tarusawa, Etsuko ^c   Saito, Yoshikazu M ^d   Sato, Takuya ^a   Yoshimura, Yumiko ^b,c   Itohara, Shigeyoshi ^d   Iwasato, Takuji ^a,b  

^a NATIONAL INSTITUTE OF GENETICS   (Japan)

^b GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^c NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

^d RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA-AMINO-3-HYDROXY-5-METHYL-4-ISOXAZOLEPROPIONIC ACID; ANIMALS; ANIMALS, NEWBORN; CEREBRAL CORTEX; DENDRITES; EXCITATORY AMINO ACID AGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MODELS, BIOLOGICAL; N-METHYLASPARTATE; NERVE TISSUE PROTEINS; NEURAL PATHWAYS; NEURONS; RECEPTORS, N-METHYL-D-ASPARTATE; THALAMUS;

EID: 84899103547     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2014.02.026     Document Type: Article

References (60)

1. Ballester-Rosado C.J., Albright M.J., Wu C.S., Liao C.C., Zhu J., Xu J., Lee L.J., Lu H.C. mGluR5 in cortical excitatory neurons exerts both cell-autonomous and -nonautonomous influences on cortical somatosensory circuit formation. J.Neurosci. 2010, 30:16896-16909.
2. Barnett M.W., Watson R.F., Kind P.C. Pathways to barrel development. Development and Plasticity in Sensory Thalamus and Cortex 2006, 138-157. Springer, New York. R. Erzurumlu, W. Guide, Z. Molnar (Eds.).
3. Barnett M.W., Watson R.F., Vitalis T., Porter K., Komiyama N.H., Stoney P.N., Gillingwater T.H., Grant S.G., Kind P.C. Synaptic Ras GTPase activating protein regulates pattern formation in the trigeminal system of mice. J.Neurosci. 2006, 26:1355-1365.
4. Boyden E.S., Zhang F., Bamberg E., Nagel G., Deisseroth K. Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci. 2005, 8:1263-1268.
5. Bureau I., von Saint Paul F., Svoboda K. Interdigitated paralemniscal and lemniscal pathways in the mouse barrel cortex. PLoS Biol. 2006, 4:e382.
6. Callaway E.M., Borrell V. Developmental sculpting of dendritic morphology of layer 4 neurons in visual cortex: influence of retinal input. J.Neurosci. 2011, 31:7456-7470.
7. Carrillo J., Nishiyama N., Nishiyama H. Dendritic translocation establishes the winner in cerebellar climbing fiber synapse elimination. J.Neurosci. 2013, 33:7641-7653.
8. Cases O., Vitalis T., Seif I., De Maeyer E., Sotelo C., Gaspar P. Lack of barrels in the somatosensory cortex of monoamine oxidase A-deficient mice: role of a serotonin excess during the critical period. Neuron 1996, 16:297-307.
9. Chen T.W., Wardill T.J., Sun Y., Pulver S.R., Renninger S.L., Baohan A., Schreiter E.R., Kerr R.A., Orger M.B., Jayaraman V., et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 2013, 499:295-300.
10. Cline H.T., Constantine-Paton M. NMDA receptor agonist and antagonists alter retinal ganglion cell arbor structure in the developing frog retinotectal projection. J.Neurosci. 1990, 10:1197-1216.
11. Crair M.C., Malenka R.C. A critical period for long-term potentiation at thalamocortical synapses. Nature 1995, 375:325-328.
12. Datwani A., Iwasato T., Itohara S., Erzurumlu R.S. NMDA receptor-dependent pattern transfer from afferents to postsynaptic cells anddendritic differentiation in the barrel cortex. Mol. Cell. Neurosci. 2002, 21:477-492.
13. Dhande O.S., Hua E.W., Guh E., Yeh J., Bhatt S., Zhang Y., Ruthazer E.S., Feller M.B., Crair M.C. Development of single retinofugal axon arbors in normal and β2 knock-out mice. J.Neurosci. 2011, 31:3384-3399.
14. Erzurumlu R.S., Jhaveri S. Thalamic axons confer a blueprint of the sensory periphery onto the developing rat somatosensory cortex. Brain Res. Dev. Brain Res. 1990, 56:229-234.
15. Erzurumlu R.S., Kind P.C. Neural activity: sculptor of 'barrels' in the neocortex. Trends Neurosci. 2001, 24:589-595.
16. Espinosa J.S., Wheeler D.G., Tsien R.W., Luo L. Uncoupling dendrite growth and patterning: single-cell knockout analysis of NMDA receptor 2B. Neuron 2009, 62:205-217.
17. Fox K. Barrel Cortex 2008, Cambridge University Press, Cambridge.
18. Goodman C.S., Shatz C.J. Developmental mechanisms that generate precise patterns of neuronal connectivity. Cell 1993, 72(Suppl):77-98.
19. Greenough W.T., Chang F.L. Dendritic pattern formation involves both oriented regression and oriented growth in the barrels of mouse somatosensory cortex. Brain Res. 1988, 471:148-152.
20. Hannan A.J., Blakemore C., Katsnelson A., Vitalis T., Huber K.M., Bear M., Roder J., Kim D., Shin H.S., Kind P.C. PLC-beta1, activated via mGluRs, mediates activity-dependent differentiation in cerebral cortex. Nat. Neurosci. 2001, 4:282-288.
21. Hubel D.H., Wiesel T.N., LeVay S. Plasticity of ocular dominance columns in monkey striate cortex. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1977, 278:377-409.
22. Inan M., Crair M.C. Development of cortical maps: perspectives from the barrel cortex. Neuroscientist 2007, 13:49-61.
23. Ince-Dunn G., Hall B.J., Hu S.C., Ripley B., Huganir R.L., Olson J.M., Tapscott S.J., Ghosh A. Regulation of thalamocortical patterning and synaptic maturation by NeuroD2. Neuron 2006, 49:683-695.
24. Iwasato T., Erzurumlu R.S., Huerta P.T., Chen D.F., Sasaoka T., Ulupinar E., Tonegawa S. NMDA receptor-dependent refinement of somatotopic maps. Neuron 1997, 19:1201-1210.
25. Iwasato T., Datwani A., Wolf A.M., Nishiyama H., Taguchi Y., Tonegawa S., Knöpfel T., Erzurumlu R.S., Itohara S. Cortex-restricted disruption of NMDAR1 impairs neuronal patterns in the barrel cortex. Nature 2000, 406:726-731.
26. Iwasato T., Katoh H., Nishimaru H., Ishikawa Y., Inoue H., Saito Y.M., Ando R., Iwama M., Takahashi R., Negishi M., Itohara S. Rac-GAP alpha-chimerin regulates motor-circuit formation as a key mediator of EphrinB3/EphA4 forward signaling. Cell 2007, 130:742-753.
27. Iwasato T., Inan M., Kanki H., Erzurumlu R.S., Itohara S., Crair M.C. Cortical adenylyl cyclase 1 is required for thalamocortical synapse maturation and aspects of layer IV barrel development. J.Neurosci. 2008, 28:5931-5943.
28. Katz L.C., Shatz C.J. Synaptic activity and the construction of cortical circuits. Science 1996, 274:1133-1138.
29. Konur S., Ghosh A. Calcium signaling and the control of dendritic development. Neuron 2005, 46:401-405.
30. Lee L.J., Iwasato T., Itohara S., Erzurumlu R.S. Exuberant thalamocortical axon arborization in cortex-specific NMDAR1 knockout mice. J.Comp. Neurol. 2005, 485:280-292.
31. Lefort S., Tomm C., Floyd Sarria J.C., Petersen C.C. The excitatory neuronal network of the C2 barrel column in mouse primary somatosensory cortex. Neuron 2009, 61:301-316.
32. Li Y., Lu H., Cheng P.L., Ge S., Xu H., Shi S.H., Dan Y. Clonally related visual cortical neurons show similar stimulus feature selectivity. Nature 2012, 486:118-121.
33. Li H., Fertuzinhos S., Mohns E., Hnasko T.S., Verhage M., Edwards R., Sestan N., Crair M.C. Laminar and columnar development of barrel cortex relies on thalamocortical neurotransmission. Neuron 2013, 79:970-986.
34. Matsui A., Tran M., Yoshida A.C., Kikuchi S.S., U M., Ogawa M., Shimogori T. BTBD3 controls dendrite orientation toward active axons in mammalian neocortex. Science 2013, 342:1114-1118.
35. Mizuno H., Hirano T., Tagawa Y. Evidence for activity-dependent cortical wiring: formation of interhemispheric connections in neonatal mouse visual cortex requires projection neuron activity. J.Neurosci. 2007, 27:6760-6770.
36. Nakai J., Ohkura M., Imoto K. A high signal-to-noise Ca(2+) probe composed of a single green fluorescent protein. Nat. Biotechnol. 2001, 19:137-141.
37. Narboux-Nême N., Evrard A., Ferezou I., Erzurumlu R.S., Kaeser P.S., Lainé J., Rossier J., Ropert N., Südhof T.C., Gaspar P. Neurotransmitter release at the thalamocortical synapse instructs barrel formation but not axon patterning in the somatosensory cortex. J.Neurosci. 2012, 32:6183-6196.
38. Niell C.M., Meyer M.P., Smith S.J. Invivo imaging of synapse formation on a growing dendritic arbor. Nat. Neurosci. 2004, 7:254-260.
39. Ohsaki K., Osumi N., Nakamura S. Altered whisker patterns induced by ectopic expression of Shh are topographically represented by barrels. Brain Res. Dev. Brain Res. 2002, 137:159-170.
40. Persico A.M., Mengual E., Moessner R., Hall F.S., Revay R.S., Sora I., Arellano J., DeFelipe J., Gimenez-Amaya J.M., Conciatori M., et al. Barrel pattern formation requires serotonin uptake by thalamocortical afferents, and not vesicular monoamine release. J.Neurosci. 2001, 21:6862-6873.
41. Petersen C.C. The functional organization of the barrel cortex. Neuron 2007, 56:339-355.
42. Saito T., Nakatsuji N. Efficient gene transfer into the embryonic mouse brain using invivo electroporation. Dev. Biol. 2001, 240:237-246.
43. Saneyoshi T., Wayman G., Fortin D., Davare M., Hoshi N., Nozaki N., Natsume T., Soderling T.R. Activity-dependent synaptogenesis: regulation by a CaM-kinase kinase/CaM-kinase I/betaPIX signaling complex. Neuron 2008, 57:94-107.
44. Sato H., Fukutani Y., Yamamoto Y., Tatara E., Takemoto M., Shimamura K., Yamamoto N. Thalamus-derived molecules promote survival and dendritic growth of developing cortical neurons. J.Neurosci. 2012, 32:15388-15402.
45. Sin W.C., Haas K., Ruthazer E.S., Cline H.T. Dendrite growth increased by visual activity requires NMDA receptor and Rho GTPases. Nature 2002, 419:475-480.
46. Staiger J.F., Flagmeyer I., Schubert D., Zilles K., Kötter R., Luhmann H.J. Functional diversity of layer IV spiny neurons in rat somatosensory cortex: quantitative morphology of electrophysiologically characterized and biocytin labeled cells. Cereb. Cortex 2004, 14:690-701.
47. Sur M., Rubenstein J.L. Patterning and plasticity of the cerebral cortex. Science 2005, 310:805-810.
48. Svoboda K., Denk W., Kleinfeld D., Tank D.W. Invivo dendritic calcium dynamics in neocortical pyramidal neurons. Nature 1997, 385:161-165.
49. Tabata H., Nakajima K. Efficient in utero gene transfer system to the developing mouse brain using electroporation: visualization of neuronal migration in the developing cortex. Neuroscience 2001, 103:865-872.
50. Tsien J.Z., Huerta P.T., Tonegawa S. The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory. Cell 1996, 87:1327-1338.
51. Van de Ven T.J., VanDongen H.M., VanDongen A.M. The nonkinase phorbol ester receptor alpha 1-chimerin binds the NMDA receptor NR2A subunit and regulates dendritic spine density. J.Neurosci. 2005, 25:9488-9496.
52. Welker E., Armstrong-James M., Bronchti G., Ourednik W., Gheorghita-Baechler F., Dubois R., Guernsey D.L., Van der Loos H., Neumann P.E. Altered sensory processing in the somatosensory cortex of the mouse mutant barrelless. Science 1996, 271:1864-1867.
53. Wong R.O., Ghosh A. Activity-dependent regulation of dendritic growth and patterning. Nat. Rev. Neurosci. 2002, 3:803-812.
54. Woolsey T.A., Van der Loos H. The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitectonic units. Brain Res. 1970, 17:205-242.
55. Woolsey T.A., Wann J.R. Areal changes in mouse cortical barrels following vibrissal damage at different postnatal ages. J.Comp. Neurol. 1976, 170:53-66.
56. Woolsey T.A., Dierker M.L., Wann D.F. Mouse SmI cortex: qualitative and quantitative classification of golgi-impregnated barrel neurons. Proc. Natl. Acad. Sci. USA 1975, 72:2165-2169.
57. Wu C.S., Ballester Rosado C.J., Lu H.C. What can we get from 'barrels': the rodent barrel cortex as a model for studying the establishment of neural circuits. Eur. J. Neurosci. 2011, 34:1663-1676.
58. Xie Z., Srivastava D.P., Photowala H., Kai L., Cahill M.E., Woolfrey K.M., Shum C.Y., Surmeier D.J., Penzes P. Kalirin-7 controls activity-dependent structural and functional plasticity of dendritic spines. Neuron 2007, 56:640-656.
59. Young P., Qiu L., Wang D., Zhao S., Gross J., Feng G. Single-neuron labeling with inducible Cre-mediated knockout in transgenic mice. Nat. Neurosci. 2008, 11:721-728.
60. Zong H., Espinosa J.S., Su H.H., Muzumdar M.D., Luo L. Mosaic analysis with double markers in mice. Cell 2005, 121:479-492.