Imaging of molecular dynamics regulated by electrical activities in neural circuits and in synapses

NeuroSignals

Volumn 16, Issue 4, 2008, Pages 260-277

  Fujii, Ritsuko ^a,b   Ichikawa, Michinori ^c   Ozaki, Miwako ^a,b,c  

^a WASEDA UNIVERSITY   (Japan)

^b Division of Cellular Signaling   (Japan)

^c Brainvision Inc   (Japan)

Author keywords

Activity dependent synaptic events; Molecular imaging; Neural circuits; Neuron glia interaction; Synapses; Voltage sensitive dye

Indexed keywords

ACTIN; DYE; EPIDERMAL GROWTH FACTOR RECEPTOR; EXPORTIN 5; MESSENGER RNA; NEU DIFFERENTIATION FACTOR;

BRAIN DEPTH STIMULATION; CAMERA; CELL ACTIVATION; CELL ACTIVITY; CELL COMMUNICATION; CELL FUNCTION; CELL MATURATION; CELL STRUCTURE; DENDRITE; DENDRITIC SPINE; ELECTRIC ACTIVITY; ELECTRIC POTENTIAL; ELECTRODE; ENCEPHALE ISOLE; EXCITATORY JUNCTION POTENTIAL; FLUORESCENCE; HUMAN; IMAGING SYSTEM; MOLECULAR DYNAMICS; MOLECULAR IMAGING; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NEUROMODULATION; NOISE; NONHUMAN; OPTICS; OSCILLATION; PROTEIN ANALYSIS; PROTEIN SYNTHESIS; QUANTITATIVE ANALYSIS; REVIEW; RNA TRANSPORT; SIGNAL NOISE RATIO; SIGNAL PROCESSING; SIGNAL TRANSDUCTION; SYNAPSE; TRANSLATION INITIATION; VERTEBRATE;

EID: 57149118449     PISSN: 1424862X     EISSN: None     Source Type: Journal    
DOI: 10.1159/000123037     Document Type: Review

References (112)

1. Yuste R, Denk W: Dendritic spines as basic functional units of neuronal integration. Nature 1995;375:682-684.
2. Fisher M, Kaech SK, Knutti D, Matus A: Rapid actin-based plasticity in dendritic spines. Neuron 1998;20:847-854.
3. Okabe S, Kim HD, Miwa A, Kuriu T, Okado H: Continual remodeling of postsynaptic density and its regulation by synaptic activity. Nat Neurosci 1999;2:804-811.
4. Star EN, Kwiatkowski DJ, Murthy VN: Rapid turnover of actin in dendritic spines and its regulation by activity. Nat Neurosci 2002;5:239-246.
5. Zheng L, Sheng M: Some assembly required: the development of neuronal synapses. Nat Rev Cell Biol 2003;4:833-841.
6. Hering H, Sheng M: Dendritic spines: structure, dynamics and regulation. Nat Rev Neurosci 2001;2:880-888.
7. Steward O, Levy WB: Preferential localization of polyribosomes under the base of dendritic spines in granule cells of dentate gyrus. J Neurosci 1982;2:284-291.
8. Eberwine J, Miyashiro K, Kacharmina JE, Job C: Local translation of classes of mRNAs that are targeted to neuronal dendrites. Proc Natl Acad Sci USA 2001;98:7080-7085.
9. Job C, Eberwine J: Localization and translation of mRNA in dendrites and axons. Nat Rev Neurosci 2001;2:889-898.
10. Kang H, Schuman EM: A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity. Science 1996;273:1402-1406.
11. Huber KM, Kayser MS, Bear MF: Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. Science 2000;288:1254-1257.
12. Yamada S, Nelson VJ: Synapses: sites of cell recognition, adhesion, and functional specification. Annu Rev Biochem 2007;76:267-294.
13. Mayford M, Baranes D, Podsypanina K, Kandel ER: The 3′-untranslated region of CaMKIIα is a cis-acting signal for the localization and translation of mRNA in dendrites. Proc Natl Acad Sci USA 1996;93:13250-13255.
14. Mori Y, Imaizumi K, Katayama T, Yoneda T, Tohyama M: Two cis-acting elements in the 3′ untranslated region of α-CaMKII regulate its dendritic targeting. Nat Nerosci 2000;3:1079-1084.
15. Shan J, Munro TP, Barbarese E, Carson JH, Smith R: A molecular mechanism for mRNA trafficking in neuronal dendrites. J Neurosci 2003;23:8859-8866.
16. Martin KC, Zukin RS: RNA trafficking and local protein synthesis in dendrites: an overview. J Neurosci 2006;26:7131-7134.
17. Tiruchinapalli DM, Oleynikov Y, Kelic S, Shenoy SM, Hartley A, Stanton PK, Singer RH, Bassell GJ: Activity-dependent trafficking and dynamic localization of zipcode binding protein 1 and β-actin mRNA in dendrites and spines of hippocampal neurons. J Neurosci 2002;23:3251-3261.
18. Bassell GJ, Zhang H, Byrd AL, Femino AM, Singer RH, Taneja KL, Lifshitz LM, Herman IM, Kosik KS: Sorting of β-actin mRNA and protein to neurites and growth cones in culture. J Neurosci 1998;18:251-265.
19. Fujii R, Okabe S, Urushido T, Inoue K, Yoshimura A, Tachibana T, Nishikawa T, Hicks GG, Takumi T: The RNA binding protein TLS is translocated to dendritic spines by mGluR5 activation and regulates spine morphology. Curr Biol 2005;15:587-593.
20. Zhang JL, Eom T, Oleynikov Y, Shenoy SM, Liebelt DA, Dictenberg JB, Singer RH, Bassell GJ: Neurotrophin-induced transport of a β-actin mRNP complex increases β-actin levels and stimulates growth cone motility. Neuron 2001;31:261-275.
21. Knowles RB, Sabry JH, Martone ME, Deerinck TJ, Ellisman MH, Bassell GJ, Kosik KS: Translocation of RNA granules in living neurons. J Neurosci 1996;16:7812-7820.
22. Krichevsky AM, Kosik KS: Neuronal RNA granules: a link between RNA localization and stimulation-dependent translation. Neuron 2001;32:683-696.
23. Kiebler MA, Hamraj I, Verkadel P, Kohrmann M, Fortes P, Marion RM, Ortin J, Dotti CG: The mammalian Staufen protein localizes to the somatodendritic domain of cultured hippocampal neurons: implications for its involvement in mRNA transport. J Neurosci 1999;19:288-297.
24. Tang SJ, Meulemans D, Vazquez L, Colaco N, Schuman EM: A role for rat homolog of Staufen in the transport of RNA to neuronal dendrites. Neuron 2001;32:463-475.
25. Eberhart DE, Malter HE, Feng Y, Warren ST: The fragile X mental retardation protein is a ribonucleoprotein containing both nuclear localization and nuclear export signals. Hum Mol Gen 1996;5:1083-1091.
26. Comery TA, Harris JB, Willems PJ, Oostra BA, Irwin SA, Weiler IJ, Greenough WT: Abnormal dendritic spines in fragile X knockout mice: maturation and pruning deficits. Proc Natl Acad Sci USA 1997;94:5401-5404.
27. Hirokawa N: mRNA transport in dendrites: RNA granules, motors and tracks. J Neurosci 2006;26:7139-7142.
28. Kanai Y, Dohmae N, Hirokawa N: Kinesin transports RNA: isolation and characterization of an RNA-transporting granule. Neuron 2004;43:513-525.
29. Miyawaki A, Nagai T, Mizuno H: Engineering fluorescent proteins. Adv Biochem Eng Biotechnol 2005;95:1-15.
30. Prasher DC, Eckenrode VK, Ward WW, Prendergast FG, Cormier MJ: Primary structure of the Aequorea victoria green-fluorescent protein. Gene 1992;111:229-233.
31. Miyawaki A, Nagai T, Mizuno H: Mechanisms of protein fluorophore formation and engineering. Curr Opin Chem Biol 2003;7:557-562.
32. Köhrmann M, Luo M, Kaether C, DesGroseillers L, Dotti CG, Kiebler MA: Microtubule-dependent recruitment of Staufen-green fluorescent protein into large RNA-containing granules and subsequent dendritic transport in living hippocampal neurons. Mol Biol Cell 1999;10:2945-2953.
33. Steward O, Worley PF: Selective targeting of newly synthesized Arc mRNA to active synapses requires NMDA receptor activation. Neuron 2001;30:227-240.
34. Mercer J, Seperack PK, Strobel MC, Copeland NG, Jenkins NA: Novel myosin heavy chain encoded by murine dilute coat colour locus. Nature 1991;349:709-713.
35. Yoshimura A, Fujii R, Watanabe Y, Okabe S, Fukui K, Takumi T: Myosin-Va facilitates the accumulation of mRNA/protein complex in dendritic spines. Curr Biol 2006;16:2345-2351.
36. Fujii R, Takumi T: TLS facilitates transport of mRNA encoding an actin-stabilizing protein to dendritic spines. J Cell Sci 2005;118:5755-5765.
37. Nimchinsky EA, Orberlander A, Svododa K: Abnormal development of dendritic spines in FMR1 knockout mice. J Neurosci 2001;21:5139-5146.
38. Miyashiro KY, Beckel-Mitchener A, Purk TP, Becker KG, Barret T, Liu L, Carbonetto S, Weiler IJ, Greenough WT, Eberwine J: RNA cargoes associating with FMRP reveal deficits in cellular functioning in Fmr1 null mice. Neuron 2003;37:417-431.
39. Antar LN, Afroz R, Dictenberg JB, Carroll RC, Bassell, GJ: Metabotropic glutamate receptor activation regulates fragile X mental retardation protein and Fmr1 mRNA localization differentially in dendrites and at synapses. J Neurosci 2004;24:2648-2655.
40. Ceman S, O'Donnell WT, Reed M, Patton S, Pohl J, Warren ST: Phosphorylation influences the translation state of FMRP-associated polyribosomes. Hum Mol Gen 2003;12:3295-3305.
41. Zalfa F, Giorgi M, Primerano B, Moro A, Di Penta A, Reis S, Oostra B, Bagni C: The fragile X syndrome protein FMRP associates with BC1 RNA and regulates the translation of specific mRNAs at synapses. Cell 2003;112:317-327.
42. Grossman AW, Aldridge GM, Weiler IJ, Greenough WT: Local protein synthesis and spine morphogenesis. J Neurosci 2006;26:7151-7155.
43. Pfeiffer EM, Huber KM: Current advances in local protein synthesis and synaptic plasticity. J Neurosci 2006;26:7147-7150.
44. Miller S, Yasuda M, Coats J, Jones Y, Martone ME, Mayford M: Disruption of dendritic translation of CaMKIIα impairs stabilization of synaptic plasticity and memory consolidation. Neuron 2002;36:507-519.
45. Aakalu G, Smith WB, Nguyen N, Jiang C, Schumann EM: Dynamic visualization of local protein synthesis in hippocampal neurons. Neuron 2001;30:489-502.
46. Ju W, Morishita W, Tsui J, Gaietta G, Deerinck TJ, Adams SR, Garner CC, Tsien RY, Ellisman MH, Malenka RC: Activity-dependent regulation of dendritic synthesis and trafficking of AMPA receptors. Nat Neurosci 2004;7:244-253.
47. Grooms SY, Noh KM, Regis R, Bassell GJ, Bryan MK, Carroll RC, Zukin RC: Activity bidirectionally regulates AMPA receptor mRNA abundance in dendrites of hippocampal neurons. J Neurosci 2006;26:8339-8351.
48. Steward O, Schuman EM: Compartmentalized synthesis and degradation of proteins in neurons. Neuron 2003;40:347-359.
49. Schuman EM, Dynes J, Steward O: Synaptic regulation of translation of dendritic mRNAs. J Neurosci 2006;26:7143-7146.
50. Colicos MA, Collins BE, Sailor MJ, Goda Y: Remodeling of synaptic actin induced by photoconductive stimulation. Cell 2001;107:605-616.
51. Matsuzaki M, Honkura N, Ellis-Davies GCR, Kasai H: Structural basis of long-term potentiation in single dendritic spines. Nature 2004;429:761-766.
52. Dillon C, Goda Y: The actin cytoskeleton: integrating form and function at the synapse. Annu Rev Neurosci 2005;28:25-55.
53. Lippman J, Dunaebsky A: Dendritic spine morphogenesis and plasticity. J Neurobiol 2005;64:47-57.
54. Matus A: Actin-based plasticity in dendritic spines. Science 2000;290:754-758.
55. Allison DW, Gelfand VI, Spector I, Craig AM: Role of actin in anchoring postsynaptic receptors in cultured hippocampal neurons: differential attachment of NMDA versus AMPA receptors. J Neurosci 1998;18:2423-2436.
56. Krucker T, Siggins GR, Halpain S: Dynamic actin filaments are required for stable long-term potentiation in area CA1 of the hippocampus. Proc Natl Acad Sci USA 2000;97:6856-6861.
57. Lisman JE, Zabotinsky A: A model of synaptic memory: a CaMKII/PP1 switch that potentiates transmission by organizing an AMPA receptor anchoring assembly. Neuron 2001;31:191-201.
58. Zhou Q, Xiao M, Nicoll RA: Contribution of cytoskeleton to the internalization of AMPA receptors. Proc Natl Acad Sci USA 2001;98:1261-1266.
59. Fukazawa Y, Saitoh Y, Ozawa F, Ohta Y, Mizuno K, Inokuchi K: Hippocampal LTP is accompanied by enhanced F-actin content within the dendritic spine that is essential for late LTP maintenance in vivo. Neuron 2003;38:447-460.
60. Gomez LL, Alam S, Smith KE, Horne E, Dell'Acqua ML: Regulation of A-kinase anchoring protein 79/150-cAMP-dependent protein kinase postsynaptic targeting by NMDA receptor activation of calcineurin and remodeling of dendritic actin. J Neurosci 2002;22:7027-7044.
61. Okamoto K, Nagai T, Miyawaki A, Hayashi Y: Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity. Nat Neurosci 2004;10:1104-1112.
62. Matsuzaki M, Ellis-Davies GCR, Nemoto T, Miyashita Y, IIno M, Kasai H: Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat Neurosci 2004;4:1086-1092.
63. Kacharmina JE, Job C, Crino P, Eberwine J: Stimulation of glutamate receptor protein synthesis and membrane insertion within isolated neuronal dendrites. Proc Natl Acad Sci USA 2000;97:11545-11550.
64. Ackermann M, Matus A: Activity-induced targeting of profilin and stabilization of dendritic spine morphology. Nat Rev Neurosci 2003;11:1194-1200.
65. Okabe S, Urushido T, Konno D, Okado H, Sobue K: Rapid redistribution of the postsynaptic density protein PSD-Zip45 (Homer 1c) and its differential regulation by NMDA receptors and calcium channels. J Neurosci 2001;21:9561-9571.
66. Sala C, Piech V, Wilson NR, Passafaro M, Liu G, Sheng M: Regulation of dendritic spine morphology and synaptic function by Shank and Homer. Neuron 2001;31:115-130.
67. Hering H, Sheng M: Activity-dependent redistribution and essential role of cortactin in dendritic spine morphogenesis. J Neurosci 2003;23:11759-11769.
68. Segal M: Dendritic spines and long-term plasticity. Nat Rev Neurosci 2005;6:277-284.
69. Haydon PG: GLIA: listening and talking to the synapse. Nat Rev Neurosci 2001;2:185-193.
70. Volterra A, Meldolesi J: Astrocytes, from brain glue to communication elements: the revolution continues. Nat Rev Neurosci 2005;6:626-640.
71. Corfas G, Roy K, Buxbaum JD: Neuregulin 1-erbB signaling and the molecular/cellular basis of schizophrenia. Nat Neurosci 2004;7:575-580.
72. Panatier A, Theodosis DT, Mothet JP, Touquet B, Pollegioni L, Poulain DA, Oliet SH: Glia-derived D-serine controls NMDA receptor activity and synaptic memory. Cell 2006;125:775-784.
73. Ventura R, Harris K: Three-dimensional relationships between hippocampal synapses and astrocytes. J Neurosci 1999;19:6897-6906.
74. Campbell RE, Tour O, Palmer AE, Steinbach PA, Baird GS, Zacharias DA, Tsien RY: A monomeric red fluorescent protein. Proc Natl Acad Sci USA 2002;99:7877-7882.
75. Haber M, Murai KK: Reshaping neuron-glial communication at hippocampal synapses. Neuron Glia Biol 2006;2:59-66.
76. Haber M, Zhou L, Murai KK: Cooperative astrocyte and dendritic spine dynamics at hippocampal excitatory synapses. J Neurosci 2006;26:8881-8891.
77. Nishida H, Okabe S: Direct astrocytic contacts regulate local maturation of dendritic spines. J Neurosci 2007;27:331-340.
78. Murai KK, Nguyen LN, Irie F, Yamaguchi Y, Pasquale EB: Control of hippocampal dendritic spine morphology through ephrin-A3/EphA4 signaling. Nat Neurosci 2003;6:153-160.
79. Grosche J, Kettenmann H, Reinbach A: Bergmann glial cells form distinct morphological structures to interact with cerebellar neurons. J Neurosci Res 2002;68:138-149.
80. Grosche J, Matyash V, Moller T, Verkhratsky A, Reichbach A, Kettenmann H: Microdomains for neuron-glia interaction: parallel fiber signaling to Bergmann glial cells. Nat Neurosci 1999;2:139-143.
81. Esper RM, Pankonin MS, Loeb JA: Neuregulins: versatile growth and differentiation factors in nervous system development and human disease. Brain Res Rev 2006;51:161-175.
82. Ozaki M, Itoh K, Miyakawa Y, Kishida H, Hashikawa T: Protein processing and release of neuregulin-1 are regulated in an activity-dependent manner. J Neurochem 2004;91:176-188.
83. Nave KA, Salzer JL: Axonal regulation of myelination by neuregulin 1. Curr Opin Neurobiol 2006;16:492-500.
84. Cannella B, Pitt D, Marchionni M, Raine CS: Neuregulin and erbB receptor expression in normal and diseased human white matter. J Neuroimmunol 1999;100:233-242.
85. Roy K, Murtie JC, El-Khodor BF, Edgar N, Sardi SP, Hooks BM, Benoit-Marand M, Chen C, Moore H, O'Donnell P, Brunner D, Corfas G: Loss of ErbB signaling in oligodendrocytes alters myelin and dopaminergic function, a potential mechanism for neuropsychiatric disorders. Proc Natl Acad Sci USA 2007;104:8131-8136.
86. Harrison PJ, Weinberger DR: Schizophrenia genes, gene expression, and neuropathology: on the matter of their convergence. Mol Psychiatry 2005;10:40-68.
87. Amanuma T, Ozaki M: Neurotrophic factor, neuregulin-1 and related molecules. Schizophr Front 2007;8:173-178.
88. Ozaki M, Ichikawa M: Profile of genes regulated by specific patterns of electrical activities. Society for Neuroscience, Annual Meeting, Atlanta 2006, abstr 537.1.
89. Tasaki I, Watanabe A, Sandlin R, Carnay L: Changes in fluorescence, turbidity, and birefringence associated with nerve excitation. Proc Natl Acad Sci USA 1968;61:883-888.
90. Cohen LB, Salzberg BM, Davila HV, Ross WN, Landowne D, Waggoner AS, Wang CH: Changes in axon fluorescence during activity: molecular probes of membrane potential. J Membr Biol 1976;19:1-36.
91. Ross WN, Salzberg BM, Cohen LB, Grinvald A, Davila HV, Waggoner AS, Wang CH: Changes in absorption, fluorescence, dichroism, and birefringence in stained giant axons: optical measurement of membrane potential. J Membr Biol 1977;6:141-183.
92. Grinvald A, Salzberg BM, Cohen LB: Simultaneous recording from several neurones in an invertebrate central nervous system. Nature 1977;14:140-142.
93. Ichikawa M, Iijima T, Matsumoto G: Real-time optical recording of neuronal activities in the brain; in Ono et al. (eds): Brain Mechanisms of Perception and Memory. Oxford, Oxford University Press, 1993, pp 639-647.
94. Iijima T, Witter MP, Ichikawa M, Tominaga T, Kajiwara R, Matsumoto G: Entorhinal-hippocampal interactions revealed by real-time imaging. Science 1996;24:1176-1179.
95. Williamson R, Ichikawa M, Matsumoto G: Neuronal circuits in cephalopod vision. Neth J Zool 1994;44:272-281.
96. Onimaru H, Homma I: Developmental changes in the spatiotemporal pattern of respiratory neuron activity in the medulla of late fetal rat. Neuroscience 2005;131:969-977.
97. Arata A, Ito M: Purkinje cell functions in the in vitro cerebellum isolated from neonatal rats in a block with the pons and medulla. Neurosci Res 2004;50:361-367.
98. Kajiwara R, Tominaga T, Takashima I: Olfactory information converges in the amygdaloid cortex via the piriform and entorhinal cortices: observations in the guinea pig isolated whole-brain preparation. Eur J Neurosci 2007;25:3648-3658.
99. Igor E, Vladimir N, Salama G: Optical imaging of the heart. Circ Res 2004;95:21-33.
100. Kaltenbach J, Zhang A: In vivo optical imaging of tone-evoked activity in the dorsal cochlear nucleus with a voltage-sensitive dye. J Neurosci Res 2004;78:908-917.
101. Ichikawa M, Tominaga T, Kawata T, Matsumoto G: Intrinsic and extrinsic optical signals in rat brain slices observed by high-speed imaging system. Society for Neuroscience, Annual Meeting, Washington 2003, abstr 759.5.
102. Slovin H, Arieli A, Hildesheim R, Grinvald A: Long-term voltage-sensitive dye imaging reveals cortical dynamics in behaving monkeys. J Neurophysiol 2002;88:3421-3438
103. Civillico EF, Contreras D: Comparison of responses to electrical stimulation and whisker deflection using two different voltage-sensitive dyes in mouse barrel cortex in vivo. J Membr Biol 2005;208:171-82.
104. Ratzlaff EH, Grinvald A: A tandem-lens epifluorescence macroscope: hundred-fold brightness advantage for wide-field imaging. J Neurosci Methods 1991;36:127-137.
105. Tominaga T, Tominaga Y, Yamada H, Matsumoto G, Ichikawa M: Quantification of optical signals with electorophysiological signals in neural activities of Di-4-ANEPPS-stained rat hippocampal slices. J Neurosci Methods 2000;102:11-23.
106. Nishimura M, Shirasawa H, Song WJ: A light-emitting diode light source for imaging of neural activities with voltage-sensitive dyes. Neurosci Res 2006;54:230-234.
107. Mann EO, Suckling JM, Hajos N, Greenfield SA, Paulsen O: Perisomatic feedback inhibition underlies cholinergically induced fast network oscillations in the rat hippocampus in vitro. Neuron 2005;45:105-117.
108. Gnatkovsky V, de Curtis M: Hippocampus-mediated activation of superficial and deep layer neurons in the medial entorhinal cortex of the isolated guinea pig brain. J Neurosci 2006;26:873-881.
109. Ferezou I, Bolea S, Petersen CC: Visualizing the cortical representation of whisker touch: voltage-sensitive dye imaging in freely moving mice. Neuron 2006;50:617-629.
110. Nishimura M, Shirasawa H, Kaizo H, Song WJ: New field with tonotopic organization in guinea pig auditory cortex. J Neurophysiol 2007;97:927-932.
111. Inoue K, Ohara S, Ichijyo H, Kakei S, Iijima T: Development of rabies virus vectors for neuron-specific and trans-synaptic delivery of a foreign gene. Society for Neuroscience, Annual Meeting, Washington 2004, abstr 124.12.
112. Bullen A, Saggau P: High-speed, random-access fluorescence microscopy. II. Fast quantitative measurements with voltage-sensitive dyes. Biophys J 1999;76:2272-2287.