Clustered Dynamics of Inhibitory Synapses and Dendritic Spines in the Adult Neocortex

Neuron

Volumn 74, Issue 2, 2012, Pages 361-373

  Chen, Jerry L ^a   Villa, Katherine L ^a   Cha, Jae Won ^b   So, Peter T C ^b   Kubota, Yoshiyuki ^c,d,e   Nedivi, Elly ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b Massachusetts Institute of Technology Cambridge   (United States)

^c NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

^d GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^e JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CRE RECOMBINASE; GEPHYRIN;

ANALYSIS OF VARIANCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENDRITIC CELL; DENDRITIC SPINE; ELECTROPORATION; IMMUNOELECTRON MICROSCOPY; IN VIVO STUDY; KINETICS; MICROSCOPY; MOLECULAR DYNAMICS; MORPHOLOGY; MOUSE; NEOCORTEX; NERVE CELL PLASTICITY; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; SIGNAL TRANSDUCTION; SYNAPSE; SYNAPTIC INHIBITION; VISUAL CORTEX;

ANIMALS; CARRIER PROTEINS; DENDRITES; ELECTROPORATION; EMBRYO, MAMMALIAN; FUNCTIONAL LATERALITY; IMAGING, THREE-DIMENSIONAL; LUMINESCENT PROTEINS; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICROSCOPY, IMMUNOELECTRON; MODELS, BIOLOGICAL; NEOCORTEX; NEURAL INHIBITION; NEURONS; NONLINEAR DYNAMICS; OPTICS AND PHOTONICS; PHOTIC STIMULATION; SENSORY DEPRIVATION; SYNAPSES;

EID: 84860274120     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2012.02.030     Document Type: Article

References (52)

1. Atasoy D., Aponte Y., Su H.H., Sternson S.M. A FLEX switch targets Channelrhodopsin-2 to multiple cell types for imaging and long-range circuit mapping. J. Neurosci. 2008, 28:7025-7030.
2. Bailey C.H., Kandel E.R. Structural changes accompanying memory storage. Annu. Rev. Physiol. 1993, 55:397-426.
3. Buonomano D.V., Merzenich M.M. Cortical plasticity: from synapses to maps. Annu. Rev. Neurosci. 1998, 21:149-186.
4. Chen J.L., Lin W.C., Cha J.W., So P.T., Kubota Y., Nedivi E. Structural basis for the role of inhibition in facilitating adult brain plasticity. Nat. Neurosci. 2011, 14:587-594.
5. Craig A.M., Banker G., Chang W., McGrath M.E., Serpinskaya A.S. Clustering of gephyrin at GABAergic but not glutamatergic synapses in cultured rat hippocampal neurons. J. Neurosci. 1996, 16:3166-3177.
6. DeFelipe J., Alonso-Nanclares L., Arellano J.I. Microstructure of the neocortex: comparative aspects. J. Neurocytol. 2002, 31:299-316.
7. Frenkel M.Y., Sawtell N.B., Diogo A.C., Yoon B., Neve R.L., Bear M.F. Instructive effect of visual experience in mouse visual cortex. Neuron 2006, 51:339-349.
8. Fuhrmann J.C., Kins S., Rostaing P., El Far O., Kirsch J., Sheng M., Triller A., Betz H., Kneussel M. Gephyrin interacts with Dynein light chains 1 and 2, components of motor protein complexes. J. Neurosci. 2002, 22:5393-5402.
9. Golding N.L., Staff N.P., Spruston N. Dendritic spikes as a mechanism for cooperative long-term potentiation. Nature 2002, 418:326-331.
10. Govindarajan A., Kelleher R.J., Tonegawa S. A clustered plasticity model of long-term memory engrams. Nat. Rev. Neurosci. 2006, 7:575-583.
11. Govindarajan A., Israely I., Huang S.Y., Tonegawa S. The dendritic branch is the preferred integrative unit for protein synthesis-dependent LTP. Neuron 2011, 69:132-146.
12. Gradinaru V., Zhang F., Ramakrishnan C., Mattis J., Prakash R., Diester I., Goshen I., Thompson K.R., Deisseroth K. Molecular and cellular approaches for diversifying and extending optogenetics. Cell 2010, 141:154-165.
13. Harauzov A., Spolidoro M., DiCristo G., De Pasquale R., Cancedda L., Pizzorusso T., Viegi A., Berardi N., Maffei L. Reducing intracortical inhibition in the adult visual cortex promotes ocular dominance plasticity. J. Neurosci. 2010, 30:361-371.
14. Harvey C.D., Svoboda K. Locally dynamic synaptic learning rules in pyramidal neuron dendrites. Nature 2007, 450:1195-1200.
15. Harvey C.D., Yasuda R., Zhong H., Svoboda K. The spread of Ras activity triggered by activation of a single dendritic spine. Science 2008, 321:136-140.
16. He H.Y., Hodos W., Quinlan E.M. Visual deprivation reactivates rapid ocular dominance plasticity in adult visual cortex. J. Neurosci. 2006, 26:2951-2955.
17. Hendry S.H., Jones E.G. Reduction in number of immunostained GABAergic neurones in deprived-eye dominance columns of monkey area 17. Nature 1986, 320:750-753.
18. Hofer S.B., Mrsic-Flogel T.D., Bonhoeffer T., Hübener M. Experience leaves a lasting structural trace in cortical circuits. Nature 2009, 457:313-317.
19. Holtmaat A.J., Trachtenberg J.T., Wilbrecht L., Shepherd G.M., Zhang X., Knott G.W., Svoboda K. Transient and persistent dendritic spines in the neocortex in vivo. Neuron 2005, 45:279-291.
20. Holtmaat A., Svoboda K. Experience-dependent structural synaptic plasticity in the mammalian brain. Nat. Rev. Neurosci. 2009, 10:647-658.
21. Holtmaat A., Bonhoeffer T., Chow D.K., Chuckowree J., De Paola V., Hofer S.B., Hübener M., Keck T., Knott G., Lee W.C., et al. Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window. Nat. Protoc. 2009, 4:1128-1144.
22. Jones E.G., Powell T.P. Morphological variations in the dendritic spines of the neocortex. J. Cell Sci. 1969, 5:509-529.
23. Kalatsky V.A., Stryker M.P. New paradigm for optical imaging: temporally encoded maps of intrinsic signal. Neuron 2003, 38:529-545.
24. Kanemoto Y., Matsuzaki M., Morita S., Hayama T., Noguchi J., Senda N., Momotake A., Arai T., Kasai H. Spatial distributions of GABA receptors and local inhibition of Ca2+ transients studied with GABA uncaging in the dendrites of CA1 pyramidal neurons. PLoS ONE 2011, 6:e22652.
25. Kawaguchi Y., Kubota Y. Neurochemical features and synaptic connections of large physiologically-identified GABAergic cells in the rat frontal cortex. Neuroscience 1998, 85:677-701.
26. Keck T., Scheuss V., Jacobsen R.I., Wierenga C.J., Eysel U.T., Bonhoeffer T., Hübener M. Loss of sensory input causes rapid structural changes of inhibitory neurons in adult mouse visual cortex. Neuron 2011, 71:869-882.
27. Knott G.W., Quairiaux C., Genoud C., Welker E. Formation of dendritic spines with GABAergic synapses induced by whisker stimulation in adult mice. Neuron 2002, 34:265-273.
28. Knott G.W., Holtmaat A., Wilbrecht L., Welker E., Svoboda K. Spine growth precedes synapse formation in the adult neocortex in vivo. Nat. Neurosci. 2006, 9:1117-1124.
29. Kubota Y., Hatada S., Kondo S., Karube F., Kawaguchi Y. Neocortical inhibitory terminals innervate dendritic spines targeted by thalamocortical afferents. J. Neurosci. 2007, 27:1139-1150.
30. Kubota Y., Hatada S.N., Kawaguchi Y. Important factors for the three-dimensional reconstruction of neuronal structures from serial ultrathin sections. Front Neural Circuits. 2009, 3:4.
31. Larkum M.E., Nevian T. Synaptic clustering by dendritic signalling mechanisms. Curr. Opin. Neurobiol. 2008, 18:321-331.
32. Lee W.C., Chen J.L., Huang H., Leslie J.H., Amitai Y., So P.T., Nedivi E. A dynamic zone defines interneuron remodeling in the adult neocortex. Proc. Natl. Acad. Sci. USA 2008, 105:19968-19973.
33. Lois C., Hong E.J., Pease S., Brown E.J., Baltimore D. Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science 2002, 295:868-872.
34. Lu Y.M., Mansuy I.M., Kandel E.R., Roder J. Calcineurin-mediated LTD of GABAergic inhibition underlies the increased excitability of CA1 neurons associated with LTP. Neuron 2000, 26:197-205.
35. Major G., Polsky A., Denk W., Schiller J., Tank D.W. Spatiotemporally graded NMDA spike/plateau potentials in basal dendrites of neocortical pyramidal neurons. J. Neurophysiol. 2008, 99:2584-2601.
36. Marik S.A., Yamahachi H., McManus J.N., Szabo G., Gilbert C.D. Axonal dynamics of excitatory and inhibitory neurons in somatosensory cortex. PLoS Biol. 2010, 8:e1000395.
37. Markram H., Toledo-Rodriguez M., Wang Y., Gupta A., Silberberg G., Wu C. Interneurons of the neocortical inhibitory system. Nat. Rev. Neurosci. 2004, 5:793-807.
38. Marsden K.C., Shemesh A., Bayer K.U., Carroll R.C. Selective translocation of Ca2+/calmodulin protein kinase IIalpha (CaMKIIalpha) to inhibitory synapses. Proc. Natl. Acad. Sci. USA 2010, 107:20559-20564.
39. Maya Vetencourt J.F., Sale A., Viegi A., Baroncelli L., De Pasquale R., O'Leary O.F., Castrén E., Maffei L. The antidepressant fluoxetine restores plasticity in the adult visual cortex. Science 2008, 320:385-388.
40. Miles R., Tóth K., Gulyás A.I., Hájos N., Freund T.F. Differences between somatic and dendritic inhibition in the hippocampus. Neuron 1996, 16:815-823.
41. Peng H., Ruan Z., Long F., Simpson J.H., Myers E.W. V3D enables real-time 3D visualization and quantitative analysis of large-scale biological image data sets. Nat. Biotechnol. 2010, 28:348-353.
42. Peters A. Examining neocortical circuits: some background and facts. J. Neurocytol. 2002, 31:183-193.
43. Rubinson D.A., Dillon C.P., Kwiatkowski A.V., Sievers C., Yang L., Kopinja J., Rooney D.L., Zhang M., Ihrig M.M., McManus M.T., et al. A lentivirus-based system to functionally silence genes in primary mammalian cells, stem cells and transgenic mice by RNA interference. Nat. Genet. 2003, 33:401-406.
44. Sato M., Stryker M.P. Distinctive features of adult ocular dominance plasticity. J. Neurosci. 2008, 28:10278-10286.
45. Schiller J., Schiller Y., Stuart G., Sakmann B. Calcium action potentials restricted to distal apical dendrites of rat neocortical pyramidal neurons. J. Physiol. 1997, 505:605-616.
46. Schmitt B., Knaus P., Becker C.M., Betz H. The Mr 93,000 polypeptide of the postsynaptic glycine receptor complex is a peripheral membrane protein. Biochemistry 1987, 26:805-811.
47. Sjöström P.J., Rancz E.A., Roth A., Häusser M. Dendritic excitability and synaptic plasticity. Physiol. Rev. 2008, 88:769-840.
48. Spolidoro M., Sale A., Berardi N., Maffei L. Plasticity in the adult brain: lessons from the visual system. Exp. Brain Res. 2009, 192:335-341.
49. Spruston N. Pyramidal neurons: dendritic structure and synaptic integration. Nat. Rev. Neurosci. 2008, 9:206-221.
50. 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.
51. Triller A., Cluzeaud F., Pfeiffer F., Betz H., Korn H. Distribution of glycine receptors at central synapses: an immunoelectron microscopy study. J. Cell Biol. 1985, 101:683-688.
52. Wierenga C.J., Becker N., Bonhoeffer T. GABAergic synapses are formed without the involvement of dendritic protrusions. Nat. Neurosci. 2008, 11:1044-1052.