DOI: 10.1016/j.neuron.2010.09.024. Single-Synapse Analysis of a Diverse Synapse Population: Proteomic Imaging Methods and Markers

Single-Synapse Analysis of a Diverse Synapse Population: Proteomic Imaging Methods and Markers

10.1016/j.neuron.2010.09.024

Crossref journal-article

Elsevier BV

Neuron (78)

Bibliography

Micheva, K. D., Busse, B., Weiler, N. C., OâRourke, N., & Smith, S. J. (2010). Single-Synapse Analysis of a Diverse Synapse Population: Proteomic Imaging Methods and Markers. Neuron, 68(4), 639â653.

Authors 5

Kristina D. Micheva (first)
Brad Busse (additional)
Nicholas C. Weiler (additional)
Nancy O'Rourke (additional)
Stephen J Smith (additional)

References 46 Referenced 293

10.1371/journal.pbio.1000074 / PLoS Biol. / A computational framework for ultrastructural mapping of neural circuitry by Anderson (2009)
{'key': '10.1016/j.neuron.2010.09.024_bib2', 'series-title': 'Computer Vision Approaches to Medical Image Analysis', 'first-page': '85', 'article-title': 'Consistent and elastic registration of histological sections using vector-spline regularization', 'author': 'Arganda-Carreras', 'year': '2006'} / Computer Vision Approaches to Medical Image Analysis / Consistent and elastic registration of histological sections using vector-spline regularization by Arganda-Carreras (2006)
10.1016/j.neuroscience.2007.02.060 / Neuroscience / Heterogeneity of glutamatergic and GABAergic release machinery in cerebral cortex by Bragina (2007)
10.1523/JNEUROSCI.18-23-09733.1998 / J. Neurosci. / The vesicular GABA transporter, VGAT, localizes to synaptic vesicles in sets of glycinergic as well as GABAergic neurons by Chaudhry (1998)
10.1016/S0166-2236(00)01724-0 / Trends Neurosci. / Generating diversity at GABAergic synapses by Cherubini (2001)
10.1038/88388 / Nat. Neurosci. / Molecular heterogeneity of central synapses: Afferent and target regulation by Craig (2001)
10.1016/S0959-4388(00)00215-4 / Curr. Opin. Neurobiol. / NMDA receptor subunits: Diversity, development and disease by Cull-Candy (2001)
10.1083/jcb.96.5.1337 / J. Cell Biol. / Synapsin I (protein I), a nerve terminal-specific phosphoprotein. I. Its general distribution in synapses of the central and peripheral nervous system demonstrated by immunofluorescence in frozen and plastic sections by De Camilli (1983)
10.1523/JNEUROSCI.5221-04.2005 / J. Neurosci. / Homeostatic scaling of vesicular glutamate and GABA transporter expression in rat neocortical circuits by De Gois (2005)
10.1113/jphysiol.1991.sp018732 / J. Physiol. / Excitation by geniculocortical synapses is not ‘vetoed’ at the level of dendritic spines in cat visual cortex by Dehay (1991)
10.1371/journal.pbio.0020329 / PLoS Biol. / Serial block-face scanning electron microscopy to reconstruct three-dimensional tissue nanostructure by Denk (2004)
10.1016/S0896-6273(00)00084-2 / Neuron / Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP by Feng (2000)
10.1016/S0896-6273(01)00344-0 / Neuron / The expression of vesicular glutamate transporters defines two classes of excitatory synapse by Fremeau (2001)
10.1016/j.tins.2008.02.006 / Trends Neurosci. / Gephyrin: Where do we stand, where do we go? by Fritschy (2008)
10.1016/S0301-0082(01)00007-7 / Prog. Neurobiol. / Alternative RNA splicing in the nervous system by Grabowski (2001)
10.1042/BST0340059 / Biochem. Soc. Trans. / The synapse proteome and phosphoproteome: a new paradigm for synapse biology by Grant (2006)
10.1016/j.brainresrev.2007.05.003 / Brain Res. Brain Res. Rev. / Toward a molecular catalogue of synapses by Grant (2007)
10.1002/cne.21592 / J. Comp. Neurol. / Vesicular glutamate transporters define two sets of glutamatergic afferents to the somatosensory thalamus and two thalamocortical projections in the mouse by Graziano (2008)
10.1523/JNEUROSCI.4074-09.2010 / J. Neurosci. / Quantitative comparison of glutamatergic and GABAergic synaptic vesicles unveils selectivity for few proteins including MAL2, a novel synaptic vesicle protein by Grønborg (2010)
10.1126/science.287.5451.273 / Science / Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex by Gupta (2000)
10.1523/JNEUROSCI.3994-06.2006 / J. Neurosci. / Uniform serial sectioning for transmission electron microscopy by Harris (2006)
10.1126/science.290.5492.739 / Science / Diversity and dynamics of dendritic signaling by Häusser (2000)
10.1098/rstb.1999.0378 / Philos. Trans. R. Soc. Lon. B Biol. Sci. / Synapsins as regulators of neurotransmitter release by Hilfiker (1999)
10.1038/nature07487 / Nature / Experience leaves a lasting structural trace in cortical circuits by Hofer (2009)
10.1016/j.conb.2004.05.007 / Curr. Opin. Neurobiol. / Glutamate transporters bring competition to the synapse by Huang (2004)
10.1523/JNEUROSCI.2970-09.2010 / J. Neurosci. / Rapid, learning-induced inhibitory synaptogenesis in murine barrel field by Jasinska (2010)
10.1242/jcs.5.2.509 / J. Cell Sci. / Morphological variations in the dendritic spines of the neocortex by Jones (1969)
10.1038/npp.2009.138 / Neuropsychopharmacology / Neurocartography by Kasthuri (2010)
10.1523/JNEUROSCI.4631-05.2006 / J. Neurosci. / Synapsin utilization differs among functional classes of synapses on thalamocortical cells by Kielland (2006)
10.1016/S0896-6273(02)00663-3 / Neuron / Formation of dendritic spines with GABAergic synapses induced by whisker stimulation in adult mice by Knott (2002)
10.1523/JNEUROSCI.3189-07.2008 / J. Neurosci. / Serial section scanning electron microscopy of adult brain tissue using focused ion beam milling by Knott (2008)
10.1523/JNEUROSCI.3846-06.2007 / J. Neurosci. / Neocortical inhibitory terminals innervate dendritic spines targeted by thalamocortical afferents by Kubota (2007)
10.1016/0006-8993(76)90002-0 / Brain Res. / Laminar patterns of geniculocortical projection in the cat by LeVay (1976)
{'key': '10.1016/j.neuron.2010.09.024_bib34', 'first-page': '120', 'article-title': 'Fast template matching', 'volume': '95', 'author': 'Lewis', 'year': '1995', 'journal-title': 'Vision Interface'} / Vision Interface / Fast template matching by Lewis (1995)
10.1113/jphysiol.2008.167742 / J. Physiol. / The synapse: center stage for many brain diseases by Lüscher (2009)
10.1016/0896-6273(90)90030-J / Neuron / Synapsins in the vertebrate retina: Absence from ribbon synapses and heterogeneous distribution among conventional synapses by Mandell (1990)
10.1073/pnas.92.25.11834 / Proc. Natl. Acad. Sci. USA / An anatomical substrate for experience-dependent plasticity of the rat barrel field cortex by Micheva (1995)
10.1016/j.neuron.2007.06.014 / Neuron / Array tomography: A new tool for imaging the molecular architecture and ultrastructure of neural circuits by Micheva (2007)
{'key': '10.1016/j.neuron.2010.09.024_bib39', 'series-title': 'Optical Imaging Techniques: A Laboratory Manual', 'first-page': '697', 'article-title': 'Array tomography: High-resolution 3D immunofluorescence', 'author': 'Micheva', 'year': '2010'} / Optical Imaging Techniques: A Laboratory Manual / Array tomography: High-resolution 3D immunofluorescence by Micheva (2010)
10.1016/j.tins.2004.07.002 / Trends Neurosci. / Diversity of inhibitory neurotransmission through GABA(A) receptors by Mody (2004)
10.1111/j.1460-9568.2007.05868.x / Eur. J. Neurosci. / Transiently increased colocalization of vesicular glutamate transporters 1 and 2 at single axon terminals during postnatal development of mouse neocortex: a quantitative analysis with correlation coefficient by Nakamura (2007)
{'key': '10.1016/j.neuron.2010.09.024_bib42', 'first-page': '45', 'article-title': 'Presynaptic Heterogeneity: Vive la difference', 'volume': '15', 'author': 'Staple', 'year': '2000', 'journal-title': 'News Physiol. Sci.'} / News Physiol. Sci. / Presynaptic Heterogeneity: Vive la difference by Staple (2000)
10.1109/83.650848 / IEEE Trans. Image Process. / A pyramid approach to subpixel registration based on intensity by Thévenaz (1998)
10.1242/jcs.109.4.787 / J. Cell Sci. / Partial colocalization of glucocorticoid and mineralocorticoid receptors in discrete compartments in nuclei of rat hippocampus neurons by van Steensel (1996)
10.1038/nature08389 / Nature / Rapid formation and selective stabilization of synapses for enduring motor memories by Xu (2009)
10.1038/nature08577 / Nature / Stably maintained dendritic spines are associated with lifelong memories by Yang (2009)

Dates

Type	When
Created	14 years, 9 months ago (Nov. 18, 2010, 4:30 a.m.)
Deposited	3 years, 10 months ago (Nov. 1, 2021, 10:49 a.m.)
Indexed	1 month, 2 weeks ago (July 14, 2025, 11:21 p.m.)
Issued	14 years, 10 months ago (Nov. 1, 2010)
Published	14 years, 10 months ago (Nov. 1, 2010)
Published Print	14 years, 10 months ago (Nov. 1, 2010)

Funders 0

None

BibTeX

@article{Micheva_2010, title={Single-Synapse Analysis of a Diverse Synapse Population: Proteomic Imaging Methods and Markers}, volume={68}, ISSN={0896-6273}, url={http://dx.doi.org/10.1016/j.neuron.2010.09.024}, DOI={10.1016/j.neuron.2010.09.024}, number={4}, journal={Neuron}, publisher={Elsevier BV}, author={Micheva, Kristina D. and Busse, Brad and Weiler, Nicholas C. and O’Rourke, Nancy and Smith, Stephen J}, year={2010}, month=nov, pages={639–653} }

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      "volume": "146",
      "author": "Bragina",
      "year": "2007",
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      "article-title": "The vesicular GABA transporter, VGAT, localizes to synaptic vesicles in sets of glycinergic as well as GABAergic neurons",
      "volume": "18",
      "author": "Chaudhry",
      "year": "1998",
      "journal-title": "J.\u00a0Neurosci."
    },
    {
      "key": "10.1016/j.neuron.2010.09.024_bib5",
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      "article-title": "Generating diversity at GABAergic synapses",
      "volume": "24",
      "author": "Cherubini",
      "year": "2001",
      "journal-title": "Trends Neurosci."
    },
    {
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      "first-page": "569",
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      "article-title": "Molecular heterogeneity of central synapses: Afferent and target regulation",
      "volume": "4",
      "author": "Craig",
      "year": "2001",
      "journal-title": "Nat. Neurosci."
    },
    {
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      "first-page": "327",
      "DOI": "10.1016/S0959-4388(00)00215-4",
      "article-title": "NMDA receptor subunits: Diversity, development and disease",
      "volume": "11",
      "author": "Cull-Candy",
      "year": "2001",
      "journal-title": "Curr. Opin. Neurobiol."
    },
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      "first-page": "1337",
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      "volume": "96",
      "author": "De Camilli",
      "year": "1983",
      "journal-title": "J.\u00a0Cell Biol."
    },
    {
      "key": "10.1016/j.neuron.2010.09.024_bib9",
      "doi-asserted-by": "crossref",
      "first-page": "7121",
      "DOI": "10.1523/JNEUROSCI.5221-04.2005",
      "article-title": "Homeostatic scaling of vesicular glutamate and GABA transporter expression in rat neocortical circuits",
      "volume": "25",
      "author": "De Gois",
      "year": "2005",
      "journal-title": "J.\u00a0Neurosci."
    },
    {
      "key": "10.1016/j.neuron.2010.09.024_bib10",
      "doi-asserted-by": "crossref",
      "first-page": "723",
      "DOI": "10.1113/jphysiol.1991.sp018732",
      "article-title": "Excitation by geniculocortical synapses is not \u2018vetoed\u2019 at the level of dendritic spines in cat visual cortex",
      "volume": "440",
      "author": "Dehay",
      "year": "1991",
      "journal-title": "J.\u00a0Physiol."
    },
    {
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    {
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      "volume": "28",
      "author": "Feng",
      "year": "2000",
      "journal-title": "Neuron"
    },
    {
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      "doi-asserted-by": "crossref",
      "first-page": "247",
      "DOI": "10.1016/S0896-6273(01)00344-0",
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      "volume": "31",
      "author": "Fremeau",
      "year": "2001",
      "journal-title": "Neuron"
    },
    {
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      "doi-asserted-by": "crossref",
      "first-page": "257",
      "DOI": "10.1016/j.tins.2008.02.006",
      "article-title": "Gephyrin: Where do we stand, where do we go?",
      "volume": "31",
      "author": "Fritschy",
      "year": "2008",
      "journal-title": "Trends Neurosci."
    },
    {
      "key": "10.1016/j.neuron.2010.09.024_bib15",
      "doi-asserted-by": "crossref",
      "first-page": "289",
      "DOI": "10.1016/S0301-0082(01)00007-7",
      "article-title": "Alternative RNA splicing in the nervous system",
      "volume": "65",
      "author": "Grabowski",
      "year": "2001",
      "journal-title": "Prog. Neurobiol."
    },
    {
      "key": "10.1016/j.neuron.2010.09.024_bib16",
      "doi-asserted-by": "crossref",
      "first-page": "59",
      "DOI": "10.1042/BST0340059",
      "article-title": "The synapse proteome and phosphoproteome: a new paradigm for synapse biology",
      "volume": "34",
      "author": "Grant",
      "year": "2006",
      "journal-title": "Biochem. Soc. Trans."
    },
    {
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      "doi-asserted-by": "crossref",
      "first-page": "445",
      "DOI": "10.1016/j.brainresrev.2007.05.003",
      "article-title": "Toward a molecular catalogue of synapses",
      "volume": "55",
      "author": "Grant",
      "year": "2007",
      "journal-title": "Brain Res. Brain Res. Rev."
    },
    {
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      "first-page": "1258",
      "DOI": "10.1002/cne.21592",
      "article-title": "Vesicular glutamate transporters define two sets of glutamatergic afferents to the somatosensory thalamus and two thalamocortical projections in the mouse",
      "volume": "507",
      "author": "Graziano",
      "year": "2008",
      "journal-title": "J.\u00a0Comp. Neurol."
    },
    {
      "key": "10.1016/j.neuron.2010.09.024_bib19",
      "doi-asserted-by": "crossref",
      "first-page": "2",
      "DOI": "10.1523/JNEUROSCI.4074-09.2010",
      "article-title": "Quantitative comparison of glutamatergic and GABAergic synaptic vesicles unveils selectivity for few proteins including MAL2, a novel synaptic vesicle protein",
      "volume": "30",
      "author": "Gr\u00f8nborg",
      "year": "2010",
      "journal-title": "J.\u00a0Neurosci."
    },
    {
      "key": "10.1016/j.neuron.2010.09.024_bib20",
      "doi-asserted-by": "crossref",
      "first-page": "273",
      "DOI": "10.1126/science.287.5451.273",
      "article-title": "Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex",
      "volume": "287",
      "author": "Gupta",
      "year": "2000",
      "journal-title": "Science"
    },
    {
      "key": "10.1016/j.neuron.2010.09.024_bib21",
      "doi-asserted-by": "crossref",
      "first-page": "12101",
      "DOI": "10.1523/JNEUROSCI.3994-06.2006",
      "article-title": "Uniform serial sectioning for transmission electron microscopy",
      "volume": "26",
      "author": "Harris",
      "year": "2006",
      "journal-title": "J.\u00a0Neurosci."
    },
    {
      "key": "10.1016/j.neuron.2010.09.024_bib22",
      "doi-asserted-by": "crossref",
      "first-page": "739",
      "DOI": "10.1126/science.290.5492.739",
      "article-title": "Diversity and dynamics of dendritic signaling",
      "volume": "290",
      "author": "H\u00e4usser",
      "year": "2000",
      "journal-title": "Science"
    },
    {
      "key": "10.1016/j.neuron.2010.09.024_bib23",
      "doi-asserted-by": "crossref",
      "first-page": "269",
      "DOI": "10.1098/rstb.1999.0378",
      "article-title": "Synapsins as regulators of neurotransmitter release",
      "volume": "354",
      "author": "Hilfiker",
      "year": "1999",
      "journal-title": "Philos. Trans. R. Soc. Lon. B Biol. Sci."
    },
    {
      "key": "10.1016/j.neuron.2010.09.024_bib24",
      "doi-asserted-by": "crossref",
      "first-page": "313",
      "DOI": "10.1038/nature07487",
      "article-title": "Experience leaves a lasting structural trace in cortical circuits",
      "volume": "457",
      "author": "Hofer",
      "year": "2009",
      "journal-title": "Nature"
    },
    {
      "key": "10.1016/j.neuron.2010.09.024_bib25",
      "doi-asserted-by": "crossref",
      "first-page": "346",
      "DOI": "10.1016/j.conb.2004.05.007",
      "article-title": "Glutamate transporters bring competition to the synapse",
      "volume": "14",
      "author": "Huang",
      "year": "2004",
      "journal-title": "Curr. Opin. Neurobiol."
    },
    {
      "key": "10.1016/j.neuron.2010.09.024_bib26",
      "doi-asserted-by": "crossref",
      "first-page": "1176",
      "DOI": "10.1523/JNEUROSCI.2970-09.2010",
      "article-title": "Rapid, learning-induced inhibitory synaptogenesis in murine barrel field",
      "volume": "30",
      "author": "Jasinska",
      "year": "2010",
      "journal-title": "J.\u00a0Neurosci."
    },
    {
      "key": "10.1016/j.neuron.2010.09.024_bib27",
      "doi-asserted-by": "crossref",
      "first-page": "509",
      "DOI": "10.1242/jcs.5.2.509",
      "article-title": "Morphological variations in the dendritic spines of the neocortex",
      "volume": "5",
      "author": "Jones",
      "year": "1969",
      "journal-title": "J.\u00a0Cell Sci."
    },
    {
      "key": "10.1016/j.neuron.2010.09.024_bib28",
      "doi-asserted-by": "crossref",
      "first-page": "342",
      "DOI": "10.1038/npp.2009.138",
      "article-title": "Neurocartography",
      "volume": "35",
      "author": "Kasthuri",
      "year": "2010",
      "journal-title": "Neuropsychopharmacology"
    },
    {
      "key": "10.1016/j.neuron.2010.09.024_bib29",
      "doi-asserted-by": "crossref",
      "first-page": "5786",
      "DOI": "10.1523/JNEUROSCI.4631-05.2006",
      "article-title": "Synapsin utilization differs among functional classes of synapses on thalamocortical cells",
      "volume": "26",
      "author": "Kielland",
      "year": "2006",
      "journal-title": "J.\u00a0Neurosci."
    },
    {
      "key": "10.1016/j.neuron.2010.09.024_bib30",
      "doi-asserted-by": "crossref",
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      "DOI": "10.1016/S0896-6273(02)00663-3",
      "article-title": "Formation of dendritic spines with GABAergic synapses induced by whisker stimulation in adult mice",
      "volume": "34",
      "author": "Knott",
      "year": "2002",
      "journal-title": "Neuron"
    },
    {
      "key": "10.1016/j.neuron.2010.09.024_bib31",
      "doi-asserted-by": "crossref",
      "first-page": "2959",
      "DOI": "10.1523/JNEUROSCI.3189-07.2008",
      "article-title": "Serial section scanning electron microscopy of adult brain tissue using focused ion beam milling",
      "volume": "28",
      "author": "Knott",
      "year": "2008",
      "journal-title": "J.\u00a0Neurosci."
    },
    {
      "key": "10.1016/j.neuron.2010.09.024_bib32",
      "doi-asserted-by": "crossref",
      "first-page": "1139",
      "DOI": "10.1523/JNEUROSCI.3846-06.2007",
      "article-title": "Neocortical inhibitory terminals innervate dendritic spines targeted by thalamocortical afferents",
      "volume": "27",
      "author": "Kubota",
      "year": "2007",
      "journal-title": "J.\u00a0Neurosci."
    },
    {
      "key": "10.1016/j.neuron.2010.09.024_bib33",
      "doi-asserted-by": "crossref",
      "first-page": "1",
      "DOI": "10.1016/0006-8993(76)90002-0",
      "article-title": "Laminar patterns of geniculocortical projection in the cat",
      "volume": "113",
      "author": "LeVay",
      "year": "1976",
      "journal-title": "Brain Res."
    },
    {
      "key": "10.1016/j.neuron.2010.09.024_bib34",
      "first-page": "120",
      "article-title": "Fast template matching",
      "volume": "95",
      "author": "Lewis",
      "year": "1995",
      "journal-title": "Vision Interface"
    },
    {
      "key": "10.1016/j.neuron.2010.09.024_bib35",
      "doi-asserted-by": "crossref",
      "first-page": "727",
      "DOI": "10.1113/jphysiol.2008.167742",
      "article-title": "The synapse: center stage for many brain diseases",
      "volume": "587",
      "author": "L\u00fcscher",
      "year": "2009",
      "journal-title": "J.\u00a0Physiol."
    },
    {
      "key": "10.1016/j.neuron.2010.09.024_bib36",
      "doi-asserted-by": "crossref",
      "first-page": "19",
      "DOI": "10.1016/0896-6273(90)90030-J",
      "article-title": "Synapsins in the vertebrate retina: Absence from ribbon synapses and heterogeneous distribution among conventional synapses",
      "volume": "5",
      "author": "Mandell",
      "year": "1990",
      "journal-title": "Neuron"
    },
    {
      "key": "10.1016/j.neuron.2010.09.024_bib37",
      "doi-asserted-by": "crossref",
      "first-page": "11834",
      "DOI": "10.1073/pnas.92.25.11834",
      "article-title": "An\u00a0anatomical substrate for experience-dependent plasticity of the rat barrel field cortex",
      "volume": "92",
      "author": "Micheva",
      "year": "1995",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "10.1016/j.neuron.2010.09.024_bib38",
      "doi-asserted-by": "crossref",
      "first-page": "25",
      "DOI": "10.1016/j.neuron.2007.06.014",
      "article-title": "Array tomography: A new tool for imaging the molecular architecture and ultrastructure of neural circuits",
      "volume": "55",
      "author": "Micheva",
      "year": "2007",
      "journal-title": "Neuron"
    },
    {
      "key": "10.1016/j.neuron.2010.09.024_bib39",
      "series-title": "Optical Imaging Techniques: A Laboratory Manual",
      "first-page": "697",
      "article-title": "Array tomography: High-resolution 3D immunofluorescence",
      "author": "Micheva",
      "year": "2010"
    },
    {
      "key": "10.1016/j.neuron.2010.09.024_bib40",
      "doi-asserted-by": "crossref",
      "first-page": "569",
      "DOI": "10.1016/j.tins.2004.07.002",
      "article-title": "Diversity of inhibitory neurotransmission through GABA(A) receptors",
      "volume": "27",
      "author": "Mody",
      "year": "2004",
      "journal-title": "Trends Neurosci."
    },
    {
      "key": "10.1016/j.neuron.2010.09.024_bib41",
      "doi-asserted-by": "crossref",
      "first-page": "3054",
      "DOI": "10.1111/j.1460-9568.2007.05868.x",
      "article-title": "Transiently increased colocalization of vesicular glutamate transporters 1 and 2 at single axon terminals during postnatal development of mouse neocortex: a quantitative analysis with correlation coefficient",
      "volume": "26",
      "author": "Nakamura",
      "year": "2007",
      "journal-title": "Eur. J. Neurosci."
    },
    {
      "key": "10.1016/j.neuron.2010.09.024_bib42",
      "first-page": "45",
      "article-title": "Presynaptic Heterogeneity: Vive la difference",
      "volume": "15",
      "author": "Staple",
      "year": "2000",
      "journal-title": "News Physiol. Sci."
    },
    {
      "key": "10.1016/j.neuron.2010.09.024_bib43",
      "doi-asserted-by": "crossref",
      "first-page": "27",
      "DOI": "10.1109/83.650848",
      "article-title": "A pyramid approach to subpixel registration based on intensity",
      "volume": "7",
      "author": "Th\u00e9venaz",
      "year": "1998",
      "journal-title": "IEEE Trans. Image Process."
    },
    {
      "key": "10.1016/j.neuron.2010.09.024_bib44",
      "doi-asserted-by": "crossref",
      "first-page": "787",
      "DOI": "10.1242/jcs.109.4.787",
      "article-title": "Partial colocalization of glucocorticoid and mineralocorticoid receptors in discrete compartments in nuclei of rat hippocampus neurons",
      "volume": "109",
      "author": "van Steensel",
      "year": "1996",
      "journal-title": "J.\u00a0Cell Sci."
    },
    {
      "key": "10.1016/j.neuron.2010.09.024_bib45",
      "doi-asserted-by": "crossref",
      "first-page": "915",
      "DOI": "10.1038/nature08389",
      "article-title": "Rapid formation and selective stabilization of synapses for enduring motor memories",
      "volume": "462",
      "author": "Xu",
      "year": "2009",
      "journal-title": "Nature"
    },
    {
      "key": "10.1016/j.neuron.2010.09.024_bib46",
      "doi-asserted-by": "crossref",
      "first-page": "920",
      "DOI": "10.1038/nature08577",
      "article-title": "Stably maintained dendritic spines are associated with lifelong memories",
      "volume": "462",
      "author": "Yang",
      "year": "2009",
      "journal-title": "Nature"
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