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Synapses on demand require dendrites at the ready: How defining stages of dendritic development in vitro could inform studies of behaviorally driven information storage in the brain

dc.contributor.authorJuraska, Janiceen_US
dc.date.accessioned2011-11-10T15:33:17Z
dc.date.available2012-09-04T15:27:32Zen_US
dc.date.issued2011-07en_US
dc.identifier.citationJuraska, Janice (2011). "Synapses on demand require dendrites at the ready: How defining stages of dendritic development in vitro could inform studies of behaviorally driven information storage in the brain." Developmental Psychobiology 53(5): 443-455. <http://hdl.handle.net/2027.42/86892>en_US
dc.identifier.issn0012-1630en_US
dc.identifier.issn1098-2302en_US
dc.identifier.urihttps://hdl.handle.net/2027.42/86892
dc.description.abstractBill Greenough's work provides a framework for thinking about synaptogenesis not only as a key step in the initial wiring of neural systems according to a species typical plan (i.e., experience‐expectant development), but also as a mechanism for storing information based an individual's unique experience over its lifetime (i.e., experience‐dependent plasticity). Analysis of synaptic development in vitro brings a new opportunity to test the limits of expectant‐expectant development at the level of the individual neuron. We analyzed dendritic growth, synapse formation, and the development of specialized cytoplasmic microdomains during development in cultured hippocampal neurons, to determine if the timing of each of these events is correlated. Taken together, the findings reported here support the hypotheses that (1) dendritic development is rate limiting in synapse formation and (2) synaptic circuits are assembled in a step‐wise fashion consistent with a stage‐specific shift from genomically pre‐programmed to activity‐dependent mechanisms. © 2011 Wiley Periodicals, Inc. Dev Psychobiol 53:443–455, 2011.en_US
dc.publisherWiley Subscription Services, Inc., A Wiley Companyen_US
dc.subject.otherDendriteen_US
dc.subject.otherDendritic Developmenten_US
dc.subject.otherSynapse Formationen_US
dc.subject.otherPostsynaptic Developmenten_US
dc.subject.otherCultured Hippocampal Neuronen_US
dc.subject.otherExperience‐Expectant Brain Developmenten_US
dc.titleSynapses on demand require dendrites at the ready: How defining stages of dendritic development in vitro could inform studies of behaviorally driven information storage in the brainen_US
dc.typeArticleen_US
dc.rights.robotsIndexNoFollowen_US
dc.subject.hlbsecondlevelEcology and Evolutionary Biologyen_US
dc.subject.hlbtoplevelScienceen_US
dc.description.peerreviewedPeer Revieweden_US
dc.contributor.affiliationumUniversity of Michigan Neuroscience Graduate Program, Ann Arbor, MI 48109.en_US
dc.contributor.affiliationotherDepartment of Biology, Whitman College, Walla Walla, WA 99362en_US
dc.contributor.affiliationotherPurdue University Ecological Science and Engineering Graduate Program, West Lafayette, IN 47907.en_US
dc.contributor.affiliationotherDepartment of Biology, Whitman College, Walla Walla, WA 99362.en_US
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/86892/1/20560_ftp.pdf
dc.identifier.doi10.1002/dev.20560en_US
dc.identifier.sourceDevelopmental Psychobiologyen_US
dc.identifier.citedreferenceAraque, A., Parpura, V., Sanzgiri, R. P., & Haydon, P. G. ( 1999 ). Tripartite synapses: Glia, the unacknowledged partner. Trends in Neuroscience, 22, 208 – 215.en_US
dc.identifier.citedreferenceArikkath, J. ( 2009 ). Regulation of dendrite and spine morphogenesis and plasticity by catenins. Molecular Neurobiology, 40 ( 1 ), 46 – 54.en_US
dc.identifier.citedreferenceBanker, G. A., & Goslin, K. ( 1998 ). Culturing nerve cells ( 2nd ed. ). Cambridge, MA: MIT Press.en_US
dc.identifier.citedreferenceBanker, G. A., & Waxman, A. B. ( 1988 ). Hippocampal neurons generate natural shapes in cell culture. In R. J. Lasek & M. M. Black (Eds.), Intrinsic determinants of neuronal form and function (pp. 61 – 82 ). New York: Alan R. Liss, Inc.en_US
dc.identifier.citedreferenceBarker, A. J., Koch, S. M., Reed, J., Barres, B. A., & Ullian, E. M. ( 2008 ). Developmental control of synaptic receptivity. Journal of Neuroscience, 28, 8150 – 8160.en_US
dc.identifier.citedreferenceBarnes, A. P., & Polleux, F. ( 2009 ). Establishment of axon‐dendrite polarity in developing neurons. Annual Review of Neuroscience, 32, 347 – 381.en_US
dc.identifier.citedreferenceBartlett, W. P., & Banker, G. A. ( 1984 ). An electron microscopic study of the development of axons and dendrites of hippocampal neurons in culture. II. Synaptic relationships. Journal of Neuroscience, 4 ( 8 ), 1954 – 1965.en_US
dc.identifier.citedreferenceBeckel‐Mitchener, A., & Greenough, W. T. ( 2004 ). Correlates across the structural, functional, and molecular phenotypes of fragile X syndrome. Mental Retardation and Developmental Disabilities Research Reviews, 10 ( 1 ), 53 – 59.en_US
dc.identifier.citedreferenceBenavides‐Piccione, R., Ballesteros‐Yanez, I., de Lagran, M. M., Elston, G., Estivill, X., Fillat, C., et al.( 2004 ). On dendrites in Down syndrome and DS murine models: A spiny way to learn. Progress in Neurobiology, 74 ( 2 ), 111 – 126.en_US
dc.identifier.citedreferenceBourne, J. N., & Harris, K. M. ( 2008 ). Balancing structure and function at hippocampal dendritic spines. Annual Review of Neuroscience, 31, 47 – 67.en_US
dc.identifier.citedreferenceBlack, J., Sirevaag, A., & Greenough, W. ( 1987 ). Complex experience promotes capillary formation in young rat visual cortex. Neuroscience Letters, 83, 351 – 355.en_US
dc.identifier.citedreferenceBrittis, P. A., Lemmon, V., Rutishauser, U., & Silver, J. ( 1995 ). Unique changes of ganglion cell growth cone behavior following cell adhesion molecule perturbations: A time‐lapse study of the living retina. Molecular and Cellular Neuroscience, 6 ( 5 ), 433 – 449.en_US
dc.identifier.citedreferenceBrittis, P. A., & Silver, J. ( 1995 ). Multiple factors govern intraretinal axon guidance: A time lapse study. Molecular and Cellular Neuroscience, 6, 413 – 432.en_US
dc.identifier.citedreferenceBushong, E. A., Martone, M. E., & Ellisman, M. H. ( 2004 ). Maturation of astroctye morphology and the establishment of astrocyte domains during postnatal hippocampal development. International Journal of Developmental Neuroscience, 22, 73 – 86.en_US
dc.identifier.citedreferenceChristie, S. B., & DeBlas, A. L. ( 2003 ). GABAergic and glutamatergic axons innervate the axon initial segment and organize GABA(A) receptor clusters of cultured hippocampal pyramidal cells. Journal of Comparative Neurology, 456 ( 4 ), 361 – 374.en_US
dc.identifier.citedreferenceChristopherson, K. S., Ullian, E. M., Stokes, C. C., Mullowney, C. E., Hell, J. W., Agah, A., et al.( 2005 ). Thrombospondins are astrocyte‐secreted proteins that promote CNS synaptogenesis. Cell, 120 ( 3 ), 421 – 433.en_US
dc.identifier.citedreferenceComery, T. A., Harris, J. B., Willems, P. J., Oostra, B. A., Irwin, S. A., Weiler, I. J., et al.( 1997 ). Abnormal dendritic spines in fragile X knockout mice: Maturation and pruning deficits. Proceedings of the National Academy of Sciences of the United States of America, 94, 5401 – 5405.en_US
dc.identifier.citedreferenceCraig, A., Blackstone, C., Huganir, R., & Banker, G. ( 1994 ). Selective clustering of glutamate and gamma‐aminobutyric acid receptors opposite terminals releasing the corresponding neurotransmitters. Proceedings of the National Academy of Sciences of the United States of America, 92, 12373 – 12377.en_US
dc.identifier.citedreferenceCraig, A., Graf, E., & Linhoff, M. ( 2006 ). How to build a central synapse: Clues from cell culture. Trends in Neuroscience, 29 ( 1 ), 8 – 20.en_US
dc.identifier.citedreferenceCraig, A. M., & Banker, G. ( 1994 ). Neuronal polarity. Annual Review Neuroscience, 17, 267 – 310.en_US
dc.identifier.citedreferenceDeitch, J. S., & Banker, G. A. ( 1993 ). An electron microscopic analysis of hippocampal neurons developing in culture: Early stages in the emergence of polarity. Journal of Neuroscience, 13 ( 10 ), 82 – 90.en_US
dc.identifier.citedreferenceDierssen, M., & Ramakers, G. J. A. ( 2006 ). Dendritic pathology in mental retardation: From molecular genetics to neurobiology. Genes Brain and Behavior, 5, 48 – 60.en_US
dc.identifier.citedreferenceDotti, C. G., Sullivan, C. A., & Banker, G. A. ( 1988 ). The establishment of polarity by hippocampal neurons in culture. Journal of Neuroscience, 8, 1454 – 1458.en_US
dc.identifier.citedreferenceEayrs, J. T., & Goodhead, B. ( 1959 ). Postnatal development of the cerebral cortex in the rat. Journal of Anatomy, 93, 385 – 402.en_US
dc.identifier.citedreferenceElmariah, S., Oh, E., Hughes, E., & Balice‐Gordon, R. ( 2005 ). Astrocytes regulate inhibitory synapse formation via Trk‐mediated modulation of postsynaptic GABA(A) receptors. Journal of Neuroscience, 25 ( 14 ), 3638 – 3650.en_US
dc.identifier.citedreferenceEroglu, C., & Barres, B. A. ( 2010 ). Regulation of synaptic connectivity by glia. Nature, 468 ( 7321 ), 223 – 231.en_US
dc.identifier.citedreferenceEsch, T., Lemmon, V., & Banker, G. ( 1999 ). Local presentation of substrate molecules directs axon specification by cultured hippocampal neurons. Journal of Neuroscience, 19 ( 15 ), 6417 – 6426.en_US
dc.identifier.citedreferenceFiala, J. C., Feinberg, M., Popov, V., & Harris, K. M. ( 1998 ). Synaptogenesis via dendritic filopodia in developing hippocampal area CA1. Journal of Neuroscience, 18, 8900 – 8911.en_US
dc.identifier.citedreferenceFletcher, T., Cameron, P., De Camilli, P., & Banker, G. ( 1991 ). The distribution of synapsin I and synaptophysin in hippocampal neurons developing in culture. Journal of Neuroscience, 11, 1617 – 1626.en_US
dc.identifier.citedreferenceFletcher, T., DeCamilli, P., & Banker, G. ( 1994 ). Synaptogenesis in hippocampal cultures: Evidence indicating the axons and dendrites become competent to form synapses at different stages of neuronal development. Journal of Neuroscience, 14 ( 11 ), 6695 – 6706.en_US
dc.identifier.citedreferenceGreenough, W., Black, J., & Wallace, C. ( 1987 ). Experience and brain development. Child Development, 58 ( 3 ), 539 – 559.en_US
dc.identifier.citedreferenceGreenough, W. T., Hwang, H. M., & Gorman, C. ( 1985 ). Evidence for active synapse formation or altered postsynaptic metabolism in visual cortex of rats reared in complex environments. Proceedings of the National Academy of Sciences of the United States of America, 82, 4549 – 4552.en_US
dc.identifier.citedreferenceGreenough, W., Withers, G. S., & Wallace, C. S. ( 1990 ). Morphological changes in the nervous system arising from behavioral experience: What is the evidence that they are involved in learning and memory? In L. R. Squire & E. Lindenlaub (Eds.), The biology of memory, symposia medica hoescht (Vol. 23, pp. 158 – 192 ) Stuttgart‐New York: F.K. Schattauder Verlag.en_US
dc.identifier.citedreferenceHirokawa, N. ( 2006 ). mRNA transport in dendrites: RNAgranules, motors, and tracks. Journal of Neuroscience, 26, 7139 – 7142.en_US
dc.identifier.citedreferenceHirokawa, N., & Takemura, R. ( 2005 ). Molecular motors and mechanisms of directional transport in neurons. Nature Reviews Neuroscience, 6 ( 3 ), 201 – 214.en_US
dc.identifier.citedreferenceHolmaat, A., & Svoboda, K. ( 2009 ). Experience‐dependent structural synaptic plasticity in the mammalian brain. Nature Reviews Neuroscience, 10, 647 – 659.en_US
dc.identifier.citedreferenceHuttenlocher, P. R. ( 1990 ). Morphometric study of human cerebral cortex development. Neuropsychologia, 28 ( 6 ), 517 – 527.en_US
dc.identifier.citedreferenceHuttenlocher, P. R. ( 1991 ). Dendritic and synaptic pathology in mental‐retardation. Pediatric Neurology, 7 ( 2 ), 79 – 85.en_US
dc.identifier.citedreferenceIrwin, S. A., Galvez, R., & Greenough, W. ( 2000 ). Dendritic spine structural anomalies in fragile‐X mental retardation syndrome. Cerebral Cortex, 10, 1038 – 1044.en_US
dc.identifier.citedreferenceJuraska, J. M., & Fifkova, E. ( 1979 ). A Golgi study of the early postnatal development of the visual cortex of the hooded rat. Journal of Comparative Neurology, 183, 247 – 256.en_US
dc.identifier.citedreferenceKollins, K. M., Bell, R. L., Butts, M., & Withers, G. S. ( 2009 ). Dendrites differ from axons in patterns of microtubule stability and polymerization during development. Neural Development, 4: 26.en_US
dc.identifier.citedreferenceLardi‐Studler, B., & Fritschy, J.‐M. ( 2007 ). Matching of pre‐and postsynaptic specializations during synaptogenesis. Neuroscientist, 13 ( 2 ), 115 – 126.en_US
dc.identifier.citedreferenceLi, Z., Okamoto, K.‐I., Hayashi, Y., & Sheng, M. ( 2004 ). The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell, 119, 873 – 887.en_US
dc.identifier.citedreferencePeng, Y. R., He, S., Marie, H., Zeng, S. Y., Ma, J., Tan, Z. J., et al.( 2009 ). Coordinated changes in dendritic arborization and synaptic strength during neural circuit development. Neuron, 61, 71 – 84.en_US
dc.identifier.citedreferencePolleux, F., Morrow, T., & Ghosh, A. ( 2000 ). Semaphorin 3A is a chemoattractant for cortical apical dendrites. Nature, 404, 567 – 573.en_US
dc.identifier.citedreferencePurpura, D. P. ( 1975 ). Dendritic differentiation in human cerebral cortex: Normal and aberrant developmental patterns. Advances in Neurology, 12, 91 – 134.en_US
dc.identifier.citedreferenceRodier, P. M. ( 1994 ). Vulnerable periods and processes during central nervous system development. Environmental Health Perspectives, 102, 121 – 124.en_US
dc.identifier.citedreferenceRose, J., Jin, S. X., & Craig, A. ( 2009 ). Heterosynaptic molecular dynamics: Locally induced propagating synaptic accumulation of CaM kinase II. Neuron, 12 ( 61 ), 351 – 358.en_US
dc.identifier.citedreferenceSanchez, A. L., Matthews, B. J., Meynard, M. M., Hu, B., Javed, S., & Cohen‐Cory, S. ( 2006 ). BDNF increases synapse density in dendritres of developing tectal neurons in vivo. Development, 133, 2477 – 2486.en_US
dc.identifier.citedreferenceSchuman, E. M., Dynes, J. L., & Steward, O. ( 2006 ). Synaptic regulation of translation of dendritic mRNAs. Journal of Neuroscience, 26, 7143 – 7146.en_US
dc.identifier.citedreferenceSebeo, J., Hsiao, K., Bozdagi, O., Dumitriu, D., Ge, Y., Zhou, Q., et al.( 2009 ). Requirement for protein synthesis at developing synapses. Journal of Neuroscience, 29 ( 31 ), 9778 – 9793.en_US
dc.identifier.citedreferenceShaw, P., Kabani, N. J., Lerch, J. P., Eckstrand, K., Lenroot, R., Gogtay, N., Greenstein, D., Clasen, L., Evans, A., Rapoport, J. L., Giedd, J. N., & Wise, S. P. ( 2008 ). Neurodevelopmental trajectories of the human cerebral cortex. Journal of Neuroscience, 28 ( 14 ), 3586 – 3594.en_US
dc.identifier.citedreferenceShi, P., Shen, K., & Kam, L. C. ( 2007 ). Local presentation of L1 and N‐cadherin in multicomponent, microscale patterns differentially direct neuron function in vitro. Journal of Neurobiology, 67 ( 13 ), 1765 – 1776.en_US
dc.identifier.citedreferenceSholl, D. A. ( 1956 ). Organization of the cerebral cortex. London: Methuen Press.en_US
dc.identifier.citedreferenceSirevaag, A., Black, J., Shafron, D., & Greenough, W. ( 1988 ). Direct evidence that complex experience increases capillary branching and surface area in visual cortex of young rats. Brain Research, 471, 299 – 304.en_US
dc.identifier.citedreferenceStevens, B. ( 2008 ). Neuron‐astrocyte signaling in the development and plasticity of neural circuits. Neurosignals, 16 ( 4 ), 278 – 288.en_US
dc.identifier.citedreferenceSteward, O. ( 1983a ). Alterations in polyribosomes associated with dendritic spines during the reinnervation of the dentate gyrus of the adult rat. Journal of Neuroscience, 3, 177 – 188.en_US
dc.identifier.citedreferenceSteward, O. ( 1983b ). Polyribosomes at the base of dendritic spines of central nervous system neurons—Their possible role in synapse construction and modification. Cold Spring Harbor Symposium on Quantitative Biology, 48, 745 – 759.en_US
dc.identifier.citedreferenceSvitkina, T., Lin, W. H., Webb, D. J., Yasuda, R., Wayman, G. A., Van Aelst, L., & Soderling, S. H. ( 2010 ). Regulation of the postsynaptic cytoskeleton: Roles in development, plasticity, and disorders. Journal of Neuroscience, 30 ( 45 ), 14937 – 14942.en_US
dc.identifier.citedreferenceSwanwick, C. C., Murthy, N. R., Mtchedlishvili, Z., Sieghart, W., & Kapur, J. ( 2006 ). Development of gamma‐aminobutyric acidergic synapses in cultured hippocampal neurons. Journal of Comparative Neurology, 495 ( 5 ), 497 – 510.en_US
dc.identifier.citedreferenceTurner, A., & Greenough, W. ( 1985 ). Differential rearing effects on rat visual cortex synapses. I. Synaptic and neuronal density and synapses per neuron. Brain Research, 329, 195 – 203.en_US
dc.identifier.citedreferenceVolkmar, F. R., & Greenough, W. ( 1972 ). Rearing complexity affects branching of dendrites in the visual cortex of the rat. Science, 176, 1445 – 1447.en_US
dc.identifier.citedreferenceWallace, C. S., Reitzenstein, J., & Withers, G. S. ( 2003 ). Diminished experidencedependent neuroanatomical plasiticy: Evidence for an improved biomarker of subtle neurotoxic damage to the developing rat brain. Environmental Health Perspectives, 111, 1294 – 1298.en_US
dc.identifier.citedreferenceWatson, R. E., DeSesso, J. M., Hurt, M. E., & Cappon, G. D. ( 2006 ). Postnatal growth and morphological development of the brain: A species comparison. Birth Defects Research (B), 77, 471 – 484.en_US
dc.identifier.citedreferenceWeiler, I. J., Irwin, S. A., Klintsova, A. Y., Spencer, C. M., Brazelton, A. D., Miyashiro, K., et al.( 1997 ). Fragile X mental retardation protein is translated near synapses in response to neurotransmitter activation. Proceedings of the National Academy of Sciences of the United States of America, 94, 5395 – 5400.en_US
dc.identifier.citedreferenceWeiler, I. J., Spangler, C. C., Klintsova, A. Y., Grossman, A. W., Kim, S. H., Bertaina‐Anglade, V., et al.( 2004 ). Fragile X mental retardation protein is necessary for neurotransmitter‐activated protein translation at synapses. Proceedings of the National Academy of Sciences of the United States of America, 101, 17504 – 17509.en_US
dc.identifier.citedreferenceWithers, G. S., & Banker, G. ( 1998 ). Characterizing and studying neuronal cultures. In G. Banker & K. Goslin (Eds.), Culturing nerve cells ( 2nd ed., pp. 113 – 151 ). Cambridge: MIT Press.en_US
dc.identifier.citedreferenceWithers, G. S., Higgins, D., Charette, M., & Banker, G. ( 2000 ). Bone morphogenetic protein‐7 enhances dendritic growth and receptivity to innervation in cultured hippocampal neurons. European Journal of Neuroscience, 12 ( 1 ), 106 – 116.en_US
dc.identifier.citedreferenceWithers, G. S., James, C. D., Kingman, C. E., Craighead, H. G., & Banker, G. A. ( 2006 ). Effects of substrate geometry on growth cone behavior and axon branching. Journal of Neurobiology, 66, 1183 – 1194.en_US
dc.identifier.citedreferenceWithers, G. S., Lambruschi, L., Brown, L., & Wallace, C. S. ( 2008 ). The absence of glia leads to increased dendritic growth in cultured hippocampal neurons. Society for Neuroscience Annual Meeting Abstracts, 524, 517.en_US
dc.identifier.citedreferenceZhang, W., & Benson, D. L. ( 2002 ). Developmentally regulated changes in cellular compartmentation and synaptic distribution of actin in hippocampal neurons. Journal of Neuroscience Research, 69 ( 4 ), 427 – 436.en_US
dc.identifier.citedreferenceZiv, N. E., & Smith, S. J. ( 1996 ). Evidence for a role of dendritic filopodia in synaptogenesis and spine formation. Neuron, 17 ( 1 ), 91 – 102.en_US
dc.owningcollnameInterdisciplinary and Peer-Reviewed


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