Biological pathways to adaptability - interactions between genome, epigenome, nervous system and environment for adaptive behavior

Genes, Brain and Behavior

Volumn 11, Issue 1, 2012, Pages 3-28

  Wolf, C ^a   Linden, D E J ^b  

^a UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^b CARDIFF UNIVERSITY SCHOOL OF MEDICINE   (United Kingdom)

Author keywords

Adaptability; Cognition; Imaging; Immediate early genes; Neuron; Plasticity; Regulation; Transcription factors

Indexed keywords

ACTIVITY REGULATED CYTOSKELETON ASSOCIATED PROTEIN; CALCINEURIN; CALCIUM ION; CALMODULIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DNA; F ACTIN; GROWTH FACTOR; METHYL CPG BINDING PROTEIN 2; MICRORNA; MYOCYTE ENHANCER FACTOR 2; NUCLEAR RECEPTOR NUR77; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PROTEIN C FOS; PROTEIN HOMER 1B; PROTEOME; RNA; RNA BINDING PROTEIN; SYNAPSIN I; SYNAPSIN II; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ELK 1; TRANSCRIPTION FACTOR NFAT; TRANSCRIPTOME;

ADAPTATION; ADAPTIVE BEHAVIOR; BEHAVIOR; BRAIN; BRAIN FUNCTION; DNA SEQUENCE; ENVIRONMENT; EPIGENETICS; GENE CONTROL; GENE INTERACTION; GENOME; HUMAN; INTRACELLULAR SIGNALING; NERVE CELL; NERVE CELL PLASTICITY; NERVOUS SYSTEM; NEUROPHYSIOLOGY; PRIORITY JOURNAL; RETROPOSON; REVIEW; SIGNAL TRANSDUCTION; TRANSPOSON;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CENTRAL NERVOUS SYSTEM; EPIGENESIS, GENETIC; GENE-ENVIRONMENT INTERACTION; GENOME; HUMANS; NEURONAL PLASTICITY; NEURONS;

ANIMALIA;

EID: 84855748513     PISSN: 16011848     EISSN: 1601183X     Source Type: Journal    
DOI: 10.1111/j.1601-183X.2011.00752.x     Document Type: Review

References (300)

1. Adams, J. & Sweatt, J. (2002) Molecular psychology: roles for the ERK MAP kinase cascade in memory. Annu Rev Pharmacol Toxicol 42, 135-163.
2. Alarcon, J.M., Malleret, G., Touzani, K., Vronskaya, S., Ishii, S., Kandel, E.R. & Barco, A. (2004) Chromatin acetylation, memory, and LTP are impaired in CBP+/- mice: a model for the cognitive deficit in Rubinstein-Taybi syndrome and its amelioration. Neuron 42, 947-959.
3. Allen, E., Horvath, S., Tong, F., Kraft, P., Spiteri, E., Riggs, A.D. & Marahrens, Y. (2003) High concentrations of long interspersed nuclear element sequence distinguish monoallelically expressed genes. Proc Natl Acad Sci U S A 100, 9940-9945.
4. Alt, S.R., Turner, J.D., Klok, M.D., Meijer, O.C., Lakke, E.A., Derijk, R.H. & Muller, C.P. (2010) Differential expression of glucocorticoid receptor transcripts in major depressive disorder is not epigenetically programmed. Psychoneuroendocrinology 35, 544-556.
5. An, J., Gharami, K., Liao, G., Woo, N., Lau, A., Vanevski, F., Torre, E., Jones, K., Feng, Y., Lu, B. & Xu, B. (2008) Distinct role of long 3' UTR BDNF mRNA in spine morphology and synaptic plasticity in hippocampal neurons. Cell 134, 175-187.
6. Ando, J., Ono, Y. & Wright, M.J. (2001) Genetic structure of spatial and verbal working memory. Behav Genet 31, 615-624.
7. Babushok, D.V. & Kazazian, H.H. Jr. (2007) Progress in understanding the biology of the human mutagen LINE-1. Hum Mutat 28, 527-539.
8. Bailey, J.A., Carrel, L., Chakravarti, A. & Eichler, E.E. (2000) Molecular evidence for a relationship between LINE-1 elements and X chromosome inactivation: the Lyon repeat hypothesis. Proc Natl Acad Sci U S A 97, 6634-6639.
9. Bailey, C.H. & Chen, M. (1983) Morphological basis of long-term habituation and sensitization in Aplysia. Science 220, 91-93.
10. Barbosa, A.C., Kim, M.S., Ertunc, M., Adachi, M., Nelson, E.D., McAnally, J., Richardson, J.A., Kavalali, E.T., Monteggia, L.M., Bassel-Duby, R. & Olson, E.N. (2008) MEF2C, a transcription factor that facilitates learning and memory by negative regulation of synapse numbers and function. Proc Natl Acad Sci U S A 105, 9391-9396.
11. Barco, A., Alarcon, J. & Kandel, E. (2002) Expression of constitutively active CREB protein facilitates the late phase of long-term potentiation by enhancing synaptic capture. Cell 108, 689-703.
12. Barria, A., Muller, D., Derkach, V., Griffith, L.C. & Soderling, T.R. (1997) Regulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation. Science 276, 2042-2045.
13. Barrot, M., Olivier, J., Perrotti, L., DiLeone, R., Berton, O., Eisch, A., Impey, S., Storm, D., Neve, R., Yin, J., Zachariou, V. & Nestler, E. (2002) CREB activity in the nucleus accumbens shell controls gating of behavioral responses to emotional stimuli. Proc Natl Acad Sci U S A 99, 11435-11440.
14. Barrot, M., Wallace, D., Bolaños, C., Graham, D., Perrotti, L., Neve, R., Chambliss, H., Yin, J. & Nestler, E. (2005) Regulation of anxiety and initiation of sexual behavior by CREB in the nucleus accumbens. Proc Natl Acad Sci U S A 102, 8357-8362.
15. Barth, A. (2007) Visualizing circuits and systems using transgenic reporters of neural activity. Curr Opin Neurobiol 17, 567-571.
16. Barth, T.K. & Imhof, A. (2010) Fast signals and slow marks: the dynamics of histone modifications. Trends Biochem Sci 35, 618-626.
17. Bayer, K.U., LeBel, E., McDonald, G.L., O'Leary, H., Schulman, H. & De Koninck, P. (2006) Transition from reversible to persistent binding of CaMKII to postsynaptic sites and NR2B. J Neurosci 26, 1164-1174.
18. Benito, E. & Barco, A. (2010) CREB's control of intrinsic and synaptic plasticity: implications for CREB-dependent memory models. Trends Neurosci 33, 230-240.
19. Bingol, B., Wang, C.F., Arnott, D., Cheng, D., Peng, J. & Sheng, M. (2010) Autophosphorylated CaMKIIalpha acts as a scaffold to recruit proteasomes to dendritic spines. Cell 140, 567-578.
20. Blokland, G., McMahon, K., Hoffman, J., Zhu, G., Meredith, M., Martin, N., Thompson, P., de Zubicaray, G. & Wright, M. (2008) Quantifying the heritability of task-related brain activation and performance during the N-back working memory task: A twin fMRI study. Biol Psychol 79, 70-79.
21. Bock, C., Walter, J., Paulsen, M. & Lengauer, T. (2008) Inter-individual variation of DNA methylation and its implications for large-scale epigenome mapping. Nucleic Acids Res 36, e55.
22. Bolger, T.A. & Yao, T.P. (2005) Intracellular trafficking of histone deacetylase 4 regulates neuronal cell death. J Neurosci 25, 9544-9553.
23. Borrelli, E., Nestler, E.J., Allis, C.D. & Sassone-Corsi, P. (2008) Decoding the epigenetic language of neuronal plasticity. Neuron 60, 961-974.
24. Bourtchuladze, R., Frenguelli, B., Blendy, J., Cioffi, D., Schutz, G. & Silva, A.J. (1994) Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein. Cell 79, 59-68.
25. Bradshaw, K.D., Emptage, N.J. & Bliss, T.V. (2003) A role for dendritic protein synthesis in hippocampal late LTP. Eur J Neurosci 18, 3150-3152.
26. Brakeman, P.R., Lanahan, A.A., O'Brien, R., Roche, K., Barnes, C.A., Huganir, R.L. & Worley, P.F. (1997) Homer: a protein that selectively binds metabotropic glutamate receptors. Nature 386, 284-288.
27. Bramham, C.R., Alme, M.N., Bittins, M., Kuipers, S.D., Nair, R.R., Pai, B., Panja, D., Schubert, M., Soule, J., Tiron, A. & Wibrand, K. (2010) The Arc of synaptic memory. Exp Brain Res 200, 125-140.
28. Bredy, T.W., Wu, H., Crego, C., Zellhoefer, J., Sun, Y.E. & Barad, M. (2007) Histone modifications around individual BDNF gene promoters in prefrontal cortex are associated with extinction of conditioned fear. Learn Mem 14, 268-276.
29. Brennecke, J., Malone, C.D., Aravin, A.A., Sachidanandam, R., Stark, A. & Hannon, G.J. (2008) An epigenetic role for maternally inherited piRNAs in transposon silencing. Science 322, 1387-1392.
30. Brunmeir, R., Lagger, S., Simboeck, E., Sawicka, A., Egger, G., Hagelkruys, A., Zhang, Y., Matthias, P., Miller, W.J. & Seiser, C. (2010) Epigenetic regulation of a murine retrotransposon by a dual histone modification mark. PLoS Genet 6, e1000927.
31. Buzdin, A., Ustyugova, S., Gogvadze, E., Vinogradova, T., Lebedev, Y. & Sverdlov, E. (2002) A new family of chimeric retrotranscripts formed by a full copy of U6 small nuclear RNA fused to the 3' terminus of l1. Genomics 80, 402-406.
32. Canestro, C., Yokoi, H. & Postlethwait, J.H. (2007) Evolutionary developmental biology and genomics. Nat Rev Genet 8, 932-942.
33. Carlezon, W.J., Duman, R. & Nestler, E. (2005) The many faces of CREB. Trends Neurosci 28, 436-445.
34. Cha-Molstad, H., Keller, D.M., Yochum, G.S., Impey, S. & Goodman, R.H. (2004) Cell-type-specific binding of the transcription factor CREB to the cAMP-response element. Proc Natl Acad Sci U S A 101, 13572-13577.
35. Chahwan, R., Wontakal, S.N. & Roa, S. (2010) Crosstalk between genetic and epigenetic information through cytosine deamination. Trends Genet 26, 443-448.
36. Champagne, F.A. (2008) Epigenetic mechanisms and the transgenerational effects of maternal care. Front Neuroendocrinol 29, 386-397.
37. Chao, L.H., Stratton, M.M., Lee, I.H., Rosenberg, O.S., Levitz, J., Mandell, D.J., Kortemme, T., Groves, J.T., Schulman, H. & Kuriyan, J. (2011) A mechanism for tunable autoinhibition in the structure of a human Ca(2+)/calmodulin- dependent kinase II holoenzyme. Cell 146, 732-745.
38. Chaudhuri, A., Nissanov, J., Larocque, S. & Rioux, L. (1997) Dual activity maps in primate visual cortex produced by different temporal patterns of zif268 mRNA and protein expression. Proc Natl Acad Sci U S A 94, 2671-2675.
39. Chin, D. & Means, A.R. (2002) Mechanisms for regulation of calmodulin kinase IIalpha by Ca(2+)/calmodulin and autophosphorylation of threonine 286. Biochemistry 41, 14001-14009.
40. Chow, J.C., Ciaudo, C., Fazzari, M.J., Mise, N., Servant, N., Glass, J.L., Attreed, M., Avner, P., Wutz, A., Barillot, E., Greally, J.M., Voinnet, O. & Heard, E. (2010) LINE-1 activity in facultative heterochromatin formation during X chromosome inactivation. Cell 141, 956-969.
41. Chow, J. & Heard, E. (2009) X inactivation and the complexities of silencing a sex chromosome. Curr Opin Cell Biol 21, 359-366.
42. Chowdhury, S., Shepherd, J., Okuno, H., Lyford, G., Petralia, R., Plath, N., Kuhl, D., Huganir, R. & Worley, P. (2006) Arc/Arg3.1 interacts with the endocytic machinery to regulate AMPA receptor trafficking. Neuron 52, 445-459.
43. Church, D.M., Goodstadt, L., Hillier, L.W., Zody, M.C., Goldstein, S., She, X., Bult, C.J., Agarwala, R., Cherry, J.L., DiCuccio, M., Hlavina, W., Kapustin, Y., Meric, P., Maglott, D., Birtle, Z., Marques, A.C., Graves, T., Zhou, S., Teague, B., Potamousis, K., Churas, C., Place, M., Herschleb, J., Runnheim, R., Forrest, D., Amos-Landgraf, J., Schwartz, D.C., Cheng, Z., Lindblad-Toh, K., Eichler, E.E. & Ponting, C.P. (2009) Lineage-specific biology revealed by a finished genome assembly of the mouse. PLoS Biol 7, e1000112.
44. Chwang, W.B., O'Riordan, K.J., Levenson, J.M. & Sweatt, J.D. (2006) ERK/MAPK regulates hippocampal histone phosphorylation following contextual fear conditioning. Learn Mem 13, 322-328.
45. Citri, A. & Malenka, R.C. (2008) Synaptic plasticity: multiple forms, functions, and mechanisms. Neuropsychopharmacology 33, 18-41.
46. Cohen, S. & Greenberg, M. (2008) Communication between the synapse and the nucleus in neuronal development, plasticity, and disease. Annu Rev Cell Dev Biol 24, 183-209.
47. Cole, A.J., Saffen, D.W., Baraban, J.M. & Worley, P.F. (1989) Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation. Nature 340, 474-476.
48. Collins, L.J. & Penny, D. (2009) The RNA infrastructure: dark matter of the eukaryotic cell? Trends Genet 25, 120-128.
49. Conkright, M.D., Canettieri, G., Screaton, R., Guzman, E., Miraglia, L., Hogenesch, J.B. & Montminy, M. (2003) TORCs: transducers of regulated CREB activity. Mol Cells 12, 413-423.
50. Cordaux, R. & Batzer, M.A. (2009) The impact of retrotransposons on human genome evolution. Nat Rev Genet 10, 691-703.
51. Costa, F. (2007) Non-coding RNAs: lost in translation? Gene 386, 1-10.
52. Cubas, P., Vincent, C. & Coen, E. (1999) An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401, 157-161.
53. de Foubert, G., O'Neill, M.J. & Zetterstrom, T.S. (2007) Acute onset by 5-HT(6)-receptor activation on rat brain brain-derived neurotrophic factor and activity-regulated cytoskeletal-associated protein mRNA expression. Neuroscience 147, 778-785.
54. de Quervain, D.J. & Papassotiropoulos, A. (2006) Identification of a genetic cluster influencing memory performance and hippocampal activity in humans. Proc Natl Acad Sci U S A 103, 4270-4274.
55. De Santa, F., Totaro, M.G., Prosperini, E., Notarbartolo, S., Testa, G. & Natoli, G. (2007) The histone H3 lysine-27 demethylase Jmjd3 links inflammation to inhibition of polycomb-mediated gene silencing. Cell 130, 1083-1094.
56. Deisseroth, K. (2011) Optogenetics. Nat Methods 8, 26-29.
57. Dewannieux, M., Esnault, C. & Heidmann, T. (2003) LINE-mediated retrotransposition of marked Alu sequences. Nat Genet 35, 41-48.
58. Di Noia, J.M. & Neuberger, M.S. (2007) Molecular mechanisms of antibody somatic hypermutation. Annu Rev Biochem 76, 1-22.
59. Dinieri, J.A., Nemeth, C.L., Parsegian, A., Carle, T., Gurevich, V.V., Gurevich, E., Neve, R.L., Nestler, E.J. & Carlezon, W.A. Jr. (2009) Altered sensitivity to rewarding and aversive drugs in mice with inducible disruption of cAMP response element-binding protein function within the nucleus accumbens. J Neurosci 29, 1855-1859.
60. Donai, H., Sugiura, H., Ara, D., Yoshimura, Y., Yamagata, K. & Yamauchi, T. (2003) Interaction of Arc with CaM kinase II and stimulation of neurite extension by Arc in neuroblastoma cells expressing CaM kinase II. Neurosci Res 47, 399-408.
61. Dong, Y., Green, T., Saal, D., Marie, H., Neve, R., Nestler, E. & Malenka, R. (2006) CREB modulates excitability of nucleus accumbens neurons. Nat Neurosci 9, 475-477.
62. Dragunow, M., Tse, C., Glass, M. & Lawlor, P. (1994) c-fos antisense reduces expression of Krox 24 in rat caudate and neocortex. Cell Mol Neurobiol 14, 395-405.
63. Dudai, Y. (2004) The neurobiology of consolidations, or, how stable is the engram? Annu Rev Psychol 55, 51-86.
64. Dwivedi, Y., Rao, J., Rizavi, H., Kotowski, J., Conley, R., Roberts, R., Tamminga, C. & Pandey, G. (2003) Abnormal expression and functional characteristics of cyclic adenosine monophosphate response element binding protein in postmortem brain of suicide subjects. Arch Gen Psychiatry 60, 273-282.
65. Egan, M., Kojima, M., Callicott, J., Goldberg, T., Kolachana, B., Bertolino, A., Zaitsev, E., Gold, B., Goldman, D., Dean, M., Lu, B. & Weinberger, D. (2003) The BDNF val66met polymorphism affects activity-dependent secretion of BDNF and human memory and hippocampal function. Cell 112, 257-269.
66. Emes, R.D., Pocklington, A.J., Anderson, C.N., Bayes, A., Collins, M.O., Vickers, C.A., Croning, M.D., Malik, B.R., Choudhary, J.S., Armstrong, J.D. & Grant, S.G. (2008) Evolutionary expansion and anatomical specialization of synapse proteome complexity. Nat Neurosci 11, 799-806.
67. Enslen, H. & Soderling, T.R. (1994) Roles of calmodulin-dependent protein kinases and phosphatase in calcium-dependent transcription of immediate early genes. J Biol Chem 269, 20872-20877.
68. Enslen, H., Sun, P., Brickey, D., Soderling, S.H., Klamo, E. & Soderling, T.R. (1994) Characterization of Ca2+/calmodulin-dependent protein kinase IV. Role in transcriptional regulation. J Biol Chem 269, 15520-15527.
69. Eriksson, T.M., Delagrange, P., Spedding, M., Popoli, M., Mathe, A.A., Ogren, S.O. & Svenningsson, P. (2011) Emotional memory impairments in a genetic rat model of depression: involvement of 5-HT/MEK/Arc signaling in restoration. Mol Psychiatry; doi:10.1038/mp.2010.131.
70. Esnault, C., Maestre, J. & Heidmann, T. (2000) Human LINE retrotransposons generate processed pseudogenes. Nat Genet 24, 363-367.
71. Estecio, M.R., Gallegos, J., Vallot, C., Castoro, R.J., Chung, W., Maegawa, S., Oki, Y., Kondo, Y., Jelinek, J., Shen, L., Hartung, H., Aplan, P.D., Czerniak, B.A., Liang, S. & Issa, J.P. (2010) Genome architecture marked by retrotransposons modulates predisposition to DNA methylation in cancer. Genome Res 20, 1369-1382.
72. Ewing, A.D. & Kazazian, H.H. Jr. (2010) High-throughput sequencing reveals extensive variation in human-specific L1 content in individual human genomes. Genome Res 20, 1262-1270.
73. Farkash, E.A. & Luning Prak, E.T. (2006) DNA damage and L1 retrotransposition. J Biomed Biotechnol 2006, 37285.
74. Feng, J., Zhou, Y., Campbell, S.L., Le, T., Li, E., Sweatt, J.D., Silva, A.J. & Fan, G. (2010) Dnmt1 and Dnmt3a maintain DNA methylation and regulate synaptic function in adult forebrain neurons. Nat Neurosci 13, 423-430.
75. Fiore, R., Khudayberdiev, S., Christensen, M., Siegel, G., Flavell, S.W., Kim, T.K., Greenberg, M.E. & Schratt, G. (2009) Mef2-mediated transcription of the miR379-410 cluster regulates activity-dependent dendritogenesis by fine-tuning Pumilio2 protein levels. EMBO J 28, 697-710.
76. Fischer, A., Sananbenesi, F., Wang, X., Dobbin, M. & Tsai, L.H. (2007) Recovery of learning and memory is associated with chromatin remodelling. Nature 447, 178-182.
77. Fish, E., Shahrokh, D., Bagot, R., Caldji, C., Bredy, T., Szyf, M. & Meaney, M. (2004) Epigenetic programming of stress responses through variations in maternal care. Ann N Y Acad Sci 1036, 167-180.
78. Flavell, S., Cowan, C., Kim, T., Greer, P., Lin, Y., Paradis, S., Griffith, E., Hu, L., Chen, C. & Greenberg, M. (2006) Activity-dependent regulation of MEF2 transcription factors suppresses excitatory synapse number. Science 311, 1008-1012.
79. Flavell, S. & Greenberg, M. (2008) Signaling mechanisms linking neuronal activity to gene expression and plasticity of the nervous system. Annu Rev Neurosci 31, 563-590.
80. Fonseca, R., Nägerl, U. & Bonhoeffer, T. (2006) Neuronal activity determines the protein synthesis dependence of long-term potentiation. Nat Neurosci 9, 478-480.
81. Foster, P.L. & Trimarchi, J.M. (1995) Adaptive reversion of an episomal frameshift mutation in Escherichia coli requires conjugal functions but not actual conjugation. Proc Natl Acad Sci U S A 92, 5487-5490.
82. Fraga, M.F., Ballestar, E., Paz, M.F., Ropero, S., Setien, F., Ballestar, M.L., Heine-Suner, D., Cigudosa, J.C., Urioste, M., Benitez, J., Boix-Chornet, M., Sanchez-Aguilera, A., Ling, C., Carlsson, E., Poulsen, P., Vaag, A., Stephan, Z., Spector, T.D., Wu, Y.Z., Plass, C. & Esteller, M. (2005) Epigenetic differences arise during the lifetime of monozygotic twins. Proc Natl Acad Sci U S A 102, 10604-10609.
83. Gao, J., Wang, W.Y., Mao, Y.W., Graff, J., Guan, J.S., Pan, L., Mak, G., Kim, D., Su, S.C. & Tsai, L.H. (2010) A novel pathway regulates memory and plasticity via SIRT1 and miR-134. Nature 466, 1105-1109.
84. Garcia-Perez, J.L., Doucet, A.J., Bucheton, A., Moran, J.V. & Gilbert, N. (2007) Distinct mechanisms for trans-mediated mobilization of cellular RNAs by the LINE-1 reverse transcriptase. Genome Res 17, 602-611.
85. Geiger, J.R., Melcher, T., Koh, D.S., Sakmann, B., Seeburg, P.H., Jonas, P. & Monyer, H. (1995) Relative abundance of subunit mRNAs determines gating and Ca2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron 15, 193-204.
86. Georgi, A., Jamra, R.A., Klein, K., Villela, A.W., Schumacher, J., Becker, T., Paul, T., Schmael, C., Hofels, S., Klopp, N., Illig, T., Propping, P., Cichon, S., Nothen, M.M., Schulze, T.G. & Rietschel, M. (2007) Possible association between genetic variants at the GRIN1 gene and schizophrenia with lifetime history of depressive symptoms in a German sample. Psychiatr Genet 17, 308-310.
87. Gibney, E.R. & Nolan, C.M. (2010) Epigenetics and gene expression. Heredity 105, 4-13.
88. Girotti, M., Pace, T.W., Gaylord, R.I., Rubin, B.A., Herman, J.P. & Spencer, R.L. (2006) Habituation to repeated restraint stress is associated with lack of stress-induced c-fos expression in primary sensory processing areas of the rat brain. Neuroscience 138, 1067-1081.
89. Gius, D., Cao, X., Rauscher, F.r., Cohen, D., Curran, T. & Sukhatme, V. (1990) Transcriptional activation and repression by Fos are independent functions: the C terminus represses immediate-early gene expression via CArG elements. Mol Cell Biol 10, 4243-4255.
90. Glahn, D.C., Thompson, P.M. & Blangero, J. (2007) Neuroimaging endophenotypes: strategies for finding genes influencing brain structure and function. Hum Brain Mapp 28, 488-501.
91. Goldberg, T. & Weinberger, D. (2004) Genes and the parsing of cognitive processes. Trends Cogn Sci 8, 325-335.
92. Goodier, J.L., Ostertag, E.M. & Kazazian, H.H. Jr. (2000) Transduction of 3'-flanking sequences is common in L1 retrotransposition. Hum Mol Genet 9, 653-657.
93. Gosso, M.F., de Geus, E.J., Polderman, T.J., Boomsma, D.I., Heutink, P. & Posthuma, D. (2008) Common variants underlying cognitive ability: further evidence for association between the SNAP-25 gene and cognition using a family-based study in two independent Dutch cohorts. Genes Brain Behav 7, 355-364.
94. Graham, T. & Boissinot, S. (2006) The genomic distribution of L1 elements: the role of insertion bias and natural selection. J Biomed Biotechnol 2006, 75327.
95. Greer, P. & Greenberg, M. (2008) From synapse to nucleus: calcium-dependent gene transcription in the control of synapse development and function. Neuron 59, 846-860.
96. Greer, P.L., Hanayama, R., Bloodgood, B.L., Mardinly, A.R., Lipton, D.M., Flavell, S.W., Kim, T.K., Griffith, E.C., Waldon, Z., Maehr, R., Ploegh, H.L., Chowdhury, S., Worley, P.F., Steen, J. & Greenberg, M.E. (2010) The Angelman Syndrome protein Ube3A regulates synapse development by ubiquitinating arc. Cell 140, 704-716.
97. Gu, Z., Liu, W. & Yan, Z. (2009) beta-Amyloid impairs AMPA receptor trafficking and function by reducing Ca2+/calmodulin-dependent protein kinase II synaptic distribution. J Biol Chem 284, 10639-10649.
98. Guo, J.U., Su, Y., Zhong, C., Ming, G.L. & Song, H. (2011) Hydroxylation of 5-methylcytosine by TET1 promotes active DNA demethylation in the adult brain. Cell 145, 423-434.
99. Guzowski, J., McNaughton, B., Barnes, C. & Worley, P. (1999) Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal ensembles. Nat Neurosci 2, 1120-1124.
100. Guzowski, J.F., Setlow, B., Wagner, E.K. & McGaugh, J.L. (2001) Experience-dependent gene expression in the rat hippocampus after spatial learning: a comparison of the immediate-early genes Arc, c-fos, and zif268. J Neurosci 21, 5089-5098.
101. Hall, B.G. (1999) Transposable elements as activators of cryptic genes in E. coli. Genetica 107, 181-187.
102. Hamilton, C.E., Papavasiliou, F.N. & Rosenberg, B.R. (2010) Diverse functions for DNA and RNA editing in the immune system. RNA Biol 7, 220-228.
103. Hammock, E.A., Lim, M.M., Nair, H.P. & Young, L.J. (2005) Association of vasopressin 1a receptor levels with a regulatory microsatellite and behavior. Genes Brain Behav 4, 289-301.
104. Hebert, S.S. & De Strooper, B. (2009) Alterations of the microRNA network cause neurodegenerative disease. Trends Neurosci 32, 199-206.
105. Hemberger, M., Dean, W. & Reik, W. (2009) Epigenetic dynamics of stem cells and cell lineage commitment: digging Waddington's canal. Nat Rev Mol Cell Biol 10, 526-537.
106. Hirabayashi, Y. & Gotoh, Y. (2010) Epigenetic control of neural precursor cell fate during development. Nat Rev Neurosci 11, 377-388.
107. Hong, E.J., McCord, A.E. & Greenberg, M.E. (2008) A biological function for the neuronal activity-dependent component of Bdnf transcription in the development of cortical inhibition. Neuron 60, 610-624.
108. Hotte, M., Thuault, S., Lachaise, F., Dineley, K.T., Hemmings, H.C., Nairn, A.C. & Jay, T.M. (2006) D1 receptor modulation of memory retrieval performance is associated with changes in pCREB and pDARPP-32 in rat prefrontal cortex. Behav Brain Res 171, 127-133.
109. Huber, K.M., Kayser, M.S. & Bear, M.F. (2000) Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. Science 288, 1254-1257.
110. Hurles, M., Dermitzakis, E. & Tyler-Smith, C. (2008) The functional impact of structural variation in humans. Trends Genet 24, 238-245.
111. Iizuka, Y., Sei, Y., Weinberger, D. & Straub, R. (2007) Evidence that the BLOC-1 protein dysbindin modulates dopamine D2 receptor internalization and signaling but not D1 internalization. J Neurosci 27, 12390-12395.
112. Inagaki, N., Nishizawa, M., Arimura, N., Yamamoto, H., Takeuchi, Y., Miyamoto, E., Kaibuchi, K. & Inagaki, M. (2000) Activation of Ca2+/calmodulin-dependent protein kinase II within post-synaptic dendritic spines of cultured hippocampal neurons. J Biol Chem 275, 27165-27171.
113. Jaenisch, R. & Bird, A. (2003) Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 33 (Suppl.), 245-254.
114. Johannessen, M., Delghandi, M.P. & Moens, U. (2004) What turns CREB on? Cell Signal 16, 1211-1227.
115. Johnson, L.J. & Tricker, P.J. (2010) Epigenomic plasticity within populations: its evolutionary significance and potential. Heredity 105, 113-121.
116. Kaati, G., Bygren, L.O., Pembrey, M. & Sjostrom, M. (2007) Transgenerational response to nutrition, early life circumstances and longevity. Eur J Hum Genet 15, 784-790.
117. Kang, H. & Schuman, E.M. (1996) A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity. Science 273, 1402-1406.
118. Kano, H., Godoy, I., Courtney, C., Vetter, M.R., Gerton, G.L., Ostertag, E.M. & Kazazian, H.H. Jr. (2009) L1 retrotransposition occurs mainly in embryogenesis and creates somatic mosaicism. Genes Dev 23, 1303-1312.
119. Kawanishi, Y., Harada, S., Tachikawa, H., Okubo, T. & Shiraishi, H. (1999) Novel variants in the promoter region of the CREB gene in schizophrenic patients. J Hum Genet 44, 428-430.
120. Kawashima, T., Okuno, H., Nonaka, M., Adachi-Morishima, A., Kyo, N., Okamura, M., Takemoto-Kimura, S., Worley, P.F. & Bito, H. (2009) Synaptic activity-responsive element in the Arc/Arg3.1 promoter essential for synapse-to-nucleus signaling in activated neurons. Proc Natl Acad Sci U S A 106, 316-321.
121. Kazazian, H.H. Jr. (2004) Mobile elements: drivers of genome evolution. Science 303, 1626-1632.
122. Kazazian, H.H. Jr. & Goodier, J.L. (2002) LINE drive. retrotransposition and genome instability. Cell 110, 277-280.
123. Kelleher, R.J. III, Govindarajan, A. & Tonegawa, S. (2004) Translational regulatory mechanisms in persistent forms of synaptic plasticity. Neuron 44, 59-73.
124. Kelley, J. & Swanson, W. (2008) Positive selection in the human genome: from genome scans to biological significance. Annu Rev Genomics Hum Genet 9, 143-160.
125. Kim, S.M., Ahn, S.M., Go, B.S., Wang, J.Q. & Choe, E.S. (2009) Alterations in AMPA receptor phosphorylation in the rat striatum following acute and repeated cocaine administration. Neuroscience 163, 618-626.
126. Kim, A.H., Reimers, M., Maher, B., Williamson, V., McMichael, O., McClay, J.L., van den Oord, E.J., Riley, B.P., Kendler, K.S. & Vladimirov, V.I. (2010a) MicroRNA expression profiling in the prefrontal cortex of individuals affected with schizophrenia and bipolar disorders. Schizophr Res 124, 183-191.
127. Kim, T.K., Hemberg, M., Gray, J.M., Costa, A.M., Bear, D.M., Wu, J., Harmin, D.A., Laptewicz, M., Barbara-Haley, K., Kuersten, S., Markenscoff-Papadimitriou, E., Kuhl, D., Bito, H., Worley, P.F., Kreiman, G. & Greenberg, M.E. (2010b) Widespread transcription at neuronal activity-regulated enhancers. Nature 465, 182-187.
128. Klein, M., Impey, S. & Goodman, R. (2005) Role reversal: the regulation of neuronal gene expression by microRNAs. Curr Opin Neurobiol 15, 507-513.
129. Knapska, E. & Kaczmarek, L. (2004) A gene for neuronal plasticity in the mammalian brain: Zif268/Egr-1/NGFI-A/Krox-24/TIS8/ZENK? Prog Neurobiol 74, 183-211.
130. Koch, L.G. & Britton, S.L. (2008) Aerobic metabolism underlies complexity and capacity. J Physiol 586, 83-95.
131. Kogan, J.H., Frankland, P.W. & Silva, A.J. (2000) Long-term memory underlying hippocampus-dependent social recognition in mice. Hippocampus 10, 47-56.
132. Kosik, K. (2006) The neuronal microRNA system. Nat Rev Neurosci 7, 911-920.
133. Kozlovsky, N., Matar, M.A., Kaplan, Z., Kotler, M., Zohar, J. & Cohen, H. (2008) The immediate early gene Arc is associated with behavioral resilience to stress exposure in an animal model of posttraumatic stress disorder. Eur Neuropsychopharmacol 18, 107-116.
134. Krol, J., Busskamp, V., Markiewicz, I., Stadler, M.B., Ribi, S., Richter, J., Duebel, J., Bicker, S., Fehling, H.J., Schubeler, D., Oertner, T.G., Schratt, G., Bibel, M., Roska, B. & Filipowicz, W. (2010) Characterizing light-regulated retinal microRNAs reveals rapid turnover as a common property of neuronal microRNAs. Cell 141, 618-631.
135. Lam, B.Y., Zhang, W., Ng, D.C., Maruthappu, M., Roderick, H.L. & Chawla, S. (2009) CREB-dependent Nur77 induction following depolarization in PC12 cells and neurons is modulated by MEF2 transcription factors. J Neurochem 112, 1065-1073.
136. Lamsa, K., Irvine, E., Giese, K. & Kullmann, D. (2007) NMDA receptor-dependent long-term potentiation in mouse hippocampal interneurons shows a unique dependence on Ca(2+)/calmodulin-dependent kinases. J Physiol 584, 885-894.
137. Lander, E.S., Linton, L.M., Birren, B., et al. (2001) Initial sequencing and analysis of the human genome. Nature 409, 860-921.
138. Lee, J.C., Kwon, Y.G., Lawrence, D.S. & Edelman, A.M. (1994) A requirement of hydrophobic and basic amino acid residues for substrate recognition by Ca2+/calmodulin-dependent protein kinase Ia. Proc Natl Acad Sci U S A 91, 6413-6417.
139. Levenson, J.M., Roth, T.L., Lubin, F.D., Miller, C.A., Huang, I.C., Desai, P., Malone, L.M. & Sweatt, J.D. (2006) Evidence that DNA (cytosine-5) methyltransferase regulates synaptic plasticity in the hippocampus. J Biol Chem 281, 15763-15773.
140. Li, G. & Reinberg, D. (2011) Chromatin higher-order structures and gene regulation. Curr Opin Genet Dev 21, 175-186.
141. Li, J.B., Levanon, E.Y., Yoon, J.K., Aach, J., Xie, B., Leproust, E., Zhang, K., Gao, Y. & Church, G.M. (2009) Genome-wide identification of human RNA editing sites by parallel DNA capturing and sequencing. Science 324, 1210-1213.
142. Liang, Z., Liu, F., Grundke-Iqbal, I., Iqbal, K. & Gong, C.X. (2007) Down-regulation of cAMP-dependent protein kinase by over-activated calpain in Alzheimer disease brain. J Neurochem 103, 2462-2470.
143. Licata, S.C. & Pierce, R.C. (2003) The roles of calcium/calmodulin-dependent and Ras/mitogen-activated protein kinases in the development of psychostimulant-induced behavioral sensitization. J Neurochem 85, 14-22.
144. Lifson, S. (1987) Chemical selection, diversity, teleonomy and the second law of thermodynamics. Reflections on Eigen's theory of self-organization of matter. Biophys Chem 26, 303-311.
145. Lin, Y., Bloodgood, B.L., Hauser, J.L., Lapan, A.D., Koon, A.C., Kim, T.K., Hu, L.S., Malik, A.N. & Greenberg, M.E. (2008) Activity-dependent regulation of inhibitory synapse development by Npas4. Nature 455, 1198-1204.
146. Lindblad-Toh, K., Wade, C.M., Mikkelsen, T.S., et al. (2005) Genome sequence, comparative analysis and haplotype structure of the domestic dog. Nature 438, 803-819.
147. Link, W., Konietzko, U., Kauselmann, G., Krug, M., Schwanke, B., Frey, U. & Kuhl, D. (1995) Somatodendritic expression of an immediate early gene is regulated by synaptic activity. Proc Natl Acad Sci U S A 92, 5734-5738.
148. Linnen, C.R., Kingsley, E.P., Jensen, J.D. & Hoekstra, H.E. (2009) On the origin and spread of an adaptive allele in deer mice. Science 325, 1095-1098.
149. Linseman, D.A., Bartley, C.M., Le, S.S., Laessig, T.A., Bouchard, R.J., Meintzer, M.K., Li, M. & Heidenreich, K.A. (2003) Inactivation of the myocyte enhancer factor-2 repressor histone deacetylase-5 by endogenous Ca(2+)//calmodulin-dependent kinase II promotes depolarization-mediated cerebellar granule neuron survival. J Biol Chem 278, 41472-41481.
150. Lisman, J.E. & McIntyre, C.C. (2001) Synaptic plasticity: a molecular memory switch. Curr Biol 11, R788-791.
151. Liu, Y., Kamitakahara, A., Kim, A. & Aguilera, G. (2008) Cyclic adenosine 3', 5'-monophosphate responsive element binding protein phosphorylation is required but not sufficient for activation of corticotropin-releasing hormone transcription. Endocrinology 149, 3512-3520.
152. Lomeli, H., Mosbacher, J., Melcher, T., Hoger, T., Geiger, J.R., Kuner, T., Monyer, H., Higuchi, M., Bach, A. & Seeburg, P.H. (1994) Control of kinetic properties of AMPA receptor channels by nuclear RNA editing. Science 266, 1709-1713.
153. Lonze, B.E. & Ginty, D.D. (2002) Function and regulation of CREB family transcription factors in the nervous system. Neuron 35, 605-623.
154. Lubin, F.D., Roth, T.L. & Sweatt, J.D. (2008) Epigenetic regulation of BDNF gene transcription in the consolidation of fear memory. J Neurosci 28, 10576-10586.
155. Ly, P.T. & Song, W. (2011) Loss of activated CaMKII at the synapse underlies Alzheimer's disease memory loss. J Neurochem 119, 673-675.
156. Lyon, M.F. (1998) X-chromosome inactivation: a repeat hypothesis. Cytogenet Cell Genet 80, 133-137.
157. Ma, D.K., Jang, M.H., Guo, J.U., Kitabatake, Y., Chang, M.L., Pow-Anpongkul, N., Flavell, R.A., Lu, B., Ming, G.L. & Song, H. (2009) Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science 323, 1074-1077.
158. Marie, H., Morishita, W., Yu, X., Calakos, N. & Malenka, R.C. (2005) Generation of silent synapses by acute in vivo expression of CaMKIV and CREB. Neuron 45, 741-752.
159. Marin, M.T., Berkow, A., Golden, S.A., Koya, E., Planeta, C.S. & Hope, B.T. (2009) Context-specific modulation of cocaine-induced locomotor sensitization and ERK and CREB phosphorylation in the rat nucleus accumbens. Eur J Neurosci 30, 1931-1940.
160. Marmorstein, R. (2001) Protein modules that manipulate histone tails for chromatin regulation. Nat Rev Mol Cell Biol 2, 422-432.
161. Mattick, J. & Gagen, M. (2001) The evolution of controlled multitasked gene networks: the role of introns and other noncoding RNAs in the development of complex organisms. Mol Biol Evol 18, 1611-1630.
162. Mattick, J. & Makunin, I. (2006) Non-coding RNA. Hum Mol Genet 15 Spec No 1, R17-R29.
163. Mattick, J.S. & Mehler, M.F. (2008) RNA editing, DNA recoding and the evolution of human cognition. Trends Neurosci 31, 227-233.
164. Mayford, M., Baranes, D., Podsypanina, K. & Kandel, E. (1996) The 3'-untranslated region of CaMKII alpha is a cis-acting signal for the localization and translation of mRNA in dendrites. Proc Natl Acad Sci U S A 93, 13250-13255.
165. Mayr, B.M., Guzman, E. & Montminy, M. (2005) Glutamine rich and basic region/leucine zipper (bZIP) domains stabilize cAMP-response element-binding protein (CREB) binding to chromatin. J Biol Chem 280, 15103-15110.
166. Mayr, B. & Montminy, M. (2001) Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat Rev Mol Cell Biol 2, 599-609.
167. McClintock, B. (1951) Chromosome organization and genic expression. Cold Spring Harb Symp Quant Biol 16, 13-47.
168. McClung, C.A. & Nestler, E.J. (2003) Regulation of gene expression and cocaine reward by CREB and DeltaFosB. Nat Neurosci 6, 1208-1215.
169. McClung, C.A. & Nestler, E.J. (2008) Neuroplasticity mediated by altered gene expression. Neuropsychopharmacology 33, 3-17.
170. McGowan, P.O., Sasaki, A., D'Alessio, A.C., Dymov, S., Labonte, B., Szyf, M., Turecki, G. & Meaney, M.J. (2009) Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat Neurosci 12, 342-348.
171. McKenzie, G.J., Harris, R.S., Lee, P.L. & Rosenberg, S.M. (2000) The SOS response regulates adaptive mutation. Proc Natl Acad Sci U S A 97, 6646-6651.
172. Mehler, M. & Mattick, J. (2006) Non-coding RNAs in the nervous system. J Physiol 575, 333-341.
173. Meitzen, J., Luoma, J.I., Stern, C.M. & Mermelstein, P.G. (2011) beta1-Adrenergic receptors activate two distinct signaling pathways in striatal neurons. J Neurochem 116, 984-995.
174. Miller, C. & Sweatt, J. (2007) Covalent modification of DNA regulates memory formation. Neuron 53, 857-869.
175. Miyashita, T., Kubik, S., Lewandowski, G. & Guzowski, J. (2008) Networks of neurons, networks of genes: an integrated view of memory consolidation. Neurobiol Learn Mem 89, 269-284.
176. Moga, D., Calhoun, M., Chowdhury, A., Worley, P., Morrison, J. & Shapiro, M. (2004) Activity-regulated cytoskeletal-associated protein is localized to recently activated excitatory synapses. Neuroscience 125, 7-11.
177. Molteni, R., Calabrese, F., Chourbaji, S., Brandwein, C., Racagni, G., Gass, P. & Riva, M.A. (2010) Depression-prone mice with reduced glucocorticoid receptor expression display an altered stress-dependent regulation of brain-derived neurotrophic factor and activity-regulated cytoskeleton-associated protein. J Psychopharmacol 24, 595-603.
178. Montminy, M.R. & Bilezikjian, L.M. (1987) Binding of a nuclear protein to the cyclic-AMP response element of the somatostatin gene. Nature 328, 175-178.
179. Moran, J.V., DeBerardinis, R.J. & Kazazian, H.H. Jr. (1999) Exon shuffling by L1 retrotransposition. Science 283, 1530-1534.
180. Morgan, H.D., Dean, W., Coker, H.A., Reik, W. & Petersen-Mahrt, S.K. (2004) Activation-induced cytidine deaminase deaminates 5-methylcytosine in DNA and is expressed in pluripotent tissues: implications for epigenetic reprogramming. J Biol Chem 279, 52353-52360.
181. Mori, Y., Imaizumi, K., Katayama, T., Yoneda, T. & Tohyama, M. (2000) Two cis-acting elements in the 3' untranslated region of alpha-CaMKII regulate its dendritic targeting. Nat Neurosci 3, 1079-1084.
182. Muckenfuss, H., Hamdorf, M., Held, U., Perkovic, M., Lower, J., Cichutek, K., Flory, E., Schumann, G.G. & Munk, C. (2006) APOBEC3 proteins inhibit human LINE-1 retrotransposition. J Biol Chem 281, 22161-22172.
183. Muotri, A.R., Marchetto, M.C., Coufal, N.G., Oefner, R., Yeo, G., Nakashima, K. & Gage, F.H. (2010) L1 retrotransposition in neurons is modulated by MeCP2. Nature 468, 443-446.
184. Muotri, A.R., Zhao, C., Marchetto, M.C. & Gage, F.H. (2009) Environmental influence on L1 retrotransposons in the adult hippocampus. Hippocampus 19, 1002-1007.
185. Murgatroyd, C., Patchev, A.V., Wu, Y., Micale, V., Bockmuhl, Y., Fischer, D., Holsboer, F., Wotjak, C.T., Almeida, O.F. & Spengler, D. (2009) Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nat Neurosci 12, 1559-1566.
186. Need, A.C., Keefe, R.S., Ge, D., Grossman, I., Dickson, S., McEvoy, J.P. & Goldstein, D.B. (2009) Pharmacogenetics of antipsychotic response in the CATIE trial: a candidate gene analysis. Eur J Hum Genet 17, 946-957.
187. Nishikura, K. (2010) Functions and regulation of RNA editing by ADAR deaminases. Annu Rev Biochem 79, 321-349.
188. Oberlander, T.F., Weinberg, J., Papsdorf, M., Grunau, R., Misri, S. & Devlin, A.M. (2008) Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics 3, 97-106.
189. Okamoto, S., Pouladi, M.A., Talantova, M., Yao, D., Xia, P., Ehrnhoefer, D.E., Zaidi, R., Clemente, A., Kaul, M., Graham, R.K., Zhang, D., Vincent Chen, H.S., Tong, G., Hayden, M.R. & Lipton, S.A. (2009) Balance between synaptic versus extrasynaptic NMDA receptor activity influences inclusions and neurotoxicity of mutant huntingtin. Nat Med 15, 1407-1413.
190. Ooi, L. & Wood, I. (2008) Regulation of gene expression in the nervous system. Biochem J 414, 327-341.
191. Ostertag, E.M., Goodier, J.L., Zhang, Y. & Kazazian, H.H. Jr. (2003) SVA elements are nonautonomous retrotransposons that cause disease in humans. Am J Hum Genet 73, 1444-1451.
192. Ostertag, E.M. & Kazazian, H.H. Jr. (2001) Biology of mammalian L1 retrotransposons. Annu Rev Genet 35, 501-538.
193. Pandey, S.C., Zhang, H., Ugale, R., Prakash, A., Xu, T. & Misra, K. (2008) Effector immediate-early gene arc in the amygdala plays a critical role in alcoholism. J Neurosci 28, 2589-2600.
194. Papaleo, F. & Weinberger, D.R. (2011) Dysbindin and Schizophrenia: it's dopamine and glutamate all over again. Biol Psychiatry 69, 2-4.
195. Papaleo, F., Yang, F., Garcia, S., Chen, J., Lu, B., Crawley, J.N. & Weinberger, D.R. (2010) Dysbindin-1 modulates prefrontal cortical activity and schizophrenia-like behaviors via dopamine/D2 pathways. Mol Psychiatry; doi:10.1038/mp.2010.106.
196. Peng, P.L., Zhong, X., Tu, W., Soundarapandian, M.M., Molner, P., Zhu, D., Lau, L., Liu, S., Liu, F. & Lu, Y. (2006) ADAR2-dependent RNA editing of AMPA receptor subunit GluR2 determines vulnerability of neurons in forebrain ischemia. Neuron 49, 719-733.
197. Penner, M.R., Roth, T.L., Chawla, M.K., Hoang, L.T., Roth, E.D., Lubin, F.D., Sweatt, J.D., Worley, P.F. & Barnes, C.A. (2011) Age-related changes in Arc transcription and DNA methylation within the hippocampus. Neurobiol Aging 32, 2198-2210.
198. Penzes, P., Cahill, M.E., Jones, K.A. & Srivastava, D.P. (2008) Convergent CaMK and RacGEF signals control dendritic structure and function. Trends Cell Biol 18, 405-413.
199. Perfeito, L., Fernandes, L., Mota, C. & Gordo, I. (2007) Adaptive mutations in bacteria: high rate and small effects. Science 317, 813-815.
200. Pham, P., Bransteitter, R. & Goodman, M.F. (2005) Reward versus risk: DNA cytidine deaminases triggering immunity and disease. Biochemistry 44, 2703-2715.
201. Pierce, R.C. & Kalivas, P.W. (1997) Repeated cocaine modifies the mechanism by which amphetamine releases dopamine. J Neurosci 17, 3254-3261.
202. Pinaud, R., Tremere, L., Penner, M., Hess, F., Robertson, H. & Currie, R. (2002) Complexity of sensory environment drives the expression of candidate-plasticity gene, nerve growth factor induced-A. Neuroscience 112, 573-582.
203. Plath, N., Ohana, O., Dammermann, B., Errington, M., Schmitz, D., Gross, C., Mao, X., Engelsberg, A., Mahlke, C., Welzl, H., Kobalz, U., Stawrakakis, A., Fernandez, E., Waltereit, R., Bick-Sander, A., Therstappen, E., Cooke, S., Blanquet, V., Wurst, W., Salmen, B., Bösl, M., Lipp, H., Grant, S., Bliss, T., Wolfer, D. & Kuhl, D. (2006) Arc/Arg3.1 is essential for the consolidation of synaptic plasticity and memories. Neuron 52, 437-444.
204. Popp, C., Dean, W., Feng, S., Cokus, S.J., Andrews, S., Pellegrini, M., Jacobsen, S.E. & Reik, W. (2010) Genome-wide erasure of DNA methylation in mouse primordial germ cells is affected by AID deficiency. Nature 463, 1101-1105.
205. Potkin, S.G., Turner, J.A., Fallon, J.A., Lakatos, A., Keator, D.B., Guffanti, G. & Macciardi, F. (2009) Gene discovery through imaging genetics: identification of two novel genes associated with schizophrenia. Mol Psychiatry 14, 416-428.
206. Potthoff, M.J. & Olson, E.N. (2007) MEF2: a central regulator of diverse developmental programs. Development 134, 4131-4140.
207. Pross, A. (2003) The driving force for life's emergence: kinetic and thermodynamic considerations. J Theor Biol 220, 393-406.
208. Radicella, J.P., Park, P.U. & Fox, M.S. (1995) Adaptive mutation in Escherichia coli: a role for conjugation. Science 268, 418-420.
209. Rajasethupathy, P., Fiumara, F., Sheridan, R., Betel, D., Puthanveettil, S.V., Russo, J.J., Sander, C., Tuschl, T. & Kandel, E. (2009) Characterization of small RNAs in aplysia reveals a role for miR-124 in constraining synaptic plasticity through CREB. Neuron 63, 803-817.
210. Ramocki, M.B. & Zoghbi, H.Y. (2008) Failure of neuronal homeostasis results in common neuropsychiatric phenotypes. Nature 455, 912-918.
211. Rando, O. & Verstrepen, K. (2007) Timescales of genetic and epigenetic inheritance. Cell 128, 655-668.
212. Rao, V.R., Pintchovski, S.A., Chin, J., Peebles, C.L., Mitra, S. & Finkbeiner, S. (2006) AMPA receptors regulate transcription of the plasticity-related immediate-early gene Arc. Nat Neurosci 9, 887-895.
213. Rasetti, R., Malone, C., Mattay, V., Rivero, O., Callicot, J., Meyer-Lindenberg, A., Rujescu, D., Straub, R. & Weinberger, D. (2007) Genetic variation in CAMK2A affects brain structure and function in normal individuals, In 37th annual meeting of the Society for Neuroscience. San Diego, CA.
214. Reese, L.C., Laezza, F., Woltjer, R. & Taglialatela, G. Dysregulated phosphorylation of Ca(2+) /calmodulin-dependent protein kinase II-alpha in the hippocampus of subjects with mild cognitive impairment and Alzheimer's disease. J Neurochem 119, 791-804.
215. Redmond, L., Kashani, A.H. & Ghosh, A. (2002) Calcium regulation of dendritic growth via CaM kinase IV and CREB-mediated transcription. Neuron 34, 999-1010.
216. Rial Verde, E., Lee-Osbourne, J., Worley, P., Malinow, R. & Cline, H. (2006) Increased expression of the immediate-early gene arc/arg3.1 reduces AMPA receptor-mediated synaptic transmission. Neuron 52, 461-474.
217. Richards, J.P., Bachinger, H.P., Goodman, R.H. & Brennan, R.G. (1996) Analysis of the structural properties of cAMP-responsive element-binding protein (CREB) and phosphorylated CREB. J Biol Chem 271, 13716-13723.
218. Ripke, S., Sanders, A.R., Kendler, K.S., et al. (2011) Genome-wide association study identifies five new schizophrenia loci. Nat Genet.
219. Roozendaal, B., Hernandez, A., Cabrera, S.M., Hagewoud, R., Malvaez, M., Stefanko, D.P., Haettig, J. & Wood, M.A. (2010) Membrane-associated glucocorticoid activity is necessary for modulation of long-term memory via chromatin modification. J Neurosci 30, 5037-5046.
220. Rose, J., Jin, S.X. & Craig, A.M. (2009) Heterosynaptic molecular dynamics: locally induced propagating synaptic accumulation of CaM kinase II. Neuron 61, 351-358.
221. Rosenberg, S.M., Longerich, S., Gee, P. & Harris, R.S. (1994) Adaptive mutation by deletions in small mononucleotide repeats. Science 265, 405-407.
222. Ross, C., Margolis, R., Reading, S., Pletnikov, M. & Coyle, J. (2006) Neurobiology of schizophrenia. Neuron 52, 139-153.
223. Royo, H. & Cavaille, J. (2008) Non-coding RNAs in imprinted gene clusters. Biol Cell 100, 149-166.
224. Runyan, J.D. & Dash, P.K. (2005) Distinct prefrontal molecular mechanisms for information storage lasting seconds versus minutes. Learn Mem 12, 232-238.
225. Russo, M., Sevetson, B. & Milbrandt, J. (1995) Identification of NAB1, a repressor of NGFI-A- and Krox20-mediated transcription. Proc Natl Acad Sci U S A 92, 6873-6877.
226. Sakamoto, K., Bardeleben, C., Yates, K., Raines, M., Golde, D. & Gasson, J. (1991) 5' upstream sequence and genomic structure of the human primary response gene, EGR-1/TIS8. Oncogene 6, 867-871.
227. Saneyoshi, T., Fortin, D.A. & Soderling, T.R. (2010) Regulation of spine and synapse formation by activity-dependent intracellular signaling pathways. Curr Opin Neurobiol 20, 108-115.
228. Saneyoshi, T., Wayman, G., Fortin, D., Davare, M., Hoshi, N., Nozaki, N., Natsume, T. & Soderling, T.R. (2008) Activity-dependent synaptogenesis: regulation by a CaM-kinase kinase/CaM-kinase I/betaPIX signaling complex. Neuron 57, 94-107.
229. Santarelli, D.M., Beveridge, N.J., Tooney, P.A. & Cairns, M.J. (2011) Upregulation of dicer and microRNA expression in the dorsolateral prefrontal cortex Brodmann area 46 in schizophrenia. Biol Psychiatry 69, 180-187.
230. Schaefer, A., Sampath, S.C., Intrator, A., Min, A., Gertler, T.S., Surmeier, D.J., Tarakhovsky, A. & Greengard, P. (2009) Control of cognition and adaptive behavior by the GLP/G9a epigenetic suppressor complex. Neuron 64, 678-691.
231. Schmitt, J.M., Guire, E.S., Saneyoshi, T. & Soderling, T.R. (2005) Calmodulin-dependent kinase kinase/calmodulin kinase I activity gates extracellular-regulated kinase-dependent long-term potentiation. J Neurosci 25, 1281-1290.
232. Schratt, G., Tuebing, F., Nigh, E., Kane, C., Sabatini, M., Kiebler, M. & Greenberg, M. (2006) A brain-specific microRNA regulates dendritic spine development. Nature 439, 283-289.
233. Schwachtgen, J., Campbell, C. & Braddock, M. (2000) Full promoter sequence of human early growth response factor-1 (Egr-1): demonstration of a fifth functional serum response element. DNA Seq 10, 429-432.
234. Sebat, J. (2007) Major changes in our DNA lead to major changes in our thinking. Nat Genet 39, S3-5.
235. Shapiro, J.A. (1995) Adaptive mutation: who's really in the garden? Science 268, 373-374.
236. Sheng, M., McFadden, G. & Greenberg, M. (1990) Membrane depolarization and calcium induce c-fos transcription via phosphorylation of transcription factor CREB. Neuron 4, 571-582.
237. Shepherd, J., Rumbaugh, G., Wu, J., Chowdhury, S., Plath, N., Kuhl, D., Huganir, R. & Worley, P. (2006) Arc/Arg3.1 mediates homeostatic synaptic scaling of AMPA receptors. Neuron 52, 475-484.
238. Shimada, M., Nakadai, T., Fukuda, A. & Hisatake, K. (2010) cAMP-response element-binding protein (CREB) controls MSK1-mediated phosphorylation of histone H3 at the c-fos promoter in vitro. J Biol Chem 285, 9390-9401.
239. Shumway, C.A. (2008) Habitat complexity, brain, and behavior. Brain Behav Evol 72, 123-134.
240. Silk, J.B. (2007) Social components of fitness in primate groups. Science 317, 1347-1351.
241. Silverman, E., Du, J., Williams, A., Wadgaonkar, R., Drazen, J. & Collins, T. (1998) cAMP-response-element-binding-protein-binding protein (CBP) and p300 are transcriptional co-activators of early growth response factor-1 (Egr-1). Biochem J 336 (Pt 1), 183-189.
242. Simmons, M., Meador-Woodruff, J.H. & Sodhi, M.S. (2010) Increased cortical expression of an RNA editing enzyme occurs in major depressive suicide victims. Neuroreport 21, 993-997.
243. Singer, T., McConnell, M.J., Marchetto, M.C., Coufal, N.G. & Gage, F.H. (2010) LINE-1 retrotransposons: mediators of somatic variation in neuronal genomes? Trends Neurosci 33, 345-354.
244. Slade, J. & Carter, D. (2000) Cyclical expression of egr-1/NGFI-A in the rat anterior pituitary: a molecular signal for ovulation? J Neuroendocrinol 12, 671-676.
245. Smith, D.L., Pozueta, J., Gong, B., Arancio, O. & Shelanski, M. (2009) Reversal of long-term dendritic spine alterations in Alzheimer disease models. Proc Natl Acad Sci U S A 106, 16877-16882.
246. Smith, H.C. (2011) APOBEC3G: a double agent in defense. Trends Biochem Sci 36, 239-244.
247. Speek, M. (2001) Antisense promoter of human L1 retrotransposon drives transcription of adjacent cellular genes. Mol Cell Biol 21, 1973-1985.
248. Steiner, B., Mandelkow, E.M., Biernat, J., Gustke, N., Meyer, H.E., Schmidt, B., Mieskes, G., Soling, H.D., Drechsel, D., Kirschner, M.W. et al. (1990) Phosphorylation of microtubule-associated protein tau: identification of the site for Ca2(+)-calmodulin dependent kinase and relationship with tau phosphorylation in Alzheimer tangles. EMBO J 9, 3539-3544.
249. Steward, O., Wallace, C., Lyford, G. & Worley, P. (1998) Synaptic activation causes the mRNA for the IEG Arc to localize selectively near activated postsynaptic sites on dendrites. Neuron 21, 741-751.
250. Steward, O. & Worley, P. (2001) Selective targeting of newly synthesized Arc mRNA to active synapses requires NMDA receptor activation. Neuron 30, 227-240.
251. Surani, M.A., Hayashi, K. & Hajkova, P. (2007) Genetic and epigenetic regulators of pluripotency. Cell 128, 747-762.
252. Sutton, M.A. & Schuman, E.M. (2006) Dendritic protein synthesis, synaptic plasticity, and memory. Cell 127, 49-58.
253. Swanberg, S.E., Nagarajan, R.P., Peddada, S., Yasui, D.H. & LaSalle, J.M. (2009) Reciprocal co-regulation of EGR2 and MECP2 is disrupted in Rett syndrome and autism. Hum Mol Genet 18, 525-534.
254. Sweatt, J.D. (2009) Experience-dependent epigenetic modifications in the central nervous system. Biol Psychiatry 65, 191-197.
255. Szymański, M., Barciszewska, M., Zywicki, M. & Barciszewski, J. (2003) Noncoding RNA transcripts. J Appl Genet 44, 1-19.
256. Takemura, M., Mishima, T., Wang, Y., Kasahara, J., Fukunaga, K., Ohashi, K. & Mizuno, K. (2009) Ca2+/calmodulin-dependent protein kinase IV-mediated LIM kinase activation is critical for calcium signal-induced neurite outgrowth. J Biol Chem 284, 28554-28562.
257. Thiel, G. (1993) Synapsin I, synapsin II, and synaptophysin: marker proteins of synaptic vesicles. Brain Pathol 3, 87-95.
258. Tsui, J., Inagaki, M. & Schulman, H. (2005) Calcium/calmodulin-dependent protein kinase II (CaMKII) localization acts in concert with substrate targeting to create spatial restriction for phosphorylation. J Biol Chem 280, 9210-9216.
259. van Rij, R.P. & Berezikov, E. (2009) Small RNAs and the control of transposons and viruses in Drosophila. Trends Microbiol 17, 163-171.
260. Vanderklish, P.W. & Edelman, G.M. (2002) Dendritic spines elongate after stimulation of group 1 metabotropic glutamate receptors in cultured hippocampal neurons. Proc Natl Acad Sci U S A 99, 1639-1644.
261. Vazdarjanova, A., McNaughton, B.L., Barnes, C.A., Worley, P.F. & Guzowski, J.F. (2002) Experience-dependent coincident expression of the effector immediate-early genes arc and Homer 1a in hippocampal and neocortical neuronal networks. J Neurosci 22, 10067-10071.
262. Vo, N., Klein, M.E., Varlamova, O., Keller, D.M., Yamamoto, T., Goodman, R.H. & Impey, S. (2005) A cAMP-response element binding protein-induced microRNA regulates neuronal morphogenesis. Proc Natl Acad Sci U S A 102, 16426-16431.
263. Volakakis, N., Kadkhodaei, B., Joodmardi, E., Wallis, K., Panman, L., Silvaggi, J., Spiegelman, B.M. & Perlmann, T. (2010) NR4A orphan nuclear receptors as mediators of CREB-dependent neuroprotection. Proc Natl Acad Sci U S A 107, 12317-12322.
264. Wahlstedt, H., Daniel, C., Enstero, M. & Ohman, M. (2009) Large-scale mRNA sequencing determines global regulation of RNA editing during brain development. Genome Res 19, 978-986.
265. Wallace, D.C. & Fan, W. (2010) Energetics, epigenetics, mitochondrial genetics. Mitochondrion 10, 12-31.
266. Wallace, D.L., Han, M.H., Graham, D.L., Green, T.A., Vialou, V., Iniguez, S.D., Cao, J.L., Kirk, A., Chakravarty, S., Kumar, A., Krishnan, V., Neve, R.L., Cooper, D.C., Bolanos, C.A., Barrot, M., McClung, C.A. & Nestler, E.J. (2009) CREB regulation of nucleus accumbens excitability mediates social isolation-induced behavioral deficits. Nat Neurosci 12, 200-209.
267. Wallace, C., Withers, G., Weiler, I., George, J., Clayton, D. & Greenough, W. (1995) Correspondence between sites of NGFI-A induction and sites of morphological plasticity following exposure to environmental complexity. Brain Res Mol Brain Res 32, 211-220.
268. Wang, X., Arai, S., Song, X., Reichart, D., Du, K., Pascual, G., Tempst, P., Rosenfeld, M.G., Glass, C.K. & Kurokawa, R. (2008a) Induced ncRNAs allosterically modify RNA-binding proteins in cis to inhibit transcription. Nature 454, 126-130.
269. Wang, H., Feng, R., Phillip Wang, L., Li, F., Cao, X. & Tsien, J.Z. (2008b) CaMKII activation state underlies synaptic labile phase of LTP and short-term memory formation. Curr Biol 18, 1546-1554.
270. Wang, D.C., Chen, S.S., Lee, Y.C. & Chen, T.J. (2006a) Amyloid-beta at sublethal level impairs BDNF-induced arc expression in cortical neurons. Neurosci Lett 398, 78-82.
271. Wang, K.H., Majewska, A., Schummers, J., Farley, B., Hu, C., Sur, M. & Tonegawa, S. (2006b) In vivo two-photon imaging reveals a role of arc in enhancing orientation specificity in visual cortex. Cell 126, 389-402.
272. Waung, M.W., Pfeiffer, B.E., Nosyreva, E.D., Ronesi, J.A. & Huber, K.M. (2008) Rapid translation of Arc/Arg3.1 selectively mediates mGluR-dependent LTD through persistent increases in AMPAR endocytosis rate. Neuron 59, 84-97.
273. Wayman, G., Davare, M., Ando, H., Fortin, D., Varlamova, O., Cheng, H., Marks, D., Obrietan, K., Soderling, T., Goodman, R. & Impey, S. (2008a) An activity-regulated microRNA controls dendritic plasticity by down-regulating p250GAP. Proc Natl Acad Sci U S A 105, 9093-9098.
274. Wayman, G., Lee, Y., Tokumitsu, H., Silva, A. & Soderling, T. (2008b) Calmodulin-kinases: modulators of neuronal development and plasticity. Neuron 59, 914-931.
275. Wayman, G., Impey, S., Marks, D., Saneyoshi, T., Grant, W., Derkach, V. & Soderling, T. (2006) Activity-dependent dendritic arborization mediated by CaM-kinase I activation and enhanced CREB-dependent transcription of Wnt-2. Neuron 50, 897-909.
276. Wayman, G.A., Kaech, S., Grant, W.F., Davare, M., Impey, S., Tokumitsu, H., Nozaki, N., Banker, G. & Soderling, T.R. (2004) Regulation of axonal extension and growth cone motility by calmodulin-dependent protein kinase I. J Neurosci 24, 3786-3794.
277. Weaver, I. (2007) Epigenetic programming by maternal behavior and pharmacological intervention. Nature versus nurture: let's call the whole thing off. Epigenetics 2, 22-28.
278. Weaver, I., Cervoni, N., Champagne, F., D'Alessio, A., Sharma, S., Seckl, J., Dymov, S., Szyf, M. & Meaney, M. (2004) Epigenetic programming by maternal behavior. Nat Neurosci 7, 847-854.
279. Weaver, I., D'Alessio, A., Brown, S., Hellstrom, I., Dymov, S., Sharma, S., Szyf, M. & Meaney, M. (2007) The transcription factor nerve growth factor-inducible protein a mediates epigenetic programming: altering epigenetic marks by immediate-early genes. J Neurosci 27, 1756-1768.
280. Weaver, I., Meaney, M. & Szyf, M. (2006) Maternal care effects on the hippocampal transcriptome and anxiety-mediated behaviors in the offspring that are reversible in adulthood. Proc Natl Acad Sci U S A 103, 3480-3485.
281. Weissman, L., Jo, D.G., Sorensen, M.M., de Souza-Pinto, N.C., Markesbery, W.R., Mattson, M.P. & Bohr, V.A. (2007) Defective DNA base excision repair in brain from individuals with Alzheimer's disease and amnestic mild cognitive impairment. Nucleic Acids Res 35, 5545-5555.
282. West, A., Chen, W., Dalva, M., Dolmetsch, R., Kornhauser, J., Shaywitz, A., Takasu, M., Tao, X. & Greenberg, M. (2001) Calcium regulation of neuronal gene expression. Proc Natl Acad Sci U S A 98, 11024-11031.
283. White, R.R., Kwon, Y.G., Taing, M., Lawrence, D.S. & Edelman, A.M. (1998) Definition of optimal substrate recognition motifs of Ca2+-calmodulin-dependent protein kinases IV and II reveals shared and distinctive features. J Biol Chem 273, 3166-3172.
284. Whitelaw, N.C. & Whitelaw, E. (2006) How lifetimes shape epigenotype within and across generations. Hum Mol Genet 15 Spec No 2, R131-137.
285. Williams, G. & Lau, L. (1993) Activation of the inducible orphan receptor gene nur77 by serum growth factors: dissociation of immediate-early and delayed-early responses. Mol Cell Biol 13, 6124-6136.
286. Wolf, C., Jackson, M.C., Kissling, C., Thome, J. & Linden, D.E. (2011) Dysbindin-1 genotype effects on emotional working memory. Mol Psychiatry 16, 145-55.
287. Wood, N., Bhattacharya, T., Keele, B.F., Giorgi, E., Liu, M., Gaschen, B., Daniels, M., Ferrari, G., Haynes, B.F., McMichael, A., Shaw, G.M., Hahn, B.H., Korber, B. & Seoighe, C. (2009) HIV evolution in early infection: selection pressures, patterns of insertion and deletion, and the impact of APOBEC. PLoS Pathog 5, e1000414.
288. Woolfe, A., Goodson, M., Goode, D.K., Snell, P., McEwen, G.K., Vavouri, T., Smith, S.F., North, P., Callaway, H., Kelly, K., Walter, K., Abnizova, I., Gilks, W., Edwards, Y.J., Cooke, J.E. & Elgar, G. (2005) Highly conserved non-coding sequences are associated with vertebrate development. PLoS Biol 3, e7.
289. Wright, B.E., Longacre, A. & Reimers, J.M. (1999) Hypermutation in derepressed operons of Escherichia coli K12. Proc Natl Acad Sci U S A 96, 5089-5094.
290. Wu, S.C. & Zhang, Y. (2010) Active DNA demethylation: many roads lead to Rome. Nat Rev Mol Cell Biol 11, 607-620.
291. Xing, J., Wang, H., Belancio, V.P., Cordaux, R., Deininger, P.L. & Batzer, M.A. (2006) Emergence of primate genes by retrotransposon-mediated sequence transduction. Proc Natl Acad Sci U S A 103, 17608-17613.
292. Yeo, J., Goodman, R.A., Schirle, N.T., David, S.S. & Beal, P.A. (2010) RNA editing changes the lesion specificity for the DNA repair enzyme NEIL1. Proc Natl Acad Sci U S A 107, 20715-20719.
293. Yin, Y., Edelman, G.M. & Vanderklish, P.W. (2002) The brain-derived neurotrophic factor enhances synthesis of Arc in synaptoneurosomes. Proc Natl Acad Sci U S A 99, 2368-2373.
294. Yuan, P., Zhou, R., Wang, Y., Li, X., Li, J., Chen, G., Guitart, X. & Manji, H.K. (2010) Altered levels of extracellular signal-regulated kinase signaling proteins in postmortem frontal cortex of individuals with mood disorders and schizophrenia. J Affect Disord 124, 164-169.
295. Yuste, R. & Bonhoeffer, T. (2004) Genesis of dendritic spines: insights from ultrastructural and imaging studies. Nat Rev Neurosci 5, 24-34.
296. Zafra, F., Hengerer, B., Leibrock, J., Thoenen, H. & Lindholm, D. (1990) Activity dependent regulation of BDNF and NGF mRNAs in the rat hippocampus is mediated by non-NMDA glutamate receptors. EMBO J 9, 3545-3550.
297. Zhang, R. & Su, B. (2008) MicroRNA regulation and the variability of human cortical gene expression. Nucleic Acids Res 36, 4621-4628.
298. Zhao, C., Xu, Z., Wang, F., Chen, J., Ng, S.K., Wong, P.W., Yu, Z., Pun, F.W., Ren, L., Lo, W.S., Tsang, S.Y. & Xue, H. (2009) Alternative-splicing in the exon-10 region of GABA(A) receptor beta(2) subunit gene: relationships between novel isoforms and psychotic disorders. PLoS ONE 4, e6977.
299. Zhou, Z., Hong, E., Cohen, S., Zhao, W., Ho, H., Schmidt, L., Chen, W., Lin, Y., Savner, E., Griffith, E., Hu, L., Steen, J., Weitz, C. & Greenberg, M. (2006) Brain-specific phosphorylation of MeCP2 regulates activity-dependent Bdnf transcription, dendritic growth, and spine maturation. Neuron 52, 255-269.
300. Zhou, Y., Takahashi, E., Li, W., Halt, A., Wiltgen, B., Ehninger, D., Li, G.D., Hell, J.W., Kennedy, M.B. & Silva, A.J. (2007) Interactions between the NR2B receptor and CaMKII modulate synaptic plasticity and spatial learning. J Neurosci 27, 13843-13853.