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Synaptic Epigenesis and the Evolution of Higher Brain Functions

  • Jean-Pierre Changeux
Chapter
Part of the Research and Perspectives in Neurosciences book series (NEUROSCIENCE)

Abstract

The epigenesis theory of development can be traced back to William Harvey (1651), who stated, in contrast to contemporary preformation views, that the embryo arises by “the addition of parts budding out from one another.” The word epigenesis was subsequently used by Conrad Waddington (Nature 150:563–565, 1942) to specify how genes might interact with their surroundings to produce a phenotype. This is also the meaning we adopted in our paper, Theory of the Epigenesis of Neuronal Networks by Selective Stabilization of Synapses (Changeux et al. Proc Nat Acad Sci U S A 70:2974–2978, 1973), according to which the environment affects the organization of connections in an evolving neuronal network through the stabilization or degeneration (pruning) of labile synapses associated with the state of activity of the network. This definition contrasts with the recent and more restricted sense of the status of DNA methylation and histone modification in a particular genomic region. The synapse selection theory was introduced to deal with two major features regarding the genetic evolution of the human brain : 1) the non-linear increase in the organizational complexity of the brain despite a nearly constant number of genes ; and 2) the long postnatal period of brain maturation (ca. 15 years in humans), during which critical and reciprocal interactions take place between the brain and its physical, social and cultural environment. This theory will be evaluated and updated in the framework of the recent human/primate genome data, analysis of gene expression patterns during postnatal development, brain imaging of cultural pathways, such as those for language learning, and current views about the neural bases of higher brain function, in particular the global neuronal workspace architectures for access to consciousness (see Dehaene and Changeux Neuron 70:200–227, 2011).

Keywords

FMR1 Gene High Brain Function Synaptic Pruning Epigenetic Variability Conscious Access 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

The author thanks Yves Christen for his faithful support and Jennifer Altman for the careful transcription and editing of this paper.

References

  1. Avale ME, Chabout J, Pons S, Serreau P, De Chaumont F, Olivo-Marin JC, Bourgeois JP, Maskos U, Changeux JP, Granon S (2011) Prefrontal nicotinic receptors control novel social interaction between mice. FASEB J 25:2145–2155PubMedCrossRefGoogle Scholar
  2. Ballesteros-Yáñez I, Benavides-Piccione R, Bourgeois JP, Changeux JP, DeFelipe J (2010) Alterations of cortical pyramidal neurons in mice lacking high-affinity nicotinic receptors. Proc Natl Acad Sci U S A 107:11567–11572PubMedCrossRefGoogle Scholar
  3. Benoit P, Changeux JP (1975) Consequences of tenotomy on the evolution of multiinnervation in developing rat soleus muscle. Brain Res 99:354–358PubMedCrossRefGoogle Scholar
  4. Benoit P, Changeux JP (1978) Consequences of blocking the nerve with a local anaesthetic on the evolution of multiinnervation at the regenerating neuromuscular junction of the rat. Brain Res 149:89–96PubMedCrossRefGoogle Scholar
  5. Bourgeois JP (1997) Synaptogenesis, heterochrony and epigenesis in the mammalian neocortex. Acta Paediatr Suppl 422:27–33PubMedCrossRefGoogle Scholar
  6. Bourgeois JP, Toutant M, Gouzé JL, Changeux JP (1986) Effect of activity on the selective stabilization of the motor innervation of fast muscle posterior latissimus dorsi from chick embryo. Int J Dev Neurosci 4:415–429PubMedCrossRefGoogle Scholar
  7. Bourgeron T (2009) A synaptic trek to autism. Curr Opin Neurobiol 19:231–234PubMedCrossRefGoogle Scholar
  8. Carreiras M, Seghier ML, Baquero S, Estévez A, Lozano A, Devlin JT, Price CJ (2009) An anatomical signature for literacy. Nature 461:983–986PubMedCrossRefGoogle Scholar
  9. Castets M, Schaeffer C, Bechara E, Schenck A, Khandjian EW, Luche S, Moine H, Rabilloud T, Mandel JL, Bardoni B (2005) FMRP interferes with the Rac1 pathway and controls actin cytoskeleton dynamics in murine fibroblasts. Hum Mol Genet 14:835–844PubMedCrossRefGoogle Scholar
  10. Castro-Caldas A, Petersson KM, Reis A, Stone-Elander S, Ingvar M (1998) The illiterate brain. Learning to read and write during childhood influences the functional organization of the adult brain. Brain 121:1053–1063PubMedCrossRefGoogle Scholar
  11. Changeux JP (1985) Neuronal man. Pantheon Books, New YorkGoogle Scholar
  12. Changeux JP (2004) The physiology of truth. Harvard University Press, Cambridge, MAGoogle Scholar
  13. Changeux JP (2006) The molecular biology of consciousness investigated with genetically modified mice. Philos Trans R Soc Lond B Biol Sci 361:2239–2259PubMedCrossRefGoogle Scholar
  14. Changeux JP (2010) Nicotine addiction and nicotinic receptors: lessons from genetically modified mice. Nat Rev Neurosci 11:389–401PubMedCrossRefGoogle Scholar
  15. Changeux JP, Danchin A (1976) Selective stabilisation of developing synapses as a mechanism for the specification of neuronal networks. Nature 264:705–712PubMedCrossRefGoogle Scholar
  16. Changeux JP, Lou HC (2011) Emergent pharmacology of conscious experience: new perspectives in substance addiction. FASEB J 25:2098–2108PubMedCrossRefGoogle Scholar
  17. Changeux JP, Courrège P, Danchin A (1973) A theory of the epigenesis of neuronal networks by selective stabilization of synapses. Proc Nat Acad Sci U S A 70:2974–2978CrossRefGoogle Scholar
  18. Cook EH, Scherer SW (2008) Copy-number variations associated with neuropsychiatric conditions. Nature 455:919–923PubMedCrossRefGoogle Scholar
  19. Dehaene S, Changeux JP (1991) The Wisconsin Card Sorting Test: theoretical analysis and modeling in a neuronal network. Cereb Cortex 1:62–79PubMedCrossRefGoogle Scholar
  20. Dehaene S, Changeux JP (2000) Reward-dependent learning in neuronal networks for planning and decision making. Prog Brain Res 126:217–229PubMedCrossRefGoogle Scholar
  21. Dehaene S, Changeux JP (2011) Experimental and theoretical approaches to conscious processing. Neuron 70:200–227PubMedCrossRefGoogle Scholar
  22. Dehaene S, Kerszberg M, Changeux JP (1998) A neuronal model of a global workspace in effortful cognitive tasks. Proc Natl Acad Sci U S A 95:14529–14534PubMedCrossRefGoogle Scholar
  23. Dehaene S, Pegado F, Braga LW, Ventura P, Nunes Filho G, Jobert A, Dehaene-Lambertz G, Kolinsky R, Morais J, Cohen L (2010) How learning to read changes the cortical networks for vision and language. Science 330:1359–1364PubMedCrossRefGoogle Scholar
  24. Dejerine J (1901) Anatomie des centres nerveux (with Augusta Marie Dejerine-Klumpke). Rueff, Paris, 2 volumesGoogle Scholar
  25. Elston GN (2003) The pyramidal neuron in occipital, temporal and prefrontal cortex of the owl monkey (Aotus trivirgatus): regional specialization in cell structure. Eur J Neurosci 17:1313–1318PubMedCrossRefGoogle Scholar
  26. Gisiger T, Kerszberg M, Changeux J-P (2005) Acquisition and performance of delayed-response tasks: a neural network model. Cereb Cortex 15:489–506PubMedCrossRefGoogle Scholar
  27. Gouzé JL, Lasry JM, Changeux J-P (1983) Selective stabilization of muscle innervation during development: a mathematical model. Biol Cybern 46:207–215PubMedCrossRefGoogle Scholar
  28. Harvey W (1651) Exercitationes de generatione animalium (On the generation of animals). Arnold Leers, The HagueGoogle Scholar
  29. Henderson CE, Benoit P, Huchet M, Guenet JL, Changeux JP (1986) Increase of neurite-promoting activity for spinal neurons in muscles of ‘paralysé’ mice and tenotomised rats. Brain Res 390:65–70PubMedGoogle Scholar
  30. Hull C (1943) Principles of behavior. Appleton-Century, OxfordGoogle Scholar
  31. Huttenlocher PR, Dabholkar AS (1997) Regional differences in synaptogenesis in human cerebral cortex. J Comp Neurol 387:167–178PubMedCrossRefGoogle Scholar
  32. Kano M, Hashimoto K (2011) Activity-dependent maturation of climbing fiber to purkinje cell synapses during postnatal cerebellar development. Cerebellum. doi: 10.1007/s12311-011-0337-3 (Epub ahead of print)
  33. Karlsgodt KH, Sun D, Jimenez AM, Lutkenhoff ES, Willhite R, van Erp TG, Cannon TD (2008) Developmental disruptions in neural connectivity in the pathophysiology of schizophrenia. Dev Psychopathol 20:1297–1327PubMedCrossRefGoogle Scholar
  34. Ko J, Soler-Llavina GJ, Fuccillo MV, Malenka RC, Südhof TC (2011) Neuroligins/LRRTMs prevent activity and Ca2+/calmodulin-dependent synapse elimination in cultured neurons. J Cell Biol 194:323–334PubMedCrossRefGoogle Scholar
  35. Levinthal F, Macagno E, Levinthal C (1976) Anatomy and development of identified cells in isogenic organisms. Cold Spring Harb Symp Quant Biol 40:321–331PubMedCrossRefGoogle Scholar
  36. Luo L, O'Leary DD (2005) Axon retraction and degeneration in development and disease. Annu Rev Neurosci 28:127–156PubMedCrossRefGoogle Scholar
  37. Mandel JL, Biancalana V (2004) Fragile X mental retardation syndrome: from pathogenesis to diagnostic issues. Growth Horm IGF Res 14(Suppl A):S158–S165PubMedCrossRefGoogle Scholar
  38. O'Brien RA, Purves RD, Vrbová G (1977) Effect of activity on the elimination of multiple innervation in soleus muscles of rats. J Physiol 271:54P–55PPubMedGoogle Scholar
  39. Petanjek Z, Judaš M, Šimic G, Rasin MR, Uylings HB, Rakic P, Kostovic I (2011) Extraordinary neoteny of synaptic spines in the human prefrontal cortex. Proc Natl Acad Sci U S A 108:13281–13286PubMedCrossRefGoogle Scholar
  40. Pugliese L, Catani M, Ameis S, Dell'Acqua F, Thiebaut de Schotten M, Murphy C, Robertson D, Deeley Q, Daly E, Murphy DG (2009) The anatomy of extended limbic pathways in Asperger syndrome: a preliminary diffusion tensor imaging tractography study. Neuroimage 47:427–434PubMedCrossRefGoogle Scholar
  41. Quartz SR, Sejnowski TJ (1997) The neural basis of cognitive development: a constructivist manifesto. Behav Brain Sci 20:537–556, discussion 556–596PubMedGoogle Scholar
  42. Scott L, Zelenin S, Malmersjö S, Kowalewski JM, Markus EZ, Nairn AC, Greengard P, Brismar H, Aperia A (2006) Allosteric changes of the NMDA receptor trap diffusible dopamine 1 receptors in spines. Proc Natl Acad Sci U S A 103:762–767PubMedCrossRefGoogle Scholar
  43. Scott-Van Zeeland AA, Abrahams BS, Alvarez-Retuerto AI, Sonnenblick LI, Rudie JD, Ghahremani D, Mumford JA, Poldrack RA, Dapretto M, Geschwind DH, Bookheimer SY (2010) Altered functional connectivity in frontal lobe circuits is associated with variation in the autism risk gene. CNTNAP2. Sci Transl Med 2:56ra80PubMedCrossRefGoogle Scholar
  44. Skinner BF (1981) Selection by consequences. Science 213:501–504PubMedCrossRefGoogle Scholar
  45. Stretavan DW, Shatz CJ, Stryker MP (1988) Modification of retinal ganglion cell axon morphology by prenatal infusion of tetrodotoxin. Nature 336:468–471CrossRefGoogle Scholar
  46. Thorndike E (1911) Animal intelligence. Macmillan, New York (reprinted Thoemmes, Bristol 1999)Google Scholar
  47. Triller A, Choquet D (2008) New concepts in synaptic biology derived from single-molecule imaging. Neuron 59:359–374PubMedCrossRefGoogle Scholar
  48. Tsigelny I, Kouznetsova V, Baitaluk M & Changeux J-P (submitted)Google Scholar
  49. Venter JC, Adams MD, Myers EW, Li PW, Mural RJ, Sutton GG, Smith HO, Yandell M, Evans CA, Holt RA, Gocayne JD, Amanatides P, Ballew RM, Huson DH, Wortman JR, Zhang Q, Kodira CD, Zheng XH, Chen L, Skupski M, Subramanian G, Thomas PD, Zhang J, Gabor Miklos GL, Nelson C, Broder S, Clark AG, Nadeau J, McKusick VA, Zinder N, Levine AJ, Roberts RJ, Simon M, Slayman C, Hunkapiller M, Bolanos R, Delcher A, Dew I, Fasulo D, Flanigan M, Florea L, Halpern A, Hannenhalli S, Kravitz S, Levy S, Mobarry C, Reinert K, Remington K, Abu-Threideh J, Beasley E, Biddick K, Bonazzi V, Brandon R, Cargill M, Chandramouliswaran I, Charlab R, Chaturvedi K, Deng Z, Di Francesco V, Dunn P, Eilbeck K, Evangelista C, Gabrielian AE, Gan W, Ge W, Gong F, Gu Z, Guan P, Heiman TJ, Higgins ME, Ji RR, Ke Z, Ketchum KA, Lai Z, Lei Y, Li Z, Li J, Liang Y, Lin X, Lu F, Merkulov GV, Milshina N, Moore HM, Naik AK, Narayan VA, Neelam B, Nusskern D, Rusch DB, Salzberg S, Shao W, Shue B, Sun J, Wang Z, Wang A, Wang X, Wang J, Wei M, Wides R, Xiao C, Yan C, Yao A, Ye J, Zhan M, Zhang W, Zhang H, Zhao Q, Zheng L, Zhong F, Zhong W, Zhu S, Zhao S, Gilbert D, Baumhueter S, Spier G, Carter C, Cravchik A, Woodage T, Ali F, An H, Awe A, Baldwin D, Baden H, Barnstead M, Barrow I, Beeson K, Busam D, Carver A, Center A, Cheng ML, Curry L, Danaher S, Davenport L, Desilets R, Dietz S, Dodson K, Doup L, Ferriera S, Garg N, Gluecksmann A, Hart B, Haynes J, Haynes C, Heiner C, Hladun S, Hostin D, Houck J, Howland T, Ibegwam C, Johnson J, Kalush F, Kline L, Koduru S, Love A, Mann F, May D, McCawley S, McIntosh T, McMullen I, Moy M, Moy L, Murphy B, Nelson K, Pfannkoch C, Pratts E, Puri V, Qureshi H, Reardon M, Rodriguez R, Rogers YH, Romblad D, Ruhfel B, Scott R, Sitter C, Smallwood M, Stewart E, Strong R, Suh E, Thomas R, Tint NN, Tse S, Vech C, Wang G, Wetter J, Williams S, Williams M, Windsor S, Winn-Deen E, Wolfe K, Zaveri J, Zaveri K, Abril JF, Guigó R, Campbell MJ, Sjolander KV, Karlak B, Kejariwal A, Mi H, Lazareva B, Hatton T, Narechania A, Diemer K, Muruganujan A, Guo N, Sato S, Bafna V, Istrail S, Lippert R, Schwartz R, Walenz B, Yooseph S, Allen D, Basu A, Baxendale J, Blick L, Caminha M, Carnes-Stine J, Caulk P, Chiang YH, Coyne M, Dahlke C, Mays A, Dombroski M, Donnelly M, Ely D, Esparham S, Fosler C, Gire H, Glanowski S, Glasser K, Glodek A, Gorokhov M, Graham K, Gropman B, Harris M, Heil J, Henderson S, Hoover J, Jennings D, Jordan C, Jordan J, Kasha J, Kagan L, Kraft C, Levitsky A, Lewis M, Liu X, Lopez J, Ma D, Majoros W, McDaniel J, Murphy S, Newman M, Nguyen T, Nguyen N, Nodell M, Pan S, Peck J, Peterson M, Rowe W, Sanders R, Scott J, Simpson M, Smith T, Sprague A, Stockwell T, Turner R, Venter E, Wang M, Wen M, Wu D, Wu M, Xia A, Zandieh A, Zhu X (2001) The sequence of the human genome. Science 291(5507):1304–1351PubMedCrossRefGoogle Scholar
  50. Von Economo C, Koskinas GN (1925) Die cytoarchitektonik der hirnrinde des erwachsenen menschen. Springer, ViennaGoogle Scholar
  51. Waddington CH (1942) Canalization of development and the inheritance of acquired characters. Nature 150:563–565CrossRefGoogle Scholar
  52. Wu X, Fu Y, Knott G, Lu J, Di Cristo G, Huang ZJ (2012) GABA signaling promotes synapse elimination and axon pruning in developing cortical inhibitory interneurons. J Neurosci 32:331–343PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Département de Neurosciences, Institut PasteurCollège de France, Place Marcellin Berthelot, ParisParisFrance

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