Skip to main content
Book cover

Epigenetics, Brain and Behavior pp 11–22Cite as

Synaptic Epigenesis and the Evolution of Higher Brain Functions

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.

This is a preview of subscription content, access via your institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • DOI: 10.1007/978-3-642-27913-3_2
  • Chapter length: 12 pages
  • Instant PDF download
  • Readable on all devices
  • Own it forever
  • Exclusive offer for individuals only
  • Tax calculation will be finalised during checkout
eBook
USD   139.00
Price excludes VAT (USA)
  • ISBN: 978-3-642-27913-3
  • Instant PDF download
  • Readable on all devices
  • Own it forever
  • Exclusive offer for individuals only
  • Tax calculation will be finalised during checkout
Softcover Book
USD   179.99
Price excludes VAT (USA)
Hardcover Book
USD   219.99
Price excludes VAT (USA)
Learn about institutional subscriptions
Fig. 1
Fig. 2

References

  • 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 25:2145–2155

    CrossRef  PubMed  CAS  Google Scholar 

  • 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 107:11567–11572

    CrossRef  PubMed  Google Scholar 

  • Benoit P, Changeux JP (1975) Consequences of tenotomy on the evolution of multiinnervation in developing rat soleus muscle. Brain Res 99:354–358

    CrossRef  PubMed  CAS  Google Scholar 

  • 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 149:89–96

    CrossRef  PubMed  CAS  Google Scholar 

  • Bourgeois JP (1997) Synaptogenesis, heterochrony and epigenesis in the mammalian neocortex. Acta Paediatr Suppl 422:27–33

    CrossRef  PubMed  CAS  Google Scholar 

  • 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 4:415–429

    CrossRef  PubMed  CAS  Google Scholar 

  • Bourgeron T (2009) A synaptic trek to autism. Curr Opin Neurobiol 19:231–234

    CrossRef  PubMed  CAS  Google Scholar 

  • Carreiras M, Seghier ML, Baquero S, Estévez A, Lozano A, Devlin JT, Price CJ (2009) An anatomical signature for literacy. Nature 461:983–986

    CrossRef  PubMed  CAS  Google Scholar 

  • 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 14:835–844

    CrossRef  PubMed  CAS  Google Scholar 

  • 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 121:1053–1063

    CrossRef  PubMed  Google Scholar 

  • Changeux JP (1985) Neuronal man. Pantheon Books, New York

    Google Scholar 

  • Changeux JP (2004) The physiology of truth. Harvard University Press, Cambridge, MA

    Google Scholar 

  • Changeux JP (2006) The molecular biology of consciousness investigated with genetically modified mice. Philos Trans R Soc Lond B Biol Sci 361:2239–2259

    CrossRef  PubMed  CAS  Google Scholar 

  • Changeux JP (2010) Nicotine addiction and nicotinic receptors: lessons from genetically modified mice. Nat Rev Neurosci 11:389–401

    CrossRef  PubMed  CAS  Google Scholar 

  • Changeux JP, Danchin A (1976) Selective stabilisation of developing synapses as a mechanism for the specification of neuronal networks. Nature 264:705–712

    CrossRef  PubMed  CAS  Google Scholar 

  • Changeux JP, Lou HC (2011) Emergent pharmacology of conscious experience: new perspectives in substance addiction. FASEB J 25:2098–2108

    CrossRef  PubMed  CAS  Google Scholar 

  • 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 70:2974–2978

    CrossRef  CAS  Google Scholar 

  • Cook EH, Scherer SW (2008) Copy-number variations associated with neuropsychiatric conditions. Nature 455:919–923

    CrossRef  PubMed  CAS  Google Scholar 

  • Dehaene S, Changeux JP (1991) The Wisconsin Card Sorting Test: theoretical analysis and modeling in a neuronal network. Cereb Cortex 1:62–79

    CrossRef  PubMed  CAS  Google Scholar 

  • Dehaene S, Changeux JP (2000) Reward-dependent learning in neuronal networks for planning and decision making. Prog Brain Res 126:217–229

    CrossRef  PubMed  CAS  Google Scholar 

  • Dehaene S, Changeux JP (2011) Experimental and theoretical approaches to conscious processing. Neuron 70:200–227

    CrossRef  PubMed  CAS  Google Scholar 

  • 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 95:14529–14534

    CrossRef  PubMed  CAS  Google Scholar 

  • 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 330:1359–1364

    CrossRef  PubMed  CAS  Google Scholar 

  • Dejerine J (1901) Anatomie des centres nerveux (with Augusta Marie Dejerine-Klumpke). Rueff, Paris, 2 volumes

    Google Scholar 

  • 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 17:1313–1318

    CrossRef  PubMed  Google Scholar 

  • Gisiger T, Kerszberg M, Changeux J-P (2005) Acquisition and performance of delayed-response tasks: a neural network model. Cereb Cortex 15:489–506

    CrossRef  PubMed  Google Scholar 

  • Gouzé JL, Lasry JM, Changeux J-P (1983) Selective stabilization of muscle innervation during development: a mathematical model. Biol Cybern 46:207–215

    CrossRef  PubMed  Google Scholar 

  • Harvey W (1651) Exercitationes de generatione animalium (On the generation of animals). Arnold Leers, The Hague

    Google Scholar 

  • 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 390:65–70

    PubMed  CAS  Google Scholar 

  • Hull C (1943) Principles of behavior. Appleton-Century, Oxford

    Google Scholar 

  • Huttenlocher PR, Dabholkar AS (1997) Regional differences in synaptogenesis in human cerebral cortex. J Comp Neurol 387:167–178

    CrossRef  PubMed  CAS  Google Scholar 

  • 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)

  • 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 20:1297–1327

    CrossRef  PubMed  Google Scholar 

  • 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 194:323–334

    CrossRef  PubMed  CAS  Google Scholar 

  • Levinthal F, Macagno E, Levinthal C (1976) Anatomy and development of identified cells in isogenic organisms. Cold Spring Harb Symp Quant Biol 40:321–331

    CrossRef  PubMed  CAS  Google Scholar 

  • Luo L, O'Leary DD (2005) Axon retraction and degeneration in development and disease. Annu Rev Neurosci 28:127–156

    CrossRef  PubMed  CAS  Google Scholar 

  • Mandel JL, Biancalana V (2004) Fragile X mental retardation syndrome: from pathogenesis to diagnostic issues. Growth Horm IGF Res 14(Suppl A):S158–S165

    CrossRef  PubMed  CAS  Google Scholar 

  • 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–55P

    PubMed  Google Scholar 

  • 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 108:13281–13286

    CrossRef  PubMed  CAS  Google Scholar 

  • 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 47:427–434

    CrossRef  PubMed  Google Scholar 

  • Quartz SR, Sejnowski TJ (1997) The neural basis of cognitive development: a constructivist manifesto. Behav Brain Sci 20:537–556, discussion 556–596

    PubMed  CAS  Google Scholar 

  • 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 103:762–767

    CrossRef  PubMed  CAS  Google Scholar 

  • 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 2:56ra80

    CrossRef  PubMed  Google Scholar 

  • Skinner BF (1981) Selection by consequences. Science 213:501–504

    CrossRef  PubMed  CAS  Google Scholar 

  • Stretavan DW, Shatz CJ, Stryker MP (1988) Modification of retinal ganglion cell axon morphology by prenatal infusion of tetrodotoxin. Nature 336:468–471

    CrossRef  Google Scholar 

  • Thorndike E (1911) Animal intelligence. Macmillan, New York (reprinted Thoemmes, Bristol 1999)

    Google Scholar 

  • Triller A, Choquet D (2008) New concepts in synaptic biology derived from single-molecule imaging. Neuron 59:359–374

    CrossRef  PubMed  CAS  Google Scholar 

  • Tsigelny I, Kouznetsova V, Baitaluk M & Changeux J-P (submitted)

    Google Scholar 

  • 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):1304–1351

    CrossRef  PubMed  CAS  Google Scholar 

  • Von Economo C, Koskinas GN (1925) Die cytoarchitektonik der hirnrinde des erwachsenen menschen. Springer, Vienna

    Google Scholar 

  • Waddington CH (1942) Canalization of development and the inheritance of acquired characters. Nature 150:563–565

    CrossRef  Google Scholar 

  • 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 32:331–343

    CrossRef  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

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

Author information

Authors and Affiliations

  1. Département de Neurosciences, Institut Pasteur, Collège de France, Place Marcellin Berthelot, Paris, 25 Rue de Docteur Roux, Paris, France

    Jean-Pierre Changeux

Authors
  1. Jean-Pierre Changeux
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jean-Pierre Changeux .

Editor information

Editors and Affiliations

  1. School of Medicine, Center for Metabolism and Epigenetics, University of California at Irvine, Sprague Hall 324, Irvine, 92697, California, USA

    Paolo Sassone Corsi

  2. Recherche Therapeutique, Fondation IPSEN pour la, quai George Gorse 65, Boulogne Billancourt Cedex, 92650, France

    Yves Christen

Rights and permissions

Reprints and Permissions

Copyright information

© 2012 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Changeux, JP. (2012). Synaptic Epigenesis and the Evolution of Higher Brain Functions. In: Sassone Corsi, P., Christen, Y. (eds) Epigenetics, Brain and Behavior. Research and Perspectives in Neurosciences. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-27913-3_2

Download citation