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Evolutionary Mechanisms and Neural Adaptation: Selective Versus Constructive Strategies in the Development and Plasticity of the Nervous System

  • Ferdinando Rossi
Chapter

Abstract

The correct function of the nervous system requires complex neural networks bearing precise connections. In principle, the high structural specificity of neural circuits could be achieved by genetically-determined processes, selected and refined during evolution. Highly conserved gene networks regulate some crucial steps of neural development, such as the regionalization of the neural tube and the initial phases of neurogenesis and synaptogenesis. A totally hardwired nervous system may meet the requirements of adaptation and natural selection at the population level. Nevertheless, it would be inadequate to allow individual organisms to cope with rapid changes of environmental conditions. Neural adaptation to external constraints can be partly achieved by introducing selective mechanisms in neural development. Accordingly, neurons are generated in excess and then partially eliminated to match the actual extension of innervation territories. Such mechanisms, however, are restricted to a set of potentialities, which must be predetermined in the ontogenetic program. On the other hand, constructive mechanisms, in which external stimuli directly influence structural modifications of neural circuits to produce adaptive responses, may allow individual organisms to cope with a wide variety of unprecedented situations. Thus, in the last ontogenetic period as well as in the adult, when the organism actively interacts with the external milieu, experience exerts a strong growth-promoting effect on neural circuits and connections inducing the emergence of specific functional properties. By this mechanism, which requires strict inhibitory control to prevent aberrant growth and dysfunction, the nervous system exploits external stimuli to create adaptive responses to unexpected situations.

Keywords

Neural Circuit Neural Development Adult Neurogenesis Neural Adaptation Selective Mechanism 
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

Acknowledgements

The scientific work of Ferdinando Rossi is supported by grants from Ministero dell’Università e della Ricerca Scientifica e Tecnologica (MIUR-PRIN 2007 prog. nr. 2007F7AJYJ), Compagnia di San Paolo (Neurotransplant Project 2008; GABAGEN Neuroscience project 2009), Regione Piemonte (Project A14/05; Ricerca Sanitaria Finalizzata, 2008, 2009), Ataxia UK; Fondazione Cavaliere del Lavoro Mario Magnetto of Turin.

References

  1. 1.
    Aigner L, Arber S, Kapfhammer JP, Laux T, Schneider C, Botteri F, Brenner H-R, Caroni P (1995) Over expression of the neural growth associated protein GAP-43 induces nerve sprouting in the adult nervous system of transgenic mice. Cell 83:269–278PubMedCrossRefGoogle Scholar
  2. 2.
    Aimone JB, Deng W, Gage FH (2010) Adult neurogenesis: integrating theories and separating functions. Trends Cogn Sci 14:325–337PubMedCrossRefGoogle Scholar
  3. 3.
    Bronner-Fraser M, Hatten ME (2003) Neural induction and pattern formation. In: Squire LR, Bloom FE, McConnell SK, Roberts JL, Spitzer NC, Zigmond MJ (eds) Fundamental neuroscience. Academic, New York/LondonGoogle Scholar
  4. 4.
    Brundin P, Winkler J, Masliah E (2008) Adult neurogenesis in neurodegenerative diseases. In: Gage FH, Kempermann G, Song H (eds) Adult neurogenesis. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 503–533Google Scholar
  5. 5.
    Burden SJ, Berg D, O’Leary DDM (2003) Target selection, topographic maps and synapse formation. In: Squire LR, Bloom FE, McConnell SK, Roberts JL, Spitzer NC, Zigmond MJ (eds) Fundamental neuroscience. Academic, New York/LondonGoogle Scholar
  6. 6.
    Byl N, Merzenich MM, Jenkins WM (1996) A primate genesis model of focal dystonia and repetitive strain injury. I. Learning-induced dedifferentiation of the representation of the hand in the primary somatosensory cortex in adult monkeys. Neurology 47:508–520PubMedGoogle Scholar
  7. 7.
    Caviness VS Jr, Nowakowski RS, Bhide PG (2009) Neocortical neurogenesis: morphogenetic gradients and beyond. Trends Neurosci 32:443–450PubMedCrossRefGoogle Scholar
  8. 8.
    Changeux JP (1983) L’homme neuronal. Fayard, ParisGoogle Scholar
  9. 9.
    Cotman C, Sampedro N, Harris EW (1981) Synapse replacement in the nervous system of adult vertebrates. Physiol Rev 61:684–784PubMedGoogle Scholar
  10. 10.
    De Villers-Sidani E, Chang EF, Bao S, Merzenich MM (2007) Critical period window for spectral tuning defined in the primary auditory cortex (A1) in the rat. J Neurosci 27:180–189PubMedCrossRefGoogle Scholar
  11. 11.
    De Villers-Sidani E, Simpson KL, Lu Y-F, Lin RCS, Merzenich MM (2008) Manipulating critical period closure across different sectors of the primary auditory cortex. Nat Neurosci 11:957–965PubMedCrossRefGoogle Scholar
  12. 12.
    Dunlap JC, Loros LJ, De Coursey P (2004) Chronobiology: biological timekeeping. Sinauer, SunderlandGoogle Scholar
  13. 13.
    Edelman G (1987) Neural Darwinism. The theory of neuronal group selection. Basic Books, New YorkGoogle Scholar
  14. 14.
    Edlund T, Jessell TM (1999) Progression from extrinsic to intrinsic signaling in cell fate specification: a view from the nervous system. Cell 96:211–224PubMedCrossRefGoogle Scholar
  15. 15.
    Fabel K, Kempermann G (2008) Physical activity and the regulation of neurogenesis in the adult and aging brain. Neuromolecular Med 10:59–66PubMedCrossRefGoogle Scholar
  16. 16.
    Fawcett JW, Rosser AE, Dunnett SB (2002) Brain damage, brain repair. Oxford University Press, OxfordGoogle Scholar
  17. 17.
    Ferretti P, Zhang F, O’Neill P (2003) Changes in spinal cord regenerative ability through phylogenesis and development: lessons to be learnt. Dev Dyn 226:245–256PubMedCrossRefGoogle Scholar
  18. 18.
    Foscarin S, Ponchione D, Pajaj E, Leto K, Gawlak M, Wilczynski GM, Rossi F, Carulli D (2011) Experience-dependent plasticity and modulation of growth regulatory molecules at central synapses. PLoS One 6:e16666PubMedCrossRefGoogle Scholar
  19. 19.
    Foster RG, Kreitzman L (2004) Rhythms of life: the biological clocks that control the daily lives of every living thing. Profile Books, LondonGoogle Scholar
  20. 20.
    Gomez-Pinilla F, Ying, Z, Agoncillo T, Frostig R (2011) The influence of naturalistic experience on plasticity markers in somatosensory cortex and hippocampus: effects of whisker use. Brain Res 1388:39–47Google Scholar
  21. 21.
    Grimaldi P, Carletti B, Rossi F (2005) Neuronal replacement and integration in the rewiring of cerebellar circuits. Brain Res Rev 49:330–342PubMedCrossRefGoogle Scholar
  22. 22.
    Harris WA, Hartenstein V (2003) Cellular determination. In: Squire LR, Bloom FE, McConnell SK, Roberts JL, Spitzer NC, Zigmond MJ (eds) Fundamental neuroscience. Academic, New York/LondonGoogle Scholar
  23. 23.
    Hashimoto K, Hichikawa R, Kitamura K, Watanade M, Kano M (2009) Translocation of a “winner” climbing fiber to the Purkinje cell dendrite and subsequent elimination of “losers” from the soma in developing cerebellum. Neuron 63:103–118CrossRefGoogle Scholar
  24. 24.
    Hensch T (2004) Critical period regulation. Annu Rev Neurosci 27:549–579PubMedCrossRefGoogle Scholar
  25. 25.
    Herrup K, Yang Y (2007) Cell cycle regulation in the postmitotic neuron: oxymoron or new biology? Nat Rev Neurosci 8:368–378PubMedCrossRefGoogle Scholar
  26. 26.
    Hockfield S, Kalb RG (1993) Activity-dependent structural changes during neuronal development. Curr Opin Neurobiol 3:87–92PubMedCrossRefGoogle Scholar
  27. 27.
    Jacobson M (1991) Developmental neurobiology. Plenum, New York/LondonGoogle Scholar
  28. 28.
    Kempermann G, Fabel K, Ehninger D, Babu H, Leal-Galicia P, Garther A, Sa W (2010) Why and how physical activity promotes experience-induced brain plasticity. Front Neurosci 4:189PubMedCrossRefGoogle Scholar
  29. 29.
    Keroughlian AS, Knudsen EI (2007) Adaptive auditory plasticity in developing and adult animals. Prog Neurobiol 82:109–121CrossRefGoogle Scholar
  30. 30.
    Levi-Montalcini R, Levi G (1944) Correlazioni nello sviluppo tra varie parti del sistema nervoso. Pont Acad Sci 8:527–568Google Scholar
  31. 31.
    Lichtman JW (1977) The reorganization of synaptic connexions in the rat submandibular gnalgion during post-natal development. J Physiol 273:155–177PubMedGoogle Scholar
  32. 32.
    Lledo PM, Saghatelyan A (2005) Integrating new neurons into the adult olfactory bulb: joining the network, life-death decisions, and the effects of sensory experience. Trends Neurosci 28:248–254PubMedCrossRefGoogle Scholar
  33. 33.
    Lukaszewicz A, Savatier P, Cortay V, Giroud P, Huissoud C, Berland M, Kennedy H, Dehay C (2005) G1 phase regulation, area-specific cell cycle control, and cytoarchitectonics in the primate cortex. Neuron 47:353–364PubMedCrossRefGoogle Scholar
  34. 34.
    Luzzati F, De Marchis S, Fasolo A, Peretto P (2007) Adult neurogenesis and local neuronal progenitors in the striatum. Neurodegener Dis 4:322–327PubMedCrossRefGoogle Scholar
  35. 35.
    Ma DK, Kim WR, Ming GL, Song H (2009) Activity-dependent extrinsic regulation of adult olfactory bulb and hippocampal neurogenesis. Ann NY Acad Sci 1170:664–673PubMedCrossRefGoogle Scholar
  36. 36.
    MacLaren RE, Pearson RA, MacNeil A, Douglas RH, Salt TH, Akimoto M, Swaroop A, Sowden JC, Ali RR (2006) Retinal repair by transplantation of photoreceptor precursors. Nature 444:203–207PubMedCrossRefGoogle Scholar
  37. 37.
    McConnell SK (1995) Strategies for the generation of neuronal diversity in the central nervous system. J Neurosci 15:6987–6998PubMedGoogle Scholar
  38. 38.
    Ming GL, Song H (2005) Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 28:223–250PubMedCrossRefGoogle Scholar
  39. 39.
    Muotri A, Gage FH (2006) Generation of neuronal variability and complexity. Nature 441:1087–1093PubMedCrossRefGoogle Scholar
  40. 40.
    Nudo RJ (2003) Retuning the misfiring brain. Proc Natl Acad Sci USA 100:7425–7427PubMedCrossRefGoogle Scholar
  41. 41.
    Oboti L, Savalli G, Giachino C, De Marchis S, Panzica GC, Fasolo A, Peretto P (2009) Integration and sensory experience-dependent survival of newly-generated neurons in the accessory olfactory bulb of female mice. Eur J Neurosci 29:679–692PubMedCrossRefGoogle Scholar
  42. 42.
    Oppenheim RW, Johnson JE (2003) Programmed cell death and neurotrophic factors. In: Squire LR, Bloom FE, McConnell SK, Roberts JL, Spitzer NC, Zigmond MJ (eds) Fundamental neuroscience. Academic, New York//LondonGoogle Scholar
  43. 43.
    Pizzorusso T, Medini P, Berardi N, Chierzi S, Fawcett JW, Maffei L (2002) Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298:1187–1189CrossRefGoogle Scholar
  44. 44.
    Purves D (1988) Body and brain: a trophic theory of neural connections. Harvard University Press, Cambridge, MA/LondonGoogle Scholar
  45. 45.
    Purves D (1994) Neural activity and the growth of the brain. Cambridge University Press, CambridgeGoogle Scholar
  46. 46.
    Purves D, Lichtman JW (1980) Synapse elimination in the developing nervous system. Science 210:153–157PubMedCrossRefGoogle Scholar
  47. 47.
    Purves D, Lichtman JW (1985) Principles of neural development. Sinauer, SunderlandGoogle Scholar
  48. 48.
    Purves D, Snider VD, Voyvodic JT (1988) Trophic regulation of nerve cell morphology and innervation in the autonomic nervous system. Nature 336:123–128PubMedCrossRefGoogle Scholar
  49. 49.
    Purves D, White LE, Riddle D (1996) Is neural development Darwinian? Trends Neurosci 19:460–464PubMedCrossRefGoogle Scholar
  50. 50.
    Raisman G, Field PM (1973) A quantitative investigation of the development of collateral reinnervation after partial deafferentation of the septal nuclei. Brain Res 50:241–264PubMedCrossRefGoogle Scholar
  51. 51.
    Reichert E (2009) Evolutionary conservation of mechanisms for neural regionalization, proliferation and interconnection in brain development. Biol Lett 5:112–116PubMedCrossRefGoogle Scholar
  52. 52.
    Robel S, Berninger B, Götz M (2011) The stem cell potential of glia: lessons from reactive gliosis. Nat Rev Neurosci 12:88–104PubMedCrossRefGoogle Scholar
  53. 53.
    Rossi F, Gianola S, Corvetti L (2007) Regulation of intrinsic neuronal properties for axon growth and regeneration. Prog Neurobiol 81:1–28PubMedCrossRefGoogle Scholar
  54. 54.
    Sale A, Berardi N, Maffei L (2009) Enrich the environment to empower the brain. Trends Neurosci 32:233–239PubMedCrossRefGoogle Scholar
  55. 55.
    Sanes JR, Lichtman JW (1999) Development of the vertebrate neuromuscular junction. Annu Rev Neurosci 22:389–442PubMedCrossRefGoogle Scholar
  56. 56.
    Schweigreiter R (2008) The natural history of the myelin-derived nerve growth inhibitor Nogo-A. Neuron Glia Biol 4:83–89PubMedCrossRefGoogle Scholar
  57. 57.
    Striedter GF (2004) Principles of brain evolution. Sinauer, SunderlandGoogle Scholar
  58. 58.
    Suh H, Weng D, Gage FH (2009) Signaling in adult neurogenesis. Annu Rev Cell Dev Biol 25:153–175CrossRefGoogle Scholar
  59. 59.
    Sur M, Frost DO, Hockfield S (1988) Expression of a surface-associated antigen on Y-Cells in the cat lateral geniculate nucleus is regulated by visual experience. J Neurosci 8:874–882PubMedGoogle Scholar
  60. 60.
    Wiesel TN (1982) Postnatal development of the visual cortex and the influence of environment. Nature 299:583–591PubMedCrossRefGoogle Scholar
  61. 61.
    Williams ME, de Wit J, Ghosh A (2010) Molecular mechanisms of synaptic specificity in developing neural circuits. Neuron 68:9–18PubMedCrossRefGoogle Scholar
  62. 62.
    Wong ROL, Lichtman JW (2003) Synapse elimination. In: Squire LR, Bloom FE, McConnell SK, Roberts JL, Spitzer NC, Zigmond MJ (eds) Fundamental neuroscience. Academic, New York/LondonGoogle Scholar
  63. 63.
    Zheng D, Purves D (1995) Effects of increased neural activity on brain growth. Proc Natl Acad Sci USA 92:1802–1806PubMedCrossRefGoogle Scholar
  64. 64.
    Zhou X, Merzenich MM (2009) Developmentally degraded cortical temporal processing restored by training. Nat Neurosci 12:26–28PubMedCrossRefGoogle Scholar
  65. 65.
    Zhou X, Ngarajan N, Mossop BJ, Merzenich MM (2008) Influences of un-modulated acoustic inputs on functional maturation and critical-period plasticity of the primary auditory cortex. Neuroscience 154:390–396PubMedCrossRefGoogle Scholar
  66. 66.
    Zipursky SL, Sanes JR (2010) Chemoaffinity revisited: dscams, protocadherins, and neural circuit assembly. Cell 143:343–353PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Italia S.r.l.  2012

Authors and Affiliations

  1. 1.Department of Neuroscience, Section of PhysiologyUniversity of TurinOrbassanoItaly

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