Skip to main content

Structural Plasticity in Adult Nervous System: An Historic Perspective

  • Chapter
  • First Online:
Endogenous Stem Cell-Based Brain Remodeling in Mammals

Part of the book series: Stem Cell Biology and Regenerative Medicine ((STEMCELL))

Abstract

In the adult central nervous system, neurons are endowed with a remarkable power: a continuous structural remodeling of their connections owing to minuscule changes of their axonal terminal branches and synaptic boutons, simultaneously with the growing and pruning of their distal dendritic branches and spines. In this review, we summarize the history of the concept of structural plasticity from its beginnings in the nineteenth century to its consolidation in our days, with the establishment of a clear relationship between the structural plasticity of neural circuits and memory and learning processes. After a short review of the morphological changes observed at all levels of highly activated neurons (dendritic spines, distal dendritic branches, axonal initial segments) in adult healthy animals, we cover a more classical topic by reporting the structural changes consecutive to neuronal lesions, particularly after axotomy or deafferentation. Finally, we discuss work done with grafts of embryonic central nervous tissue in adult mice with genetic or experimental brain lesions in order to determine the capability of the embryonic cells to substitute missing neurons in the adult animals. We present in particular the “adaptive rejuvenation,” i.e., the plasticity induced in the host adult cells by the grafted immature neural cells to allow their interaction and subsequent integration in the adult circuit. Our conclusion is the remarkable capacity for structural plasticity of adult neural cells, which still needs the full understanding of their genetic regulation.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

6OHDA:

6-Hydroxydopamine

AChE:

Acetylcholinesterase

AIS:

Axonal initial segments

ChABC:

Chondroitinase ABC

CLSM:

Confocal laser scanning microscopy

CNS:

Central nervous system

CST:

Corticospinal tract

DA:

Dopamine

E:

Embryonic day

LTP:

Long-term potentiation

MFB:

Medial forebrain bundle

P:

Postnatal day

PC:

Purkinje cell

Pcd:

Purkinje cell degeneration mutant strain of mice

PSDs:

Postsynaptic differentiations

TEA:

Tetraethylammonium

TPLSM:

Two-photon laser scanning microscopy

References

  • Agnati LF, Fuxe K, Zoli M, Ozini I, Toffano G, Ferraguti F (1986) A correlation analysis of the regional distribution of central encephalin and beta-endorphin immunoreactive terminals and of opiate receptors in the adult and old male rats. Evidence for the existence of two main types of communication in the central nervous system: the volume transmission and the wiring transmission. Acta Physiol Scand 128:201–207

    CAS  PubMed  Google Scholar 

  • Aguayo AJ (1985) Axonal regeneration from injured neurons in the adult mammalian central nervous system. In: Cotman CW (ed) Synaptic plasticity. Guilford, New York, pp 457–538

    Google Scholar 

  • Andres KH (1965) Uber die Feinstruktur besonderer Einrichtungen in markhaltigen Nervenfasern des Kleinhirns der Ratte. Z Zellforsch Mikroskop Anat 65:701

    CAS  Google Scholar 

  • Angaut P, Sotelo C (1973) The fine structure of the cerebellar nuclei of the cat. II. Synaptic organization. Exp Brain Res 16:431–454

    CAS  PubMed  Google Scholar 

  • Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O (2002) Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 8:963–970

    CAS  PubMed  Google Scholar 

  • Bailey CH, Kandel ER (1993) Structural changes accompanying memory storage. Annu Rev Physiol 55:397–426

    CAS  PubMed  Google Scholar 

  • Bain A (1855) The senses and the intellect. John W Parker and Son, London

    Google Scholar 

  • Bain A (1873) Mind and body. The theories of their relation. D Appleton & Comp, New York

    Google Scholar 

  • Bareyre FM, Kerschensteiner M, Raineteau O, Mettenleiter TC, Weinmann O, Schwab ME (2004) The injured spinal cord spontaneously forms a new intraspinal circuit in adult rats. Nat Neurosci 7:269–277

    CAS  PubMed  Google Scholar 

  • Bawden HH (1900) A digest and criticism of the data upon which is based the theory of the amoeboid movements of the neurone. J Comp Neurol 10:243–264

    Google Scholar 

  • Beale L (1862) Note on the minute structure of the grey matter of the convolutions of the brain of man, the sheep, cat, and dog. Proc R Soc Lond 12:671–673

    Google Scholar 

  • Beale L (1963) Indications of the paths taken by the nerve-currents as they traverse the caudate nerve-cells of the spinal cord and encephalon. Proc R Soc Lond 13:386–392

    Google Scholar 

  • Beaudet A, Sotelo C (1981) Synaptic remodeling of serotonin axon terminals in rat agranular cerebellum. Brain Res 206:305–329

    CAS  PubMed  Google Scholar 

  • Bennett EL, Diamond MC, Krech D, Rosenzweig MR (1964) Chemical and anatomical plasticity of brain changes in brain through experience, demanded by learning theories, are found in experiments with rats. Science 146:610–619

    CAS  PubMed  Google Scholar 

  • Berlucchi G, Buchtel HA (2009) Neuronal plasticity: historical roots and evolution of meaning. Exp Brain Res 192:307–319

    CAS  PubMed  Google Scholar 

  • Bhatt DH, Zhang S, Gao W-B (2009) Dendritic spines dynamics. Annu Rev Plant Physiol Plant Mol Biol 71:261–282

    CAS  Google Scholar 

  • Björklund A, Stenevi U, Svendgaard NA (1976) Growth of transplanted monoaminergic neurones into the adult hippocampus along the perforant path. Nature 262:787–790

    PubMed  Google Scholar 

  • Björklund A, Stenevi U (1979) Reconstruction of the nigrostriatal dopamine pathway by intracerebral nigral transplants. Brain Res 177:555–560

    PubMed  Google Scholar 

  • Björklund LM, Sanchez-Pernaute R, Chung S, Andersson T, Chen IY, McNaught KS, Brownell AL, Jenkins BG, Wahlestedt C, Kim KS, Isacson O (2002) Embryonic stem cells develop into functional dopaminergic neurons after transplantation in a Parkinson rat model. Proc Natl Acad Sci U S A 99:2344–2349

    PubMed Central  PubMed  Google Scholar 

  • Bliss TVP, Lømo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 232:331–356

    CAS  PubMed  Google Scholar 

  • Brodal A (1973) Self-observations and neuro-anatomical considerations after a stroke. Brain 96:675–694

    CAS  PubMed  Google Scholar 

  • Cajal SR (1888) Estructura de los centros nerviosos de las aves. Rev Trim Histol Norm Patol 1:1–10

    Google Scholar 

  • Cajal SR (1890) À propos des certains éléments bipolaires du cervelet avec quelques détails nouveaux sur l’évolution des fibres cérébelleuses. Int Msch Anat Physiol 7:12–30, French translation of the Spanish paper: Sobre ciertos elementos bipolares del cerebelo joven y algunos detalles más acerca del crecimiento y evolución de las fibras cerebelosas. Gaceta Sanitaria de Barcelona

    Google Scholar 

  • Cajal SR (1892) Nuevo concepto de la histología de los centros nerviosos. Revista Ciencias Medicas de Barcelona 18:5–68

    Google Scholar 

  • Cajal SR (1894) The Croonian Lecture: La fine structure des centres nerveux. Proc R Soc Lond 55:444–468

    Google Scholar 

  • Cajal SR (1895) Algunas conjeturas sobre el mecanismo anatómico de la ideación, asociación y atención. Rev Med Cirug Práct 19:497–508

    Google Scholar 

  • Cajal SR (1896) Las espinas colaterales de las células del cerebro teñidas con el azul de metileno. Rev Trim Micrográfica 1:123–136

    Google Scholar 

  • Cajal SR (1913/1914) Estudios sobre la Degeneración y Regeneración del Sistema Nervioso. Tomo I (1913) Degeneración y Regeneración de los Nervios. Tomo II (1914) Degeneración y Regeneración de los Centros Nerviosos. Imprenta Hijos de Nicolas Moya (Madrid)

    Google Scholar 

  • Cajal SR (1928) Degeneration and regeneration of the nervous system. Oxford Univ, Press (London)

    Google Scholar 

  • Carpenter WB (1874) Principles of mental physiology, with their applications to the training and discipline of the mind, and study of its morbid conditions. D Appleton & Company, New York

    Google Scholar 

  • Carulli D, Pizzorusso T, Kwok JCF, Putignano E, Poli A, Forostyak S, Andrews MR, Deepa SS, Glant TT, Fawcett JW (2010) Animals lacking link protein have attenuated perineuronal nets and persistent plasticity. Brain 133:2331–2347

    PubMed  Google Scholar 

  • Ceccarelli B, Clementi F, Mantegazza P (1971) Synaptic transmission in the superior cervical ganglion of the cat after reinnervation by vagus fibres. J Physiol Lond 216:87–98

    CAS  PubMed  Google Scholar 

  • Comery TA, Shah R, Greenough WT (1995) Differential rearing alters spine density on medium-sized spiny neurons in the rat corpus striatum: evidence for association of morphological plasticity with early response gene expression. Neurobiol Learn Mem 63:217–219

    CAS  PubMed  Google Scholar 

  • Comery TA, Stamoudis CX, Irwin SA, Greenough WT (1996) Increased density of multiple-head dendritic spines on médium-sized spiny neurons of the striatum in rats reared in complex environment. Neurobiol Learn Mem 66(2):93–96

    CAS  PubMed  Google Scholar 

  • Coombs JS, Curtis DR, Eccles JC (1957) The interpretation of spike potentials of motoneurons. J Physiol 139:198–231

    CAS  PubMed  Google Scholar 

  • Crepel F, Mariani J, Delhaye-Bouchaud N (1976) Evidence for e multiple innervation of Purkinje cells by climbing fibers in the immature rat cerebellum. J Neurobiol 7:567–578

    CAS  PubMed  Google Scholar 

  • Das GD, Altman J (1971) Transplanted precursors of nerve cells: their fate in the cerebellums of young rats. Science 173:637–638

    CAS  PubMed  Google Scholar 

  • DeFelipe J (2006) Brain plasticity and mental processes: cajal again. Nat Rev Neurosci 7:811–817

    CAS  PubMed  Google Scholar 

  • Del Conte G (1907) Einpfanzungen von Embryonalem Gewebe im Gehirn. Ziegler’s Beitrage zur pathol Anat, u z allg Pathol Bd 42(1):62–67

    Google Scholar 

  • Dellman HD, Rodriguez EM (1970) Herring bodies; an electron microscopic study of local degeneration and regeneration of neurosecretory axons. Z Zellforsch 111:293–315

    Google Scholar 

  • Deng W, Aimone JB, Gage FH (2010) New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nature Rev Neurosci 11:339–350

    CAS  Google Scholar 

  • Desmond NL, Levy WB (1990) Morphological correlates of long-term potentiation imply the modification of existing synapses, not synaptogenesis, in the hippocampal dentate gyrus. Synapse 5:139–143

    CAS  PubMed  Google Scholar 

  • Diamond MC, Krech D, Rosenzweig MR (1964) The effects of an enriched environment on the rat cerebral cortex. J Comp Neurol 123:111–119

    CAS  PubMed  Google Scholar 

  • Dusart I, Ghoumari AM, Wehrle R, Morel MP, Bouslama-Oueghlani L, Camand E, Sotelo C (2005) Cell death and axon regeneration of purkinje cells after axotomy: challenges of classical hypotheses of axon regeneration. Brain Res Rev 49:300–316

    CAS  PubMed  Google Scholar 

  • Duval M (1895) Hypohèses sur la physiologie des centres nerveux: théorie histologique du sommeil. Comptes Rendus de la Société de Biologie 2 et 9 Février 47:74–77

    Google Scholar 

  • Engert F, Bonhoeffer T (1999) Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399:66–70

    CAS  PubMed  Google Scholar 

  • Espuny-Camacho I, Michelsen K, Gall D, Linaro D, Hasche A, Bonnefont J, Bali C, Orduz D, Bilheu A, Herpoel A, Lambert N, Gaspard N, Péron S, Schiffmann SN, Giugliano M, Gaillard A, Vanderhaeghen P (2013) Pyramidal neurons derived from human pluripotent stem cells integrate efficiently into mouse brain circuits in vivo. Neuron 77:440–456

    CAS  PubMed  Google Scholar 

  • Fernandez-Gonzalez A, La Spada AR, Treadaway J, Higdon JC, Harris BS, Sidman RL, Morgan JI, Zuo J (2002) Purkinje cell degeneration (pcd) phenotypes caused by mutations in the axotomy-induced gene. Nna1 Sci 295:1904–1906

    CAS  Google Scholar 

  • Fiala BA, Joyce JN, Greenough WT (1978) Environmental complexity modulates growth of granule cells dendrites in developing but not adult hippocampus of rats. Exp Neurol 59:372–383

    CAS  PubMed  Google Scholar 

  • Fifková E, Anderson CL (1981) Stimulation-induced changes in dimensions of stalks of dendritic spines in the centate molecular layer. Exp Neurol 74:621–627

    PubMed  Google Scholar 

  • Fifková E, Van Harreveld A (1977) Long-lasting morphological changes in dendritic spines of dentate granular cells following stimulation of the entorhinal area. J Neurocytol 6:211–230

    PubMed  Google Scholar 

  • Filbin MT (2003) Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS. Nat Rev Neurosci 4:703–713

    CAS  PubMed  Google Scholar 

  • Finger S (1994) Origins of neuroscience: a history of explorations into brain function. Oxford University Press, New York

    Google Scholar 

  • Freund P, Schmidlin E, Wannier T, Bloch J, Mir A, Schwab ME, Rouiller EM (2006) Nogo-A-specific antibody treatment enhances sprouting and functional recovery after cervical lesion in adult primates. Nat Med 12:790–792

    Google Scholar 

  • Freund J, Brandmaier AM, Lewenjohann L, Kirste I, Kritzler M, Krüger A, Sachser N, Lindenberger U, Kempermann G (2013) Emergence of individuality in genetically identical mice. Science 340:756–759

    Google Scholar 

  • Gaillard A, Gaillard F, Roger M (1998) Neocortical grafting to newborn and adult rats: development, anatomical and functional aspects. Adv Anat Embryol Cell Biol 148:1–86

    CAS  PubMed  Google Scholar 

  • Gaillard A, Prestoz L, Dumartin B, Cantereau A, Morel F, Roger M, Jaber M (2007) Reestablishment of damaged adult motor pathways by grafted embryonic cortical neurons. Nat Neurosci 10:1294–1299

    CAS  PubMed  Google Scholar 

  • Galimberti I, Gogolla N, Alberi S, Santos AF, Muller D, Caroni P (2006) Long-term rearrangements of hippocampal mossy fiber terminal connectivity in the adult regulated by experience. Neuron 50:749–763

    CAS  PubMed  Google Scholar 

  • Galtrey CM, Fawcett JW (2007) The role of chondroitin sulfate proteoglycans in regeneration and plasticity in the central nervous system. Brain Res Rev 54:1–18

    CAS  PubMed  Google Scholar 

  • Gardette R, Crepel F, Alvarado-Mallart RM, Sotelo C (1990) Fate of grafted embryonic Purkinje cells in the cerebellum of the adult “Purkinje cell degeneration” mutant mouse. II. Development of synaptic responses : an in vitro study. J Comp Neurol 295:188–196

    CAS  PubMed  Google Scholar 

  • Gaspard N, Bouschet T, Hourez R, Dimidschstein J, Naeije G, van den Ameele J, Espuny- Camacho I, Herpoel A, Passante L, Schiffmann SN, Gaillard A, Vanderhaeghen P (2008) An intrinsic mechanism of corticogenesis from embryonic stem cells. Nature 455:351–357

    CAS  PubMed  Google Scholar 

  • Geinisman Y, Morrell F, deToledo-Morrell L (1989) Perforated synapses on double-headed dendritic spines: a possible structural substrate of synaptic plasticity. Brain Res 480:326–329

    CAS  PubMed  Google Scholar 

  • Gentschev T, Sotelo C (1973) Degenerative patterns in the ventral cochlear nucleus of the rat after primary deafferentation. An ultra-structural study. Brain Res 62:37–60

    CAS  PubMed  Google Scholar 

  • Gerlach J (1871) Von dem Rückenmark. In: Stricker S (ed) Handbuch der Lehre von den Geweben des Menschen und der Thiere. Wilhelm Engelmann, Leipzig, pp 665–693

    Google Scholar 

  • Golgi C (1873) Sulla struttura della sostanza grigia del cervello. Gazzetta Medica Italiana Lombardia 33:244–246

    Google Scholar 

  • Gray EG (1959) Electron microscopy of synaptic contacts on dendrite spines of the cerebral cortex. Nature 183:1592–1593

    CAS  PubMed  Google Scholar 

  • Gray EG, Hamlyn LH (1962) Electron microscopy of experimental degeneration in the avian optic tectum. J Anat 96:309–316

    CAS  PubMed  Google Scholar 

  • Greenough WT, Volkmar FR (1973) Pattern of dendritic branching in occipital cortex of rats reared in complex environments. Exp Neurol 40:491–504

    CAS  PubMed  Google Scholar 

  • Greenough WT, McDonald JW, Parnisari RM, Camel JE (1986) Environmental conditions modulate degeneration and new dendrite growth in cerebellum of senescent rats. Brain Res 380:136–143

    CAS  PubMed  Google Scholar 

  • Grubb MS, Burrone J (2010) Activity-dependent relocation of the axon initial segment fine-tunes neuronal excitability. Nature 465:1070–1074

    CAS  PubMed Central  PubMed  Google Scholar 

  • Grutzendler J, Kasthuri N, Gan W-B (2002) Long-term dendritic spine stability in the adult cortex. Nature 420:812–816

    CAS  PubMed  Google Scholar 

  • Harris KM, Fiala JC, Ostroff L (2003) Structural changes at dendritic spines synapses during long-term potentiation. Phil Trans R Soc Lond B 358:745–748

    Google Scholar 

  • Hashimoto PH, Palay SL (1965) Peculiar axons with enlarged endings in the nucleus gracilis. Anat Rec 151:454–455

    Google Scholar 

  • Hatton GI (1997) Function-related plasticity in hypothalamus. Annu Rev Neurosci 20:375–397

    CAS  PubMed  Google Scholar 

  • Hebb DO (1949) The organization of behavior. A neuropsychological theory. Chapter 4, “the first stage of perception: growth of the assembly”. Wiley, New York, pp 60–78

    Google Scholar 

  • His W (1886) Zur Geschichte des menschlichen Rückenmarkes und der Nervenwurzeln. Abhandl Kgl sächsGes. Wissensch math-phys Kl 13:479–513

    Google Scholar 

  • His W (1889) Die Neuroblasten und deren Entstehung in embryonalen Mark. Abhandl Kgl sächs Ges. Wissensch math-phys K1 15:313–372

    Google Scholar 

  • Hunt CC, Nelson PG (1965) Structural and functional changes in the frog sympathetic ganglion following cutting of the presynaptic nerve fibres. J Physiol 177:1–20

    CAS  PubMed  Google Scholar 

  • James W (1890) The principles of psychology, vol 1. Macmillan, London

    Google Scholar 

  • Jones EG (1994) Santiago Ramón y cajal and the croonian lecture, march 1894. Trends Neurosci 17:190–192

    CAS  PubMed  Google Scholar 

  • Jones EG (2000) Plasticity and neuroplasticity. J Hist Neurosci 9:37–39

    Google Scholar 

  • Juraska JM, Greenough WT, Elliott C, Mack KJ, Berkowitz R (1980) Plasticity in adult rat visual cortex: an examination of several cell populations after differential rearing. Behav Neural Biol 29:157–167

    CAS  PubMed  Google Scholar 

  • Kasai H, Hayama T, Ishikawa M, Watanabe S, Yagishita S, Noguchi J (2010) Learning rules and persistence of dendritic spines. Eur J Neurosci 32:241–249

    PubMed  Google Scholar 

  • Koelliker A (1896) Handbuch der Gewebelehre des Menschen und der Thiere, vol II, 6th edn. Wilhelm Engelmann Verlag, Leipzig

    Google Scholar 

  • Kole MH, Ilschner SU, Kampa BM, Williams SR, Ruben PC, Stuart GJ (2008) Action potential generation requires a high sodium channel density in the axon initial segment. Nat Neurosci 11:178–186

    CAS  PubMed  Google Scholar 

  • Konorski J (1948) Conditioned reflexes and neuron organization. Cambridge Univ. Press, Cambridge, p 267, Reprinted with a supplementary chapter in 1968, New York: Hafner Publ. Co

    Google Scholar 

  • Kuba H (2012) Structural tuning and plasticity of the axon initial segment in auditory neurons. J Physiol 590:5571–5579

    CAS  PubMed  Google Scholar 

  • Kuba H, Ishii TM, Ohmori H (2006) Axonal site of spike initiation enhances auditory coincidence detection. Nature 444:1069–1072

    CAS  PubMed  Google Scholar 

  • Kuba H, Oichi Y, Ohmori H (2010) Presynaptic activity regulates Na + channel distribution at the axon initial segment. Nature 465:1075–1078

    CAS  PubMed  Google Scholar 

  • Lai CS, Franke TF, Gan WB (2012) Opposite effects of fear conditioning and extinction on dendritic spine remodeling. Nature 483:87–91

    CAS  PubMed  Google Scholar 

  • LaMantia AS, Pomeroy SL, Purves D (1992) Vital imaging of glomeruli in the mouse olfactory bulb. J Neurosci 12:976–988

    CAS  PubMed  Google Scholar 

  • Lendahl U, Zimmerman LB, McKay RD (1990) CNS stem cells express a new class of intermediate filament protein. Cell 60:585–595

    CAS  PubMed  Google Scholar 

  • Lepousez G, Valley MT, Lledo PM (2013) The impact of adult neurogenesis on olfactory bulb circuits and computations. Annu Rev Physiol 75:339–363

    CAS  PubMed  Google Scholar 

  • Leuner B, Shors TJ (2004) New spines, new memories. Mol Neurobiol 29:117–130

    CAS  PubMed Central  PubMed  Google Scholar 

  • Li Y, Field PM, Raisman G (1997) Repair of adult rat corticospinal tract by transplants of olfactory ensheathing cells. Science 277:2000–2002

    CAS  PubMed  Google Scholar 

  • Liebscher T, Schnell L, Schnell D, Scholl J, Schneider R, Gullo M, Fouad K, Mir A, Rausch M, Kindler D, Hamers FPT, Schwab ME (2005) Nogo-A antibody improves regeneration and locomotion of spinal cord-injured rats. Ann Neurol 58:706–719

    CAS  PubMed  Google Scholar 

  • Lin XY, Glanzman DL (1994) Long-term potentiation in Aplysia sensorimotor synapses in cell culture: regulation by postsynaptic voltage. Proc Biol Sci 255:113–118

    CAS  PubMed  Google Scholar 

  • Liu CN, Chambers WW (1958) Intraspinal sprouting of dorsal root axons; development of new collaterals and preterminals following partial denervation of the spinal cord in the cat. AMA Arch Neurol Psychiatry 79:46–61

    CAS  PubMed  Google Scholar 

  • Lu P, Yang H, Jones LL, Filbin MT, Tuszynski MH (2004) Combinatorial therapy with neurotrophins and cAMP promotes axonal regeneration beyond sites of spinal cord injury. J Neurosci 24:6402–6409

    CAS  PubMed  Google Scholar 

  • Lugaro E (1909) Modern problems in psychiatry (English translation of the book published in 1906). The University Press, Manchester

    Google Scholar 

  • Lund RD (1969) Synaptic patterns of the superficial layers of the superior colliculus of the rat. J Comp Neurol 135:179–208

    CAS  PubMed  Google Scholar 

  • Maier IC, Ichiyama RM, Courtine G, Schnell L, Lavrov I, Edgerton VR, Schwab ME (2009) Differential effects of anti-nogo-A antibody treatment and treadmill training in rats with incomplete spinal cord injury. Brain 132:1426–1440

    PubMed  Google Scholar 

  • Markham JA, Greenough WT (2004) Experience-driven brain plasticity: beyond the synapse. Neuron Glia Biol 1:351–363

    PubMed Central  PubMed  Google Scholar 

  • Martino G, Pluchino S, Bonfanti L, Schwartz M (2011) Brain regeneration in physiology and pathology: the immune signature driving therapeutic plasticity of neural stem cells. Physiol Rev 91:1281–1304

    CAS  PubMed Central  PubMed  Google Scholar 

  • McDonald JW, Liu XZ, Qu Y, Liu S, Mickey SK, Turetsky D, Gottlieb DI, Choi DW (1999) Transplanted embryonic stem cells survive, differentiate and promote recovery in injured rat spinal cord. Nat Med 5:1410–1412

    CAS  PubMed  Google Scholar 

  • Mobley P, Greengard P (1985) Evidence for widespread effects of noradrenaline on axon terminals in the rat frontal cortex. Proc Natl Acad Sci U S A 82:945–947

    CAS  PubMed Central  PubMed  Google Scholar 

  • Moore DL, Goldberg JL (2011) Multiple transcription factor families regulate axon growth and regeneration. Devel Neurobio 12:1186–1211

    Google Scholar 

  • Mugnaini E, Walberg F, Hauglie-Hanssen E (1967) Observations on the fine structure of the lateral vestibular nucleus (Deiters' nucleus) in the cat. Exp Brain Res 4:146–186

    CAS  PubMed  Google Scholar 

  • Mullen RJ, Eicher EM, Sidman RL (1976) Purkinje cell degeneration, a new neurological mutation in the mouse. Proc Natl Acad Sci U S A 73:208–212

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nageotte J (1906) Note sur la régénération collatérale des neurones radiculaires postérieurs dans le tabes. Compt Rend Soc Biol Paris 60:745

    Google Scholar 

  • Nageotte J (1907) Greffe de ganglions rachidiens survie des éléments nobles et transformation des cellules unipolaires en cellules multipolaires. Compt Rend Soc Biol Paris 62:63

    Google Scholar 

  • Paillard J (1976) Réflexions sur l’usage du concept de plasticité en neurobiologie. J Psychol Norm Pathol 1:33–47

    Google Scholar 

  • Palay SL, Sotelo C, Peters A, Orkand PM (1968) The axon hillock and the initial segment. J Cell Biol 38:193–201

    CAS  PubMed  Google Scholar 

  • Pinching AJ (1969) Persistence of post-synaptic membrane thickenings after degeneration of olfactory nerves. Brain Res 16:277–281

    CAS  PubMed  Google Scholar 

  • Purves D, Hadley RD, Voyvodic JT (1986) Dynamic changes in the dendritic geometry of individual neurons visualized over periods up to three months in the superior cervical ganglion of living mice. J Neurosci 6:1051–1060

    CAS  PubMed  Google Scholar 

  • Rabl-Rückhard H (1890) Sind die Ganglienzellen amöboid? Eine Hypothese zur Mechanik psychischer Vorgänge. Neurologische Centralblatt 7:199–200

    Google Scholar 

  • Raisman G (1969) Neuronal plasticity in the septal nuclei of the adult rat. Brain Res 14:25–48

    CAS  PubMed  Google Scholar 

  • Raineteau O, Schwab ME (2001) Plasticity of motor systems after incomplete spinal cord injury. Nat Rev Neurosci 2:263–273

    CAS  PubMed  Google Scholar 

  • Ranson SW (1909) Transplantation of the spinal ganglion to the brain. Quart Bull Northwestern Univ Med School 11:176

    Google Scholar 

  • Ranson SW (1914) Transplantation of the spinal ganglion, with observations on the significance of the complex types of spinal ganglion cells. J Comp Neurol 24:547–558

    Google Scholar 

  • Renfranz PJ, Cunningham MG, McKay RD (1991) Region-specific differentiation of the hippocampal stem cell line HiB5 upon implantation into developing mammalian brain. Cell 66:713–729

    CAS  PubMed  Google Scholar 

  • Rhodes KE, Fawcett JW (2004) Chondroitin sulphate proteoglycans: preventing plasticity or protecting the CNS? J Anat 204:33–48

    CAS  PubMed  Google Scholar 

  • Rosenzweig MR (2007) Modification of brain circuits through experience. In: Bermudez-Rattoni F (ed) Neural plasticity and memory: from genes to brain imaging. CRC Press, Boca Raton

    Google Scholar 

  • Ruediger S, Vittori C, Bednarek E, Genoud C, Strata P, Sacchetti B, Caroni P (2011) Learning-related feedforward inhibitory connectivity growth required for memory precision. Nature 473:514–518

    CAS  PubMed  Google Scholar 

  • Rustioni A, Sotelo C (1974) Some effects of chronic deafferentation on the ultrastructure of the nucleus gracilis of the cat. Brain Res 28:527–533

    Google Scholar 

  • Saha B, Jaber M, Gaillard A (2012) Potentials of endogenous neural stem cells in cortical repair. Frontiers Cell Neurosci. doi:10.3389/fncel.2012.00014

    Google Scholar 

  • Saltykow S (1905) Versuche über Gehirnplantation, zugleich ein Beitrag zur Kenntnis der Vorgänge an den zelligen Gehirne-elementen. Arch Psychiatr Nervenkr 40:329–388

    Google Scholar 

  • Sandbank U, Lerman P, Geifman M (1970) Infantile neuroaxonal dystrophy: cortical axonic and presynaptic changes. Acta Neuropathol 16:342–352

    CAS  PubMed  Google Scholar 

  • Schnell L, Schwab ME (1993) Sprouting and regeneration of lesioned corticospinal tract fibres in the adult rat spinal cord. Eur J Neurosci 5:1156–1171

    CAS  PubMed  Google Scholar 

  • Schwab ME (2004) Nogo and axon regeneration. Curr Opin Neurobiol 14:118–124

    CAS  PubMed  Google Scholar 

  • Sherrington CS (1897) The central nervous system. In: Foster M (ed) A textbook of physiology, vol III, 7th edn. Macmillan, London

    Google Scholar 

  • Silver J, Miller JH (2004) Regeneration beyond the glial scar. Nat Rev Neurosci 5:146–156

    CAS  PubMed  Google Scholar 

  • Sirevaag AM, Greenough WT (1985) Differential rearing effects on Rat visual cortex synapses. II. Synaptic morphometry. Dev Brain Res 19:215–226

    Google Scholar 

  • Snyder EY, Deitcher DL, Walsh C, Arnold-Aldea S, Hartwieg EA, Cepko CL (1992) Multipotent neural cell lines can engraft and participate in development of mouse cerebellum. Cell 66:33–51

    Google Scholar 

  • Song A-H, Wang D, Chen G, Li Y, Luo J, Duan S, M-m P (2009) A selective filter for cytoplasmic transport at the axon initial segment. Cell 136:1148–1160

    CAS  PubMed  Google Scholar 

  • Sotelo C (1968) Permanence of postsynaptic specializations in the frog sympathetic ganglion cells after denervation. Exp Brain Res 6:294–305

    CAS  PubMed  Google Scholar 

  • Sotelo C (1975) Synaptic remodeling in mutants and experimental animals. In: Vital-Durand F, Jeannerod M (eds) Aspects of neuronal plasticity. Editions de l’INSERM, Paris, pp 167–190, Colloques de l’ INSERM Vol 43

    Google Scholar 

  • Sotelo C (2003) Viewing the brain through the master hand of Ramón y Cajal. Nat Rev Neurosci 4:71–77

    CAS  PubMed  Google Scholar 

  • Sotelo C (2004) Cellular and genetic regulation of the development of the cerebellar system. Prog Neurobiol 72:295–339

    CAS  PubMed  Google Scholar 

  • Sotelo C (2008) Viewing the cerebellum through the eyes of Ramón y Cajal. Cerebellum 7:517–522

    PubMed  Google Scholar 

  • Sotelo C, Alvarado-Mallart RM (1986) Growth and differentiation of cerebellar suspensions transplanted into the adult cerebellum of mice with heredodegenerative ataxia. Proc Natl Acad Sci U S A 83:1135–1139

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sotelo C, Alvarado-Mallart RM (1987) Embryonic and adult neurons interact to allow Purkinje cell replacement in mutant cerebellum. Nature 327:421–423

    CAS  PubMed  Google Scholar 

  • Sotelo C, Angaut P (1973) The fine structure of the cerebellar nuclei of the cat. I. Neurons and neuroglial cells. Exp Brain Res 16:410–430

    CAS  PubMed  Google Scholar 

  • Sotelo C, Palay SL (1968) The fine structure of the lateral vestibular nucleus in the rat. Neurons and neuroglial cells. J Cell Biol 36:151–179

    Google Scholar 

  • Sotelo C, Palay SL (1971) Altered axons and axon terminals in the lateral vestibular nucleus of the rat. Possible example of axonal remodeling. Lab Investig 25:653–671

    CAS  PubMed  Google Scholar 

  • Sotelo C, Alvarado-Mallart RM, Frain M, Vernet M (1994) Molecular plasticity of adult Bergmann fibers is associated with radial migration of grafted Purkinje cells. J Neurosci 14:124–133

    CAS  PubMed  Google Scholar 

  • Stahnisch FW (2003) Making the brain plastic: early neuroanatomical staining techniques and the pursuit of structural plasticity, 1910–1970. J Hist Neurosci 12:413–435

    PubMed  Google Scholar 

  • Starkey ML, Bartus K, Barritt AW, Bradbury EJ (2012) Chondroitinase ABC promotes compensatory sprouting of the intact corticospinal tract and recovery of forelimb function following unilateral pyramidotomy in adult mice. Eur J Neurosci 36:3665–3678

    PubMed  Google Scholar 

  • Stenevi U, Björklund A, Svendgaard NA (1976) Transplantation of central and peripheral monoamine neurons to the adult rat brain: techniques and conditions for survival. Brain Res 114:1–20

    CAS  PubMed  Google Scholar 

  • Tanzi E (1893) I fatti e le induzioni dell’odierna istologia del sistema nervoso. Riv Sper Fren Med Leg 19:419–472

    Google Scholar 

  • Tellez I, Terry RD (1968) Fine structure of early changes in the vestibular nuclei of the thiamine-deficient rat. Am J Pathol 54:777–794

    Google Scholar 

  • Thallmair M, Metz GA, Z’Graggen WJ, Raineteau O, Kartje GL, Schwab ME (1998) Neurite growth inhibitors restrict plasticity and functional recovery following corticospinal tract lesions. Nat Neurosci 1:124–131

    CAS  PubMed  Google Scholar 

  • Thompson WG (1890) Successful brain grafting. NY Medical J 51:701–702

    Google Scholar 

  • Thuret S, Moon LD, Gage FH (2006) Therapeutic interventions after spinal cord injury. Nat Rev Neurosci 7:628–643

    CAS  PubMed  Google Scholar 

  • Totoiu MO, Keirstead HS (2005) Spinal cord injury is accompanied by chronic progressive demyelination. J Comp Neurol 486:373–383

    PubMed  Google Scholar 

  • Townes-Anderson E, Raviola G (1978) Degeneration and regeneration of autonomic nerve endings in the anterior part of the rhesus monkey ciliary muscle. J Neurocytol 7:583–600

    CAS  PubMed  Google Scholar 

  • Trommald M, Hulleberg G, Andersen P (1996) Long-term potentiation is associated with new excitatory spine synapses on rat dentate granule cells. Learn Mem 3:218–228

    CAS  PubMed  Google Scholar 

  • Turner AM, Greenough WT (1985) Differential rearing effects on rat visual cortex synapses. I. Synaptic and neuronal density per neuron. Brain Res 329:195–203

    CAS  PubMed  Google Scholar 

  • Van Harreveld A, Fifková E (1975) Swelling of dendritic spines in the fascia dentata after stimulation of the perforant fibers as a mechanism of post-tetanic potentiation. Exp Neurol 49:736–749

    PubMed  Google Scholar 

  • Volkmar FR, Greenough WT (1972) Rearing complexity affects branching of dendrites in the visual cortex of the Rat. Science 176:1445–1447

    CAS  PubMed  Google Scholar 

  • Wassef M, Simons J, Tappaz ML, Sotelo C (1986) Non-Purkinje cell GABAergic innervation of the deep cerebellar nuclei : a quantitative immunocytochemical study. Brain Res 399:125–135

    CAS  PubMed  Google Scholar 

  • Westrum LE (1969) Electron microscopy of degeneration in the lateral olfactory tract and plexiform layer of the prepyriform cortex of the rat. Z Zellforsch 98:157–187

    CAS  PubMed  Google Scholar 

  • Yiu G, He Z (2006) Glial inhibition of CNS axon regeneration. Nat Rev Neurosci 7:617–627

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhao RR, Andrews MR, Wang D, Warren P, Gullo M, Schnell L, Schwab ME, Fawcett JW (2013) Combination treatment with anti-Nogo-A and chondroitinase ABC is more effective than single treatments at enhancing functional recovery after spinal cord injury. Eur J Neurosci. doi:10.1111/ejn.12276

    Google Scholar 

  • Zhao S, Studer D, Chai X, Graber W, Brose N, Nestel S, Young C, Rodriguez EP, Saetzler K, Frotscher M (2012) Structural plasticity of hippocampal mossy fiber synapses as revealed by high-pressure freezing. J Comp Neurol 520:2340–2351

    PubMed  Google Scholar 

  • Zuo Y, Lin A, Chang P, Gan W-B (2005) Development of long-term dendritic spine stability in diverse regions of cerebral cortex. Neuron 46:181–189

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Constantino Sotelo .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Science+Business Media New York

About this chapter

Cite this chapter

Sotelo, C., Dusart, I. (2014). Structural Plasticity in Adult Nervous System: An Historic Perspective. In: Junier, MP., Kernie, S. (eds) Endogenous Stem Cell-Based Brain Remodeling in Mammals. Stem Cell Biology and Regenerative Medicine. Springer, Boston, MA. https://doi.org/10.1007/978-1-4899-7399-3_2

Download citation

Publish with us

Policies and ethics