Skip to main content
Log in

Ageing and the nervous system: insights from studies on invertebrates

  • Published:
Biogerontology Aims and scope Submit manuscript

Abstract

Ageing can have profound effects on the post-mitotic organ ofbehaviour, the brain. As yet the precise causes of thesedeleterious effects are unknown. However, clear insights intothe putative mechanisms and consequences of ageing in the CNShave been achieved through the use of invertebrate models. It isnow clear that ageing alters the endogenous properties ofneurones, their morphology, the efficacy of the connections thatthe neurones make with their targets and may even lead to neuroneloss. While the precise mechanisms underlying these changes arepresently unclear clues from post-mitotic organisms such as C.elegans have provided putative targets which are currently beinginvestigated. It is clear to date that the age-induced changesin CNS function observed in invertebrates are conserved inmammalian species and that further work on invertebrates mayprovide informative insights in to the mechanisms of neuronalageing.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Ali NN,Allen MC,Gard PR andYeoman MS (2000a) Behavioural consequences of age-induced changes in a neural network. Mech Aging Dev (Abstract in press)

  • Ali NN,Allen MC,Gard PR,Janse C andYeoman MS (2000b) Age-induced changes in a pair of well characterised neurones can account for the defcit in rhythmic motor behaviour seen in aged animals. Eur J Neurosci 12 (Suppl): 242

  • Alvarez JC,Diaz C,Suarez C,Fernandez JA anddelRey CG (2000) Ageing and the human vestibular nuclei: morphometric analysis. Mech Ageing Dev 114 (3): 149–172

    Google Scholar 

  • Alvarez-Maubecin V,Garcia-Hernandez F,Williams JT andVan Bocksaele EJ (2000) Functional coupling between neurones and glia. J Neurosci 20: (11) 4091–4098

    Google Scholar 

  • Apfeld J andKenyon C (1999) Regulation of lifespan by sensory perception in Caenorhabditis elegans. Nature 402: 804–809

    Google Scholar 

  • Atwood HL (1992) Age-dependent alterations of synaptic performance and plasticity in crustacean motor systems. Exp Gerontol 27: 51–61

    Google Scholar 

  • Bergado JA,Fernandez CI,GomezSoria A andGonzalez O (1997) Chronic intraventricular infusion with NGF improves LTP in old chronically-impaired rats. Brain Res 770 (1–2): 1–9

    Google Scholar 

  • Bergman E,Fundin BT andUlhhake B (1999) Effects of aging and axotomy on the expression of neurotrophin receptors in primary sensory neurons. J Comp Neurol 410 (3) 368–386

    Google Scholar 

  • BertoniFreddari C,Fattoretti P,Peironi M,MeierRuge W andUlrich J (1992) Enlargement of synaptic size as a compensative reaction in ageing and dementia. Pathol Res Prac 188 (4–5): 612–615

    Google Scholar 

  • BertoniFreddari C,Fattoretti P,Paoloni R,Caselli U,Galeazzi L andMeierRuge W (1996) Synaptic structural dynamics and aging. Gerontology 42 (3): 170–180

    Google Scholar 

  • Camicioli R,Moore MM,Sexton G,Howieson DB andKaye JA (1999) Age-related changes associated with motor function in healthy older people. J Am Geriatr Soc 47: 330–334

    Google Scholar 

  • Chen S andHilman DE (1999) Dying-back of Purkinje cell dendrites with synapse loss in ageing rats. J Neurocytol 28 (3): 187–196

    Google Scholar 

  • Corfas G andDudai Y (1991) Morphology of a sensory neuron in Drosophila is abnormal in memory mutants and changes during aging. Proc Natl Acad Sci USA 88: 7252–7256

    Google Scholar 

  • Cowen T,Jenner C,Song, GX,Santosa AWB andGavazzi I (1997) Responses of mature and aged sympathetic neurones to laminin and NGF: an in vitro study. Neurochem Res 22 (8): 1003–1011

    Google Scholar 

  • Faragher RGA (2000) Cell senescence and human aging: where's the link? Biochem Soc Trans 28: 221–226

    Google Scholar 

  • Frey D,Schneider C,Xu L,Borg J,Spooren W andCaroni P (2000) Early and selective loss of neuromuscular sprouting competence in motoneurone disease. J Neurosci 20 (7): 2534–2542

    Google Scholar 

  • Frolkis VV,Stupina AS,Martinenko OA,Toth S andTimchenko AI (1984) Aging of neurons in the mollusc Lymnaea stagnalis. Structure, function and sensitivity to neurotransmitters. Mech Ageing Dev 25: 91–102

    Google Scholar 

  • Frolkis VV,Stupina AS,Martinenko OA andTimchenko AI (1991) Potential-dependent calcium channels of neurons in the mollusk Lymnaea stagnalis in aging-effect of norepinephrine. Mech Ageing Dev 58: 75–83

    Google Scholar 

  • Frolkis VV,Kvitnitskayaryzhova TY andMartynenko OA (1995) Aging of neurons in the mollusk Lymnaea stagnalis small parietal ganglion-a morphological comparison of the same neuron. Exp Gerontol 30: 533–544

    Google Scholar 

  • Govind CK (1992) Age-related remodelling of lobster neuromuscular terminals. Exp Gerontol 27: 63–74

    Google Scholar 

  • Grewal SS,York RD andStork PJS (1999) Extracellular signalregulated kinase signalling in neurons. Curr Opin Neurobiol 9

  • Hirsch HR andPeretz B (1984) Survival and ageing of a small laboratory population of a marine mollusk, Aplysia californica. Mech Ageing Dev 27: 43–62

    Google Scholar 

  • Hori N,Hirotsu I,Davis PJ, andCarpenter DO (1992) Longterm potentiation is lost in aged rats but preserved by calorie restriction. Neuroreport 3 (12): 1085–1088

    Google Scholar 

  • Izumi Y andZorumski CF (1995) Developmental-changes in longterm potentiation in CA1 of rat hippocampal slices. Synapse 20: 19–23

    Google Scholar 

  • Janse C,van der Roest M andSlob W (1986) Age-related decrease in the electrical coupling of two identified neurons in the mollusc Lymnaea stagnalis. Brain Res 376: 208–212

    Google Scholar 

  • Janse C,Slob W,Popelier CM andVogelaar JW (1988) Survival characteristics of the mollusc Lymnaea stagnalis under constant culture conditions: effects of aging and disease. Mech Ageing Dev 42: 263–274

    Google Scholar 

  • Janse C,Wildering WC andPopelier CM (1989) Age-related changes in female reproductive activity and growth in the mollusc Lymnaea stagnalis. J Gerontol 44: B148-B155

  • Janse C,ter Maat A andPieneman AW (1990) Molluscan ovulation hormone containing neurons and age-related reproductive decline. Neurobiol Aging 11: 457–463

    Google Scholar 

  • Janse C,Wildering WC andvan der Roest M (1991) Neuroendocrine and neural aging in the pond snail Lymnaea stagnalis. In: Kits KS,Boer, HH andJoosse J (eds) Molluscan Neurobiology, pp 179–185. North Holland Publishing, Amsterdam

    Google Scholar 

  • Janse C,van der Roest M,Jansen RF,Montagne-Wajer C andBoer HH (1996) Atrophy and degeneration of peptidergic neurons and cessation of egg laying in the aging pond snail Lymnaea stagnalis. J Neurobiol 29 (2): 202–212

    Google Scholar 

  • Janse C,Peretz B,van der Roest M andDubelaar EJG (1999) Excitability and branching of neuroendocrine cells during reproductive senescence. Neurobiol Aging 20: 675–683

    Google Scholar 

  • Johnson RJR,Schemann M,Santer RM andCowen T (1998) The effects of age on the overall population and on subpopulations of myenteric neurons in the rat small intestine. J Anat 192: 479–488

    Google Scholar 

  • Kaplan DR andMiller FD (2000) Neurotrophin signal transduction in the nervous system. Curr Opin Neurobiol 10: 381–391

    Google Scholar 

  • Kemper TL,Moss MB,Rosene DL, andKillany RJ (1997) Agerelated neuronal loss in the nucleus centralis superior of the rhesus monkey. Acta Neuropathol 94 (2): 124–130

    Google Scholar 

  • Kenyon C,Chang S,Gensch E,Rudner A andTabtiang R (1993) A Caenorhabditis elegans mutant that lives twice as long as the wild type. Nature 366: 461–464

    Google Scholar 

  • Klass MR (1977) Ageing in the nematode Caenorhabditis elegans: major biological and environmental factors influencing life span. Mech Ageing Dev 6: 413–429

    Google Scholar 

  • Kops GJ,de Ruiter ND,De Vries-Smits AM,Powell DR,Bos JL andBurgering BM (1999) Direct control of the Forkhead transcription factor AFX by protein kinase B. Nature 398: 630–634

    Google Scholar 

  • Kostyuk P,Pronchuk N,Savchenko A andVerkratsky A (1993) Calcium currents in aged rat dorsal root ganglion neurons. J Physiol Lond 461: 467–483

    Google Scholar 

  • Korr H,Horsmann C,Schurmann M andDelaunoy JP (1994) Problems encountered when immunocytochemistry is used for quantitative glial cell identification in autoradiographic studies of cell proliferation in the brain of the unlesioned adult mouse. Cell Tiss Res 278 ( 1): 85–95

    Google Scholar 

  • Kuchel GA,Crutcher KA,Naheed U,Thrasivoulou C andCowen T (1999) NGF expression in the aged rat pineal gland does not correlate with loss of sympathetic axonal branches and varicosities. Neurobiol Aging 20(6): 685–693

  • Lakowski B andHekimi S (1998) The genetics of caloric restriction in Caenorhabditis elegans. Proc Natl Acad Sci USA 95: 13091–13096

    Google Scholar 

  • Larsen P,Albert P andRiddle A (1996) Genes that regulate both development and longevity in Caenorhabditis elegans. Genetics 139: 1567–1583

    Google Scholar 

  • McGahon BM,Murray CA,Horrobin DF andLynch MA (1999) Age-related changes in oxidative mechanisms and LTP are reversed by dietary manipulation. Neurobiol Aging 20(6): 643–653

    Google Scholar 

  • Masliah E,Mallory M,Hansen L,Deteresa R andTerry RD (1993) Quantitative synaptic alterations in the human cortex during normal ageing. Neurology 43(1): 192–197

    Google Scholar 

  • Masoro EJ (1995) Dietary restriction. Exp Gerontol 30: 291–298

    Google Scholar 

  • Matsumoto A (1998) Synaptic changes in perineal motoneurons of aged male rats. J Comp Neurol 400(1): 103–109

    Google Scholar 

  • Moore CI,Browning MD andRose GM (1993) Hippocampal plasticity induced by primed burst but not long-term potentiation, stimulation is impaired in area CA1 of aged Fischer-344 rats. Hippocampus 3: 57–66

    Google Scholar 

  • Morris J,Tissenbaum H andRuvkun G (1996) A phosphatidylinositol-3-OH kinase member regulating longevity in Caenorhabditis elegans. Nature 382: 536–539

    Google Scholar 

  • Morrison JH andHof PR (1997) Life and death of neurons in the aging brain. Science 278(5337): 412–419

    Google Scholar 

  • Orike N,Thrasivoulou C andCowen T (2000) Neurotrophinindependent survival and cell death in adult sympathetic neurons: the role of PI3-kinase. J Auton Neurosci (Abstract in press)

  • Orr W andSohal R (1994) Extension of lifespan by the overexpression of superoxide dismutase and catalase. Science 263: 1128–1130

    Google Scholar 

  • Paradis S andRuvkun G (1998) Caenorhabditis elegans Akt/PKB transduces insulin receptor-like signals from AGE-1PI3 kinase to the DAF-16 transcription factor. Gene Dev 12(16): 2488–2498

    Google Scholar 

  • Peretz B andSrivatsan M (1996) Chronic stimulation increases acetylcholinesterase activity in old Aplysia. Behav Brain Res 80: 203–210 97

    Google Scholar 

  • Peretz B,Romanenko A andMarkesbery W (1984) Functional history of two motor neurons and the morphometry of their neuromuscular junctions in the gill of Aplysia. Evidence for differential aging. Proc Natl Acad Sci USA 81: 4232–4236

  • PerezCampo R,Rojas C andBarja G (1998) The rate of free radical production as a determinant of the rate of aging: evidence from a comparative approach. J Comp Physiol B 168: 149–158

    Google Scholar 

  • Phelan P (2000) Gap junction communication in invertebrates: the innexin gene family. Curr Top Membr 49: 389–422

    Google Scholar 

  • Ponten J,Shall S andStein WD (1983) A quantitative analysis of the ageing of human glial cells in culture. J Cell Physiol 117(3): 342–352

    Google Scholar 

  • Roubos EW andvan der Wal-Divendal RM (1980) Ultrastructural analysis of peptide-hormone release b exocytosis. Cell Tiss Res 207: 267–275

    Google Scholar 

  • Scheff SW,Scott SA andDekosky ST (1991) Quantitation of synaptic density in the septal nuclei of young and aged Fischer 344 rats. Neurobiol Aging 12(1): 3–12

    Google Scholar 

  • Shanker S,Teyler TJ andRobbins N (1998) Aging differentially alters forms of long-term potentiation in the rat hippocampal area CA1. J Neurophysiol 79(1): 334–371

    Google Scholar 

  • Shen JM,Barnes CA,McNaughton BL,Skaggs WE andWeaver KL (1997) The effects of aging on experience-dependent plasticity of hippocampal place cells. J Neurosci 17(17): 6769–6782

    Google Scholar 

  • Shores MM,White SS,Veith RC andSzot P (1999) Tyrosine hydroxylase mRNA is increased in old age and norepinephrine uptake transporter mRNA is decreased in middle age in locus coeruleus of Brown-Norway rats. Brain Res 826(1): 143–147

  • Siddiqi Z,Kemper TL andKilliany R (1999) Age-related neuronal loss from the substantia nigra-pars compacta and ventral tegmental area of the rhesus monkey. J Neuropathol Exp Neurol 58(9): 959–971

    Google Scholar 

  • Smith DE,Roberts J,Gage FH andTuszynski MH (1999) Ageassociated neuronal atrophy occurs in the primate brain and is reversible by growth factor gene therapy. PNAS (USA) 96(19): 10893–10898

    Google Scholar 

  • Sohal RS andWeindruch R (1996) Oxidative stress, caloric restriction and aging. Science 273: 59–63

    Google Scholar 

  • Srivatsan M andPeretz B (1996) Effect of acetylchoinesterase inhibition on behaviour is age-dependent in freely moving Aplysia. Behav Brain Res 77: 115–124

    Google Scholar 

  • Srivatsan M,Peretz B,Hallahan B andTalwalker R (1992) Effect of age on acetylcholinesterase and other haemolymph proteins in Aplysia. J Comp Physiol B 162: 29–37

  • Stefano GB andJanse C (1990) Molluscan models in ageing studies in the central nervous system. Mytilus and Lymnaea. In: Stefano GB (ed) Neurobiology of Mytilus edulis, pp 289–308. Manchester University Press, New York

    Google Scholar 

  • Steinmetz PN,Roy A,Fitzgerald PJ,Hsiao SS,Johnson KO andNiebur E (2000) Attention modulates synchronised neuronal firing in primate somatosensory cortex. Nature 404: 187–190 Verkhratsky A and Toescu EC (1998) Calcium and neuronal ageing. Trends Neurosci 21: 2–7

  • Vohra BPS andSharma SP (1997) Regional specificity of neuronal loss with age in the cerebellum, motor cortex and cervical spinal cord. Natl Acad Sci Lett-India 20(11–12): 164–167

    Google Scholar 

  • Ward MTOler JA andMarkus EJ (1999) Hippocampal dysfunction during ageing 1: deficits in memory consolidation. Neurobiol Aging 20(4): 363–372

    Google Scholar 

  • Wildering WC,van der Roest M,de Vlieger TA andJanse C (1991) Age-related changes in the junctional and non-junctional conductance's in two electrically coupled peptidergic neurons of the mollusc Lymnaea stagnalis. Brain Res 547: 89–98

    Google Scholar 

  • Wong A,Boutis P andHekimi S (1995) Mutations in the CLK-1 gene of Caenorhabditis affect developmental and behavioural timing. Genetics 139: 1247–1259

    Google Scholar 

  • Woodhead AD (1985) Feral fishes. Interdiscip Top Gerontol 21: 22–50

  • Xie HQ andHu WW (1994) Modulation of gap junctions in senescent endothelial cells. Exp Cell Res 214: 172–176

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yeoman, M., Faragher, R. Ageing and the nervous system: insights from studies on invertebrates. Biogerontology 2, 85–97 (2001). https://doi.org/10.1023/A:1011597420036

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1011597420036

Navigation