Skip to main content
Log in

Neuroglial cells: morphological changes during normal aging

  • Review
  • Published:
Rendiconti Lincei Aims and scope Submit manuscript

Abstract

Morphological changes in neuroglial cells of the central nervous system during aging include astrocytic hypertrophy, myelin alterations, shape changes of microglial cells, and decreased volume of the extracellular space. Age-related changes in neuroglial cells of the peripheral nervous system include myelin alterations, decrease in volume of perineuronal satellite cell sheaths, and increased surface area of sensory ganglion neurons unprotected by the satellite cell envelopment. Some of these changes probably contribute to the behavioral impairment and cognitive decline that often accompany normal aging.

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

  • Adinolfi A, Yamuy J, Morales FR, Chase MH (1991) Segmental demyelination in peripheral nerves of old cats. Neurobiol Aging 12:175–179

    Article  CAS  Google Scholar 

  • Aston-Jones G, Rogers J, Shaver RD, Dinan TG, Moss DE (1985) Age-impaired impulse flow from nucleus basalis to cortex. Nature 318:462–464

    Article  CAS  Google Scholar 

  • Bargmann W, Katritsis E (1966) Über die sog. Filamente und das Pigment im Plexus chorioideus des Menschen. Z Zellforsch 75:366–370

    Article  CAS  Google Scholar 

  • Bhatnagar M, Cintra A, Chadi G, Lindberg J, Oitzl M, De Kloet ER, Möller A, Agnati LF, Fuxe K (1997) Neurochemical changes in the hippocampus of the Brown Norway rat during aging. Neurobiol Aging 18:319–327

    Article  CAS  Google Scholar 

  • Biondi G (1933) Ein neuer histologischer Befund am Epithel des Plexus chorioideus. Z ges Neurol Psychiatr 144:161–165

    Article  Google Scholar 

  • Bondareff W, Narotzky R (1972) Age changes in the neuronal microenvironment. Science 176:1135–1136

    Article  CAS  Google Scholar 

  • Brizzee KR, Sherwood N, Timiras PS (1968) A comparison of cell populations at various depth levels in cerebral cortex of young adult and aged Long-Evans rats. J Gerontol 23:289–297

    Article  CAS  Google Scholar 

  • Ceballos D, Cuadras J, Verdú E, Navarro X (1999) Morphometric and ultrastructural changes with ageing in mouse peripheral nerve. J Anat 195:563–576

    Article  Google Scholar 

  • Chen L, Lu W, Yang Z, Yang S, Li C, Shi X, Tang Y (2011) Age-related changes of the oligodendrocytes in rat subcortical white matter. Anat Rec 294:487–493

    Article  Google Scholar 

  • Choo D, Malmgren LT, Rosenberg SI (1990) Age-related changes in Schwann cells of the internal branch of the rat superior laryngeal nerve. Otolaryngol Head Neck Surg 103:628–636

    CAS  Google Scholar 

  • Conde JR, Streit WJ (2006) Microglia in the aging brain. J Neuropathol Exp Neurol 65:199–203

    Google Scholar 

  • Feldman ML, Peters A (1998) Ballooning of myelin sheaths in normally aged macaques. J Neurocytol 27:605–614

    Article  CAS  Google Scholar 

  • Fiori MG (1987) Intranuclear inclusions in Schwann cells of aged fowl ciliary ganglia. J Anat 154:201–214

    CAS  Google Scholar 

  • Geinisman Y, Bondareff W, Dodge JT (1978) Hypertrophy of astroglial processes in the dentate gyrus of the senescent rat. Am J Anat 153:537–544

    Article  CAS  Google Scholar 

  • Goemaere-Vanneste J, van den Bosch de Aguilar P (1987) Étude des fibres nerveuses périphériques au cours du vieillissement chez le rat. La Cellule 74:263–280

    CAS  Google Scholar 

  • Griffiths IR, Duncan ID, McQueen A (1975) Age changes in the dorsal and ventral lumbar nerve roots of dogs. Acta Neuropathol 32:75–85

    Article  CAS  Google Scholar 

  • Grover-Johnson N, Spencer PS (1981) Peripheral nerve abnormalities in aging rats. J Neuropathol Exp Neurol 40:155–165

    Article  CAS  Google Scholar 

  • Gutiérrez R, Boison D, Heinemann U, Stoffel W (1995) Decompaction of CNS myelin leads to a reduction of the conduction velocity of action potentials in optic nerve. Neurosci Lett 195:93–96

    Article  Google Scholar 

  • Huang TY, Hanani M, Ledda M, De Palo S, Pannese E (2006) Aging is associated with an increase in dye coupling and in gap junction number in satellite glial cells of murine dorsal root ganglia. Neuroscience 137:1185–1192

    Article  CAS  Google Scholar 

  • Jalenques I, Albuisson E, Despres G, Romand R (1995) Distribution of glial fibrillary acidic protein (GFAP) in the cochlear nucleus of adult and aged rats. Brain Res 686:223–232

    Article  CAS  Google Scholar 

  • Kane CJM, Sims TJ, Gilmore SA (1997) Astrocytes in the aged rat spinal cord fail to increase GFAP mRNA following sciatic nerve axotomy. Brain Res 759:163–165

    Article  CAS  Google Scholar 

  • Keirstead HS, Blakemore WF (1997) Identification of post-mitotic oligodendrocytes incapable of remyelination within the demyelinated adult spinal cord. J Neurophatol Exp Neurol 56:1191–1201

    Article  CAS  Google Scholar 

  • Knox CA, Kokmen E, Dyck PJ (1989) Morphometric alteration of rat myelinated fibers with aging. J Neuropathol Exp Neurol 48:119–139

    Article  CAS  Google Scholar 

  • Kohama SG, Goss JR, Finch CE, McNeill TH (1995) Increases of glial fibrillary acidic protein in the aging female mouse brain. Neurobiol Aging 16:59–67

    Article  CAS  Google Scholar 

  • Lafarga M, Berciano MT, Pérez-Fígares JM, Andrés MA, Maquiera E (1991) Influence of age on nuclear bodies and nuclear volume in pituicytes of the rat neurohypophysis. Anat Rec 230:319–324

    Article  CAS  Google Scholar 

  • Landfield PW, Rose GR, Sandles L, Wohlstadter TC, Lynch G (1977) Patterns of astroglial hypertrophy and neuronal degeneration in the hippocampus of aged, memory-deficient rats. J Gerontol 32:3–12

    Article  CAS  Google Scholar 

  • Ledda M, Barni L, Altieri L, Pannese E (1999) Amount and distribution of lipofuscin in nerve and satellite cells from spinal ganglia of young adult and aged rabbits. J Submicrosc Cytol Pathol 31:237–246

    CAS  Google Scholar 

  • Ledda M, Barni L, Altieri L, Pannese E (2003) The Golgi apparatus of satellite cells associated with spinal ganglion neurons: changes with age in the rabbit. J Submicrosc Cytol Pathol 35:267–270

    CAS  Google Scholar 

  • Lindsey JD, Landfield PW, Lynch G (1979) Early onset and topographical distribution of hypertrophied astrocytes in hippocampus of aging rats: a quantitative study. J Gerontol 34:661–671

    Article  CAS  Google Scholar 

  • Long JM, Kalehua AN, Muth NJ, Calhoun ME, Jucker M, Hengemihle JM, Ingram DK, Mouton PR (1998) Stereological analysis of astrocyte and microglia in aging mouse hippocampus. Neurobiol Aging 19:497–503

    Article  CAS  Google Scholar 

  • Martinelli C, Sartori P, De Palo S, Ledda M, Pannese E (2005) Increase in number of the gap junctions between satellite neuroglial cells during lifetime: an ultrastructural study in rabbit spinal ganglia from youth to extremely advanced age. Brain Res Bull 67:19–23

    Article  CAS  Google Scholar 

  • Martinelli C, Sartori P, De Palo S, Ledda M, Pannese E (2006) The perineuronal glial tissue of spinal ganglia. Quantitative changes in the rabbit from youth to extremely advanced age. Anat Embryol 211:455–463

    Article  CAS  Google Scholar 

  • Martinelli C, Sartori P, Ledda M, Pannese E (2007) Mitochondria in perineuronal satellite cell sheaths of rabbit spinal ganglia: quantitative changes during life. Cells Tissues Organs 186:141–146

    Article  Google Scholar 

  • McTigue DM, Tripathi RB (2008) The life, death, and replacement of oligodendrocytes in the adult CNS. J Neurochem 107:1–19

    Article  CAS  Google Scholar 

  • Miller KR, Streit WJ (2007) The effects of aging, injury and disease on microglial function: a case for cellular senescence. Neuron Glia Biol 3:245–253

    Article  Google Scholar 

  • Morgan TE, Xie Z, Goldsmith S, Yoshida T, Lanzrein A-S, Stone D, Rozovsky I, Perry G, Smith MA, Finch CE (1999) The mosaic of brain glial hyperactivity during normal aging and its attenuation by food restriction. Neuroscience 89:687–699

    Article  CAS  Google Scholar 

  • Mouton PR, Long JM, Lei D-L, Howard V, Jucker M, Calhoun ME, Ingram DK (2002) Age and gender effects on microglia and astrocyte numbers in brains of mice. Brain Res 956:30–35

    Article  CAS  Google Scholar 

  • Nichols NR, Day JR, Laping NJ, Johnson SA, Finch CE (1993) GFAP mRNA increases with age in rat and human brain. Neurobiol Aging 14:421–429

    Article  CAS  Google Scholar 

  • O’Callaghan JP, Miller DB (1991) The concentration of glial fibrillary acidic protein increases with age in the mouse and rat brain. Neurobiol Aging 12:171–174

    Article  Google Scholar 

  • Oksche A, Kirschstein H (1972) Entstehung und Ultrastruktur der Biondi-Körper in den Plexus chorioidei des Menschen (Biopsiematerial). Z Zellforsch 124:320–341

    Article  CAS  Google Scholar 

  • Pannese E (1981) The satellite cells of the sensory ganglia. Adv Anat Embryol Cell Biol 65:1–111

    Article  CAS  Google Scholar 

  • Pannese E (2011) Morphological changes in nerve cells during normal aging. Brain Struct Funct 216:85–89

    Article  Google Scholar 

  • Pannese E, Procacci P, Ledda M, Conte V (1996) Age-related reduction of the satellite cell sheath around spinal ganglion neurons in the rabbit. J Neurocytol 25:137–146

    Article  CAS  Google Scholar 

  • Pannese E, Ledda M, Martinelli C, Sartori P (1997) Age-related decrease of the perineuronal satellite cell number in the rabbit spinal ganglia. J Periph Nerv Syst 2:77–82

    CAS  Google Scholar 

  • Pelvig DP, Pakkenberg H, Stark AK, Pakkenberg B (2008) Neocortical glial cell numbers in human brains. Neurobiol Aging 29:1754–1762

    Article  CAS  Google Scholar 

  • Perry VH, Matyszak MK, Fearn S (1993) Altered antigen expression of microglia in the aged rodent CNS. Glia 7:60–67

    Article  CAS  Google Scholar 

  • Peters A (1996) Age-related changes in oligodendrocytes in monkey cerebral cortex. J Comp Neurol 371:153–163

    Article  CAS  Google Scholar 

  • Peters A (2002) The effects of normal aging on myelin and nerve fibers: a review. J Neurocytol 31:581–593

    Article  Google Scholar 

  • Peters A, Sethares C (2002) The effects of age on the cells in layer 1 of primate cerebral cortex. Cer Cortex 12:27–36

    Article  Google Scholar 

  • Peters A, Sethares C (2003) Is there remyelination during aging of the primate central nervous system? J Comp Neurol 460:238–254

    Article  Google Scholar 

  • Peters A, Sethares C (2004) Oligodendrocytes, their progenitors and other neuroglial cells in the aging primate cerebral cortex. Cer Cortex 14:995–1007

    Article  Google Scholar 

  • Peters A, Josephson K, Vincent SL (1991) Effects of aging on the neuroglial cells and pericytes within area 17 of the rhesus monkey cerebral cortex. Anat Rec 229:384–398

    Article  CAS  Google Scholar 

  • Peters A, Moss MB, Sethares C (2000) Effects of aging on myelinated nerve fibers in monkey primary visual cortex. J Comp Neurol 419:364–376

    Article  CAS  Google Scholar 

  • Peters A, Verderosa A, Sethares C (2008) The neuroglial population in the primary visual cortex of the aging rhesus monkey. Glia 56:1151–1161

    Article  Google Scholar 

  • Peters A, Sethares C, Moss MB (2010) How the primate fornix is affected by age. J Comp Neurol 518:3962–3980

    Article  Google Scholar 

  • Procacci P, Magnaghi V, Pannese E (2008) Perineuronal satellite cells in mouse spinal ganglia express the gap junction protein connexin43 throughout life with decline in old age. Brain Res Bull 75:562–569

    Article  CAS  Google Scholar 

  • Robertson A, Day B, Pollock M, Collier P (1993) The neuropathy of elderly mice. Acta Neuropathol 86:163–171

    Article  CAS  Google Scholar 

  • Rogers J, Zornetzer SF, Bloom FE (1981) Senescent pathology of cerebellum: Purkinje neurons and their parallel fiber afferents. Neurobiol Aging 2:15–25

    Article  CAS  Google Scholar 

  • Sandell JH, Peters A (2002) Effects of age on the glial cells in the rhesus monkey optic nerve. J Comp Neurol 445:13–28

    Article  Google Scholar 

  • Sandell JH, Peters A (2003) Disrupted myelin and axon loss in the anterior commissure of the aged rhesus monkey. J Comp Neurol 466:14–30

    Article  Google Scholar 

  • Sharma AK, Bajada S, Thomas PK (1980) Age changes in the tibial and plantar nerves of the rat. J Anat 130:417–428

    CAS  Google Scholar 

  • Sheffield LG, Berman NEJ (1998) Microglial expression of MHC class II increases in normal aging of nonhuman primates. Neurobiol Aging 19:47–55

    Article  CAS  Google Scholar 

  • Sloane JA, Hollander W, Rosene DL, Moss MB, Kemper T, Abraham CR (2000) Astrocytic hypertrophy and altered GFAP degradation with age in subcortical white matter of the rhesus monkey. Brain Res 862:1–10

    Article  CAS  Google Scholar 

  • Sturrock RR (1976) Changes in neuroglia and myelination in the white matter of aging mice. J Gerontol 31:513–522

    Article  CAS  Google Scholar 

  • Syková E, Mazel T, Šimonová Z (1998) Diffusion constraints and neuron-glia interaction during aging. Exp Gerontol 33:837–851

    Article  Google Scholar 

  • Sylvia AL, Rosenthal M (1979) Effects of age on brain oxidative metabolism in vivo. Brain Res 165:235–248

    Article  CAS  Google Scholar 

  • Tigges J, Herndon JG, Peters A (1992) Axon terminals on Betz cell somata of area 4 in rhesus monkey throughout adulthood. Anat Rec 232:305–315

    Article  CAS  Google Scholar 

  • van den Bosch de Aguilar P, Goemaere-Vanneste J, Klosen P, Terao E (1992) Ageing changes of spinal ganglion neurons. In: Fujisawa K, Morimatsu Y (eds) Development and involution of neurones. Japan Scientific Societies Press, Tokyo, pp 109–150

    Google Scholar 

  • Vaughan DW, Peters A (1974) Neuroglial cells in the cerebral cortex of rats from young adulthood to old age: an electron microscope study. J Neurocytol 3:405–429

    Article  CAS  Google Scholar 

  • Verdú E, Ceballos D, Vilches JJ, Navarro X (2000) Influence of aging on peripheral nerve function and regeneration. J Periph Nerv Syst 5:191–208

    Article  Google Scholar 

  • Wen GY, Wiśniewski HM, Kascsak RJ (1999) Biondi ring tangles in the choroid plexus of Alzheimer’s disease and normal aging brains: a quantitative study. Brain Res 832:40–46

    Article  CAS  Google Scholar 

  • Wiśniewski HM, Terry RD (1973) Morphology of the aging brain, human and animal. Progress Brain Res 40:167–186

    Article  Google Scholar 

  • Xi M-C, Liu R-H, Engelhardt JK, Morales FR, Chase MH (1999) Changes in the axonal conduction velocity of pyramidal tract neurons in the aged cat. Neuroscience 92:219–225

    Article  CAS  Google Scholar 

Download references

Conflict of interest

None.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ennio Pannese.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pannese, E. Neuroglial cells: morphological changes during normal aging. Rend. Fis. Acc. Lincei 24, 101–106 (2013). https://doi.org/10.1007/s12210-012-0218-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12210-012-0218-9

Keywords

Navigation