Skip to main content Accessibility help

The structure of the perineuronal sheath of satellite glial cells (SGCs) in sensory ganglia*

  • Ennio Pannese (a1)


In sensory ganglia each nerve cell body is usually enveloped by a satellite glial cell (SGC) sheath, sharply separated from sheaths encircling adjacent neurons by connective tissue. However, following axon injury SGCs may form bridges connecting previously separate perineuronal sheaths. Each sheath consists of one or several layers of cells that overlap in a more or less complex fashion; sometimes SGCs form a perineuronal myelin sheath. SGCs are flattened mononucleate cells containing the usual cell organelles. Several ion channels, receptors and adhesion molecules have been identified in these cells. SGCs of the same sheath are usually linked by adherent and gap junctions, and are functionally coupled. Following axon injury, both the number of gap junctions and the coupling of SGCs increase markedly. The apposed plasma membranes of adjacent cells are separated by 15–20 nm gaps, which form a potential pathway, usually long and tortuous, between connective tissue and neuronal surface. The boundary between neuron and SGC sheath is usually complicated, mainly by many projections arising from the neuron. The outer surface of the SGC sheath is covered by a basal lamina. The number of SGCs enveloping a nerve cell body is proportional to the cell body volume; the volume of the SGC sheath is proportional to the volume and surface area of the nerve cell body. In old animals, both the number of SGCs and the mean volume of the SGC sheaths are significantly lower than in young adults. Furthermore, extensive portions of the neuronal surface are not covered by SGCs, exposing neurons of aged animals to damage by harmful substances.


Corresponding author

Correspondence should be addressed to: Ennio Pannese, Viale San Michele del Carso 15, I-20144, Milano, Italy phone: +39.02.435854 email:


Hide All

In memory of the late Professor Enrico Reale (1927–2006), untiring researcher and dear friend, whose expertise made possible the freeze-fracture studies cited in the present review.



Hide All
Ajima, H., Kawano, Y., Takagi, R., Aita, M., Gomi, H., Byers, M.R. et al. (2001) The exact expression of glial fibrillary acidic protein (GFAP) in trigeminal ganglion and dental pulp. Archives of Histolgy and Cytology 64, 503511.
Berger, U.V. and Hediger, M.A. (2000) Distribution of the glutamate transporters GLAST and GLT-1 in rat circumventricular organs, meninges, and dorsal root ganglia. Journal of Comparative Neurology 421, 385399.
Bernardini, N., Levey, A.I. and Augusti-Tocco, G. (1999) Rat dorsal root ganglia express m1-m4 muscarinic receptor proteins. Journal of the Peripheral Nervous System 4, 222232.
Bruzzone, R., White, T.W. and Paul, D.L. (1996) Connections with connexins: the molecular basis of direct intercellular signaling. European Journal of Biochemistry 238, 127.
Bunge, M.B., Bunge, R.P., Peterson, E.R. and Murray, M.R. (1967) A light and electron microscope study of long-term organized cultures of rat dorsal root ganglia. Journal of Cell Biology 32, 439466.
Citkowitz, E. and Holtzman, E. (1973) Peroxisomes in dorsal root ganglia. Journal of Histochemistry and Cytochemistry 21, 3441.
Coggeshall, R.E. (1967) A light and electron microscope study of the abdominal ganglion of Aplysia californica. Journal of Neurophysiology 30, 12631287.
Dogiel, A.S. (1896) Der Bau der Spinalganglien bei den Säugetieren. Anatomischer Anzeiger 12, 140152.
Dogiel, A.S. (1897) Zur Frage über den feineren Bau der Spinalganglien und deren Zellen bei Säugetieren. Internationale Monatsschrift für Anatomie und Physiologie 14, 73116.
Ebendal, T. (1975) Effects of nerve growth factor on the synthesis of nucleic acids and proteins in cultured chick embryo trigeminal ganglia. Zoon 3, 159167.
Ehrlich, P. (1886) Ueber die Methylenblaureaction der lebenden Nervensubstanz. Deutsche Medizinische Wochenschrift 12, 4952.
Elson, K., Ribeiro, R.M., Perelson, A.S., Simmons, A. and Speck, P. (2004) The life span of ganglionic glia in murine sensory ganglia estimated by uptake of bromodeoxyuridine. Experimental Neurology 186, 99103.
Friede, R.L. and Johnstone, M.A. (1967) Responses of thymidine labeling of nuclei in gray matter and nerve following sciatic transection. Acta Neuropathologica 7, 218231.
Gotow, T., Yoshikawa, H. and Hashimoto, P.H. (1985) Distribution patterns of orthogonal arrays and alkaline phosphatase in plasma membranes of satellite cells in rat spinal ganglia. Anatomy and Embryology 171, 171179.
Hanani, M. (2005) Satellite glial cells in sensory ganglia: from form to function. Brain Research Reviews 48, 457476.
Hanani, M., Huang, T.Y., Cherkas, P.S., Ledda, M. and Pannese, E. (2002) Glial cell plasticity in sensory ganglia induced by nerve damage. Neuroscience 114, 279283.
Hess, A. (1955) The fine structure of young and old spinal ganglia. Anatomical Record 123, 399423.
Hibino, H., Horio, Y., Fujita, A., Inanobe, A., Doi, K., Gotow, T. et al. (1999) Expression of an inwardly rectifying K+ channel, Kir4.1, in satellite cells of rat cochlear ganglia. American Journal of Physiology 277, C638C644.
Holmgren, E. (1901) Beiträge zur Morphologie der Zelle. I. Nervenzellen. Anatomische Hefte 18, 267325.
Holmgren, E. (1902) Einige Worte über das ‘Trophospongium’ verschiedener Zellarten. Anatomischer Anzeiger 20, 433440.
Hösli, E. and Hösli, L. (1978) Autoradiographic localization of the uptake of [3H]-GABA and [3H]L-glutamic acid in neurones and glial cells of cultured dorsal root ganglia. Neuroscience Letters 7, 173176.
Huang, T.Y., Cherkas, P.S., Rosenthal, D.W. and Hanani, M. (2005) Dye coupling among satellite glial cells in mammalian dorsal root ganglia. Brain Research 1036, 4249.
Huang, T.Y., Hanani, M., Ledda, M., De Palo, S. and 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, 11851192.
Humbertson, A. Jr., Zimmermann, E. and Leedy, M. (1969) A chronological study of mitotic activity in satellite cell hyperplasia associated with chromatolytic neurons. Zeitschrift für Zellforschung und mikroskopische Anatomie 100, 507515.
Jessen, K.R., Thorpe, R. and Mirsky, R. (1984) Molecular identity, distribution and heterogeneity of glial fibrillary acidic protein: an immunoblotting and immunohistochemical study of Schwann cells, satellite cells, enteric glia and astrocytes. Journal of Neurocytology 13, 187200.
Kawamata, T., Ninomiya, T., Toriyabe, M., Yamamoto, J., Niiyama, Y., Omote, K. et al. (2006) Immunohistochemical analysis of acid-sensing ion channel 2 expression in rat dorsal root ganglion and effects of axotomy. Neuroscience 143, 175187.
Keast, J.R. and Anderson, T.M. (2000) Glutamate and aspartate immunoreactivity in dorsal root ganglion cells supplying visceral and somatic targets and evidence for peripheral axonal transport. Journal of Comparative Neurology 424, 577587.
Kobayashi, K., Fukuoka, T., Yamanaka, H., Dai, Y., Obata, K., Tokunaga, A. et al. (2006) Neurons and glial cells differentially express P2Y receptor mRNAs in the rat dorsal root ganglion and spinal cord. Journal of Comparative Neurology 498, 443454.
Kumar, N.M. and Gilula, N.B. (1996) The gap junction communication channel. Cell 84, 381388.
Ledda, M., Barni, L., Altieri, L. and Pannese, E. (2003) The Golgi apparatus of satellite cells associated with spinal ganglion neurons: changes with age in the rabbit. Journal of Submicroscopic Cytology and Pathology 35, 267270.
Lodin, Z., Booher, J. and Kasten, F.H. (1970) Phase-contrast cinematographic study of dissociated neurons from embryonic chick dorsal root ganglia cultured in the Rose chamber. Experimental Cell Research 60, 2739.
Lodin, Z., Faltin, J., Booher, J., Hartman, J. and Sensenbrenner, M. (1973) Formation of intercellular contacts in cultures of dissociated neurons from embryonic chicken dorsal root ganglia. Neurobiology 3, 376390.
Martinelli, C., Sartori, P., De Palo, S., Ledda, M. and 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 Research Bulletin 67, 1923.
Martinelli, C., Sartori, P., De Palo, S., Ledda, M. and Pannese, E. (2006) The perineuronal glial tissue of spinal ganglia. Quantitative changes in the rabbit from youth to extremely adavanced age. Anatomy and Embryology 211, 455463.
Martinelli, C., Sartori, P., Ledda, M. and Pannese, E. (2007) Mitochondria in perineuronal satellite cell sheaths of rabbit spinal ganglia: quantitative changes during life. Cells Tissues Organs 186, 141146.
Masaki, T., Matsumura, K., Hirata, A., Yamada, H., Hase, A., Shimizu, T. et al. (2001) Expression of dystroglycan complex in satellite cells of dorsal root ganglia. Acta Neuropathologica 101, 174178.
Matsuda, S., Kobayashi, N., Terashita, T., Shimokawa, T., Shigemoto, K., Mominoki, K. et al. (2005) Phylogenetic investigation of Dogiel's pericellular nests and Cajal's initial glomeruli in the dorsal root ganglion. Journal of Comparative Neurology 491, 234245.
Matsumoto, E. and Rosenbluth, J. (1986) Structure of the satellite cell sheath around the cell body, axon hillock, and initial segment of frog dorsal root ganglion cells. Anatomical Record 215, 182191.
Miller, K.E., Richards, B.A. and Kriebel, R.M. (2002) Glutamine-, glutamine synthetase-, glutamate dehydrogenase- and pyruvate carboxylase-immunoreactivities in the rat dorsal root ganglion and peripheral nerve. Brain Research 945, 202211.
Miller, R., Varon, S., Kruger, L., Coates, P.W. and Orkand, P.M. (1970) Formation of synaptic contacts on dissociated chick embryo sensory ganglion cells in vitro. Brain Research 24, 356358.
Mirsky, R., Jessen, K.R., Schachner, M. and Goridis, C. (1986) Distribution of the adhesion molecules N-CAM and L1 on peripheral neurons and glia in adult rats. Journal of Neurocytology 15, 799815.
Nicholson, B.J., Weber, P.A., Cao, F., Chang, H.-C., Lampe, P. and Goldberg, G. (2000) The molecular basis of selective permeability of connexins is complex and includes both size and charge. Brazilian Journal of Medical and Biological Research 33, 369378.
Palay, S.L. (1957) Contributions of electron microscopy to neuroanatomy. In Windle, W.F. (ed) New Research Techniques of Neuroanatomy. Springfield, Illinois: C.C. Thomas, pp. 516.
Pannese, E. (1960) Observations on the morphology, submicroscopic structure and biological properties of satellite cells (s.c.) in sensory ganglia of mammals. Zeitschrift für Zellforschung und mikroskopische Anatomie 52, 567597.
Pannese, E. (1963) Investigations on the ultrastructural changes of the spinal ganglion neurons in the course of axon regeneration and cell hypertrophy. II. Changes during cell hypertrophy and comparison between the ultrastructure of nerve cells of the same type under different functional conditions. Zeitschrift für Zellforschung und mikroskopische Anatomie 61, 561586.
Pannese, E. (1964) Number and structure of perisomatic satellite cells of spinal ganglia under normal conditions or during axon regeneration and neuronal hypertrophy. Zeitschrift für Zellforschung und mikroskopische Anatomie 63, 568592.
Pannese, E. (1969) Electron microscopical study on the development of the satellite cell sheath in spinal ganglia. Journal of Comparative Neurology 135, 381422.
Pannese, E. (1974) The histogenesis of the spinal ganglia. Advances in Anatomy Embryology and Cell Biology 47, fasc. 5, 197.
Pannese, E. (1981) The satellite cells of the sensory ganglia. Advances in Anatomy Embryology and Cell Biology 65, 1111.
Pannese, E. and Procacci, P. (2002) Ultrastructural localization of NGF receptors in satellite cells of the rat spinal ganglia. Journal of Neurocytology 31, 755763.
Pannese, E., Bianchi, R., Calligaris, B., Ventura, R. and Weibel, E.R. (1972) Quantitative relationships between nerve and satellite cells in spinal ganglia. An electron microscopical study. I. Mammals. Brain Research 46, 215234.
Pannese, E., Ventura, R. and Bianchi, R. (1975) Quantitative relationships between nerve and satellite cells in spinal ganglia: an electron microscopical study. II. Reptiles. Journal of Comparative Neurology 160, 463476.
Pannese, E., Luciano, L., Iurato, S. and Reale, E. (1977) Intercellular junctions and other membrane specializations in developing spinal ganglia: a freeze-fracture study. Journal of Ultrastructure Research 60, 169180.
Pannese, E., Luciano, L. and Reale, E. (1978) Intercellular junctions in developing spinal ganglia. Zoon 6, 129138.
Pannese, E., Ledda, M., Arcidiacono, G. and Rigamonti, L. (1991) Clusters of nerve cell bodies enclosed within a common connective tissue envelope in the spinal ganglia of the lizard and rat. Cell and Tissue Research 264, 209214.
Pannese, E., Procacci, P., Ledda, M. and Conte, V. (1993) The percentage of nerve cell bodies arranged in clusters decreases with age in the spinal ganglia of adult rabbits. Anatomy and Embryology 187, 331334.
Pannese, E., Procacci, P., Ledda, M. and Conte, V. (1996) Age-related reduction of the satellite cell sheath around spinal ganglion neurons in the rabbit. Journal of Neurocytology 25, 137146.
Pannese, E., Ledda, M., Martinelli, C. and Sartori, P. (1997) Age-related decrease of the perineuronal satellite cell number in the rabbit spinal ganglia. Journal of the Peripheral Nervous System 2, 7782.
Pannese, E., Ledda, M., Cherkas, P.S., Huang, T.Y. and Hanani, M. (2003) Satellite cell reactions to axon injury of sensory ganglion neurons: Increase in number of gap junctions and formation of bridges connecting previously separate perineuronal sheaths. Anatomy and Embryology 206, 337347.
Pazour, G.J. and Witman, G.B. (2003) The vertebrate primary cilium is a sensory organelle. Current Opinion in Cell Biology 15, 105110.
Pineda, A., Maxwell, D.S. and Kruger, L. (1967) The fine structure of neurons and satellite cells in the trigeminal ganglion of cat and monkey. American Journal of Anatomy 121, 461488.
Pomerat, C.M., Hendelman, W.J., Raiborn, C.W. Jr. and Massey, J.F. (1967) Dynamic activities of nervous tissue in vitro. In Hydén, H. (ed) The Neuron. Amsterdam: Elsevier, pp. 119178.
Procacci, P., Magnaghi, V. and Pannese, E. (2008) Perineuronal satellite cells in mouse spinal ganglia express the gap junction protein connexin43 throughout life with decline in old age. Brain Research Bulletin 75, 562569.
Ramón y Cajal, S. (1890) Sobre la existencia de terminaciones nerviosas pericelulares en los ganglios nerviosos raquidianos. Pequeñas Comunicaciones Anatómicas, Barcelona, pp. 15.
Rash, J.E., Yasumura, T., Hudson, C.S., Agre, P. and Nielsen, S. (1998) Direct immunogold labeling of aquaporin-4 in square arrays of astrocyte and ependymocyte plasma membranes in rat brain and spinal cord. Proceedings of the National Academy of Sciences of the U.S.A. 95, 1198111986.
Retzius, G. (1894) Zur Frage von den freien Nervenendigungen in den Spinalganglien. Biologische Untersuchungen N.F. 6, 5961.
Rosenbluth, J. (1962) The fine structure of acoustic ganglia in the rat. Journal of Cell Biology 12, 329359.
Rosenbluth, J. (1963) The visceral ganglion of Aplysia californica. Zeitschrift für Zellforschung und mikroskopische Anatomie 60, 213236.
Rosenbluth, J. and Palay, S.L. (1961) The fine structure of nerve cell bodies and their myelin sheaths in the eighth nerve ganglion of the goldfish. Journal of Biophysical and Biochemical Cytology 9, 853877.
Sakuma, E., Wang, H.J., Asai, Y., Tamaki, D., Amano, K., Mabuchi, Y. et al. (2001) Gap junctional communication between the satellite cells of rat dorsal root ganglia. Acta Anatomica Nipponica 76, 297302.
Sandelin, M., Zabihi, S., Liu, L., Wicher, G. and Kozlova, E.N. (2004) Metastasis-associated S100A4 (Mts1) protein is expressed in subpopulations of sensory and autonomic neurons and in Schwann cells of the adult rat. Journal of Comparative Neurology 473, 233243.
Scharf, J.H. (1958) Sensible Ganglien. In Möllendorff, W. and Bargmann, W. (eds) Handbuch der mikroskopischen Anatomie des Menschen Bd. 4/3. Springer, S. 14–15 and 290300.
Schon, F. and Kelly, J.S. (1974a) Autoradiographic localisation of [3H]GABA and [3H]glutamate over satellite glial cells. Brain Research 66, 275288.
Schon, F. and Kelly, J.S. (1974b) The characterisation of [3H]GABA uptake into the satellite glial cells of rat sensory ganglia. Brain Research 66, 289300.
Shimizu, Y. (1965) The satellite cells in cultures of dissociated spinal ganglia. Zeitschrift für Zellforschung und mikroskopische Anatomie 67, 185195.
Stephenson, J.L. and Byers, M.R. (1995) GFAP immunoreactivity in trigeminal ganglion satellite cells after tooth injury in rats. Experimental Neurology 131, 1122.
Sylvia, A.L. and Rosenthal, M. (1979) Effects of age on brain oxidative metabolism in vivo. Brain Research 165, 235248.
Tennyson, V.M. (1970) The fine structure of the developing nervous system. In Himwich, W.A. (ed) Developmental Neurobiology. Springfield, Illinois: C.C. Thomas, pp. 47116.
Valentin, G. (1836) Über den Verlauf und die letzten Enden der Nerven. Verhandlungen der Kaiserlichen Leopoldinisch-Carolinischen Akademie der Naturforscher 18, 51240.
Valentin, G. (1839) Ueber die Scheiden der Ganglienkugeln und deren Fortsetzungen. Müller's Archiv für Anatomie, Physiologie und wissenschaftliche Medicin S. 139164
Van Gehuchten, A. (1892) Nouvelles recherches sur les ganglions cérébro-spinaux. La Cellule 8, 233253.
Varon, S., Raiborn, C. and Tyszka, E. (1973) In vitro studies of dissociated cells from newborn mouse dorsal root ganglia. Brain Research 54, 5163.
Vega, J.A., Del Valle-Soto, M.E., Calzada, B. and Alvarez-Mendez, J.C. (1991) Immunohistochemical localization of S-100 protein subunits (α and β) in dorsal root ganglia of the rat. Cellular and Molecular Biology 37, 173181.
Verbavatz, J.-M., Ma, T., Gobin, R. and Verkman, A.S. (1997) Absence of orthogonal arrays in kidney, brain and muscle from transgenic knockout mice lacking water channel aquaporin-4. Journal of Cell Science 110, 28552860.
Vit, J.-P., Jasmin, L., Bhargava, A. and Ohara, P.T. (2006) Satellite glial cells in the trigeminal ganglion as a determinant of orofacial neuropathic pain. Neuron Glia Biology 2, 247257.
Waxman, S.G., Dichter, M.A., Hartwieg, E.A. and Matheson, J.K. (1977) Recapitulation of normal neuro-glial relations in dissociated cell cultures of dorsal root ganglia. Brain Research 122, 344350.
Weick, M., Cherkas, P.S., Härtig, W., Pannicke, T., Uckermann, O., Bringmann, A. et al. (2003) P2 receptors in satellite glial cells in trigeminal ganglia of mice. Neuroscience 120, 969977.
Wetmore, C. and Olson, L. (1995) Neuronal and nonneuronal expression of neurotrophins and their receptors in sensory and sympathetic ganglia suggest new intercellular trophic interactions. Journal of Comparative Neurology 353, 143159.
Woodham, P., Anderson, P.N., Nadim, W. and Turmaine, M. (1989) Satellite cells surrounding axotomised rat dorsal root ganglion cells increase expression of a GFAP-like protein. Neuroscience Letters 98, 812.
Wyburn, G.M. (1958) The capsule of spinal ganglion cells. Journal of Anatomy 92, 528533.
Zhang, H., Mei, X., Zhang, P., Ma, C., White, F.A., Donnelly, D.F. et al. (2009) Altered functional properties of satellite glial cells in compressed spinal ganglia. Glia 57, 15881599.
Zhang, X.-F., Han, P., Faltynek, C.R., Jarvis, M.F. and Shieh, C.-C. (2005) Functional expression of P2X7 receptors in non-neuronal cells of rat dorsal root ganglia. Brain Research 1052, 6370.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Neuron Glia Biology
  • ISSN: 1740-925X
  • EISSN: 1741-0533
  • URL: /core/journals/neuron-glia-biology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *



Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed