Cited by 266

The DOI matches its Crossref record; 3 of the 3 references it cites were found in a registry or an index.

The “Big‐Bang” for modern glial biology: Translation and comments on Pío del Río‐Hortega 1919 series of papers on microglia

Sierra, Amanda, de Castro, Fernando, del Río‐Hortega, Juan, Rafael Iglesias‐Rozas, José, Garrosa, Manuel, Kettenmann, Helmut·2016·Glia

Abstract

The word “glia” was coined in the mid‐19th century and defined as “the nerve glue”. For decades, it was assumed to be a uniform matrix, until cell theorists raised the “neuron doctrine” which stipulated that nervous tissue was composed of individual cells. The term “astrocytes” was introduced in the late 19th century as a synonym for glial cells, but it was Santiago Ramón y Cajal who defined a “third element” distinct from glial cells (astrocytes) and neurons. It was not until 1919 when Pío del Río‐Hortega, an alumnus of the Cajal School, introduced the modern terms we use today, and thoroughly described both “oligodendrocytes” and “microglia” to clearly distinguish them from astrocytes. In a series of four papers published that year in Spanish, Río‐Hortega described the distribution and morphological phenotype of microglia. He also noted that these cells were the origin of the rod cells described earlier in pathologic tissue, and recognized that resting microglia transformed into an ameboid phenotype in different types of brain diseases and pathologies. He also noted the mesodermal origin of these cells and recognized their phagocytic capacity. We here provide the first English translation of these landmark series of papers, which paved the way for modern glial research. To heighten the value and accessibility of these classic papers and their original figures, an introduction to this critical period of neuroscience is provided, along with unpublished photographs. By adding comments to the translated text, we provide sufficient context so that contemporary scientists may fully appreciate it. GLIA 2016;64:1801–1840

Overview

Integrity signals

Registry

Crossref · 10.1002/glia.23046

Cites

3 of 3 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Verification

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Citations

Cites

Flagged first, then by citations

Show all 3 references

Research works printed but not linked: 71

  1. Anton y Wohlwill: Multiple nichteitrige Encephalomyelitis und multipIe Sklerose. Zeitschr. für d. ges. Neurol. und Psych. tomo XII 1912. · DOI
  2. Eisath: Weitere Beobachtungen über die menschlichen Neuroglia.Arch. für Psychiatr. und Nervenkrankheiten tomo XXXVIII 1911 · DOI
  3. Friedmann: Studien zur pathologischen Anatomie der akuten Encephalitis.Arch.f. Psych. tomo XXI 1890. · DOI
  4. Jacob: Zur Pathologie der diffusen infiltrierten Encephalomyelitis in ihren Beziehungen zur diffusen und multiplen Sklerose.Zeitschr. für die ges. Neurol. und Psch. tomo XXVII 1914. · DOI
  5. Schaffer: Zur Kenntnis der normalen und pathologischen Neuroglia.Hirnpat. Beiträge aus dem hirnhistopath. Inst. der Univ. Budapest 1915. · DOI
  6. (Ref. 4)Virchow: Kongenitale Encephalitis und Myelitis.Virchow's Arch. tomo XXXVIII. pág. 129 1867. · DOI
  7. (Ref. 7)Jastrowitz: Encephalitis und Myelitis des ersten Kindesalters. Arch. f. Psych. tomo II pág. 389 1870 y tomo III pág. 162 1872. · DOI
  8. (Ref. 8)Boll: Die Histologie und Histogenese der nervösen Zentralorgane.Arch. f Psych. tomo IV pág. 1 1874. · DOI
  9. (Ref. 9)Eichhorst: Ueber die Entwicklung des menschlichen Rückenmark und seiner Formelemente.Virchow‘s Arch. tomo LXIV página 424 1875. · DOI
  10. Achúcarro N., 1908, Sur la formation de cellules á bâtonnet (Stäbchenzellen) et d'autres éléments similaries dans le système nerveux central, Trab Lab Invest Biol Univer Madrid, 98
  11. Achúcarro N., 1909, Cellules allongées et Stäbchenzellen: Cellules neurogliques et cellules granulo‐adipeuses à la corne d'Ammon du lapin, Trab Lab Invest Biol Univer Madrid, 4, 2
  12. Achúcarro N., 1910, Algunos datos relativos a la naturaleza de las celulas en bastoncito de la corteza cerebral humana obtenidos con el método de Cajal, Trab. del Lab. de Invest. biol, tomo
  13. Achúcarro N., 1911, Nuevo método para el estudio de la neuroglía y del tejido conjuntivo
  14. Achúcarro N., 1913, Notas sobre la estructura y funciones de la neuroglía y en particular de la neuroglía de la corteza cerebral humana, Trab Lab Invest Biol Univer Madrid, 3, 1
  15. Achúcarro N, 1914, Nuevos estudios sobre la histopatología de la parálisis general con el método al cloruro de oro y sublimado de Cajal, Bol Soc Esp Biol Sesión 26 de Febrero de, 1914, 1
  16. Alzheimer A., 1910, Histologische und Histopathologische Arbeiten über die Grosshirnrinde
  17. 10.1523/JNEUROSCI.3751-14.2015 · DOI
  18. 10.1007/BF00325030 · DOI
  19. Cano Díaz P, 1985, Una contribución a la ciencia histológica: la obra de don Pío del Río‐Hortega, 230
  20. Castellano B, 1995, Contribuciones científicas de Don Pío del Río Hortega en la neurociencia, Neurología, 10, 265
  21. Cerletti U., 1905, Sopra alcuni rapporti fra le “cellule a bastoncello” (Stäbchenzellen) e gli elementí nervosi nella Paralisi progressiva, Riv sperim Freniatria, tomo, XXXI
  22. 10.1002/path.1700590143 · DOI
  23. 10.1080/01616412.1980.11739566 · DOI
  24. 10.1016/B978-0-12-397266-8.00035-1 · DOI
  25. 10.1002/(SICI)1097-4547(19971101)50:3<477::AID-JNR14>3.0.CO;2-3 · DOI
  26. Fernández‐Santarén JA., 2014, Santiago Ramón y Cajal Epistolario
  27. 10.1016/j.tins.2007.06.008 · DOI
  28. Garrosa M, 2015, Updates in histology, 22
  29. 10.1227/01.NEU.0000255448.97730.34 · DOI
  30. 10.1038/nn.4222 · DOI · Paper page
  31. 10.1038/nrm2641 · DOI
  32. 10.5414/NP301001 · DOI
  33. Iglesias‐Rozas JR, 2013, Río‐Hortega's third contribution to the morphological knowledge and functional interpretation of the oligodendroglia
  34. Jakob A., 1913, Über die feinere Histologie der sekundären Faserdegeneration in der weissen Substanz des Rückenmarks (mit besonderer Berücksichtigung der Abbauvorgänge), Histologische und Histopathologische Arbeiten über die Großhirnrinde. Jena: Gustav Fischer Verlag., 5, 1
  35. Lenhossek M., 1895, Bau des Nervensystems
  36. Lewis B., 1889, Text‐book of mental diseases
  37. López Sánchez JM., 2012, Una escuela, dos laboratorios: Neurociencias en la Junta para Ampliación de Estudios, Rev Asoc Esp Neurospsiq, 32, 805
  38. Lorente de Nó R, 1923, A propósito de la homología entre la glía de escasa radiaciones y la célula de Schwann y endocapsulares, Bol Soc Esp Biol, 63
  39. Lugaro E., 1907, Sulle funzioni della nevroglia, Riv Patol Nerv Ment, 225
  40. Mallory FB., 1891, Phospho‐molybdic acid‐haematoxylin, Anatomischer Anzeiger, 6, 375
  41. 10.1093/med/9780190221591.001.0001 · DOI
  42. Merzbacher L., 1909, Zentralnervensystem. Histologische und Histopathologische Arbeiten über die Großhirnrinde, 1
  43. 10.1007/BF02885808 · DOI
  44. Nissl F., 1904, Zur Histopathologie der paralytischen Rindenerkrankungen, 315
  45. PanneseE.1994.Neurocytology. Fine structure of neurons nerve processes and neuroglial cells. Stuttgart: Georg Thieme Verlag.
  46. 10.1093/brain/47.4.430 · DOI
  47. Ramón y, 1897, Algo sobre la significación fisiológica de la neuroglía, Revista Trimestral Micrográfica, 2, 33
  48. Ramón y, 1913, Contribución al conocimiento de la neuroglía del cerebro humano, Trab Lab Invest Biol Univer Madrid, 215
  49. Ramón y, 1920, Algunas consideraciones sobre la mesoglía de Robertson y Río Hortega, Trab Lab Invest Biol Univers Madrid, 129
  50. Ramón y Cajal S., 1933, Neuronismo o reticularismo? Las pruebas objetivas de la unidad anatómica de las células nerviosas, Arch. Neurobiol, 13, 217
  51. Río‐Hortega P., 1919, El “tercer elemento” de los centros nerviosos. I. La microglía en estado normal, Bol Soc Esp Biol, 67
  52. Río‐Hortega P., 1919, El “tercer elemento de los centros nerviosos”. II. Intervención de la microglía en los procesos patológicos (células en bastoncito y cuerpos gránuloadiposos), Bol Soc Esp Biol, 91
  53. Río‐Hortega P., 1919, El “tercer elemento” de los centros nerviosos. III. Naturaleza probable de la microglía, Bol Soc Esp Biol, 108
  54. Río‐Hortega P., 1919, El “tercer elemento de los centros nerviosos”. IV. Poder fagocitario y movilidad de la microglía, Bol Soc Esp Biol
  55. Río‐Hortega P., 1921, Glía con pocas prolongaciones (oligodendroglía), Bol Soc Esp Biol
  56. Río‐Hortega P., 1922, ¿Son homologables la glía de escasas radiaciones y la célula de Schwann?, Bol Soc Esp Biol, 1
  57. Río‐Hortega P., 1928, Tercera aportación al conocimiento morfológico e interpretación funcional de la oligodendroglía, Mem Soc Esp Biol, 5
  58. Río‐Hortega P., 1993, Cronobiografía, edición e índices de Juan del Río‐Hortega Bereciartu
  59. Robertson WF., 1899, On a new method of obtaining a black reaction in certain tissue‐elements of the central nervous system (platinum method), Scott Med Surg J, 4, 23
  60. 10.1192/bjp.46.195.724 · DOI
  61. 10.1007/BF02970930 · DOI
  62. 10.1017/S0025727300020482 · DOI
  63. 10.1016/j.brainresbull.2014.09.005 · DOI
  64. 10.3389/fnana.2015.00045 · DOI
  65. 10.1159/000209731 · DOI
  66. Virchow R., 1856, Gesammelte Abhandlungen zur wissenschaftlichen Medizin
  67. Virchow R. 1867. Kongenitale Encephalitis und Myelitis. Virchow's Arch. tomo XXXVIII. pag. 129. · DOI
  68. Vitoria Ortiz M., 1977, Vida y obra de Nicolás Achúcarro
  69. von Kölliker A., 1896, Handbuch der Gewebelehre des Menschen, Verlag Wilhelm Engelmann: Leipzig.
  70. Weigert C., 1895, Beiträge zu Kenntnis der normalen menschlichen Glia
  71. 10.1111/ejn.13256 · DOI

Cited by

Sorted by citations

See all 266

Metadata

Authors
Sierra, A., de Castro, F., del Río‐Hortega, J., Rafael Iglesias‐Rozas, J., Garrosa, M., & Kettenmann, H.
Venue
Glia
Publisher
Wiley
Published
2016-09-16
Volume
64
Issue
11
Pages
1801-1840
ISSN
  • 0894-1491
  • 1098-1136
Cited by
266
References
3
Language
en
Funders
  • Spanish Ministry of Economy and Competitiveness with FEDER (BFU2012-32089, BFU2015-66689, and RYC-2013-12817, RD12-0032)
  • Cnsejo Superior de Investigaciones Científicas to FdC (CSIC 2015201023)
  • Deutsche Forschungsgemeinschaft (SFB TR43 and Neurocure)

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review