Quantitative Cytoarchitectonics of the Cerebral Cortices of Several Prosimian Species

  • Karl Zilles
  • Heinz Stephan
  • Axel Schleicher


The classical architectonic studies represented by the works of Meynert (1872), Betz (1881), Campbell (1905), Elliot-Smith (1904, 1907), Vogt (1904, 1906, 1910), Vogt and Vogt (1907), Brodmann (1908, 1909), Economo and Koskinas (1925) and many others reached a “golden age” in the first decades of our century. These studies were based mainly on qualitative descriptions of structural forms, nerve cell morphology, and myelinization in different regions of the cortex. The investigations were mostly done on histological sections stained with Nissl-methods (cytoarchitectonic studies) and with methods demonstrating myelin (myeloarchitectonic studies). Important results were obtained, when (1) brains of many different mammalian species were compared (e.g., Brodmann, 1909) or (2) data from morphological and physiological studies were compared (e.g., Vogt and Vogt, 1907). Unfortunately these approaches were not followed by most later researchers, with the result that subjective and nonreproducible descriptions of minute morphological differences in the laminae or in cell structure increasingly prevailed. The discussions (1) about “haarscharfe Grenzen” (= boundaries fine as a hair) between brain regions, and (2) about the exact number of laminae in a given region of the cortex finally left the realm of science and were not even semantic problems. The consequence of this “development” was severe criticism of cytoarchitectonic studies (Lashley and Clark, 1946; Bailey and v. Bonin, 1951). Since that time workers using cytoarchitectonic methods have had to overcome a wall of more or less justified suspicion. A general suspicion about this type of brain research, however, is not justified, as the results of Hassler on the substantia nigra (1937) and the thalamic nuclei (1959) and the work of Stephan on the allocortex (1975) demonstrate. In these and other cases, the important traditions of classical investigations are apparent—the significance of the morphological structures are ascertained by comparisons among species and with the results of independent physiological studies. The mass of modern axonal transport and electrophysiological studies clearly show by the coincidence of architectonic and functional entities that cytoarchitectonic studies can be a useful tool in working out the function of a brain structure, as for instance, vertical structures such as ocular dominance columns (Hubel and Wiesel, 1963, 1977), barrel fields (Woolsey and Van der Loos, 1970), and dendritic bundles (Fleischhauer, 1974; Fleischhauer et al., 1972).


Granular Layer Areal Pattern Primary Auditory Cortex Areal Fraction Striate Area 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Allman, J.M., and Kaas, J.H., 1971a, A representation of the visual field in the caudal third of the middle temporal gyrus of the owl monkey (Aotus trivirgatus). Brain Res., 31:85–105.CrossRefGoogle Scholar
  2. Allman, J.M. and Kaas, J.H., 1971b. Representation of the visual field in striate and adjoining cortex of the owl monkey (Aotus trivirgatus). Brain Res., 35:89–106.CrossRefGoogle Scholar
  3. Allman, J.M., and Kaas, J.H., 1974a, The organization of the second visual area (VII) in the owl monkey: a second order transformation of the visual hemifield. Brain Res., 76:247–265.CrossRefGoogle Scholar
  4. Allman, J.M., and Kaas, J.H., 1974b, A crescent-shaped cortical visual area surrounding the middle temporal area (MT) in the owl monkey (Aotus trivirgatus). Brain Res., 81:199.CrossRefGoogle Scholar
  5. Allman, J.M., and Kaas, J.H., 1975, The dorsomedial cortical visual area: a third tier area in the occipital lobe of the owl monkey (Aotus trivirgatus). Brain Res., 100:473–487.CrossRefGoogle Scholar
  6. Allman, J.M., and Kaas, J.H., 1976, Representation of the visual field on the medial wall of occipital-parietal cortex in the owl monkey. Science, 191:572–575.CrossRefGoogle Scholar
  7. Allman, J.M., Campbell, C.B.G., and McGuinness, E., 1979, The dorsal third tier area in Galago senegalensis. Brain Res., 179:355–361.CrossRefGoogle Scholar
  8. Allman, J.M., Kaas, J.H., and Lane, R.H., 1973, The middle temporal visual area (MT) in the bushbaby, Galago senegalensis. Brain Res., 57:197–202.CrossRefGoogle Scholar
  9. Bailey, P., and v. Bonin, G., 1951. The Isocortex of Man, University of Illinois Press, Urbana.Google Scholar
  10. Betz, W., 1881, Über die feinere Struktur der Grosshirnrinde des Menschen. Centralbl. f. d. mediz. Wiss., 19:193–195.; 209-213; 231-234.Google Scholar
  11. Braak, H., 1972a, Zur Pigmentarchitektonik der Grosshirnrinde des Menschen. I. Regio entorhinalis. Z. Zellforsch, 127:407–438.CrossRefGoogle Scholar
  12. Braak, H., 1972b, Zur Pigmentarchitektonik der Grosshirnrinde des Menschen. II. Subiculum. Z. Zellforsch, 131:235–254.CrossRefGoogle Scholar
  13. Braak, H., 1976a, A primitive gigantopyramidal field buried in the depth of the cingulate sulcus of the human brain. Brain Res., 109:219–233.CrossRefGoogle Scholar
  14. Braak, H., 1976b, On the striata area of the human isocortex. A Golgi-and pigmentarchitectonic study. J. Comp. Neurol., 166:341–364.CrossRefGoogle Scholar
  15. Braak, H., 1977, The pigmentarchitectonic of the human occipital lobe. Anat. Embryol., 150:229–250.CrossRefGoogle Scholar
  16. Brodmann, K., 1908, Beitrage zur histologischen Lokalisation der Grosshirnrinde. VII. Mitteilung: Die cytoarchitektonische Cortexgliederung der Halbaffen (Lemuriden). J. Psychol. Neurol., 10:287–334.Google Scholar
  17. Brodmann, K., 1909. Vergleichende Lokalisationslehre der Grosshirnrinde in ihren Prinzipien dargestellt auf Grund des Zellenbaus. J.A. Barth, Leipzig.Google Scholar
  18. Campbell, A.W., 1905. Histological Studies on the Localisation of Cerebral Function, University Press, Cambridge.Google Scholar
  19. Carlson, M., and Welt, C., 1980, Somatic sensory cortex (Sml) of the prosimian primate Galago crassicaudatus: organization of mechanoreceptive input from the hand in relation to cytoarchitecture. J. Comp. Neurol., 189:249–271.CrossRefGoogle Scholar
  20. Cartmill, M., 1975. Strepsirhine basicranial structures and affinities of the cheirogaleidae. In, Phylogeny of the Primates, W.P. Luckett and F.S. Szalay, eds., Plenum Press, New York and London, pp. 313–354.Google Scholar
  21. Economo, C. von and Koskinas, G.N., 1925. Die Cytoarchitektonik der Hirnrinde des erwachsenen Menschen, Springer, Berlin.Google Scholar
  22. Elliot-Smith, G., 1904, The morphology of the occipital region of the cerebral hemisphere in man and apes. Anat. Anz., 24:436–451.Google Scholar
  23. Elliot-Smith, G., 1907, A new topographical survey of the human cerebral cortex, being an account of the distribution of the anatomically distinct cortical areas and their relationship to the cerebral sulci. J. Anat. Physiol., 41:237–254.Google Scholar
  24. Fleischhauer, K., 1974, On different patterns of dendritic bundling in the cerebral cortex of the cat. Z. Anat. Entwickl. Gesch., 143:115–126.CrossRefGoogle Scholar
  25. Fleischhauer, K., Petsche, H., and Wittkowski, W., 1972, Vertical bundles of dendrites in the neocortex. Z. Anat. Entwickl. Gesch., 136:213–223.CrossRefGoogle Scholar
  26. Graham, J., Lin, C.S., and Kaas, J.H., 1979, Subcortical projections of six visual cortical areas in the owl monkey, Aotus trivirgatus. J. Comp. Neurol., 187:557–580.CrossRefGoogle Scholar
  27. Gregory, W.K., 1915, On the classification and phylogeny of the Lemuroidea. Bull. Geol. Soc. Am., 26:426–446.Google Scholar
  28. Hassler, R., 1937. Zur Normalanatomie der Substantia nigra. Versuch einer architektonischen Gliederung. J. Psychol. Neurol. Lpz., 48:1–55.Google Scholar
  29. Hassler, R., 1959. Anatomie des Thalamus. In, Einführung in die sterotaktischen Operationen, G. Schaltenbrand and P. Bailey, eds., Thieme Verlag, Stuttgart, pp. 230–290.Google Scholar
  30. Haug, H., 1956, Remarks on the determination and significance of the gray cell coefficient. J. Comp. Neurol., 104:473–492.CrossRefGoogle Scholar
  31. Haug, H., 1958. Quantitative Untersuchungen an der Sehrinde, Thieme Verlag, Stuttgart.Google Scholar
  32. Haug, H., 1972, Stereological methods in the analysis of neuronal parameters in the central nervous system. J. Microscopy, 95:165–180.CrossRefGoogle Scholar
  33. Haug, H., 1976, Die verschiedenen Verfahren zur Werteerfassung in der biologischen Morphometrie und Sterologie. Microscopica Acta, 78:197–220.Google Scholar
  34. Haug, J., Kebbel, J., and Wiedermeyer, G.L., 1971, Die Messung der mittleren Zelldichte und ihre Verteilung in Geweben mit erheblichen Zelldichteunterschieden (Auswertung am Cortex cerebri als Beispiel). Microscopica Acta, 71:121–128.Google Scholar
  35. Heath, C.J., Höre, J., and Phillips, C.G., 1976, Inputs from low threshold muscle and cutaneous afférents of hand and forearm to areas 3a and 3b of baboon’s cerebral cortex. J. Physiol. Lond., 257:199–227.Google Scholar
  36. Hopf, A., 1966, Über eine Methode zur objectiven Registrierung der Myloarchitektonik der Hirnrinde. J. Hirnforsch., 8:301–313.Google Scholar
  37. Höre, J., Preston, J.B., Durkovic, R.G., and Cheney, P.D., 1976, Responses of cortical neurons (areas 3a and 4) to rump stretch of hindlimb muscles in the baboon. J. Neurophysiol., 39:484–500.Google Scholar
  38. Hubel, D.H., and Wiesel, T.N., 1963, Shape and arrangement of columns in cat’s striate cortex. J. Physiol., 165:559–568.Google Scholar
  39. Hubel, D.H., and Wiesel, T.N., 1977. Functional architecture of macaque monkey visual cortex. Proc. R. Soc. Lond., B198:1–59.CrossRefGoogle Scholar
  40. Hudspeth, A.J., Ruark, J.E., and Kelly, J.P., 1976, Cytoarchitectonic mapping by microdensitometry. Proc. Natl. Acad. Sci. 73:2928–2931.CrossRefGoogle Scholar
  41. Imig, T.J., Ruggero, M.A., Kitzel, L.M., Javel, E., and Brugge, J.F., 1977, Organization of auditory cortex in the owl monkey (Aotus trivirgatus). J. Comp. Neurol., 171:111–128.CrossRefGoogle Scholar
  42. Jones, E.G., 1975, Lamination and differential distribution of thalamic afférents within the sensory motor cortex of the squirrel monkey. J. Comp. Neurol., 160:167–204.CrossRefGoogle Scholar
  43. Jones, E.G., and Porter, R., 1980, What is Area 3a?. Brain Res. Reviews, 2:1–43.CrossRefGoogle Scholar
  44. Krishnamurti, A., Sanides, F., and Welker, W.I., 1976, Microelectrode mapping of modality-specific somatic sensory cerebral neocortex in slow loris. Brain Behav. Evol., 13:267–283.CrossRefGoogle Scholar
  45. Lashley, K.S., and Clark, G., 1946, The cytoarchitecture of the cerebral cortex of Ateles: a critical examination of architectonic studies. J. Comp. Neurol., 85:223–305.CrossRefGoogle Scholar
  46. Lucier, G.E., Ruegg, D.C., and Wiesendanger, M., 1975, Responses of neurons in motor cortex and in area 3a to controlled stretches of forelimb muscles in cebus monkey. J. Physiol. Lond., 251:833–853.Google Scholar
  47. Martin, R.D., 1972, Adaptive radiation and behavior of the Malagasy lemurs, Philos. Trans. R. Soc. London, Ser B 264:295–352.CrossRefGoogle Scholar
  48. Meynert, R., 1872. Der Bau der Grosshirnrinde und seine örtlichen Verschiedenheiten, nebst einem pathologisch-anatomischen Corollarium, JH Heuser, Neuwied.Google Scholar
  49. Mott, E.W., and Halliburton, W.D., 1908, Localization of function in the lemur’s brain. Proc. Royal Soc. London, Ser B 80:136–147.CrossRefGoogle Scholar
  50. Mott, E.W., and Kelly, A.M., 1908, Complete survey of the cell lamination of the cerebral cortex of the lemur. Proc. Royal Soc. London, Ser B 80:488–506.CrossRefGoogle Scholar
  51. Phillips, C.G., Powell, T.P.S., and Wiesendanger, M., 1971, Projection from low threshold muscle afférents of hand and forearm to area 3a baboon’s cortex. J. Physiol. Lond., 217:419–446.Google Scholar
  52. Prewitt, J.M.S., 1965, The selection of sampling rate for digital scanning. IEEE transact. Bio-Med. Engineering, 1:14–21.CrossRefGoogle Scholar
  53. Prewitt, J.M.S., and Mendelssohn, M.L., 1966, The analysis of cell images. Ann. New York Acad. Sci., 128:1035.CrossRefGoogle Scholar
  54. Raczkowski, D., and Diamond, I.T., 1978, Connections of the striate cortex in Galago senegalensis. Brain Res., 144:383–388.CrossRefGoogle Scholar
  55. Rosenfeld, A., and Kak, A., 1976. Digital Picture Processing, Academic Press, New York.Google Scholar
  56. Ryzen, M., and Campbell, B., 1955, Organization of the Cerebral Cortex II. Cortex of Sorex pacificus. J. Comp. Neurol., 102:365–424.CrossRefGoogle Scholar
  57. Sanides, F., 1968, The architecture of the cortical taste nerve areas in squirrel monkey (Saimiri sciureus) and their relationships to insular, sensorimotor and prefrontal regions. Brain Res., 8:97–124.CrossRefGoogle Scholar
  58. Sanides, F., and Krishnamurti, A., 1967, Cytoarchitectonic subdivisions of sensorimotor and prefrontal regions and of bordering insular and limbic fields in slow loris (Nycticebus coucang coucang)s. J. Hirnforsch., 9:225–252.Google Scholar
  59. Schleicher, A., Zilles, K., and Kretschmann, H.J., 1978. Automatische Registrierung und Auswertung eines Grauwertindex in histologischen Schnitten. Anat. Anz., 144 (Erg-Heft):413–415.Google Scholar
  60. Schwarz, D.W.F., Deecke, L., and Frederickson, J.M., 1973, Cortical projection of group I muscle afférents to areas 2, 3a, and the vestibular field in the rhesus monkey. Exp. Brain Res., 17:516–526.CrossRefGoogle Scholar
  61. Serra, J., 1972, Stereology and structuring elements. J. Microscopy. 95:93.CrossRefGoogle Scholar
  62. Stephan, H., 1969. Quantitative investigation on visual structures in primate brains. In, Proc. 2nd Int. Congr. Primatol. Soc, Atlanta GA 1968, Karger, Basel New York, Vol 3, pp. 34–42.Google Scholar
  63. Stephan, H., 1975. Allocortex. In, Handbuch der mikroskopischen Anatomie des Menschen, W. Bargmann, ed., 4. Bd Nervensystem, Teil 9, Springer, Berlin.Google Scholar
  64. Stephan, H., and Andy, O.J., 1970. The Allocortex in Primates. In, The Primate Brain, C.R. Noback, and W. Montagna, eds., Appleton-Century-Crofts, New York, pp. 109–135.Google Scholar
  65. Sur, M., Nelson, R.J., and Kaas, J.H., 1980, Representation of the body surface in somatic koniocortex in the prosimian Galago. J. Comp. Neurol., 189:381–402.CrossRefGoogle Scholar
  66. Symonds, L.L., and Kaas, J.H., 1978, Connections of striate cortex in the prosimian, Galago senegalensis. J. Comp. Neurol., 181:477–512.CrossRefGoogle Scholar
  67. Vogt, O., and Vogt, O., 1907, Zur Kenntnis der elektrisch erregbaren Hirnrindengebiete bei den Säugetieren. J. Psychol. Neurol., 8:277–456.Google Scholar
  68. Vogt, O., and Vogt, O., 1919, Allgemeinere Ergebnisse unserer Hirnforschung. J. Psychol. Neurol., (Lpz.), 25:279–462.Google Scholar
  69. Vogt, O., 1906. Über strukturelle Hirnzentra, mit besonderer Berücksichtigung der strukturellen Felder des Cortex pallii. Anat. Anz., 29:(Erg Bd) 74–114.Google Scholar
  70. Vogt, O., 1910, Die myeloarchitektonische Felderung des menschlichen Stirnhirns. J. Psychol. Neurol., 15:221–232.Google Scholar
  71. Weibel, E.R., 1979. Stereological Methods, Volume 1: Practical methods for biological morphometry, Academic Press, London.Google Scholar
  72. Wiesendanger, M., 1973, Input from muscle and cutaneous nerves of the hand and forearm to neurones of the precentral gyrus of baboons and monkeys. J. Physiol. (Lond)., 228:203–219.Google Scholar
  73. Woolsey, T.A., and Van der Loos, H., 1970, The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. Brain Res., 17:205–242.CrossRefGoogle Scholar
  74. Wree, C., Zilles, K. and Schleicher, A., 1981, A quantitative approach to cytoarchitectonics. VII. The areal pattern of the cortex of the guinea pig. Anat. Embryol. 162:81–103.CrossRefGoogle Scholar
  75. Zilles, K., Schleicher, A., and Kretschmann, H.J., 1978a, A quantitative approach to cytoarchitectonics. I. The areal pattern of the cortex of Tupaia belangen. Anat. Embryol., 153:195–212.CrossRefGoogle Scholar
  76. Zilles, K., Schleicher, A., and Kretschmann, H.J., 1978b, A quantitative approach to cytoarchitectonics. II. The allocortex of Tupaia belangen. Anat. Embryol., 154:335–352.CrossRefGoogle Scholar
  77. Zilles, K., Schleicher, A., and Kretschmann, H.J., 1978c. Quantitative Darstellung cytoarchitektonischer Areale im Cortex von Tupaia belangeri und SPF-Katze. Anat. Anz., 144(Erg-Heft):409-411.Google Scholar
  78. Zilles, K., Rehkamper, G., Stephan, K., and Schleicher, A., 1979a, A quantitative approach to cytoarchitectonics. IV. The areal pattern of the cortex of Galago demidovii (E Geoffroy, 1976), (Lorisidae, Primates). Anat. Embryol., 157:81–103.CrossRefGoogle Scholar
  79. Zilles, K., Rehkamper, G., and Schleicher, A., 1979b, A quantitative approach to cytoarchitectonics. V. The areal pattern of the cortex of Microcebus murinus (E Geoffroy, 1828), (Lemuridae, Primates). Anat. Embryol., 157:269–289.CrossRefGoogle Scholar
  80. Zilles, K., and Schleicher, A., 1980, Similarities and differences in the cortical areal patterns of Galago demidovii (E Geoffroy, 1796), (Lorisidae, Primates) and Microcebus murinus (E Geoffroy, 1828), (Lemuridae, Primates). Folia Primatol., 33:161–171.CrossRefGoogle Scholar
  81. Zilles, K., Zilles, K., and Schleicher, A., 1980, A quantitative approach to cytoarchitectonics. VI. The areal pattern of the cortex of the albino rat. Anat. Embryol., 159:335–360.CrossRefGoogle Scholar
  82. Zilles, K., and Schleicher, A., 1980, Quantitative Analyse der laminären Struktur menschlicher Cortexareale. Anat. Anz., (Erg-Heft), 146:725–726.Google Scholar

Copyright information

© Plenum Press, New York 1982

Authors and Affiliations

  • Karl Zilles
    • 1
    • 2
  • Heinz Stephan
  • Axel Schleicher
  1. 1.Anatomical Institute (KZ and AS)University KielKielGermany
  2. 2.Max-Planck-Institute for Brain Research (HSt)Frankfurt/M.Germany

Personalised recommendations