Skip to main content
SpringerLink
Log in

Postnatal development of the human primary motor cortex: a quantitative cytoarchitectonic analysis

  • Original Article
  • Published:
Anatomy and Embryology Aims and scope Submit manuscript

Abstract

The postnatal development of the human primary motor cortex (area 4) was analyzed in 54 individuals ranging in age from birth to 90 years. Three parameters defining major cytoarchitectonic features (areal fraction, numerical density and mean area of cells) were measured in vertical columns extending from the pial surface to the border between cortex and underlying white matter. The data were compiled in profile curves that reveal a more detailed laminar pattern than the classical cytoarchitectonic descriptions. The most pronounced decreases in numerical density and areal fraction of Nissl-stained cell profiles during early postnatal ontogeny are observed in layer II. A clearly delineable layer IV, which is still recognizable in the newborn, disappears gradually during the first postnatal months. Although the width of the cortex as a whole increases during this period, layer V, the main source of pyramidal tract fibers, is the only lamina that also increases in relative thickness. The other layers remain stable or become relatively thinner. These results reveal specific laminar growth processes in area 4, which take place in parallel with the functional maturation of the cortical motor system.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Adams R, Victor M (1989) Principles of neurology. McGraw-Hill, New York

    Google Scholar 

  • Amunts K (1993) Computergestützte Mikroskopbildauswertung in der biomedizinischen Forschung. Vision Jahrb 1:24–32

    CAS  PubMed  Google Scholar 

  • Amunts K, Istomin V (1992) Verfahren zur automatischen Bildauswertung in der Neurobiologie. Vision Voice Mag 6:18–22

    Google Scholar 

  • Anderson JM, Hubbard BM, Coghill BR, Slidders W (1983) The effect of advanced old age on the neurone content of the cerebral cortex. Observation with an automatic image analyser point counting method. J Neurol Sci 58:233–244

    Google Scholar 

  • Ang LC, George DH, Shul D, Wang DQ, Munoz DG (1992) Delayed changes of chromogranin A immunoreactivity (CgA ir) in human striate cortex during postnatal development. Brain Res Dev Brain Res 67:333–341

    Google Scholar 

  • Blackstad TW, Bjaalie JG (1988) Computer programs for neuroanatomy: three-dimensional reconstruction and analysis of populations of cortical neurons and other bodies with a laminar distribution. Comput Biol Med 18:321–340

    Google Scholar 

  • Blakemore C, Molnar Z (1990) Factors involved in the establishment of specific interconnections between thalamus and cerebral cortex. Cold spring Harbor Symp Quant Biol 55:491–504

    Google Scholar 

  • Blinkov SM, Glezer II (1968) Das Zentralnervensystem in Zahlen und Tabellen. Fischer, Jena

    Google Scholar 

  • Bogolepova IN (1981) Structural features of the organization of some cortical formations in the left and right hemispheres of the human brain (in Russian). Korsakov J Neurol Psychiatry 7:974–977

    Google Scholar 

  • Borit A, McIntosh GC (1981) Myelin basic protein and glial fibrillary acidic protein in human fetal brain. Neuropathol Appl Neurobiol 7:279–287

    Google Scholar 

  • Braak H (1979) The pigment architecture of the human frontal lobe. Anat Embryol 157:35–68

    Google Scholar 

  • Brodmann K (1909) Vergleichende Lokalisationslehre der Großhirnrinde in ihren Prinzipien dargestellt auf Grund des Zellenbaues. Barth Leipzig

    Google Scholar 

  • Brody H (1955) Organisation of the cerebral cortex. 3. A study of aging in the human cerebral cortex. J Comp Neurol 102:551–556

    Google Scholar 

  • Brody H (1970) Structural changes in the aging nervous system. Interdiscip Top Gerontol 7:9–21

    Google Scholar 

  • Candy JM, Perry EK, Perry RH, Bloxham CA, Thompson J, Johnson M, Oakley AE, Edwardson JA (1985) Evidence for the early prenatal development of cortical cholinergic afferents from the nucleus of Meynert in the human foetus. Neurosci Lett 61:911–915

    Google Scholar 

  • Cepeda C, Peacock W, Levine MS, Buchwald NA (1991) Ionotrophic application of NMDA produces different types of excitatory responses in developing human cortical and caudate neurons. Neurosci Lett 126:167–171

    Google Scholar 

  • Chiron C, Raynaud C, Maziere B, Zilbovicius M, Laflamme L, Masure MC, Dulac O, Bourguignon M, Syrota A (1992) Changes in regional cerebral blood flow during brain maturation in children and adolescents. J Nucl Med 33:696–703

    Google Scholar 

  • Chugani HT, Phelps ME (1986) Maturational changes in cerebral function in infants determined by 18FDG positron emission tomography. Science 231:840–843

    Google Scholar 

  • Cragg B (1972) The development of synapses in the cat visual cortex. Invest Ophtalmol Vis Sci 11:377–385

    Google Scholar 

  • Dietrich RB (1990) Magnetic resonance imaging of normal brain maturation. Semin Perinatol 14:201–211

    Google Scholar 

  • Dobbing J, Sand J (1975) Quantitative growth and development of human brain. Arch Dis Child 48:757–767

    Google Scholar 

  • Eayrs JT, Goodhead B (1959) Postnatal development of the cerebral cortex in the rat. J Anat 93:385–402

    Google Scholar 

  • Economo C von, Koskinas GN (1925) Die Cytoarchitektonik der Hirnrinde des erwachsenen Menschen. Springer, Wien Berlin

    Google Scholar 

  • Ferrer I, Soriano E, Del Rio JA, Alcantara S, Auladell C (1992) Cell death and removal in the cerebral cortex during development. Prog Neurobiol 39:1–43

    Google Scholar 

  • Filimonov JN (1929) Zur embryonalen und postembryonalen Entwicklung der Großhirnrinde des Menschen. J Psychol Neurol 39:323–389

    Google Scholar 

  • Flechsig P (1927) Meine myelogenetische Hirnlehre mit biographischer Einleitung. Springer, Berlin

    Google Scholar 

  • Fritschey JM, Garey LH (1986) Quantitative changes in morphological parameters in the developing visual cortex of the Marmorset Monkey. Brain Res Dev Brain Res 29:173–188

    Google Scholar 

  • Garey LJ (1984) Structural development of the visual system of man. Hum Neurobiol 3:75–80

    Google Scholar 

  • Garey LJ, Courten C de (1983) Structural development of the lateral geniculate nucleus and visual cortex in monkey and man. Behav Brain Res 10:3–13

    Google Scholar 

  • Giguere M, Goldman-Rakic PS (1988) Mediodorsal nucleus: areal, laminar, and tangential distribution of afferents and efferents in the frontal lobe of rhesus monkey. J Comp Neurol 277:195–213

    Google Scholar 

  • Goldman-Rakic P, Rakic P (1984) Experimental modification of gyral patterns. In: Geschwind N, Galaburda AM (eds) Cerebral dominance. The biological foundation. University Press, Cambridge London pp 179–192

    Google Scholar 

  • Gonzalez RC, Wintz P (1987) Digital image processing. Addison-Wesley, Reading

    Google Scholar 

  • Gundersen HJG, Bendtsen TF, Korbo L, Marcussen N, Moeller A, Nielsen K, Nyengaard, Pakkenberg B, Sörensen FB, Vesterby A, West MJ (1988) Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. APMIS 96:379–394

    CAS  PubMed  Google Scholar 

  • Haug H (1980) Die Abhängigkeit der Einbettungsschrumpfung des Gehirngewebes vom Lebensalter. Verh Anat Ges 74:699–700

    Google Scholar 

  • Haug H (1984) Macroscopic and microscopic morphometry of the human brain and cortex. A survey in the light of new results Brain Pathol 1:123–149

    Google Scholar 

  • Haug H (1987) Brain sizes, surfaces, and neuronal sizes of the cortex cerebri: a stereological investigation of man and his variability and a comparison with some mammals (primates, whales, marsupials, insectivores, and one elephant) Am J Anat 180:126–142

    Google Scholar 

  • Haug H (1989) The aging human cerebral cortex: morphometry of areal differences and their functional meaning (In: Platt D (ed), Gerontology). Springer, Berlin Heidelberg New York, pp 139–158

    Google Scholar 

  • Henderson G, Tomlinson BE, Weightman D (1975) Cell counts in the human cerebral cortex using a traditional and an automatic method. J Neurol Sci 25:129–144

    Google Scholar 

  • Henderson G, Tomlinson BE, Gibson PH (1980) Cell count in human cerebral cortex in normal adults throughout life using an image analysing computer. J Neurol Sci 46:113–136

    Google Scholar 

  • Ho KH, Roessmann U, Hause L, Monroe G (1986) Correlation of perinatal brain growth with age, body size, sex, and race. J Neuropathol Exp Neurol 45:179–188

    Google Scholar 

  • Huttenlocher PR (1979) Synaptic density in human frontal cortex — developmental changes and effects of aging. Brain Res 163:195–205

    Google Scholar 

  • Istomin VV (1985) Principles of adaptive brain sections staining for automated structure analysis (in Russian). Korsakov J Neurol Psychiatry 7:1024–1032

    Google Scholar 

  • Istomin VV (1988) Quantitative cytoarchitectural analysis of some cerebral cortical fields according to the data of automated morphocorticography. Neurosci Behav Physiol 18:344–349

    Google Scholar 

  • Istomin VV, Amunts K (1992) Application of mathematical morphology algorithms for automatic quantification of the cytoarchitecture of human neocortex. Vision Voice Mag 6:142–153

    Google Scholar 

  • Istomin VV, Shkliarov MI (1984) Automated investigation of the human cerebral cortex with a TV-based image analysis system (in Russian). Korsakov J Neuro Psychiatry 7:969–974

    Google Scholar 

  • Jacobson M (1991) Developmental neurobiology. Plenum Press, New York London

    Google Scholar 

  • Jernigan TL, Trauner DA, Hesselink JR, Tallal PA (1991) Maturation of human cerebrum observed in vivo during adolescence. Brain 114:2037–2049

    Google Scholar 

  • Jones EG, Wise SP (1977) Size, laminar and columnar distribution of efferent cells in the sensory-motor cortex of monkeys. J Comp Neurol 175:391–438

    Google Scholar 

  • Jouandet ML, Deck MDF (1993) Prenatal growth of the human cerebral cortex: brainprint analysis. Pediatr Radiol 188:765–774

    Google Scholar 

  • Klekamp J, Riedel A, Harper C, Kretschmann HJ (1991) Quantitative changes during postnatal maturation of the human visual cortex. J Neurol Sci 103:136–143

    Google Scholar 

  • Koh THHG, Eyre JA (1988) Maturation of corticospinal tracts assessed by electromagnetic stimulation of the motor cortex. Arch Dis Child 63:1347–1362

    Google Scholar 

  • Kononova EP (1940) Postnatal development of the frontal lobe (in Russian) In: Sarkisov SA, Filimonov IN (eds) Reports of the Brain Research Institute, vol 5. Medgiz, Moscow, pp 73–124

    Google Scholar 

  • Kordower JH, Mufson EJ (1992) Nerve growth factor receptor-immunoreactive neurons within the developing human cortex. J Comp Neurol 323:25–41

    Google Scholar 

  • Kostovic I, Skavic J, Strinovic D (1988) Acetylcholinesterase in the human frontal associative cortex during the period of cognitive development: early shifts and late innervation of pyramidal neurons. Neurosci Lett 90:107–112

    Google Scholar 

  • Kretschmann HJ, Schleicher A, Grottschreiber JF, Kullmann W (1979) The Yakovlev collection — a pilot study of its suitability for the morphometric documentation of the human brain. J Neurol Sci 43:111–126

    Google Scholar 

  • Kretschmann HJ, Kammradt G, Cowart EC, Hopf A, Krauthausen I, Lange HW, Sauer B (1982) The Yakovlev collection. A unique resource for brain research and the basis for a multi-national data bank. J Hirnforsch 23:647–656

    Google Scholar 

  • Lee H, Choi BH (1992) Density and distribution of excitatory amino acid receptors in the developing fetal brain: a quantitative autoradiographic study. Exp Neurol 118:284–290

    Google Scholar 

  • Marin-Padilla M (1970) Prenatal and early postnatal ontogenesis of the human motor cortex: a Golgi-study. I. The sequential development of the cortical layers. Brain Res 23:167–183

    Google Scholar 

  • Marin-Padilla M (1992) Ontogenesis of the pyramidal cell of the mammalian neocortex and developmental cytoarchitectonics: a unifying theory. J Comp Neurol 321:223–240

    Google Scholar 

  • Marin-Padilla M, Marin-Padilla TM (1982) Origin, prenatal development and structural organization of layer I of the human cerebral (motor) cortex. Anat Embryol 164:161–206

    Google Scholar 

  • Matthews BC (1991) The human stretch reflex and the motor cortex. Trends Neurosci 114:615–627

    Google Scholar 

  • Meyer G (1987) Forms and spatial arrangement of neurons in the primary motor cortex of man. J Comp Neurol 262:402–428

    Google Scholar 

  • Molliver ME, Kostovic I, Loos H van der (1973) The development of synapses in cerebral cortex of human fetus. Brain Res 50:403–407

    Google Scholar 

  • Mrzljak L, Uylings HBM, Kostovic I, Eden CG van (1992) Prenatal development of neurons in the human prefrontal cortex. II. A quantitative Golgi study. J Comp Neurol 316:485–496

    Google Scholar 

  • Müller K, Hömberg V (1992) Development of speed of receptive movements in children is determined by structural changes in corticospinal efferents. Neurosci Lett 144:57–60

    Google Scholar 

  • Müller K, Hömberg V, Lenard HG (1991) Magnetic stimulation of motor cortex and nerve roots in children. Maturation of cortico-motoneuronal projections. Electroencephalogr Clin Neurophysiol 82:63–70

    Google Scholar 

  • Petit TL, LeBoutillier JC, Alfano DP, Becker LE (1984) Synaptic development in the human foetus: a morphometric analysis of normal and Down's syndrome neocortex. Exp Neurol 83:13–23

    Google Scholar 

  • Piggott MA, Perry EK, Perry RH, Court JA (1992) [3H]MK-801 binding sites to the NMDA receptor complex, and its modulation in human frontal cortex during development and aging. Brain Res 588:277–286

    Google Scholar 

  • Piggott MA, Perry EK, Court JA, Perry RH (1994) Modulation of [3H]MK-801 binding sites by polyamines in human development and aging. Neurosci Res Commun 15:49–58

    Google Scholar 

  • Poliakov GI (1948) Ontogenesis of the human isocortex (in Russian) In: Sarkisov SA, Filimonov IN (eds) Reports of the Brain Research Institute, vol 6. Medgiz, Moscow Leningrad, pp 151–173

    Google Scholar 

  • Poliakov GI (1961) Some results of research into the development of the neuronal structure of cortical ends of the analyzers in man. J Comp Neurol 117:197–212

    Google Scholar 

  • Poliakov GI (1973) Principles of systematization of neurons in human neocortex (in Russian). Medizina, Moscow

    Google Scholar 

  • Povlishock JT (1976) The fine structure of the axons and growth cones of the human fetal cerebral cortex. Brain Res 114:379–389

    Google Scholar 

  • Rabinovicz T (1967) Quantitative appraisal of the cerebral cortex of the premature infant of 8 months. In: Minkovsky AM (ed) Regional development of the brain in early life. Blackwell, Oxford, pp 92–118

    Google Scholar 

  • Rakic P (1988) Specification of cerebral cortex areas. Science 241:170–176

    Google Scholar 

  • Rakic P, Goldman-Rakic PS (1980) Development and modifiability of cerebral cortex. Neurosci Res Program, Bull 20:433–607

    Google Scholar 

  • Rapoport SI (1990) Integrated phylogeny of the primate brain, with special reference to humans and their diseases. Brain Res Rev 15:267–294

    Google Scholar 

  • Ravikumar BV, Sastry PS (1985) Muscarinic cholinergic receptors in human foetal brain: characterization and ontogeny of [3H]Quinuclidinyl benzilate binding sites in frontal cortex. J Neurochem 44:240–246

    Google Scholar 

  • Reznikov KY, Fülöp Z, Hajos F (1984) Mosaicism of the ventricular layer as the developmental basis of neocortical columnar organization. Anat Embryol 170:99–105

    Google Scholar 

  • Sanides F (1964) The cyto-myeloarchitecture of the human frontal lobe, and its relation to phylogenetic differentiation of the cerebral cortex. J Hirnforsch 6:269–282

    Google Scholar 

  • Sarkisov SA, Filimonov IN, Preobrashenskaya NS (1949) Cytoarchitecture of the human cortex cerebri (in Russian). Medgiz, Moscow

    Google Scholar 

  • Sauer B (1983a) Semi-automatic analysis of microscopic images of the human cerebral cortex using the grey level index. J Microsc 129:75–87

    Google Scholar 

  • Sauer B (1983b) Lamina boundaries of the human striate area compared with automatically-obtained grey level index profiles. J Hirnforsch 24:79–87

    Google Scholar 

  • Sauer B (1983c) Quantitative analysis of the laminae of the striate area in man. An application of automatic image analysis. J Hirnforsch 24:87–97

    Google Scholar 

  • Schefer VF (1971) The volumes of neuronal cell bodies, nuclei and nucleoli during aging in normal and pathologically altered brain (in Russian). Arch Anat Histol Embryol 2:42–48

    Google Scholar 

  • Schleicher A, Zilles K, Kretschmann HJ (1978) Automatische Registrierung und Auswertung eines Grauwertindex in histologischen Schnitten. Verh Anat Ges 72:413–415

    Google Scholar 

  • Schleicher A, Zilles K, Wree A (1986) A quantitative approach to cytoarchitectonics: software and hardware aspects of a system for the evaluation and analysis of structural inhomogeneities in nervous tissue. J Neurosci Methods 18:211–235

    Google Scholar 

  • Schultz U, Hunziker O, Frey H (1978) The stereology of neurons in the cerebral cortex of aging individuals. In: Chermant JL (ed) Quantitative analysis of microstructures in material science, biology and medicine. Riederer, Stuttgart, pp 260–270

    Google Scholar 

  • Schwartz ML, Goldman-Rakic PS (1984) Callosal and intrahemispheric connectivity of the prefrontal association cortex in rhesus monkey: relation between intraparietal and principal sulcal cortex. J Comp Neurol 226:403–420

    Google Scholar 

  • Serra J (1988) Image analysis and mathematical morphology, vol 2. Theoretical advances. Academic Press, New York London

    Google Scholar 

  • Skullerud K (1985) Variations in the size of the human brain. Acta Neurol Scand 71:1–94

    Google Scholar 

  • Sloper JJ, Powell JPS (1979) An experimental electron microscopic study of afferent connections to the primate motor and somatic sensory cortices. Philos Trans R Soc Lond Biol 285:199–226

    Google Scholar 

  • Strick PL, Sterling P (1974) Synaptic termination of afferents from the ventro-lateral nucleus of the thalamus in the cat motor cortex. A light and electron microscopic study. J Comp Neurol 153:77–106

    Google Scholar 

  • Takashima S, Chan F, Becker LE, Armstrong DL (1980) Morphology of the developing visual cortex of the human infant. A quantitative and qualitative Golgi study. J Neuropathol Exp Neurol 39:487–501

    Google Scholar 

  • Terkelsen OBF, Janas MS, Bock E, Mollgard K (1992) NCAM as a differentiation marker of postmigratory immature neurons in the developing human nervous system. Int J Dev Neurosci 10:505–516

    Google Scholar 

  • Terry RD, De Teresa R, Hansen LA (1987) Neocortical cell counts in normal human adult aging. Ann Neurol 21:530–539

    Google Scholar 

  • Timiras PS (1972) Developmental physiology and aging. Macmillan, London

    Google Scholar 

  • Toyoshima K, Sakai H (1982) Exact cortical extent of the origin of the corticospinal tract (CST) and quantitative contribution to the CST in different cytoarchitectonic areas. A study with horseradish peroxidase in the monkey. J Hirnforsch 23:257–269

    Google Scholar 

  • Tukey JW (1977) Exploratory data analysis. Addison-Wesley, Reading, Mass

    Google Scholar 

  • Valk J, Knaap MS van der (1989) Magnetic resonance of myelin, myelination, and myelin disorders. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Vierordt H (1893) Anatomische, physiologische und physikalische Daten und Tabellen zum Gebrauch für Mediziner. Fischer-Verlag, Jena

    Google Scholar 

  • Viktorov I (1969) Nervous tissue staining in buffered solution of cresyl-violet (in Russian) Moscow Brain Institute, Moscow

    Google Scholar 

  • Vogt C, Vogt O (1919) Allgemeinere Ergebnisse unserer Hirnforschung. J Psychol Neurol 25:292–398

    Google Scholar 

  • Wolff JR, Missler M (1992) Synaptic reorganization in developing and adult nervous systems. Ann Anat 174:393–403

    Google Scholar 

  • Yakovlev PI (1962) Morphological criteria of growth and maturation of the nervous system in man. Mental retardation. Research Publications, pp 3–46

  • Yakovlev PI, Lecours AR (1967) The myelogenetic cycles of regional maturation of the brain. In: Minkovsky A (ed) Regional development of the brain in early life. Science Publications, Oxford, pp 3–70

    Google Scholar 

  • Yamaura H, Ito M, Kubota K, Matsuzava T (1980) Brain atrophy during aging: a quantitative study with computed tomography. J Gerontol 35:492–498

    Google Scholar 

  • Zilles K, Schleicher A (1980) Quantitative Analyse der laminären Struktur menschlicher Cortexareale. Verh Anat Ges 74:725–726

    Google Scholar 

  • Zilles K, Werners R, Büsching U, Schleicher A (1986) Ontogenesis of the laminar structures in area 17 and 18 of the human visual cortex. Anat Embryol 174:129–144

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. C. & O. Vogt Brain Research Institute, Heinrich Heine University Düsseldorf, P.O. Box 10 10 07, D-40001, Düsseldorf, Germany

    Katrin Amunts, Axel Schleicher & Karl Zilles

  2. Department of Psychiatry, Mount Sinai Hospital, One Gustave Levy Place, 10029-6574, New York, NY, USA

    Vadim Istomin

Authors
  1. Katrin Amunts
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vadim Istomin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Axel Schleicher
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Karl Zilles
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Amunts, K., Istomin, V., Schleicher, A. et al. Postnatal development of the human primary motor cortex: a quantitative cytoarchitectonic analysis. Anat Embryol 192, 557–571 (1995). https://doi.org/10.1007/BF00187186

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00187186

Key words

Search

Navigation