Summary
Neurons in the human cerebral cortical white matter below motor, visual, auditory and prefrontal orbital areas have been studied with the Golgi method, immunohistochemistry and diaphorase histochemistry. The majority of white matter neurons are pyramidal cells displaying the typical polarized, spiny dendritic system. The morphological variety includes stellate forms as well as bipolar pyramidal cells, and the expression of a certain morphological phenotype seems to depend on the position of the neuron. Spineless nonpyramidal neurons with multipolar to bitufted dendritic fields constitute less than 10% of the nuerons stained for microtubule associated protein (MAP-2). Only 3% of the MAP-2 immunoreactive neurons display nicotine adenine dinucleotide-diaphorase activity. The white matter pyramidal neurons are arranged in radial rows continuous with the columns of layer VI neurons. Neuron density is highest below layer VI, and decreases with increasing distance from the gray matter. White matter neurons are especially abundant below the primary motor cortex, and are least frequent below the visual cortex area 17. In contrast to other mammalian species, the white matter neurons in man are not only present during development, but persist throughout life.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Antonini A, Shatz CJ (1990) Relation between putative transmitter phenotype and connectivity of subplate neurons during cerebral cortical development. Eur J Neurosci 2:744–761
Bayer SA, Altman J (1990) Development of layer I and the subplate in the rat neocortex. Exp Neurol 107:48–62
Boulder Committee (1970) Embryonic vertebrate central nervous system: revised terminology. Anat Rec 166:267–272
Bouras C, Magistretti PJ, Morrison JH (1986) An immunohistochemical study of six biologically active peptides in the human brain. Human Neurobiol 5:213–226
Braitenberg V, Guglielmotti U, Sada E (1967) Correlation of crystal growth with the staining of axons by the Golgi procedure. Stain Technol 42:277–283
Brodmann K (1909) Vergleichende Lokalisationslehre der Großhirnrinde. Barth, Leipzig
Campbell MJ, Morrison JA (1989) A monoclonal antibody to neurofilament protein (SMI-32) labels a subpopulation of pyramidal neurons in the human and monkey neocortex. J Comp Neurol 282:191–205
Cavanagh M, Parnavelas JG (1990) Development of Neuropeptide Y (NPY) immunoreactive neurons in rat occipital cortex: a combined immunohistochemical and autoradiographic study. J Comp Neurol 284:637–645
Chan-Palay V, Allen YS, Lang W, haesler U, Polak JM (1985) Cytology and distribution in normal human cerebral cortex of neurons immunoreactive with antisera against neuropeptide Y. J Comp Neurol 238:382–389
Chun JJM, Shatz CJ (1989a) Interstitial cells of the adult neocortical white matter are the remnant of the early generated subplate neuron population J Comp Neurol 282:555–569
Chun JJM, Shatz CJ (1989b) The earliest generated neurons of the cat neocortex: characterization by MAP-2 and transmiter immunohistochemistry during fetal life. J Neurosci 9:1648–1667
Chun JJM, Nakamura MJ, Shatz CJ (1987) Transient cells of the developing mammalian telencephalon are petide immunoreactive neurons. Nature 325:617–620
Das GD, Kreutzberg GW (1968) Evaluation of interstitial nerve cells in the central nervous system. A correlative study using acetylcholine esterase and Golgi techniques. Ergebn Anat Entwickl Gesch 41:1–59
Dotti CG, Sullivan CA, Banker GA (1988) The establishment of polarity by hippocampal neurons in culture. J Neurosci 8:1454–1468
Economo C von, Koskinas GN (1925) Cytoarchitektonik der Hirnrinde des erwachsenen Menschen. Springer, Berlin
Giguere M, Goldman-Rakic P (1988) Mediodorsal nucleus: Areal, laminar, and tangential distribution of afferents and efferents in the frontal lobe of the rhesus monkey. J Comp Neurol 277:195–213
Hendry SHC, Jones EG, Emson PC (1984) Morphology, distribution and synaptic relations of somatostatin- and neuropeptide Y-immunoreactive neurons in rat and monkey neocortex. J Neurosci 4:2497–2517
Jackson CA, Peduzzi JD, Hickey TL (1989) Visual cortex development in the ferret. I. Genesis and migration of visual cortical neurons. J Neurosci 9:1242–1253
Kostovic I, Molliver ME (1974) A new interpretation of the laminar development of the cerebral cortex: synaptogenesis in different layers of neopallium in the human fetus. Anat Rec 178:398
Kostovic I, Rakic P (1980) Cytology and time of origin of interstitial neurons in the white matter in infant and adult human and monkey telencephalon. J Neurocytol 9:219–242
Kostovic I, Rakic P (1990) Developmental history of the transient subplate zone in the visual and somatosensory cortex of macaque monkey and human brain. J Comp Neurol 297:441–470
Lund JS, Lund RD, Hendrickson AE, Bunt AH, Fuchs F (1975) The origin of efferent pathways from the primary visual cortex, area 17, of the macaque monkey as shown by retrograde transport of horseradish peroxidase. J Comp Neurol 164:287–304
Luskin MB, Shatz CJ (1985) Studies of the earliest generated cells of the cat visual cortex: Cogeneration of subplate and marginal zone. J Neurosci 5:1062–1075
Marin-Padilla M (1988) Early ontogenesis of the human cerebral cortex. In: Peters A, Jones EG (eds) Cerebral cortex, vol 7. Plenum, New York, 1–34
McConnell SK, Gosh A, Shatz CJ (1990) Subplate neurons pioneer the first acon pathway from the cerebral cortex. Science 245:978–982
Meyer G (1987) Forms and spatial arrangement of neurons in primary motor cortex of man. J Comp Neurol 228:226–244
Meyer G, Wahle P (1990) Morphology, distribution and quantitative development of neurons in the white matter of the human cortex. Soc Neurosci Abstr 16:332
Meyer G, Gonzalez-Hernandez T, Ferres-Torres R (1989) The spiny stellate neurons in layer IV of the human auditory cortex. A Golgi study. Nerusicence 33:489–498
Mizukawa K, Vincent SP, McGeer PL, McGeer EG (1988) Reduced nicotine adenine dinucleotide phosphate (NADPH)-diaphorase-positive neurons in cat cerebral white matter. Brain Res 461:274–281
Mollgard K, Dziegielewska MK, Saunders NR, Zakut H, Soreq H (1988) Synthesis and localization of plasma proteins in the developing human brain. Dev Biol 128:207–221
Naegele JR, Barnstable CJ, Wahle P (1991) Expression of a novel 56 kD polypeptide by neurons in the subplate zone of developing cerebral cortex. Proc Natl Acad Sci USA 88:330–334
Peduzzi JD (1988) Genesis of GABA-immunoreactive neurons in the ferret visual cortex. J Neurosci 8:920–931
Pinto-Lord MC, Caviness VS Jr (1979) Determinants of cell shape and orientations: A comparative Golgi analysis of cell-axon interrelationships in developing neocortex of normal and reeler mice. J Comp Neurol 187:49–70
Ramon y Cajal S (1991) Histologie du systeme nerveux de l'homme et des vertebres. Maloine, Paris
Sandell JH (1986) NADPH diaphorase histochemistry in the macaque striate cortex. J Comp Neurol 251:388–397
Shatz CJ, Luskin MB (1986) The relationship between geniculocortical afferents and their cortical target cells during development of the cat's primary visual cortex. J Neurosci 6:3655–3668
Somogyi P, Hodgson A, Smith AD, Nunzi MG, Gorio A, Wu JY (1984) Different populations of GABAergic neurons in the visual cortex and hippocampus of cat contain somatostatin-and cholecystokinin-immunoreactive material. J Neurosci 4:2590–2603
Van Eden CG, Mrzljak, L, Voorn P, Uylings HBM (1989) Prenatal development of GABAergic neurons in the neocortex of the rat. J Comp Neurol 289:213–227
Valverde F, Facal-Valverde MV (1988) Postnatal development of interstitial (subplate) cells in the white matter of the temporal cortex of kittens: a correlated Golgi and electron microscopic study. J Comp Neurol 268:168–192
Valverde F, Facal-Valverde MV, Santacana M, Heredia M (1989) Development and differentiation of early generated cells of sublayer VIb in somatosensory cortex of the rat: a correlated Golgi and autoradiographic study. J Comp Neurol 290:118–140
Wahle P, Meyer G (1987) Morphology and quantitative changes of transient NPY-ir neuronal populations during early postnatal development of the cat visual cortex. J Comp Neurol 261:165–192
Wahle P, Meyer G (1989) Early postnatal development of vasoactive intestinal polypeptide and peptide histidine isoleucine immunoreactive structures in cat visual cortex. J Comp Neurol 282:215–248
Wahle P, Meyer G, Wu JY, Albus K (1987) Morphology and axon terminal pattern of glutamate decarboxylase-immunoreactive cell types in the white matter of cat occipital cortex during early postnatal development. Dev Brain Res 36:53–61
Wahle P, Lübke J, Naegele JR (1990) Subplate-1: A molecular marker for excitatory neurons in subplate zone of developing cat cortex? Soc Neurosci Abstr 16:987
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Meyer, G., Wahle, P., Castaneyra-Perdomo, A. et al. Morphology of neurons in the white matter of the adult human neocortex. Exp Brain Res 88, 204–212 (1992). https://doi.org/10.1007/BF02259143
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF02259143