Skip to main content
Log in

Cytology and time of origin of interstitial neurons in the white matter in infant and adult human and monkey telencephalon

  • Published:
Journal of Neurocytology

Summary

The fine structure, synaptic relationships, distribution and time of origin of interstitial neurons situated within the white matter subjacent to the visual, somatosensory and motor cortices were studied in the human and monkey telencephalon. The analysis was carried out on Nissl-stained serial sections, rapid Golgi impregnations, by acetylcholinesterase (AChE) histochemistry, electron microscopy and [3H]thymidine ([3H]TdR) autoradiography. Interstitial neurons have a similar distribution, morphology and histochemistry in both human and monkey telencephalon. Their highest density and the most extensive distribution is found in the neonatal period in both species. The number of interstitial neurons decreases during infancy, but numerous cells remain in the adult.

Two types of interstitial neuron can be recognized in Golgi preparations:polymorphic cells, usually situated close to the cortex andfusiform cells, located predominantly in the depths of the white matter. The polymorphic cell type is prevalent during neonatal and infant stages, while fusiform cells are relatively more numerous in the adult. Interstitial cells have ultrastructural features and organelles typical of neurons of the central nervous system with well-defined axosomatic and axodendritic synapses of both symmetrical and asymmetrical types. About 20% of the interstitial cells show strong specific AChE activity.

Autoradiographic analysis of postnatal monkeys exposed to [3H]TdR at various embryonic (E) and early postnatal days indicates that interstitial neurons which lie beneath the visual and somatosensory-motor cortices are generated between E38 and E48. Contrary to the prevailing notion that interstitial neurons are the latest generated cells arrested during migration across the maturing white matter, they prove to be produced at the end of the first third of the 165-day gestation in the rhesus monkey concomitantly with the generation of neurons destined for the deep neocortical layers. These findings raise the possibility that interstitial cells represent a vestige of the transient embryonic subplate layer.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Austin, L. &Phillis, J. W. (1965) The distribution of cerebellar cholinesterase in several species.Journal of Neurochemistry 12, 709–17.

    PubMed  Google Scholar 

  • Billings-Gagliardi, S., Chan-Palay, V. &Palay, S. L. (1974) A review of lamination in area 17 of the visual cortex ofMacaca mulatta.Journal of Neurocytology 3, 619–29.

    PubMed  Google Scholar 

  • Blinkov, S. M. &Glezer, I. I. (1968)The Human Brain in Figures and Tables. A Quantitative Handbook. New York: Plenum.

    Google Scholar 

  • Broderson, S. H., Westrum, L. E. &Sutton, A. E. (1974) Studies of the direct coloring thicholine method for localizing cholinesterase activity.Histochemistry 40, 13–23.

    PubMed  Google Scholar 

  • Cammermeyer, J. (1978) Is the solitary dark neuron a manifestation of postmortem trauma to the brain inadequately fixed by perfusion?Histochemistry 56, 97–115.

    PubMed  Google Scholar 

  • Caviness, V. S., Jr. &Rakic, P. (1978) Mechanisms of cortical development: a view from mutations in mice.Annual Review of Neuroscience 1, 297–326.

    PubMed  Google Scholar 

  • Caviness, V. S., Jr. &Williams, R. S. (1978) Cellular pathology of developing human cortex. InCongenital and Acquired Cognitive Disorders (edited byKatzman, R.), pp. 69–89. New York: Raven Press.

    Google Scholar 

  • Chan-Palay, V., Palay, S. L. &Billings-Gagliardi, S. M. (1974) Meynert cells in the primate visual cortex.Journal of Neurocytology 3, 631–58.

    PubMed  Google Scholar 

  • Clarke, P. H. G. &Cowan, W. M. (1975) Ectopic neurons and aberrant connections during neural development.Proceedings of the National Academy of Sciences (U.S.A.) 72, 4455–8.

    Google Scholar 

  • Das, G. D. (1970) An evaluation of the interstitial nerve cells in the cerebellum.Zeitschrift für Anatomie und Entwicklungsgeschichte 131, 283–90.

    Google Scholar 

  • Das, G. D. &Kreutzberg, G. W. (1968) Evaluation of interstitial nerve cells in the central nervous system: A correlative study using acetylcholinesterase and Golgi techniques.Ergebnisse der Anatomie und Entwicklungsgeschichte 41, 1–58.

    Google Scholar 

  • Duncan, D. (1953) On the incidence and location of nerve cells in the spinal white matter of two species of primates, man and cynomolgus monkey.Journal of Comparative Neurology 99, 103–15.

    PubMed  Google Scholar 

  • Economo, C. &Koskinas, G. N. (1925)Die Cytoarchitektonik der Hirnrinde des erwachsenen Menschen. Vienna: Julius Springer.

    Google Scholar 

  • Giordano, D. L. &Cunningham, T. J. (1978) Naturally occuring neuron death in the superior colliculus of the postnatal rat.Anatomical Record 190, 402 (abstract).

    Google Scholar 

  • Godina, G. (1951) Istogensi e differenziazione dei neuroni e degli elementi gliali della corteccia cérébrale.Zeitschrift für Zellforschung und mikroskopische Anatomie 36, 401–35.

    Google Scholar 

  • Goldman, P. S. &Galkin, T. W. (1978) Prenatal removal of frontal association cortex in the fetal rhesus monkey: Anatomical and functional consequences in postnatal life.Brain Research 152, 451–8.

    PubMed  Google Scholar 

  • Herrick, C. J. (1920)The Brain of the Tiger Salamander. Chicago: University of Chicago Press.

    Google Scholar 

  • Knyihar, E., Csillik, B. &Rakic, P. (1978) Transient synapses in the embryonic primate spinal cord.Science 202, 1206–9.

    PubMed  Google Scholar 

  • Kostović, I. &Molliver, M. E. (1974) A new interpretation of the laminar development of cerebral cortex: synaptogenesis in different layers of neopallium in the human fetus.Anatomical Record 178, 395 (abstract).

    Google Scholar 

  • Krnjevic, K. &Silver, A. (1965) A histochemical study of cholinergic fibers in the cerebral cortex.Journal of Anatomy 99, 711–59.

    PubMed  Google Scholar 

  • Krnjevic, K. &Silver, A. (1966) Acetylcholinesterase in the developing forebrain.Journal of Anatomy 100, 63–89.

    PubMed  Google Scholar 

  • Lund, J. S., Lund, R. D., Hendrickson, A. E., Bunt, A. H. &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.Journal of Comparative Neurology 164, 287–304.

    Google Scholar 

  • Marin-Padilla, M. (1978) Dual origin of the mammalian neocortex and evolution of the cortical plate.Anatomy and Embryology 152, 109–26.

    PubMed  Google Scholar 

  • Molliver, M. E. &Kristt, D. A. (1975) The fine structural demonstration of monoaminergic synapses in immature rat neocortex.Neuroscience Letters 1, 305–10.

    Google Scholar 

  • Molliver, M. E. &Van Der Loos, H. (1970) The ontogenesis of cortical circuitry: The spatial distribution of synapses in somesthetic cortex of newborn dog.Ergebnisse der Anatomie und Entwicklungsgeschichte 42, 1–53.

    Google Scholar 

  • Neuburger, K. (1922) Zur Histopathologie der multiplen Sklerose im Kindesalter.Zeitschrift für Neurologie 76, 384–414.

    Google Scholar 

  • Peters, A., Palay, S. L. &Webster, H. deF. (1976)The Fine Structure of the Nervous System: The Neurons and Supporting Cells. Philadelphia: Saunders.

    Google Scholar 

  • Pilar, G. &Landmesser, L. (1976) Ultrastructural differences during embryonic cell death in normal and peripherially deprived ciliary ganglia.Journal of Cell Biology 68, 339–56.

    PubMed  Google Scholar 

  • Pinto-Lord, M. C. &Caviness, V. S., Jr. (1979) Determinants of cell shape and orientation: A comparative Golgi analysis of cell-axon interrelationships in developing neocortex of normal and reeler mouse.Journal of Comparative Neurology 187, 49–69.

    PubMed  Google Scholar 

  • Poljak, S. (1922) Über die sogenannten versprengten Ganglienzellen in der weissen Substanz des menschlichen Ruckenmarks.Arbeiten aus dem neurologischen Institute Wien 23, 1–20.

    Google Scholar 

  • Rakic, P. (1971) Neuron-glia relationship during granule cell migration in developing cerebellar cortex. A Golgi and electronmicroscopic study inMacacus rhesus.Journal of Comparative Neurology 141, 283–312.

    PubMed  Google Scholar 

  • Rakic, P. (1972) Mode of cell migration to the superficial layers of fetal monkey neocortex.Journal of Comparative Neurology 145, 61–84.

    PubMed  Google Scholar 

  • Rakic, P. (1973) Kinetics of proliferation and latency between final cell division and onset of differentiation of cerebellar stellate and basket neurons.Journal of Comparative Neurology 147, 523–46.

    PubMed  Google Scholar 

  • Rakic, P. (1974) Neurons in rhesus monkey visual cortex: systematic relation between time of origin and eventual disposition.Science 183, 425–7.

    PubMed  Google Scholar 

  • Rakic, P. (1975a) Cell migration and neuronal ectopias in the brain. InMorphogenesis and Malformation of the Face and Brain, Original Series, Vol. 9, (edited byBergsma, D.), pp. 95–129. New York: Liss.

    Google Scholar 

  • Rakic, P. (1975b) (editor) Local circuit neurons.Neuroscience Research Program Bulletin 13, 289–446.

    Google Scholar 

  • Rakic, P. (1975c) Timing of major ontogenetic events in the visual cortex of the rhesus monkey. InBrain Mechanisms in Mental Retardation (edited byBuchwald, N. A. andBrazier, M.), pp. 3–40. New York: Academic Press.

    Google Scholar 

  • Rakic, P. (1976a) Differences in the time of origin and in eventual distribution of neurons in areas 17 and 18 of visual cortex in rhesus monkey.Experimental Brain Research. Suppl.1, 244–8.

    Google Scholar 

  • Rakic, P. (1976b) Prenatal genesis of connections subserving ocular dominance in the rhesus monkey.Nature 261, 467–71.

    PubMed  Google Scholar 

  • Rakic, P. (1977a) Prenatal development of the visual system in the rhesus monkey.Philosophical Transactions of the Royal Society of London, Series B 278, 245–60.

    Google Scholar 

  • Rakic, P. (1977b) Genesis of the dorsal lateral geniculate nucleus in the rhesus monkey: site and time of origin, kinetics of proliferation, routes of migration and pattern of distribution of neurons.Journal of Comparative Neurology 176, 23–52.

    PubMed  Google Scholar 

  • Rakic, P. &Sidman, R. L. (1968) Subcommissural organ and adjacent ependyma: autoradiographic study of their origin in the mouse brain.American Journal of Anatomy 122, 317–36.

    PubMed  Google Scholar 

  • Ramon-Moliner, E. &Nauta, W. J. H. (1966) The isodendritic core of the brain stem.Journal of Comparative Neurology 126, 311–36.

    PubMed  Google Scholar 

  • Ramón Y Cajal, S. (1900)Studien uber der Hirnrinde des Menschen. L Heft: Die Sehrinde, Leipzig: Barth.

    Google Scholar 

  • Ramón Y Cajal, S. (1911)Histologie du Système Nerveux de l'Homme at des Vertébrés. Paris: Maloine. (Reprinted in 2 volumes by Consejo Superior de Investigaciones Cientificas, Madrid, 1955).

    Google Scholar 

  • Ranke, O. (1901) Beiträge zur Kenntnis der normalen und pathologischen Hirnrindenbildung.Beiträge zur Pathologische Anatomie und zur allgemeinen Pathologie 47, 51–125.

    Google Scholar 

  • Rice, F. L. &Van Der Loos, H. (1977) Development of the barrel field in the somatosensory cortex of the mouse.Journal of Comparative Neurology 171, 545–60.

    PubMed  Google Scholar 

  • Richardson, K. C., Jarett, L. &Finke, E. H. (1960) Embedding in epoxy resins for ultrathin sectioning in electronmicroscopy.Stain Technology 35, 313–23.

    PubMed  Google Scholar 

  • Rickmann, M., Chronwall, B. M. &Wolff, J. R. (1977) On the development of non-pyramidal neurons and axons outside the cortical plate: The early marginal zone as a palliai anlage.Anatomy and Embryology 151, 285–307.

    PubMed  Google Scholar 

  • Rio Hortega, P. (1956) Tercera aportacion al conocimiento morfologico e interpretacion functional de la oliogodendroglia.Archivos de Hisologia (Buenos Aires) 6, 132–83.

    Google Scholar 

  • Scheibel, M. E. &Scheibel, A. B. (1967) Anatomical basis of attention mechanisms in vertebrate brains. InThe Neurosciences: A Study Program (edited byQuarton, G., Melnechuk, T. andSchmitt, F. O.), pp. 577–602. New York: The Rockefeller University Press.

    Google Scholar 

  • Sherrington, C. S. (1891) On outlying nerve cells in the mammalian spinal cord.Philosophical Transactions of the Royal Society of London, Series B 181, 33–48.

    Google Scholar 

  • Siwe, S. A. (1927) Das Gehirn: Die mikroskopische Entwicklung des Grosshirns nach der Geburt. InHandbuch der Anatomie des Kindes (editedPeter, K., Wetzel, G. andHeindrich, F.), pp. 609–632. Munich: Bargman.

    Google Scholar 

  • Soteeo, C. &Trieler, A. (1979) Fate of presynaptic afferents to Purkinje cells in the adultnervous mutant mouse: A model to study presynaptic stabilization.Brain Research 175, 11–36.

    PubMed  Google Scholar 

  • Van Der Eoos, H. (1965) The ‘improperly’ oriented pyramidal cell in the cerebral cortex and its possible bearing on problems of neuronal growth and cell orientation.Bulletin of the Johns Hopkins Hospital 117, 228–50.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kostovic, I., Rakic, P. 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 (1980). https://doi.org/10.1007/BF01205159

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01205159

Keywords

Navigation