Skip to main content
SpringerLink
Log in

The organization of pyramidal and non-pyramidal cell dendrites in relation to thalamic afferent terminations in the monkey somatic sensory cortex

  • Published:
Journal of Neurocytology

Summary

Golgi-stained neurons of the monkey first somatic sensory cortex (areas 3b and 1–2) and the adjacent area 5 were examined in thionin-counterstained preparations and their dendritic fields related to the position of the major thalamic afferent plexuses (in layers IV and IIIB in area 3b, in layer IIIB only in the other areas and in a subsidiary plexus at the border of layers V and VI). Many types of pyramidal cells of layers IIIB, V and VI have dendrites that consistently branch within the laminae of the thalamic axon terminations:

  1. 1.

    The largest, most deeply situated layer IIIB pyramidal cells have basal dendrites which descend into layer IV of area 3b but become progressively more horizontally oriented in layer IIIB of areas 1–2 and 5.

  2. 2.

    Some layer V pyramidal cells, particularly medium-to-large cells of layer VA, have apical dendrites which give off many branches and spines in both layer IV and layer IIIB of area 3b but only in layer IIIB of areas 1–2 and 5.

  3. 3.

    Some of the modified pyramidal cells of layer VI give rise to apical dendrites that branch profusely in layer IV of area 3b and in layer IIIB of areas 1–2.

Many of the non-pyramidal cell types have somata and dendrites among the thalamic afferent plexus. The small spiny (type 7) cells have their somata confined to layer IV of all areas but have an ascending dendritic tuft which is relatively short in area 3b, often barely reaching the upper border of layer IV, but is considerably longer in areas 1–2 and 5, reaching the layer IIIB/IIIA border. Several classes of small aspiny non-pyramidal cells have their somata in layers IIIB and IV of areas 3b and 1–2 but only in layer IIIB of area 5. Large, multipolar neurons (basket or type 1 cells) with somata in layers IIIB to VI of each area have dendrites that branch extensively either in layers IIIB and IV or at the layer V/VI border.

It is concluded that virtually all pyramidal cells in layers IIIB, V and VI have substantial dendritic ramifications among the terminations of thalamic afferents. The dendrites of many pyramidal and non-pyramidal cells change their dendritic branching patterns and in some cases the positions of their somata, in a manner that conforms to the change in position of the thalamic afferent plexus from area to area. These observations suggest a close relationship between thalamic terminations and cell form, and may imply that all cells with dendrites among the thalamic terminations in monkey somatic sensory and parietal cortex receive significant numbers of thalamic synapses.

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

  • Berman, N. &Cynader, M. (1972) Comparison of receptive-field organization of the superior colliculus in Siamese and normal cats.Journal of Physiology 224, 363–89.

    Google Scholar 

  • Bullier, J. &Henry, G. H. (1979) Laminar distribution of first order neurons and afferent terminals in the cat striate cortex.Journal of Neurophysiology 42, 1271–81.

    Google Scholar 

  • Cajal, S., Ramon, Y. (1911)Histologie du Système de l'Homme et des Vertébrés Vol. 2 (Translated byAzoulay, L.) Paris: Maloine.

    Google Scholar 

  • Catsman-Berrevoets, C. E. &Kuypers, H. G. J. M. (1978) Differential laminar distribution of corticothalamic neurons projecting to the VL and the center median. An HRP study in the cynomolgus monkey.Brain Research 154, 359–65.

    Google Scholar 

  • Choudhury, B. P., Whitteridge, D. &Wilson, M. E. (1965) The function of the callosal connections of the visual cortex.Quarterly Journal of Experimental Physiology 50, 214–9.

    Google Scholar 

  • Colonnier, M. (1964) The tangential organization of the visual cortex.Journal of Anatomy 98, 327–44.

    Google Scholar 

  • Davis, T. L. &Sterling, P. (1979) Microcircuitry of cat visual cortex: classification of neurons in layer IV of area 17, and identification of the patterns of lateral geniculate input.Journal of Comparative Neurology 188, 599–628.

    Google Scholar 

  • Fairen, A., Peters, A. &Saldanha, J. (1977) A new procedure for examining Golgi impregnated neurons by light and electron microscopy.Journal of Neurocytology 6, 311–37.

    Google Scholar 

  • Fromm, C. &Evarts, E. V. (1981) Relation of size and activity of motor cortex pyramidal tract neurons during skilled movements in the monkey.Journal of Neuroscience 1, 453–60.

    Google Scholar 

  • Geisert, E. E., Langsetmo, A. &Spear, P. D. (1981) Influence of the cortico-geniculate pathway on response properties of cat lateral geniculate neurons.Brain Research 208, 409–15.

    Google Scholar 

  • Gilbert, C. D. (1977) Laminar differences in receptive field properties of cells in cat primary visual cortex.Journal of Physiology 268, 391–421.

    Google Scholar 

  • Globus, A. &Scheibel, A. B. (1967a) Synaptic loci on visual cortical neurons of the rabbit: the specific afferent radiation.Experimental Neurology 18, 116–31.

    Google Scholar 

  • Globus, A. &Scheibel, A. B. (1967b) The effect of visual deprivation on cortical neurons: a Golgi study.Experimental Neurology 19, 331–45.

    Google Scholar 

  • Harvey, A. R. (1978) Characteristics of corticothalamic neurons in area 17 of the cat.Neuroscience Letters 7, 177–81.

    Google Scholar 

  • Harvey, A. R. (1980) A physiological analysis of subcortical and commissural projections of areas 17 and 18 of the cat.Journal of Physiology 302, 507–34.

    Google Scholar 

  • Hendry, S. H. C. &Jones, E. G. (1980) Electron microscopic demonstration of thalamic axon terminations on identified commissural neurons in monkey sensory cortex.Brain Research 196, 253–7.

    Google Scholar 

  • Hendry, S. H. C. &Jones, E. G. (1981) Sizes and distributions of intrinsic neurons incorporating tritiated GABA in monkey sensory-motor cortex.Journal of Neuroscience 1, 390–408.

    Google Scholar 

  • Hendry, S. H. C. &Jones, E. G. (1983) Thalamic inputs to identified commissural neurons in the monkey somatic sensory cortex.Journal of Neurocytology 12, 299–316.

    Google Scholar 

  • Hersch, S. M. &White, E. L. (1981) Thalamocortical synapses involving identified neurons in mouse primary somatosensory cortex: a terminal degeneration and Golgi/EM study.Journal of Comparative Neurology 195, 253–63.

    Google Scholar 

  • Hornung, J. P. &Garey, L. J. (1981) The thalamic projection to cat visual cortex: ultrastructure of neurons identified by Golgi impregnation or retrograde horseradish peroxidase transport.Neuroscience 6, 1053–68.

    Google Scholar 

  • Hubel, D. H. &Wiesel, T. N. (1967) Cortical and callosal connections concerned with the vertical meridian of visual fields in the cat.Journal of Neurophysiology 30, 1561–73.

    Google Scholar 

  • Innocenti, G. M., Manzoni, T. &Spidalieri, G. (1974) Patterns of the somesthetic messages transferred through the corpus callosum.Experimental Brain Research 19, 447–66.

    Google Scholar 

  • Jones, E. G. (1975a) Lamination and differential distribution of thalamic afferents within the sensory-motor cortex of the squirrel monkey.Journal of Comparative Neurology 160, 167–204.

    Google Scholar 

  • Jones, E. G. (1975b) Varieties and distribution of non-pyramidal cells in the somatic sensory cortex of the squirrel monkey.Journal of Comparative Neurology 160, 205–68.

    Google Scholar 

  • Jones, E. G. &Burton, H. (1976) Areal differences in the laminar distribution of thalamic afferents in cortical fields of insular, parietal and temporal regions of primates.Journal of Comparative Neurology 168, 197–248.

    Google Scholar 

  • Jones, E. G., Coueter, J. D., Burton, H. &Porter, R. (1977) Cells of origin and terminal distribution of corticostriatal fibers arising in the sensory-motor cortex of monkeys.Journal of Comparative Neurology 173, 53–80.

    Google Scholar 

  • Jones, E. G. &Poweel, T. P. S. (1970) An electron microscopic study of the laminar pattern and mode of termination of afferent fibre pathways in the somatic sensory cortex of the cat.Philosophical Transactions of the Royal Society of London, Series B 257, 45–62.

    Google Scholar 

  • Jones, E. G. &Wise, S. P. (1977) Size, laminar and columnar distribution of efferent cells in the sensory-motor of monkeys.Journal of Comparative Neurology 175, 391–438.

    Google Scholar 

  • Eorente De No, R. (1949) Cerebral cortex: architecture, intracortical connections, motor projections. InPhysiology of the Nervous System 3rd edn, (edited byFulton, J. F.), pp. 288–313. London: Oxford University Press.

    Google Scholar 

  • Lund, J. S. (1973) Organization of neurons in the visual cortex, area 17, of the monkey (Macaca mulatta).Journal of Comparative Neurology 147, 455–96.

    Google Scholar 

  • Lund, J. S. &Boothe, R. G. (1975) Interlaminar connections and pyramidal neuron organisation in the visual cortex, area 17, of the macaque monkey.Journal of Comparative Neurology 159, 305–34.

    Google Scholar 

  • Marin-Padilla, M. (1969) Origin of the pericellular baskets of the pyramidal cells of the human motor cortex: a Golgi study.Brain Research 14, 633–46.

    Google Scholar 

  • Molotchnikoff, S., Richard, D. &Lachapelle, P. (1980) Influence of the visual cortex upon receptive field organization of lateral geniculate cells in rabbits.Brain Research 193, 383–99.

    Google Scholar 

  • Murray, E. A. &Coulter, J. D. (1981) Organization of corticospinal neurons in the monkey.Journal of Comparative Neurology 195, 339–65.

    Google Scholar 

  • O'leary, J. L. (1941) Structure of area striata of the cat.Journal of Comparative Neurology 75, 131–64.

    Google Scholar 

  • O'leary, J. L. &Bishop, G. H. (1938) The optically excitable cortex of the rabbit.Journal of Comparative Neurology 68, 423–77.

    Google Scholar 

  • Palmer, L. A. &Rosenquist, A. C. (1974) Visual receptive fields of single striate cortical units projecting to the superior colliculus in the cat.Brain Research 67, 27–42.

    Google Scholar 

  • Peters, A. &Feldman, M. L. (1976) The projection of the lateral geniculate nucleus to area 17 of the rat cerebral cortex. I. General description.Journal of Neurocytology 5, 63–84.

    Google Scholar 

  • Peters, A., Feldman, M. L. &Saldanha, J. (1976) The projection of the lateral geniculate nucleus to area 17 of the rat cerebral cortex. II. Terminations upon neuronal perikarya and dendritic shafts.Journal of Neurocytology 5, 85–107.

    Google Scholar 

  • Peters, A., Proskauer, C. C., Feldman, M. L. &Kimerer, L. (1979) The projection of the lateral geniculate nucleus to area 17 of the rat cerebral cortex. V. Degenerating axon terminals synapsing with Golgi impregnated neurons.Journal of Neurocytology 8, 331–57.

    Google Scholar 

  • Ryugo, R., Ryugo, D. K. &Killackey, H. P. (1975) Differential effect of enucleation on two populations of layer V pyramidal cells.Brain Research 88, 554–9.

    Google Scholar 

  • Shanks, M. F. &Powell, T. P. S. (1981) An electron microscopic study of the termination of thalamocortical fibres in areas 3b, 1 and 2 of the somatic sensory cortex in the monkey.Brain Research 218, 35–47.

    Google Scholar 

  • Sloper, J. J. &Powell, T. P. S. (1979) An experimental electron microscopic study of afferent connections to the primate motor and somatic sensory cortices.Philosophical Transactions of the Royal Society of London, Series B 285, 199–226.

    Google Scholar 

  • Somogyi, P. (1978) The study of Golgi stained cells and of experimental degeneration under the electron microscope: a direct method for the identification in the visual cortex of three successive links in a neuron chain.Neuroscience 3, 167–80.

    Google Scholar 

  • Steriade, M., Deschênes, M. &Oakson, G. (1974) Inhibitory processes and interneuronal apparatus in motor cortex during sleep and waking. I. Background firing and responsiveness of pyramidal tract neurons and interneurons.Journal of Neurophysiology 37, 1065–92.

    Google Scholar 

  • Strick, P. &Sterling, P. (1974) Synaptic termination of afferents from the ventrolateral nucleus of the thalamus in the cat motor cortex. A light and electron microscope study.Brain Research 61, 218–41.

    Google Scholar 

  • Szentagothai, J. (1973) Synaptology of the visual cortex. InHandbook of Sensory Physiology Volume VII/3 Central Processing of Visual Information, Part B, Visual Centers of the Brain (edited byJung, R.), pp. 269–324. Berlin: Springer-Verlag.

    Google Scholar 

  • Szentagothai, J. &Arbib, M. A. (1974) Conceptual models of neural organization.Neuroscience Research Program Bulletin 12, 307–510.

    Google Scholar 

  • Takahashi, E. (1965) Slow and fast groups of pyramidal tract cells and their respective membrane properties.Journal of Neurophysiology 28, 908–24.

    Google Scholar 

  • Toyama, K., Matsunami, K., Ohno, T. &Takashiki, S. (1974) An intracellular study of neuronal organization in the visual cortex.Brain Research 14, 518–20.

    Google Scholar 

  • Valverde, F. (1967) Apical dendritic spines of the visual cortex and light deprivation of the mouse.Experimental Brain Research 3, 337–52.

    Google Scholar 

  • Valverde, F. (1968) Structural changes in the area striata of the mouse after enucleation.Experimental Brain Research 5, 274–92.

    Google Scholar 

  • Valverde, F. (1970) The Golgi method. A tool for comparative structural analysis. InContemporary Research Methods in Neuroanatomy (edited byNauta, W. J. H. andEbbeson, S. O. E.), pp. 11–312. New York: Springer-Verlag.

    Google Scholar 

  • Valverde, F. (1971) Short axon neuronal subsystems in the visual cortex of the monkey.International Journal of Neuroscience 1, 181–97.

    Google Scholar 

  • Van Der Loos, H. (1956) Une combinaison de deux vieilles methodes histologiques pour le système nerveux central.Monatsschrift für Psychiatrie und Neurologie 132, 330–4.

    Google Scholar 

  • White, E. L. (1978) Identified neurons in mouse SmI cortex which are postsynaptic to thalamocortical axon terminals: a combined Golgi-electron microscopic and degeneration study.Journal of Comparative Neurology 181, 627–62.

    Google Scholar 

  • White, E. L. (1979) Thalamocortical synaptic relations: a review with emphasis on the projections of specific thalamic nuclei to the primary sensory areas of the neocortex.Brain Research Reviews 1, 275–311.

    Google Scholar 

  • White, E. L. &Hersch, S. M. (1981) Thalamocortical synapses of pyramidal cells which project from SmI to MsI cortex in the mouse.Journal of Comparative Neurology 198, 167–91.

    Google Scholar 

  • White, E. L. &Hersch, S. M. (1982) A quantitative study of thalamocortical and other synapses involving apical dendrites of corticothalamic projection cells in mouse SmI cortex.Journal of Neurocytology 11, 137–57.

    Google Scholar 

  • White, E. L. &Rock, M. P. (1980) Three dimensional aspects and synaptic relationships of a Golgi-impregnated spiny stellate cell reconstructed from serial thin sections.Journal of Neurocytology 9, 615–36.

    Google Scholar 

  • White, E. L. &Rock, M. P. (1981) A comparison of thalamocortical and other synaptic inputs to dendrites to two non-spiny neurons in a single barrel of mouse SmI cortex.Journal of Comparative Neurology 195, 265–77.

    Google Scholar 

  • Wickelgren, B. G. &Sterling, P. (1969) Influence of visual cortex on receptive fields of cat superior colliculus.Journal of Neurophysiology 32, 16–23.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. James L. O'Eeary Division of Experimental Neurology and Neurological Surgery and McDonnell Center for the Study of Higher Brain Function, Washington University School of Medicine, 660 South Euclid Avenue, 63110, Saint Louis, Missouri, USA

    S. H. C. Hendry & E. G. Jones

Authors
  1. S. H. C. Hendry
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. G. Jones
    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

Hendry, S.H.C., Jones, E.G. The organization of pyramidal and non-pyramidal cell dendrites in relation to thalamic afferent terminations in the monkey somatic sensory cortex. J Neurocytol 12, 277–298 (1983). https://doi.org/10.1007/BF01148465

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01148465

Keywords

Search

Navigation