Journal of Neurocytology

, Volume 26, Issue 12, pp 779–797 | Cite as

The organization of double bouquet cells in monkey striate cortex

  • A. Peters
  • C. Sethares
Article

Abstract

In previous publications we proposed a model of cortical organization in which the pyramidal cells of the cerebral cortex are organized into modules. The modules are centred around the clusters of apical dendrites that originate from the layer 5 pyramidal cells. In monkey striate cortex such modules have an average diameter of 23 μm and the outputs originating from the modules are contained in the vertical bundles of myelinated axons that traverse the deeper layers of the cortex. The present study is concerned with how the double bouquet cells in layer 2/3 of striate cortex relate to these pyramidal cell modules. The double bouquet cells are visualized with an antibody to calbindin, and it has been shown that their vertically oriented axons, or horse tails, are arranged in a regular array, such that there is one horse tail per pyramidal cell module. Within layer 2/3 the double bouquet cell axons run alongside the apical dendritic clusters, while in layer 4C they are closely associated with the myelinated axon bundles. However, the apical dendrites are not the principal targets of the double bouquet cell axons. Most of the neuronal elements post-synaptic to them are the shafts of small dendrites (60%) and dendritic spines, with which they form symmetric synapses. This regular arrangement of the axons of the double-bouquet cells and their relationship to the components of the pyramidal cells modules supports the concept that there are basic, repeating neuronal circuits in the cortex.

Keywords

Pyramidal Cell Dendritic Spine Neuronal Circuit Myelinated Axon Apical Dendrite 

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References

  1. Cajal, Ramon y S. (1911) Histologic du Système Nerveux de l'Homme et des Vertébrés (transl. by AZOULAY, L.), vol. 2. Paris: Maloine.Google Scholar
  2. Carder, R. K., Leclerc, S. S. & Hendry, S. H. C. (1996) Regulation of calcium-binding protein immunoreactivity in GABA neurons of macaque primary visual cortex. Cerebral Cortex 6, 271–87.Google Scholar
  3. Celio, M. R., Scharer, L., Morrison, J. H., Norman, A. W. & Bloom, F. E. (1986) Calbindin immunoreactivity alternates with cytochrome oxidase c-rich zones in some layers of the primate visual cortex. Nature 323, 715–17.Google Scholar
  4. Defelipe, J., Hendry, S. H. C., Hashikawa, T., Molinari, M. & Jones, E. G. (1990) A microcolumnar structure of cerebral cortex revealed by immunocytochemical studies of double bouquet cell axons. Neuroscience 37, 655–73.Google Scholar
  5. Defelipe, J., Hendry, S. H. C. & Jones, E. G. (1989) Synapses of double bouquet cells in monkey cerebral cortex visualized by calbindin immunoreactivity. Brain Research 503, 49–54.Google Scholar
  6. Defelipe, J. & Jones, E. G. (1992) High-resolution light and electron microscopic immunocytochemistry of colocalized GABA and calbindin D-28k in somata and double bouquet cell axons of monkey somatosensory cortex. European Journal of Neuroscience 4, 46–60.Google Scholar
  7. Del Rio, M. R. & Defelipe, J. (1995) A light and electron microscopic study of calbindin D-28k immunoreactive double bouquet cells in the human temporal cortex. Brain Research 690, 133–40.Google Scholar
  8. FairÉn, A., Defelipe, J. & Regidor, J. (1984) Nonpyramidal neurons: General account. In Cellular Components of the Cerebral Cortex (edited by Peters, A. & Jones, E. G.) Cerebral Cortex vol. 1, pp. 201–54. New York: Plenum Press.Google Scholar
  9. Fitzpatrick, D., Lund, J. S. & Blasdel, G. G. (1985) Intrinsic connections of macaque striate cortex. Afferent and efferent connections of lamina 4C. Journal of Neuroscience 5, 3329–49.Google Scholar
  10. Frost, D. O. (1981) Orderly anomalous retinal projections to the medial geniculate, ventrobasal, and lateral posterior nuclei of the hamster. Journal of Comparative Neurology 203, 227–56.Google Scholar
  11. Frost, D. O. & Metin, C. (1985) Induction of functional retinal projections to the somatosensory system. Nature 317, 162–4.Google Scholar
  12. Guido, W., Spear, P. D. & Tong, L. (1990) Functional compensation in the lateral suprasylvian visual area following bilateral visual cortex damage in kittens. Experimental Brain Research 83, 219–24.Google Scholar
  13. Guido, W., Spear, P. D. & Tong, L. (1992) How complete is the physiological compensation in extrastriate cortex after visual cortex damage in kittens? Experimental Brain Research 91, 455–66.Google Scholar
  14. Hendry, S. H. C. & Carder, R. K. (1993) Neurochemical compartmentation of monkey and human visual cortex: Similarities and variations in calbindin immunoreactivity across species. Visual Neuroscience 10, 1109–20.Google Scholar
  15. Hendry, S. H. C., Jones, E. G., Emson, P. C., Lawson, D. E. M., Heizmann, C. W. & Streit, P. (1989) Two classes of cortical GABA neurons defined by differential calcium-binding protein immunoreactivities. Experimental Brain Research 76, 467–472.9Google Scholar
  16. Hendry, S. H. C., Schwark, H. D., Jones, E. G. & Yan, J. (1987) Numbers and proportions of GABA immunoreactive neurons in different areas of monkey cerebral cortex. Journal of Neuroscience 7, 1503–19.Google Scholar
  17. Jones, E. G. (1975) 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
  18. Lund, J. S., Yoshika, T. & Levitt, J. B. (1994) Substrates for interlaminar connections in area VI of macaque monkey cerebral cortex. In Primary Visual Cortex in Primates (edited by Peters, A. & Rockland, K. S.) Cerebral Cortex vol. 10, pp. 32–60. New York: Plenum Press.Google Scholar
  19. Metin, C. & Frost, D. O. (1989) Visual responses of neurons in somatosensory cortex of hamsters with experimentally induced retinal projections to somatosensory thalamus. Proceedings of the National Academy of Sciences USA 86, 357–61.Google Scholar
  20. Mountcastle, V. B. (1978) An organizing principle for cerebral function. The unit module and the distributed system. In The Mindful Brain (edited by Edelman, G. M. & Mountcastle, V. B.) pp. 7–50. Cambridge, MA.: M.I.T. Press.Google Scholar
  21. Payne, B. R., Lomber, S. G., Villa, A. E. & Bullier, J. (1996) Reversible deactivation of cerebral network components. Trends in Neuroscience 19, 535–42.Google Scholar
  22. Peters, A. (1971) Stellate cells of the rat parietal cortex. Journal of Comparative Neurology 141, 345–374.Google Scholar
  23. Peters, A. & FairÉn, A. (1978) Smooth and sparselyspined stellate cells in the visual cortex of the rat: a study using a combined Golgi-electron microscope technique. Journal of Comparative Neurology 181, 129–72.Google Scholar
  24. Peters, A. & Jones, E. G. (1984) Classification of cortical neurons. In Cellular Components of the Cerebral Cortex (edited by Peters, A. & Jones, E. G.) Cerebral Cortex vol. 1, pp. 107–22. New York: Plenum Press.Google Scholar
  25. Peters, A. & Kara, D. A. (1987) The neuronal composition of area 17 of rat visual cortex. IV. The organization of pyramidal cells. Journal of Comparative Neurology 260, 573–90.Google Scholar
  26. Peters, A. & Sethares, C. (1991a) Organization of pyramidal neurons in area 17 of monkey visual cortex. Journal of Comparative Neurology 306, 1–23.Google Scholar
  27. Peters, A. & Sethares, C. (1991b) Layer IVA of rhesus monkey primary visual cortex. Cerebral Cortex 1, 445–462.Google Scholar
  28. Peters, A. & Sethares, C. (1996) Myelinated axons and the pyramidal cell modules in monkey primary visual cortex. Journal of Comparative Neurology 365, 232–55.Google Scholar
  29. Peters, A. & Walsh, T. M. (1972) A study of the organization of apical dendrites in the somatic sensory cortex of the rat. Journal of Comparative Neurology 144, 253–68.Google Scholar
  30. Peters, A. & Yilmaz, E. (1993) Neuronal organization in area 17 of cat visual cortex. Cerebral Cortex 3, 49–68.Google Scholar
  31. Roe, A. E., Pallas, S. L., Hahm, J. O. & Sur, M. (1990) A map of visual space induced into primary auditory cortex. Science 250, 818–20.Google Scholar
  32. Roe, A. W., Pallas, S. L., Kwon, Y. H. & Sur, M. (1992) Visual projections to the auditory cortex in ferrets: receptive fields of visual neurons in primary auditory cortex. Journal of Neuroscience 12, 3651–664.Google Scholar
  33. Somogyi, P. & Cowey, A. (1981) Combined Golgi and electron microscopic study of the synapses formed by double bouquet cells in the visual cortex of the cat and monkey. Journal of Comparative Neurology 195, 547–66.Google Scholar
  34. Somogyi, P. & Cowey, A. (1984) Double bouquet cells. In Cellular Components of the Cerebral Cortex (edited by Peters, A. & Jones, E. G.) Cerebral Cortex vol. 1, pp. 337–60. New York: Plenum Press.Google Scholar
  35. Sur, M., Garraghty, P. E. & Roe, A. W. (1988) Experimentally induced projections into auditory thalamus and cortex. Science 242, 1437–41.Google Scholar
  36. SzentÀgothai, J. (1973) Synaptology of the visual cortex. In Handbook of Sensory Physiology, vol. VII 3B. Central Processing of Visual Information (edited by JUNG, R.) pp. 269–324. Berlin: Springer.Google Scholar
  37. Valverde, F. (1985) The organizing principles of the primary visual cortex in the monkey. In Visual Cortex (edited by Peters, A. & Jones, E. G.) Cerebral Cortex vol. 3, pp. 208–58. New York: Plenum Press.Google Scholar
  38. Van Brederode, J. F. M., Mulligan, K. A. & Herickson, A. E. (1990) Calcium-binding proteins as markers for subpopulations of GABAergic neurons in monkey striate cortex. Journal of Comparative Neurology 298, 1–22.Google Scholar
  39. WÄssle, H. & Reimann, H. J. (1978) The mosaic of nerve cells in the mammalian retina. Proceedings of the Royal Society, London (Biol.) 200, 441–61.Google Scholar
  40. West, M. J. (1993) New stereological methods for counting neurons. Neurobiology of Aging 14, 275–85.Google Scholar
  41. White, E. L. & Peters, A. (1993) Cortical modules in the posteromedial barrel subfield (Sm1) of the mouse. Journal of Comparative Neurology 334, 86–96.Google Scholar
  42. Wong-Riley, M. T. T., Merzenich, M. M. & Leake, P. A. (1978) Changes in endogenous enzymatic activity to DAB induced by neuronal inactivity. Brain Research 141, 185–92.Google Scholar

Copyright information

© Chapman and Hall 1997

Authors and Affiliations

  • A. Peters
    • 1
  • C. Sethares
  1. 1.Department of Anatomy and NeurobiologyBoston University School of MedicineBostonUSA

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