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Neuroanatomy pp 561-581 | Cite as

Columnar Distribution of Cortico-Cortical Fibers in the Frontal Association, Limbic, and Motor Cortex of the Developing Rhesus Monkey

  • Patricia S. Goldman
  • Walle J. H. Nauta
Part of the Contemporary Neuroscientists book series (CN)

Summary

The terminal distribution of cortico-cortical connections was examined by autoradiography 7–8 days following injections of tritium labeled amino acids into the dorsal bank of the principal sulcus, the posterior part of the medial orbital gyrus, or the hand and arm area of the primary motor cortex in monkeys ranging in age from 4 days to 5.5 months. Labeled axons originating in these various regions of the frontal lobe have topographically diverse ipsilateral and contralateral destinations but virtually all of these projections share a common mode of distribution: they terminate in distinct vertically oriented columns, 200–500 μm wide, that extend across all layers of cortex and alternate in regular sequence with columns of comparable width in which grains do not exceed background. Spatial periodicity in the pattern of transported label in such regions as the prefrontal association cortex, the retro-splenial limbic cortex and the motor cortex indicates that columniation in the intra-cortical distribution of afferent fibers is not unique to sensory specific cortex but is instead a general feature of neocortical organization.

A columnar mode of distribution of cortico-cortical projections is present in monkeys at all ages investigated but is especially well delineated in the youngest of them. Thus, grain concentrations within columns are very high in monkeys injected at 4 days of age, somewhat lower in monkeys injected at 39–45 days of age, and least dense in those injected at 5.5 months. The distinctness of the spatially segregated pattern of innervation in the cortex of neonates indicates that the columnar organization of association-fiber systems in the frontal and limbic cortex is achieved before or shortly after birth.

Keywords

Motor Cortex Commissural Fiber Young Monkey Callosal Fiber Columnar Organization 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Abeles, M. and Goldstein, M. N., Jr., Functional architecture in cat primary auditory cortex: columnar organization according to depth, J. Neurophysiol, 33 (1970) 172–187.Google Scholar
  2. 2.
    Asanuma, H. and Sakata, H., Functional organization of a cortical efferent system examined with focal depth stimulation in cats, J. Neurophysiol, 30 (1967) 35–54.Google Scholar
  3. 3.
    Cowan, W. M., Gottlieb, D. I., Hendrickson, A. E., Price, J. E. and Woolsey, T. A., The autoradiographic demonstration of axonal connections in the central nervous system, Brain Research, 37(1972)21–51.CrossRefGoogle Scholar
  4. 4.
    Crossland, W. J., Currie, J. R., Rogers, L. A. and Cowan, W. M., Evidence for a rapid phase of axoplasmic transport at early stages in the development of the visual system of the chick and frog, Brain Research, 78 (1974) 483–489.CrossRefGoogle Scholar
  5. 5.
    Droz, B. and Leblond, C. P., Axonal migration of proteins in the central nervous system and peripheral nerves as shown by radioautography, J. comp. Neurol., 121 (1963) 325–345.CrossRefGoogle Scholar
  6. 6.
    Goldman, P. S., Age, sex and experience as related to the neural basis of cognitive development. In N. Buchwald and M. Brazier (Eds.), Brain Mechanisms in Mental Retardation, Academic Press, New York, 1975, pp. 379–392.Google Scholar
  7. 7.
    Goldman, P. S., Maturation of the mammalian nervous system and the ontogeny of behavior. In J. S. Rosenblatt, R. Hinde, E. Shaw and C. Beer (Eds.), Advances in the Study of Behavior, Academic Press, New York, 1976, pp. 1–90.Google Scholar
  8. 8.
    Graybiel, A. M., Wallerian degeneration and anterograde tracer methods. In W. M. Cowan and M. Cuénod (Eds.), The Use of Axonal Transport for Studies of Neuronal Connectivity, Elsevier, Amsterdam, 1975, pp. 173–216.Google Scholar
  9. 9.
    Gremo, F. and Marchisio, P. C., Dynamic properties of axonal transport of proteins and glycoproteins: a study based on the effects of metaphase blocking drugs in the developing optic pathway of chick embryos, CellTiss. Res., 161 (1975) 303–316.Google Scholar
  10. 10.
    Hendrickson, A. E. and Cowan, W. M., Changes in the rate of axoplasmic transport during postnatal development of the rabbit’s optic nerve and tract, Exp. Neurol., 30 (1971) 403–422.CrossRefGoogle Scholar
  11. 11.
    Herkenham, M., The nigro-thalamo-cortical connection mediated by the nucleus ventralis medialis thalami: evidence for a wide cortical distribution in the rat, Anat. Rec, 184 (1976) 426.Google Scholar
  12. 12.
    Hubel, D. H. and Wiesel, T. N., Receptive fields, binocular interaction, and functional architecture in the cat’s visual cortex, J. Physiol. (Lond.), 160 (1962) 106–152.Google Scholar
  13. 13.
    Hubel, D. H. and Wiesel, T. N., Receptive fields and functional architecture of monkey striate cortex, J. Physiol. (Lond.), 195 (1968) 215–243.Google Scholar
  14. 14.
    Hubel, D. H., Wiesel, T. N. and LeVay, S., Plasticity of ocular dominance columns in monkey striate cortex, Phil Trans, roy. Soc. B, (1976) in press.Google Scholar
  15. 15.
    Hyvärinen, J. and Poranen, A., Function of the parietal associative area 7 as revealed from cellular discharges in alert monkeys, Brain, 97 (1974) 673–692.CrossRefGoogle Scholar
  16. 16.
    Jones, E. G., Burton, H. and Porter, R., Commissural and cortico-cortical ‘columns’ in the somatic sensory cortex of primates, Science, 190 (1975) 572–574.CrossRefGoogle Scholar
  17. 17.
    Killackey, H. P., Anatomical evidence for cortical subdivisions based on vertically discrete thalamic projections from the ventral posterior nucleus to cortical barrels in the rat, Brain Research, 51(1973)326–331.CrossRefGoogle Scholar
  18. 18.
    Killackey, H. P., Belford, G., Ryugo, R. and Ryugo, D. K., Anomalous organization of thalamocortical projections consequent to vibrissae removal in the newborn rat and mouse, Brain Research, 104(1976)309–315.CrossRefGoogle Scholar
  19. 19.
    Lasek, R. J., Axoplasmic transport in cat dorsal root ganglion cells as studied with L-[3H]leucine, Brain Research, 7 (1968) 360–377.CrossRefGoogle Scholar
  20. 20.
    Lasek, R. J., Protein transport in neurons, Int. Rev. Neurobiol., 13 (1970) 289–324.CrossRefGoogle Scholar
  21. 21.
    Lasek, R. J., Axonal transport of proteins in dorsal root ganglion cells of the growing cat: a comparison of growing and mature neurons, Brain Research, 20 (1970) 121–126.CrossRefGoogle Scholar
  22. 22.
    Lorente de No, R., The cerebral cortex: architecture, intracortical connections and motor projections. In J. F. Fulton (Ed.), Physiology of the Nervous System, Oxford Univ. Press, New York, 1938, pp. 291–339.Google Scholar
  23. 23.
    Marchisio, P. C. and Sjöstrand, J., Axonal transport in the avian optic pathway during development, Brain Research, 26 (1971) 204–211.CrossRefGoogle Scholar
  24. 24.
    Mountcastle, V. B., Modality and topographic properties of single neurons of cat’s somatic sensory cortex, J. Neurophysiol., 20 (1957) 408–434.Google Scholar
  25. 25.
    Mountcastle, V. B. and Powell, T. P. S., Central nervous mechanisms subserving position sense and kinesthesis, Bull. Johns Hopk. Hosp., 105 (1959) 173–200.Google Scholar
  26. 26.
    Ryugo, R. and Killackey, H. P., Cortico-cortical connections of the barrel field of the rat somatosensory cortex, Neurosci. Abstr., 1 (1975) 126.Google Scholar
  27. 27.
    Shanks, M. F., Rockel, A. J. and Powell, T. P. S., The commissural fiber connections of the primary somatic sensory cortex, Brain Research, 98 (1975) 166–171.CrossRefGoogle Scholar
  28. 28.
    Van der Loos, H. and Woolsey, T. A., Somatosensory cortex: structural alterations following early injury to sense organs, Science, 179 (1973) 395–397.CrossRefGoogle Scholar
  29. 29.
    Wiesel, T. N., Hubel, D. H. and Lam, D. M. K., Autoradiographic demonstration of ocular-dominance columns in the monkey’s striate cortex by means of transneuronal transport, Brain Research, 79 (1974) 273–279.CrossRefGoogle Scholar
  30. 30.
    Woolsey, T. A. and Van der Loos, H., The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex, Brain Research, 17 (1970) 205–242.CrossRefGoogle Scholar

Copyright information

© Elsevier/North-Holland Biomedical Press, Amsterdam 1993

Authors and Affiliations

  • Patricia S. Goldman
    • 1
    • 2
  • Walle J. H. Nauta
    • 1
    • 2
  1. 1.Laboratory of NeuropsychologyNational Institute of Mental HealthBethesdaUSA
  2. 2.Department of PsychologyMassachusetts Institute of TechnologyCambridgeUSA

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