Advertisement

Experimental Brain Research

, Volume 38, Issue 4, pp 381–394 | Cite as

Postnatal shaping of callosal connections from sensory areas

  • G. M. Innocenti
  • R. Caminiti
Article

Summary

Horseradish peroxidase (HRP) was injected unilaterally into the first and second visual areas (VI and V2; areas 17 and 18) of 20 kittens aged between 2 and 90 days and into the second somatosensory area (S2) of 16 kittens aged between 1 and 52 days. The radial and tangential (normal and parallel to the pial surface, respectively) distributions of neurones giving origin to callosal axons (callosal neurones) were studied. In adult cats, callosal efferent zones (CZs) are defined by the distribution of callosal neurones. CZs occupy, in the visual cortices, tangentially and radially restricted parts of areas 17, 18, 19 of the lateral suprasylvian gyms and in the somatosensory cortices, parts of SI and S2. At birth, callosal neurones are distributed throughout the tangential extent of visual and somatosensory areas; they are also more widespread in depth than in the adult. During the first postnatal month, as a result of the gradual disappearence of callosal neurones from parts of the visual and somatosensory areas, the adult CZs emerge. The CZ in areas 17 and 18 undergoes a further tangential reduction during the second and third postnatal months.

Key words

Corpus callosum Visual cortex Somatosensory cortex Development 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Adams J C (1977) Technical considerations on the use of horseradish peroxidase as a neuronal marker. Neuroscience 2: 141–145Google Scholar
  2. Angevine J B Jr, Sidman R L (1961) Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse. Nature 192: 766–768Google Scholar
  3. Anker R L, Cragg B G (1974) Development of the extrinsic connections of the visual cortex in the cat. J Comp Neurol 154: 29–42Google Scholar
  4. Berlucchi G, Gazzaniga M S, Rizzolatti G (1967) Microelectrode analysis of transfer of visual information by the corpus callosum. Arch Ital Biol 105: 583–596Google Scholar
  5. Bilge M, Bingle A, Seneviratne K N, Whitteridge D (1967) A map of the visual cortex in the cat. J Physiol (Lond) 191: 116P-118PGoogle Scholar
  6. Cajal S-R (1894) Les nouvelles idées sur la structure du systéme nerveux chez l'homme et chez les vertébrés. Reinwald, Paris p 59–63Google Scholar
  7. Cajal S-R (1911) Histologie du systéme nerveux de l'homme et des vertébrés. Maloine, ParisGoogle Scholar
  8. Caminiti R, Innocenti G M, Manzoni T (1979) The anatomical substrate of callosal messages from SI and SII in the cat. Exp Brain Res 34: 453–470Google Scholar
  9. Changeux J-P, Danchin A (1976) Selective stabilisation of developing synapses as a mechanism for the specification of neuronal networks. Nature 264: 705–712Google Scholar
  10. Choudhury B P, Whitteridge D, Wilson M E (1965) The function of the callosal connections of the visual cortex. Quart J Exp Physiol 50: 214–219Google Scholar
  11. Cowan W M (1973) Neuronal death as a regulative mechanism in the control of cell number in the nervous system. In: Rockstein M (ed) Development and aging in the nervous system. Academic Press, New York, p 19–41Google Scholar
  12. Cragg B G (1975) The development of synapses in the visual system of the cat. J Comp Neurol 160: 147–166Google Scholar
  13. Dürsteier M R, Garey L J, Movshon J A (1976) Reversal of the morphological effects of monocular deprivation in the kitten's lateral geniculate nucleus. J Physiol (Lond) 261: 189–210Google Scholar
  14. Ebner F F, Myers R E (1965) Distribution of corpus callosum and anterior commissure in cat and raccoon. J Comp Neurol 124: 353–366Google Scholar
  15. Elberger A J (1979) The role of the corpus callosum in the development of interocular eye alignment and the organization of the visual field in the cat. Exp Brain Res 36: 71–85Google Scholar
  16. Fleischhauer K, Schlüter G (1970) Über das postnatale Wachstum des Corpus callosum der Katze (Felis domestica). Z Anat Entwick-Gesch 132: 228–239Google Scholar
  17. Fleischhauer K, Wartenberg H (1967) Elektronenmikroskopische Untersuchungen über das Wachstum der Nervenfasern und über das Auftreten von Markscheiden im Corpus callosum der Katze. Z Zellforsch 83: 568–581Google Scholar
  18. Garey L J, Blakemore C (1977) Monocular deprivation: Morphological effects on different classes of neurons in the lateral geniculate nucleus. Science 195: 414–416Google Scholar
  19. Gfeller-Leuba G (1977) Maturation postnatale quantitative de lécorce cérébrale de la souris. Thése, Université de Lausanne, Faculté des SciencesGoogle Scholar
  20. Glaser E M, Van der Loos H (1965) A semi-automatic computer microscope for the analysis of neuronal morphology. IEEE Trans Bio-Med Engin 12: 22–31Google Scholar
  21. Goldman P S, Nauta W J H (1977) Columnar distribution of cortico-cortical fibers in the frontal association, limbic, and motor cortex of the developing rhesus monkey. Brain Res 122: 393–413Google Scholar
  22. Grafstein B (1963) Postnatal development of the transcallosal evoked response in the cerebral cortex of the cat. J Neurophysiol 26: 79–99Google Scholar
  23. Graham R C Jr, Karnovsky M J (1966) The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney: Ultrastructural cytochemistry by a new technique. J Histochem Cytochem 14: 291–302Google Scholar
  24. Guillery R W (1972) Binocular competition in the control of geniculate cell growth. J Comp Neurol 144: 117–130Google Scholar
  25. Guillery R W, Stelzner D J (1970) The differential effects of unilateral lid closure upon the monocular and binocular segments of the dorsal lateral geniculate nucleus in the cat. J Comp Neurol 139: 413–422Google Scholar
  26. Hassler R, Muhs-Clement K (1964) Architektonischer Aufbau des sensomotorischen und parietalen Cortex der Katze. J Hirnforsch 6: 377–420Google Scholar
  27. Henneman E, Somjen G, Carpenter D O (1965) Functional significance of cell size in spinal motoneurons. J Neurophysiol 28: 560–599Google Scholar
  28. Hetzko D (1968) Über die postnatale Zunahme des Capillarvolumens im Corpus callosum der Katze. Z Anat Entwickl-Gesch 127: 138–144Google Scholar
  29. Hillebrand H (1966) Quantitative Untersuchungen über postnatale Veränderungen der Glia im Corpus callosum der Katze. Z Zellforsch 73: 303–312Google Scholar
  30. Hubel D H, Wiesel T N (1967) Cortical and callosal connections concerned with the vertical meridian of the visual fields in the cat. J. Neurophysiol 30: 1561–1573Google Scholar
  31. Innocenti G M (1978) Postnatal development of interhemispheric connections of the cat visual cortex. Arch Ital Biol 116: 463–470Google Scholar
  32. Innocenti G M (1979a) Adult and neonatal characteristics of the callosal zone at the boundary between areas 17 and 18 in the cat. In: Steele, Rüssel I, Van Hof M W, Berlucchi G (eds) Structure and function of the cerebral commissures. Macmillan, London, pp 244–258Google Scholar
  33. Innocenti G M (1979b) A hypothesis on the efferent system from the visual cortex. In: Freeman R D (ed) Developmental neurobiology of vision. Plenum Press, New York, pp 227–234Google Scholar
  34. Innocenti G M (1979c) (in press) The primary visual pathway through the corpus callosum: morphological and functional aspects in the cat. Arch Ital BiolGoogle Scholar
  35. Innocenti G M, Fiore L (1976) Morphological correlates of visual field transformation in the corpus callosum: Neurosci Letters 2: 245–252Google Scholar
  36. Innocenti G M, Fiore L, Caminiti R (1977) Exuberant projection into the corpus callosum from the visual cortex of newborn cats. Neurosci Letters 4: 237–242Google Scholar
  37. Innocenti G M, Frost D O (1978) Visual. experience and the development of the efferent system to the corpus callosum. Neurosci Abstr 4: 475Google Scholar
  38. Innocenti G M, Frost D O (1979) Effects of visual experience on the maturation of the efferent system to the corpus callosum. Nature 280: 231–234Google Scholar
  39. Jacobson M (1978) Developmental neurobiology, 2nd ed. Plenum Press, New York LondonGoogle Scholar
  40. Jones E G, Powell T P S (1968) The commissural connexions of the somatic sensory cortex in the cat. J Anat 103: 433–455PubMedGoogle Scholar
  41. Kuypers H G J M, Bentivoglio M, VanderKooy D, Catsman-Berrevoets C E (1979) Retrograde transport of bisbenzimide and propidium iodide through axons to their parent cell bodies. Neurosci Letters 12: 1–7Google Scholar
  42. Maciewicz R J (1974) Afferents to the lateral suprasylvian gyrus of the cat traced with horseradish peroxidase. Brain Res 78: 139–140Google Scholar
  43. Mesulam M-M (1978) A tetramethyl benzidine method for the light microscopic tracing of neural connections with horseradish peroxidase (HRP) neurohistochemistry. Society for Neuroscience, Short Course, St. LouisGoogle Scholar
  44. Meyerson B A (1968) Ontogeny of interhemispheric functions. An electrophysiological study in pre- and postnatal sheep. Acta Physiol Scand [Suppl] 312: 1–111Google Scholar
  45. Rakic P, Yakovlev P I (1968) Development of the corpus callosum and cavum septi in man. J Comp Neurol 132: 45–72PubMedGoogle Scholar
  46. Rubel E W (1971) Comparison of somatotopic organization in sensory neocortex of newborn kittens and adult cats. J Comp Neurol 143: 447–480Google Scholar
  47. Sanderson K J (1971) The projection of the visual field to the lateral geniculate and medial interlaminar nuclei in the cat. J Comp Neurol 143: 101–118Google Scholar
  48. Sanides D, Donate-Oliver F (1978) Identification and localisation of some relay cells in cat visual cortex. In: Brazier M A B, Petsche H (eds) Architectonics of the cerebral cortex. Raven Press, New York, pp 227–234Google Scholar
  49. Seggie J, Berry M (1972) Ontogeny of interhemispheric evoked potentials in the rat: Significance of myelination of the corpus callosum. Exp Neurol 35: 215–232Google Scholar
  50. Shanks M F, Rockel A J, Powell T P S (1975) The commissural fibre connections of the primary somatic sensory cortex. Brain Res 98: 166–171Google Scholar
  51. Shatz C (1977a) Abnormal interhemispheric connections in the visual system of Boston Siamese cats: A physiological study. J Comp Neurol 171: 229–246Google Scholar
  52. Shatz C (1977b) Anatomy of interhemispheric connections in the visual system of Boston Siamese and ordinary cats. J Comp Neurol 173: 497–518Google Scholar
  53. Shoumura K (1974) An attempt to relate the origin and distribution of commissural fibers to the presence of large and medium pyramids in layer III in the cat's visual cortex. Brain Res 67: 13–25Google Scholar
  54. Sidman R L, Rakic P (1973) Neuronal migration, with special reference to developing human brain: a review. Brain Res 62: 1–35Google Scholar
  55. So K-F, Schneider G E (1978) Postnatal development of retinogeniculate projections in Syrian hamsters: An anterograde HRP study. Neurosci Abstr 4: 127Google Scholar
  56. Stone J, Fukuda Y (1974) Properties of cat retinal ganglion cells: A comparison of W-cells with X- and Y-cells. J Neurophysiol 37: 722–748Google Scholar
  57. Tusa R J, Palmer L A, Rosenquist A C (1978) The retinotopic organization of area 17 (striate cortex) in the cat. J Comp Neurol 177: 213–236Google Scholar
  58. Westheimer G, Mitchell D E (1969) The sensory stimulus for disjunctive eye movements. Vision Res 9: 749–755Google Scholar
  59. Wiesel T N, Hubel D H (1965) Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. J Neurophysiol 28: 1029–1040Google Scholar
  60. Wise S P, Jones E G (1976) The organization and postnatal development of the commissural projection of the rat somatic sensory cortex. J Comp Neurol 168: 313–344Google Scholar
  61. Wise S P, Jones E G (1978) Developmental studies of thalamocortical and commissural connections in the rat somatic sensory cortex. J Comp Neurol 178: 187–208Google Scholar

Copyright information

© Springer-Verlag 1980

Authors and Affiliations

  • G. M. Innocenti
    • 1
  • R. Caminiti
    • 2
  1. 1.Institute of AnatomyUniversity of LausanneLausanne-CHUVSwitzerland
  2. 2.Institute of PhysiologyUniversity of AnconaAnconaItaly

Personalised recommendations