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Experimental Brain Research

, Volume 90, Issue 2, pp 346–358 | Cite as

Emergence of callosally projecting neurons with stellate morphology in the visual cortex of the kitten

  • A. Vercelli
  • F. Assal
  • G. M. Innocenti
Article

Summary

Callosally projecting neurons in areas 17 and 18 of the adult cat can be classified into two types on the basis of their dendritic morphology: pyramidal and stellate cells. The latter are nearly exclusively of the spinous type and are predominantly located in upper layer IV. Retrograde transport of the carbocyanine dye DiI, applied to the corpus callosum, showed that, up to P6, all callosally projecting neurons resemble pyramids in the possession of an apical dendrite reaching layer I. At P10, however, callosally projecting neurons with stellate morphology were found. A study was designed to distinguish whether these neurons are late in extending their axons to the corpus callosum or, alternatively, have transient apical dendrites. To this end, callosally projecting neurons were retrogradely labeled by fluorescent beads injected in areas 17 and 18 at P1–P3 and then either relabeled with DiI applied to the corpus callosum at P10 or intracellularly injected with Lucifer Yellow at P57. Double-labeled stellate and pyramidal cells were found in similar proportions to those found for the total, single-labeled population of callosally projecting neurons. It is therefore concluded that callosally projecting spiny stellate cells initially possess an apical dendrite and a pyramidal morphology. At P6, i.e. close to the time when stellate cells appear, layer IV neurons with an atrophic apical dendrite were found, suggestive of an apical dendrite in the process of being eliminated.

Key words

Cerebral cortex Corpus callosum Dendrites Spiny stellate neurons Kitten 

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References

  1. Armengol J-A, Sotelo C (1991) Early dendritic development of Purkinje cells in the rat cerebellum. A light and electron microscopic study using axonal tracing in “in vitro” slices. Dev Brain Res 64: 95–114Google Scholar
  2. Assal F, Vercelli A, Innocenti GM (1991) The morphology of immature callosal neurons in area 17 and 18 of the cat. Eur J Neurosci [Suppl] 4: 283Google Scholar
  3. Blaser PF, Catsicas S, Clarke PGH (1990) Retrograde modulation of dendritic geometry in the vertebrate brain during development. Dev Brain Res 57: 139–142Google Scholar
  4. Bolz J, Hübener M, Kehrer I, Novak N (1991) Structural organization and development of identified projection neurons in primary visual cortex. In: Bagnoli P, Hodos W (eds) The changing visual system: maturation and aging in the central nervous system (Nato ASI Series), Plenum Press, New York, pp 233–246Google Scholar
  5. Boothe RG, Greenough WT, Lund JS, Wrege K (1979) A quantitative investigation of spine and dendrite development of neurons in visual cortex (area 17) of Macaca nemestrina monkeys. J Comp Neurol 186: 473–490Google Scholar
  6. Buhl EH, Singer W (1989) The callosal projection in cat visual cortex as revealed by a combination of retrograde tracing and intracellular injection. Exp Brain Res 75: 470–476Google Scholar
  7. Cajal Ramón y S (1911) Histologie du système nerveux de l'homme et des vertébrés. Maloine, ParisGoogle Scholar
  8. Callaway EM, Katz LC (1990) Emergence and refinement of clustered horizontal connections in cat striate cortex. J Neurosci 10: 1134–1153Google Scholar
  9. Chalupa LM, Killackey HP (1989) Process elimination underlies ontogenetic change in the distribution of callosal projection neurons in the postcentral gyrus of the fetal rhesus monkey. Proc Natl Acad Sci USA 86: 1076–1079Google Scholar
  10. Cragg BG (1975) The development of synapses in the visual system of the cat. J Comp Neurol 160: 147–166Google Scholar
  11. Dann JF, Buhl EH, Peichl L (1988) Postnatal dendritic maturation of alpha and beta ganglion cells in cat retina. J Neurosci 8: 1485–1499Google Scholar
  12. Derer P, Derer M (1990) Cajal-Retzius cell ontogenesis and death in mouse brain visualized with horseradish peroxidase and electron microscopy. Neuroscience 36: 839–856Google Scholar
  13. Fairén A, Valverde F (1979) Specific thalamo-cortical afferents and their presumptive targets in the visual cortex. A Golgi study. In: Cuénod M, Kreutzberg GW, Bloom FE (eds) Development and chemical specificity of neurons (Progress in brain research, vol 51). Eisevier North-Holland Biomedical Press, Amsterdam, pp 420–438Google Scholar
  14. Frost DO, Moy YP (1989) Effects of dark rearing on the development of visual callosal connections. Exp Brain Res 78: 203–213Google Scholar
  15. Gilbert CD, Wiesel TN (1979) Morphology and intracortical projections of functionally characterized neurones in the cat visual cortex. Nature 280: 120–125Google Scholar
  16. Glaser EM, Van der Loos H (1965) A semi-automatic computer-microscope for the analysis of neuronal morphology. IEEE Transactions Biomed Eng 12: 22–31Google Scholar
  17. Godement P, Vanselow J, Thanos S, Bonhoeffer F (1987) A study in developing visual systems with a new method of staining neurones and their processes in fixed tissue. Development 101: 697–713Google Scholar
  18. Hornung JP, Garey LJ (1980) A direct pathway from thalamus to visual callosal neurons in cat. Exp Brain Res 38: 121–123Google Scholar
  19. Innocenti GM (1980) The primary visual pathway through the corpus callosum: morphological and functional aspects in the cat. Arch Ital Biol 118: 124–188Google Scholar
  20. Innocenti GM (1981a) Growth and reshaping of axons in the establishment of visual callosal connections. Science 212: 824–827Google Scholar
  21. Innocenti GM (1981b) Transitory structures as substrate for developmental plasticity of the brain. In: van Hof MW, Mohn G (eds) Functional recovery from brain damage (Developments in Neuroscience, vol. 13). Elsevier/North-Holland Biomedical Press, Amsterdam New York Oxford, pp 305–333Google Scholar
  22. Innocenti GM (1986) General organization of callosal connections in the cerebral cortex. In: Jones EG, Peters A (eds) Cerebral cortex, vol 5. Plenum, New York, pp 291–353Google Scholar
  23. Innocenti GM (1990) Pathways between development and evolution. In: Finlay B, Innocenti G and Scheich H (eds) The neocortex, ontogeny and phylogeny. Plenum, New York, pp 43–52Google Scholar
  24. Innocenti GM (1991) The development of projections from cerebral cortex. Prog Sens Physiol 12: 65–114Google Scholar
  25. Innocenti GM, Fiore L (1976) Morphological correlates of visual field transformation in the corpus callosum. Neurosci Lett 21: 245–252Google Scholar
  26. Innocenti GM, Clarke S, Kraftsik R (1986) Interchange of callosal and association projections in the developing visual cortex. J Neurosci 6: 1384–1409Google Scholar
  27. Ivy GO, Killackey HP (1982) Ontogenetic changes in the projections of neocortical neurons. J Neurosci 2: 735–743Google Scholar
  28. Jacobson M (1978) Developmental neurobiology. Plenum Press, New YorkGoogle Scholar
  29. Jhaveri S, Morest DK (1982) Sequential alterations of neuronal architecture in nucleus magnocellularis of the developing chicken: a Golgi study. Neuroscience 7: 837–853PubMedGoogle Scholar
  30. Jones EG (1975) Varieties and distribution of non-pyramidal cells in the somatic sensory cortex of the Squirrel Monkey. J Comp Neurol 160: 205–268Google Scholar
  31. Katz LC, Iarovici DM (1990) Green fluorescent latex microspheres: a new retrograde tracer. Neuroscience 34: 511–520Google Scholar
  32. Kelly JP, Van Essen DC (1974) Cell structure and function in the visual cortex of the cat. J Physiol 238: 515–547Google Scholar
  33. Koester SE, O'Leary DDM (1990) Dendritic distinctions between callosal and subcortically projecting pyramidal neurons develop from an initial common morphology by elimination of exuberant apical dendrites. Soc Neurosci Abst 16: 1126Google Scholar
  34. LeVay S (1973) Synaptic patterns in the visual cortex of the cat and monkey: electron microscopy of Golgi preparations. J Comp Neurol 150: 53–86Google Scholar
  35. Lin CS, Friedlander MJ, Sherman SM (1979) Morphology of physiologically identified neurons in the visual cortex of the cat. Brain Res 172: 344–348Google Scholar
  36. Lorente de Nó R (1922) La corteza cerebral del ratón. Trab Lab Invest biol Univ Madrid 20: 41–78Google Scholar
  37. Lorente de Nó R (1938) Architectonics and structure of the cerebral cortex. In: Fulton JF (eds) Physiology of the nervous system. Oxford University Press, pp 291–330Google Scholar
  38. Lund JS (1984) Spiny stellate neurons. In: Peters A, Jones EG (eds) Cerebral cortex, vol 1. Plenum, New York, pp 255–308Google Scholar
  39. Lund JS, Boothe RG, Lund RD (1977) Development of neurons in the visual cortex (area 17) of the monkey (Macaca nemestrina): a Golgi study from fetal day 127 to postnatal maturity. J Comp Neurol 176: 149–188Google Scholar
  40. Lund JS, Hendrickson AE, Ogren MP, Tobin EA (1981) Anatomical organization of primate visual cortex area, VII. J Comp Neurol 202: 19–45PubMedGoogle Scholar
  41. Lund JS, Harper TR (1991) Postnatal development of thalamic recipient neurons in the monkey striate cortex. III. Somatic inhibitory synapse acquisition by spiny stellate neurons of layer 4C. J Comp Neurol 309: 141–149Google Scholar
  42. Lund JS, Holbach SM (1991) Postnatal development of thalamic recipient neurons in the monkey striate cortex. I. Comparison of spine acquisition and dendritic growth of layer 4C alpha and beta spiny stellate neurons. J Comp Neurol 309: 115–128Google Scholar
  43. Lund JS, Holbach SM, Chung WW (1991) Postnatal development of thalamic recipient neurons in the monkey striate cortex. II. Influence of afferent driving on spine acquisition and dendritic growth of layer 4C spiny stellate neurons. J Comp Neurol 309: 129–140Google Scholar
  44. Marin-Padilla M (1984) Neurons of layer I. A developmental analysis. In: Peters A, Jones EG (eds) Cerebral cortex, vol 1. Plenum Press, New York, pp 447–478Google Scholar
  45. Martin KAC, Whitteridge D (1984) Form, function and intracortical projections of spiny neurones in the striate visual cortex of the cat. J Physiol 353: 463–504Google Scholar
  46. Mates SL, Lund JS (1983a) Neuronal composition and development in lamina 4C of monkey striate cortex. J Comp Neurol 221: 60–90Google Scholar
  47. Mates SL, Lund JS (1983b) Spine formation and maturation of type 1 synapses on spiny stellate neurons in primate visual cortex. J Comp Neurol 221: 91–97Google Scholar
  48. Mates SL, Lund JS (1983c) Developmental changes in the relationship between type 2 synapses and spiny neurons in the monkey visual cortex. J Comp Neurol 221: 98–105Google Scholar
  49. Meyer G, Albus K (1981) Spiny stellates as cells of origin of association fibres from area 17 to area 18 in the cat's neocortex. Brain Res 210: 335–341Google Scholar
  50. Meyer G, Ferres-Torres R (1984) Postnatal maturation of nonpyramidal neurons in the visual cortex of the cat. J Comp Neurol 228: 226–244Google Scholar
  51. Morest DK (1969) The growth of dendrites in the mammalian brain. Z Anat Entwickl-Gesch 128: 290–317Google Scholar
  52. Morgane PJ, Glezer II, Jacobs MS (1990) Comparative and evolutionary anatomy of the visual cortex of the dolphin. In: Jones G, Peters A (eds) Cerebral cortex, vol 8B. Plenum, New York, pp 215–261Google Scholar
  53. Parks TN, Jackson H (1984) A developmental gradient of dendritic loss in the avian cochlear nucleus occurring independently of primary afferents. J Comp Neurol 227: 459–466Google Scholar
  54. Parnavelas JG, Barfield JA, Franke E, Luskin MB (1991) Separate progenitor cells give rise to pyramidal and non-pyramidal neurons in the rat telencephalon. Cereb Cortex 1: 463–468Google Scholar
  55. Peinado A, Katz LC (1990) Development of cortical spiny stellate cells: retraction of a transient apical dendrite. Soc Neurosci Abst 16: 1127Google Scholar
  56. Peters A, Payne BR, Josephson K (1990) Transcallosal non-pyramidal cell projections from visual cortex in the cat. J Comp Neurol 302: 124–142Google Scholar
  57. Purves D, Snider WD, Voyvodic JT (1988) Trophic regulation of nerve cell morphology and innervation in the autonomic nervous system. Nature 336: 123–128Google Scholar
  58. Ramoa AS, Campbell G, Shatz CJ (1988) Dendritic growth and remodeling of cat retinal ganglion cells during fetal and post-natal development. J Neurosci 8: 4239–4261Google Scholar
  59. Riederer BM, Guadano-Ferraz A, Innocenti GM (1990) Difference in distribution of microtubule-associated proteins 5a and 5b during the development of cerebral cortex and corpus callosum in cats: dependence on phosphorylation. Dev Brain Res 56: 235–243Google Scholar
  60. Saint Marie RL, Peters A (1985) The morphology and synaptic connections of spiny stellate neurons in monkey visual cortex (area 17): a Golgi-electron microscopic study. J Comp Neurol 233: 213–235Google Scholar
  61. Stanfield BB, O'Leary DDM, Fricks C (1982) Selective collateral elimination in early postnatal development restricts cortical distribution of rat pyramidal tract neurones. Nature 298: 371–373Google Scholar
  62. Valverde F (1983) A comparative approach to neocortical organization based on the study of the brain of the hedgehog (Erinaceus europaeus). In: Grisolia, Guerri, Samson, Norton, Reinoso-Suarez (eds) Ramón y Cajal's contribution to the neurosciences. Elsevier Science Amsterdam, pp 149–170Google Scholar
  63. Valverde F (1986) Intrinsic neocortical organization: some comparative aspects. Neuroscience 18: 1–23Google Scholar
  64. Voigt T, LeVay S, Stammes MA (1988) Morphological and immunocytochemical observations on the visual callosal projections in the cat. J Comp Neurol 272: 450–460Google Scholar
  65. Weisskopf M, Innocenti GM (1991) Neurons with callosal projections in visual areas of newborn kittens: an analysis of their dendritic phenotype with respect to the fate of the callosal axon and of its target. Exp Brain Res 86: 151–158Google Scholar
  66. White EL (1978) Identified neurons in mouse SmI cortex which are postsynaptic to thalamocortical axon terminals: a combined Golgi-electron microscopic and degeneration study. J Comp Neurol 181: 627–662Google Scholar
  67. Winfield DA (1981) The postnatal development of synapses in the visual cortex of the cat and the effects of eyelid closure. Brain Res 206: 166–171Google Scholar

Copyright information

© Springer-Verlag 1992

Authors and Affiliations

  • A. Vercelli
    • 1
  • F. Assal
    • 1
  • G. M. Innocenti
    • 1
  1. 1.Institut d'AnatomieLausanneSwitzerland

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