Skip to main content
Log in

The development of major projections to the inferior olivary nucleus

Experimental studies using the North American opossum

  • Published:
Anatomy and Embryology Aims and scope Submit manuscript

Summary

We have employed degeneration techniques to study the ontogeny of major projections to the inferior olivary nucleus in the North American opossum, a species which is born 12 days after conception and which enjoys a protracted development in an external pouch. Subsequent to spinal lesions a small amount of axonal degeneration can be produced within the edge of the olive before subnuclei can be distinguished (7 days after birth, 24 mm, snout-rump length). Degenerating axons are present more deeply within the olive in animals operated 12 days after birth (30 mm, snout-rump length) and by at least day 16 (36 mm, snout-rump length), they are found in all of the regions they occupy in the adult animal. Subsequent to lesions which undercut all descending mesencephalic and diencephalic systems, a small amount of axonal degeneration is found at the dorsolateral edge of the olive by day 7 (23 mm, snout-rump length). Degenerating axons fill more of the olive, particularly caudally, after comparable lesions in older animals and by day 17 (38 mm, snout-rump length), degeneration is present in all of the olivary regions innervated by midbrain and thalamic axons in the adult opossum. There is some evidence that spinal, mesencephalic and diencephalic axons follow a caudal to rostral gradient in their intraolivary growth. Lesions which undercut neurites growing out of the cerebellum produce evidence for cerebello-olivary connections by day 17. Axons from the cerebral cortex reach their olivary targets considerably later than those from either the spinal cord, mesencephalon, diencephalon or cerebellum. It is not until approximately postnatal day 30 (55 mm, snout-rump length) that degenerating axons can be traced into the olive after lesions of the cortical mantle. These data indicate that the inferior olive receives major connections early in development and that there is an orderly sequence to their growth.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Altman J (1969) Postnatal development of the cerebellar cortex in the rat. II. Phases in the maturation of Purkinje cells and of the molecular layer. J Comp Neurol 145:399–464

    Google Scholar 

  • Altman J, Bayer SA (1978) Prenatal development of the cerebellar system in the rat. II. Cytogenesis and histogenesis of the inferior olive, pontine gray, and the precerebellar reticular nuclei. J Comp Neurol 179:49–76

    Google Scholar 

  • Armstrong DM (1974) Functional significance of connections of the inferior olive. Physiological Review 54:358–417

    Google Scholar 

  • Armstrong DM, Harvey RJ, Schild RF (1974) Topographical localization in the olivo-cerebellar projection: An electrophysiological study of the cat. J Comp Neurol 154:287–302

    Google Scholar 

  • Bowman MH, King JS (1973) The conformation, cytology and synaptology of the opossum inferior olivary nucleus. J Comp Neurol 148:491–524

    Google Scholar 

  • Bowman JP, Sladek JR (1973) Morphology of the inferior olivary complex of the rhesus monkey (Macaca mulatta). J Comp Neurol 152:299–316

    Google Scholar 

  • Bradley P, Berry M (1976) The effects of reduced climbing and parallel fibre input on Purkinje cell dendritic growth. Brain Res 109:133–151

    Google Scholar 

  • Brodal A (1940) Experimentelle Untersuchungen über die olivo-cerebellare Lokalisation. Z Ges Neurol u Psychiat 169:1–153 (1940)

    Google Scholar 

  • Brodal A (1976) The olivocerebellar projection in the cat studied with the method of retrograde axonal transport of horseradish peroxidase. II. The projection to the uvula. J Comp Neurol 166:417–426

    Google Scholar 

  • Brodal A, Walberg F (1977) The olivocerebellar projection in the cat studied with the method of retrograde axonal transport of horseradish peroxidase. IV. The projection to the anterior lobe. J Comp Neurol 172:85–108

    Google Scholar 

  • Cavalcante LA, Rocha-Miranda CE (1978) Postnatal development of retinogeniculate, retinopretectal and retinotectal projections in the opossum. Brain Res 146:231–248

    Google Scholar 

  • Cutts JH, Krause WJ, Leeson CR (1978) General observations on the growth and development of the pouch young opossum. Biol Neonate 33:264–272

    Google Scholar 

  • Fink RP, Heimer L (1967) Two methods of selective silver impregnation of degenerating axons and their synaptic endings in the central nervous systems. Brain Res 4:369–374

    Google Scholar 

  • Gilbert M, Stelzner DJ (1979) The development of descending and dorsal root connections in the lumbosacral spinal cord of the postnatal rat. J Comp Neurol 184:821–838

    Google Scholar 

  • Gwyn DG, Nicholson GP, Flumerfelt BA (1977) The inferior olivary nucleus of the rat: A light and electron microscopy study. J Comp Neurol 174:489–520

    Google Scholar 

  • Hartman CG (1952) Possums. University of Texas, Austin

    Google Scholar 

  • King JS (1976) The synaptic cluster (glomerulus) in the inferior olivary nucleus. J Comp Neurol 165:387–400

    Google Scholar 

  • King JS, Maley BE, Martin GF (1979) The ontogeny of the inferior olivary complex in the opossum. Society for Neuroscience Abstracts 5:101

    Google Scholar 

  • Kooy FH (1917) The inferior olive in vertebrates. Folia Neurobiol 10:205–369

    Google Scholar 

  • Land PW, Lund RD (1979) Development of the rats uncrossed retinotectal pathway and its relation to plasticity studies. Science 205:698–700

    Google Scholar 

  • Leonard CM (1973) A method for assessing stages of neuronal maturation. Brain Res 53:412–416

    Google Scholar 

  • Leonard CM (1974) Degeneration argyrophilia as an index of neuronal maturation: Studies on the optic tract of the Golden Hamster. J Comp Neurol 156:435–459

    Google Scholar 

  • Leonard CM (1975) Developmental changes in olfactory bulb projections revealed by degeneration argyrophilia. J Comp Neurol 162:467–486

    Google Scholar 

  • Linauts M, Martin GF (1978a) An autoradiographic study of midbrain-diencephalic projections to the inferior olivary nucleus in the opossum (Didelphis virginiana). J Comp Neurol 179:325–354

    Google Scholar 

  • Linauts M, Martin GF (1978b) The organization of olivo-cerebellar projections in the opossum, Didelphis virginiana, as revealed by the retrograde transport of horseradish peroxidase. J Comp Neurol 179:355–382

    Google Scholar 

  • Llinas R, Walton R, Hillman DE (1975) Inferior olive: Its role in motor learning. Science 190: 1230–1231

    Google Scholar 

  • Martin GF, Dom R, King JS, RoBards M, Watson CRR (1975) The inferior olivary nucleus of the opossum (Didelphis marsupialis virginiana), its organization and connections. J Comp Neurol 160:507–534

    Google Scholar 

  • Martin GF, Henkel CK, King JS (1976) Cerebello-olivary fibers: Their origin, course and distribution in the North American opossum. Exp Brain Res 24:219–236

    Google Scholar 

  • Martin GF, Beals JK, Culberson JL, Dom R, Goode G, Humbertson AO (1978) Observations on the development of brainstem-spinal systems in the North American opossum. J Comp Neurol 181:271–290

    Google Scholar 

  • Martin GF, Culberson J, Laxson C, Linauts M, Panneton M, Tschismadia I (1980) Afferent connections of the inferior olivary nucleus with preliminary notes on their development. Studies using the North American opossum. In: J Courville, Y Lamarre and C de Montigay (eds) The Inferior Olivary Nucleus-Anatomy and Physiology. Raven Press, New York

    Google Scholar 

  • McCrady E (1938) The embryology of the opossum. Amer Anat Memoirs, No. 16, The Wistar Institute of Anatomy and Biology, Philadelphia, Pennsylvania

    Google Scholar 

  • Oswaldo-Cruz E, Rocha-Miranda CE (1968) The brain of the opossum (Didelphis marsupialis). Instituto de Biofisica, Universidade Federal do Rio de Janeiro, Rio de Janeiro pp. 99

    Google Scholar 

  • Ramon y Cajal S (1960) Studies on Vertebrate Neurogenesis. Translated by L Guth. Thomas, Springfield, Illinois

    Google Scholar 

  • Robertson LT, Stotler WA (1974) The structure and connections of the developing inferior olivary nucleus of the rhesus monkey. J Comp Neurol 158:167–170

    Google Scholar 

  • Schneider GE (1969) Two visual systems. Science 163:895–902

    Google Scholar 

  • Watson CRR, Herron P (1977) The inferior olivary complex of marsupials. J Comp Neurol 176:527–538

    Google Scholar 

  • West MJ, del Cerro M (1976) Early formation of synapses in the molecular layer of the fetal rat cerebellum. J Comp Neurol 165:137–160

    Google Scholar 

  • Wise SP, Hendry SHC, Jones EG (1977) Prenatal development of sensorimotor cortical projections in cats. Brain Res 138:538–544

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

This investigation was supported by U.S.P.H.S. Grants NS-07410 and NS-08798 and The West Virginia University Medical Corporation.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Martin, G.F., Culberson, J.L. & Tschismadia, I. The development of major projections to the inferior olivary nucleus. Anat Embryol 160, 187–202 (1980). https://doi.org/10.1007/BF00301860

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00301860

Key words

Navigation