Abstract
Development of the central olfactory system was studied in the rat with an electron microscope at three main structures: the olfactory bulb, the lateral olfactory tract, and the primary olfactory cortex (the piriform cortex). As a parameter of development, the synaptic density was examined quantitatively in the bulbar glomerulus and layer Ia (termination of bulbofugal fibers) of the piriform cortex, which are the key stations of the olfactory pathway. The synaptic densities in the glomerulus and those in layer Ia were 5.7% and 4.6% on embryonic day 19, 15.8% and 12.5% on postnatal day (P) 0, and 57.3% and 37.2% on P10, as compared with the adult (100%). As another parameter of development, the density of myelinated axons in the lateral olfactory tract was examined quantitatively. The densities of myelinated axons in the tract were 0% on P5, 15.1% on P10, and 73.5% on P21 of the adult density. Maturation in the tract was still progressing, even at P21, in terms of bundle formation and the thickness of myelin sheaths. The results show that synaptogenesis in the bulbar glomerulus is followed by synaptogenesis in layer Ia of the piriform cortex, and that myelination in the lateral olfactory tract occurs over a prolonged period, even in the stages after P21.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alberts JR, May B (1980) Ontogeny of olfaction: development of the rats' sensitivity to urine and amyl acetate. Physiol Behav 24:965–970
Altman J (1969) Autoradiographic and histological studies of postnatal neurogenesis. IV. Cell proliferation and migration in the anterior forebrain, with special reference to persisting neurogenesis in the olfactory bulb. J Comp Neurol 137:433–458
Bayer SA (1983) 3H-thymidine-radiographic studies of neurogenesis in the rat olfactory bulb. Exp Brain Res 50:329–340
Derer P, Caviness VS Jr, Sidman RL (1977) Early cortical histogenesis in the primary olfactory cortex of the mouse. Brain Res 123:27–40
Farbman AI (1991) Developmental neurobiology of the olfactory system. In: Getchell TV, Doty RL, Bartoshuk LM, Snow JB Jr (eds) Smell and taste in health and disease. Raven, New York, pp 19–33
Gesteland RC, Yancey RA, Farbman AI (1982) Development of olfactory receptor neuron selectivity in the rat fetus. Neuroscience 7:3127–3136
Graziadei PPC, Kaplan MS (1980) Regrowth of olfactory sensory axons into transplanted neural tissue. I. Development of connections with the occipital cortex. Brain Res 201:39–44
Graziadei PPC, Levine RR, Monti Graziadei GA (1978) Regeneration of olfactory axons and synapse formation in the forebrain after bulbectomy in neonatal mice. Proc Natl Acad Sci USA 75:5320–5324
Graziadei PPC, Levine RR, Monti Graziadei GA (1979) Regeneration into the forebrain following bulbectomy in the neonatal mouse. Neuroscience 4:713–727
Greer CA (1991) Structural organization of the olfactory system. In: Getchell TV, Doty RL, Bartoshuk LM, Snow JB Jr (eds) Smell and taste in health and disease. Raven, New York, pp 65–81
Greer CA, Stewart WB, Teicher MH, Shepherd GM (1982) Functional development of the olfactory bulb and a unique glomerular complex in the neonatal rat. J Neurosci 2:1744–1759
Gregory EW, Pfaff DW (1971) Development of olfactory guided behavior in infant rats. Physiol Behav 6:573–576
Haberly L, Behan M (1983) Structure of the piriform cortex of the opossum. III. Ultrastructural characterization of synaptic terminals of association and olfactory bulb afferent fibers. J Comp Neurol 219:448–460
Hinds JW, Hinds PL (1976) Synapse formation in the mouse olfactory bulb. I. Quantitative studies. J Comp Neurol 169:15–40
Hofer MA, Shair H, Singh P (1976) Evidence that maternal ventral skin substances promote suckling in infant rats. Physiol Behav 17:131–136
Hudson R, Distel H (1983) Nipple location by newborn rabbits: behavioral evidence for pheromonal guidance. Behavior 85:260–275
Jacobson S (1963) Sequence of myelinization in the brain of the albino rat. A. Cerebral cortex, thalamus and related structures. J Comp Neurol 121:5–29
Magrassi L, Graziadei PPC (1985) Interaction of the transplanted olfactory placode with the optic stalk and the diencephalon in Xenopus laevis embryos. Neuroscience 15:903–921
Mair RG, Gellman RL, Gesteland RC (1982) Postnatal proliferation and maturation of olfactory bulb neurons in the rat. Neuroscience 7:3105–3116
Mair RG, Gesteland RC (1982) Response properties of mitral cells in the olfactory bulb of the neonatal rat. Neuroscience 7:3117–3125
Pedersen PE, Stewart WB, Greer CA, Shepherd GM (1983) Evidence for olfactory function in utero. Science 221:478–480
Price JL (1973) An autoradiographic study of complementary laminar patterns of terminations of afferent fibers to the olfactory cortex. J Comp Neurol 150:87–108
Schwob JE, Haberly LB, Price JL (1984) The development of physiological responses of the piriform cortex in rats to stimulation of the lateral olfactory tract. J Comp Neurol 223:223–237
Stout RP, Graziadei PPC (1980) Influence of the olfactory placode on the development of the brain in Xenopus laevis (daudin). I. Axonal growth and connections of the transplanted olfactory placode. Neuroscience 5:2175–2186
Teicher MH, Blass EM (1975) Suckling in newborn rats: eliminated by nipple lavage, reinstated by pup saliva. Science 193:422–425
Teicher MH, Blass EM (1977) First suckling response of the newborn albino rat: the roles of olfaction and amniotic fluid. Science 198:635–636
Teicher MH, Stewart WB, Kauer JS, Shepherd GM (1980) Suckling pheromone stimulation of a modified glomerular region in the developing rat olfactory bulb revealed by the 2-deoxyglucose method. Brain Res 194:530–535
Westrum LE (1975) Electron microscopy of synaptic structures in olfactory cortex of early postnatal rats. J Neurocytol 4:713–732
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Moriizumi, T., Sakashita, H., Furukawa, M. et al. Electron microscopic study of synaptogenesis and myelination of the olfactory centers in developing rats. Exp Brain Res 103, 385–392 (1995). https://doi.org/10.1007/BF00241497
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00241497