Olfactory experience modulated apoptosis in the developing olfactory bulb.

Early sensory stimulation plays a key role in shaping the structure and function of the developing olfactory system. Here, we provide the first direct evidence for apoptotic cell death in the olfactory bulbs of rat pups during normal development and we also demonstrate that olfactory deprivation by unilateral naris occlusion causes a dramatic increase in apoptotic cell death in the glomerular and granule cell layers of the deprived bulb. The accessory olfactory bulbs displayed a remarkably high basal level of apoptosis but the occluded accessory bulb did not differ in that regard from the control accessory bulb. These results suggest that apoptosis may be an important mechanism by which the olfactory system can adjust its cell numbers in response in sensory stimuli experienced in early life, thereby underlying one form of plasticity in the developing olfactory system.

[1]  M. Leon,et al.  Olfactory deprivation increases dopamine D2 receptor density in the rat olfactory bulb , 1991, Synapse.

[2]  P. Brunjes,et al.  Unilateral odor deprivation: Early postnatal changes in olfactory bulb cell density and number , 1988, The Journal of comparative neurology.

[3]  H. Baker Unilateral, neonatal olfactory deprivation alters tyrosine hydroxylase expression but not aromatic amino acid decarboxylase or gaba immunoreactivity , 1990, Neuroscience.

[4]  K. Szabó,et al.  Developmental studies on the rat vomeronasal organ: vascular pattern and neuroepithelial differentiation. I. Light microscopy. , 1988, Brain research.

[5]  Peter C. Brunjes,et al.  Unilateral naris closure and olfactory system development , 1994, Brain Research Reviews.

[6]  E. Rubel,et al.  Afferent regulation of neurons in the brain stem auditory system. , 1990, Journal of neurobiology.

[7]  J. Hinds Autoradiographic study of histogenesis in the mouse olfactory bulb. II. Cell proliferation and migration , 1968, The Journal of comparative neurology.

[8]  R. Oppenheim Cell death during development of the nervous system. , 1991, Annual review of neuroscience.

[9]  D. Wilson,et al.  Functional consequences of unilateral olfactory deprivation: Time-course and age sensitivity , 1992, Neuroscience.

[10]  P. Brunjes,et al.  Early postnatal cellular proliferation and survival in the olfactory bulb and rostral migratory stream of normal and unilaterally odor‐deprived rats , 1989, The Journal of comparative neurology.

[11]  A. Wyllie,et al.  Apoptosis: A Basic Biological Phenomenon with Wide-ranging Implications in Tissue Kinetics , 1972, British Journal of Cancer.

[12]  L. Rosselli-Austin,et al.  Enriched neonatal odor exposure leads to increased numbers of olfactory bulb mitral and granule cells. , 1990, Brain research. Developmental brain research.

[13]  D. Korol,et al.  Rapid changes in 2-deoxyglucose uptake and amino acid incorporation following unilateral odor deprivation: a laminar analysis. , 1990, Brain research. Developmental brain research.

[14]  Esmail Meisami,et al.  Neural growth and differentiation , 1979 .

[15]  D. Bredesen,et al.  bcl-2 inhibits death of central neural cells induced by multiple agents. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[16]  Gwyn T. Williams,et al.  Molecular regulation of apoptosis: Genetic controls on cell death , 1993, Cell.

[17]  T. Deckwerth,et al.  Molecular mechanisms of developmental neuronal death. , 1993, Annual review of neuroscience.

[18]  P. Brennan,et al.  Olfactory recognition: a simple memory system. , 1990, Science.

[19]  M. Leon,et al.  Early unilateral deprivation modifies olfactory bulb function , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  A. Davies,et al.  The proto-oncogene bcl-2 can selectively rescue neurotrophic factor-dependent neurons from apoptosis , 1993, Cell.

[21]  M. Leon,et al.  Increase in a focal population of juxtaglomerular cells in the olfactory bulb associated with early learning , 1991, The Journal of comparative neurology.

[22]  S. Korsmeyer,et al.  bcl-2 protein expression is widespread in the developing nervous system and retained in the adult PNS. , 1994, Development.

[23]  H A Quigley,et al.  Retinal ganglion cell loss is size dependent in experimental glaucoma. , 1991, Investigative ophthalmology & visual science.

[24]  T. Benson,et al.  Effects of sensory deprivation on the developing mouse olfactory system: a light and electron microscopic, morphometric analysis , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  E. Meisami,et al.  Lasting effects of early olfactory deprivation on the growth, DNA, RNA and protein content, and Na-K-ATPase and AchE activity of the rat olfactory bulb. , 1981, Brain research.

[26]  E. Meisami,et al.  Early olfactory deprivation and the mitral cells of the olfactory bulb: A Golgi study , 1986, International Journal of Developmental Neuroscience.

[27]  Esmail Meisami,et al.  A quantitative study of the effects of early unilateral olfactory deprivation on the number and distribution of mitral and tufted cells and of glomeruli in the rat olfactory bulb , 1981, Brain Research.

[28]  D. Durham,et al.  Rapid increase in mitochondrial volume in nucleus magnocellularis neurons following cochlea removal , 1994, The Journal of comparative neurology.

[29]  D. Bredesen,et al.  Bcl-2 inhibition of neural death: decreased generation of reactive oxygen species. , 1993, Science.

[30]  B. Barres,et al.  Programmed cell death and the control of cell survival: lessons from the nervous system. , 1993, Science.

[31]  D. Hubel,et al.  The development of ocular dominance columns in normal and visually deprived monkeys , 1980, The Journal of comparative neurology.

[32]  G. Shepherd,et al.  Evidence for olfactory function in utero. , 1983, Science.

[33]  P. Brunjes,et al.  Early postnatal differentiation of granule cell dendrites in the olfactory bulbs of normal and unilaterally odor-deprived rats. , 1989, Brain research. Developmental brain research.

[34]  D. Vaux Toward an understanding of the molecular mechanisms of physiological cell death. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[35]  M. Raff Cell death genes: Drosophila enters the field. , 1994, Science.

[36]  T. Woolsey,et al.  Somatosensory Cortex: Structural Alterations following Early Injury to Sense Organs , 1973, Science.

[37]  J. Martinou,et al.  Prevention of programmed cell death of sympathetic neurons by the bcl-2 proto-oncogene. , 1992, Science.

[38]  A. Farbman,et al.  Ablation of the olfactory bulb up-regulates the rate of neurogenesis and induces precocious cell death in olfactory epithelium , 1992, Experimental Neurology.

[39]  P. Brunjes,et al.  Maturation and plasticity in the olfactory system of vertebrates , 1986, Brain Research Reviews.

[40]  L. David Tomei,et al.  Apoptosis: The Molecular Basis of Cell Death , 1991 .

[41]  P. Brunjes Unilateral odor deprivation: Time course of changes in laminar volume , 1985, Brain Research Bulletin.

[42]  A. Riesen THE DEVELOPMENTAL NEUROPSYCHOLOGY OF SENSORY DEPRIVATION , 1977 .

[43]  J. Altman 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 , 1969, The Journal of comparative neurology.

[44]  Z. Oltvai,et al.  Bcl-2 functions in an antioxidant pathway to prevent apoptosis , 1993, Cell.

[45]  E. Meisami Effects of olfactory deprivation on postnatal growth of the rat olfactory bulb utilizing a new method for production of neonatal unilateral anosmia , 1976, Brain Research.

[46]  H. Horvitz,et al.  Mechanisms and functions of cell death. , 1991, Annual review of cell biology.

[47]  S. Ben‐Sasson,et al.  Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation , 1992, The Journal of cell biology.