Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-8448b6f56d-dnltx Total loading time: 0 Render date: 2024-04-23T15:06:19.341Z Has data issue: false hasContentIssue false

5 - Olfactory Neurogenesis: A Window on Brain Development

from Section I - Neurology, Neurophysiology and Neuropsychology: Olfactory Clues to Brain Development and Disorder

Published online by Cambridge University Press:  17 August 2009

By
Françios Féron ,
Richard McCurdy ,
John McGrath  and
Alan Mackay-Sim
Edited by
Warrick J. Brewer ,
David Castle  and
Christos Pantelis
Foreword by
Peter Doherty
Warrick J. Brewer
Affiliation:
Mental Health Research Institute of Victoria, Melbourne
David Castle
Affiliation:
University of Melbourne
Christos Pantelis
Affiliation:
University of Melbourne
Get access

Summary

Introduction

It is understandable that members of the public are surprised to learn that a biopsy taken from inside the nose may be able to provide clues into neurological and psychiatric disorders. Those with the knowledge of the development of Freudian psychoanalysis may have a particular shudder of recognition at any project that links psychiatry with surgical procedures on the nose. Wilhelm Fliess (1858–1928) was a Berlin-based Ear, Nose and Throat specialist (oto-rhino-laryngologist), who was preoccupied with the influence of biological rhythms on health and disease. He also developed a bizarre theory linking the erectile tissue in the nose with sexuality. Sigmund Freud, the father of psychoanalysis, corresponded with Fliess over many years. They shared a belief that surgery on the nose could interrupt ‘reflex nasal neuroses’, and thus be an effective treatment for various neurotic disorders thought to be connected to sexuality. The details of this theory do not warrant further scrutiny apart from one incidence that became pivotal in the development of psychoanalysis. Freud had sent one of his most celebrated patients (Emma Eckstein) to Fliess for the nasal surgery as a treatment for her ‘psychological’ condition. In an act of gross negligence, Fleiss left a nasal pack in situ after the surgery and did not provide appropriate follow-up or after-care. After much suffering, another surgeon discovered the mistake, and the nasal pack was removed.

Keywords

adult olfactory epitheliumbrain developmentneurodevelopmental disorderolfactory neurogenesisschizophrenia
Type
Chapter
Information
Olfaction and the Brain , pp. 83 - 102
Publisher: Cambridge University Press
Print publication year: 2006

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

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, 433–57.Google Scholar
Altman, J. & Das, G. D. (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol, 124, 319–35.Google Scholar
Alvarez-Buylla, A. & Garcia-Verdugo, J. M. (2002) Neurogenesis in adult subventricular zone. J Neurosci, 22, 629–34.Google Scholar
Arnold, S. E., Han, L. Y., Moberg, P. J., et al. (2001) Dysregulation of olfactory receptor neuron lineage in schizophrenia. Arch Gen Psychiatry, 58, 829–35.Google Scholar
Asson-Batres, M. A., Zeng, M. S., Savchenko, V., et al. (2003) Vitamin A deficiency leads to increased cell proliferation in olfactory epithelium of mature rats. J Neurobiol, 54, 539–54.Google Scholar
Banasr, M., Hery, M., Printemps, R., et al. (2004) Serotonin-induced increases in adult cell proliferation and neurogenesis are mediated through different and common 5-HT receptor subtypes in the dentate gyrus and the subventricular zone. Neuropsychopharmacol, 29, 450–60.Google Scholar
Bassett, A. S., Hodgkinson, K., Chow, E. W., et al. (1998) 22q11 deletion syndrome in adults with schizophrenia. Am J Med Genet, 81, 328–37.Google Scholar
Bayer, S. A. (1983) 3H-thymidine-radiographic studies of neurogenesis in the rat olfactory bulb. Exp Brain Res, 50, 329–40.Google Scholar
Belvindrah, R., Rougon, G. & Chazal, G. (2002) Increased neurogenesis in adult mCD24-deficient mice. J Neurosci, 22, 3594–607.Google Scholar
Bernabeu, R. & Sharp, F. R. (2000) NMDA and AMPA/kainate glutamate receptors modulate dentate neurogenesis and CA3 synapsin-I in normal and ischemic hippocampus. J Cereb Blood Flow Metab, 20, 1669–80.Google Scholar
Bernier, P. J., Vinet, J., Cossette, M., et al. (2000) Characterization of the subventricular zone of the adult human brain: evidence for the involvement of Bcl-2. Neurosci Res, 37, 67–78.Google Scholar
Blackshaw, S. & Livesey, R. (2002) Applying genomics technologies to neural development. Curr Opin Neurobiol, 12, 110–14.Google Scholar
Bogerts, B. (1993) Recent advances in the neuropathology of schizophrenia. Schizophr Bull, 19, 431–45.Google Scholar
Bonfanti, L. & Theodosis, D. T. (1994) Expression of polysialylated neural cell adhesion molecule by proliferating cells in the subependymal layer of the adult rat, in its rostral extension and in the olfactory bulb. Neuroscience, 62, 291–305.Google Scholar
Brezun, J. M. & Daszuta, A. (1999) Depletion in serotonin decreases neurogenesis in the dentate gyrus and the subventricular zone of adult rats. Neuroscience, 89, 999–1002.Google Scholar
Caggiano, M., Kauer, J. S. & Hunter, D. D. (1994) Globose basal cells are neuronal progenitors in the olfactory epithelium: a lineage analysis using a replication-incompetent retrovirus. Neuron, 13, 339–52.Google Scholar
Cameron, H., Hazel, T. & Mckay, R. (1998) Regulation of neurogenesis by growth factors and neurotransmitters. J Neurobiol, 36, 287–306.Google Scholar
Carleton, A., Petreanu, L. T., Lansford, R., et al. (2003) Becoming a new neuron in the adult olfactory bulb. Nat Neurosci, 6, 507–18.Google Scholar
Carlson, C., Papolos, D., Pandita, R. K., et al. (1997) Molecular analysis of velo-cardio-facial syndrome patients with psychiatric disorders. Am J Hum Genet, 60, 851–9.Google Scholar
Cecchini, T., Ciaroni, S., Ferri, P., et al. (2003) Alpha-tocopherol, an exogenous factor of adult hippocampal neurogenesis regulation. J Neurosci Res, 73, 447–55.Google Scholar
Chazal, G., Durbec, P., Jankovski, A., et al. (2000) Consequences of neural cell adhesion molecule deficiency on cell migration in the rostral migratory stream of the mouse. J Neurosci, 20, 1446–57.Google Scholar
Chen, G., Rajkowska, G., Du, F., et al. (2000) Enhancement of hippocampal neurogenesis by lithium. J Neurochem, 75, 1729–34.Google Scholar
Chojnacki, A., Shimazaki, T., Gregg, C., et al. (2003) Glycoprotein 130 signaling regulates Notch1 expression and activation in the self-renewal of mammalian forebrain neural stem cells. J Neurosci, 23, 1730–41.Google Scholar
Ciaroni, S., Cecchini, T., Ferri, P., et al. (2002) Neural precursor proliferation and newborn cell survival in the adult rat dentate gyrus are affected by vitamin E deficiency. Neurosci Res, 44, 369–77.Google Scholar
Ciaroni, S., Cuppini, R., Cecchini, T., et al. (1999) Neurogenesis in the adult rat dentate gyrus is enhanced by vitamin E deficiency. J Comp Neurol, 411, 495–502.Google Scholar
Conover, J. C., Doetsch, F., Garcia-Verdugo, J. M., et al. (2000) Disruption of Eph/ephrin signaling affects migration and proliferation in the adult subventricular zone. Nat Neurosci, 3, 1091–7.Google Scholar
Cooper-Kuhn, C. M., Winkler, J. & Kuhn, H. G. (2004) Decreased neurogenesis after cholinergic forebrain lesion in the adult rat. J Neurosci Res, 77, 155–65.Google Scholar
Craig, C. G., Tropepe, V., Morshead, C. M., et al. (1996) In vivo growth factor expansion of endogenous subependymal neural precursor cell populations in the adult mouse brain. J Neurosci, 16, 2649–58.Google Scholar
Curtis, M. A., Penney, E. B., Pearson, A. G., et al. (2003) Increased cell proliferation and neurogenesis in the adult human Huntington's disease brain. Proc Natl Acad Sci USA, 100, 9023–7.Google Scholar
Doetsch, F. & Alvarez-Buylla, A. (1996) Network of tangential pathways for neuronal migration in adult mammalian brain. Proc Natl Acad Sci USA, 93, 14895–900.Google Scholar
Doetsch, F., Caille, I., Lim, D. A., et al. (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell, 97, 703–16.Google Scholar
Duman, R. S., Nakagawa, S. & Malberg, J. (2001) Regulation of adult neurogenesis by antidepressant treatment. Neuropsychopharmacology, 25, 836–44.Google Scholar
Engstrom, C., Linde, A. & Thilander, B. (1982) Craniofacial morphology and growth in the rat. Cephalometric analysis of the effects of a low calcium and vitamin D-deficient diet. J Anat, 134 (Pt 2), 299–314.Google Scholar
Enwere, E., Shingo, T., Gregg, C., et al. (2004) Aging results in reduced epidermal growth factor receptor signaling, diminished olfactory neurogenesis, and deficits in fine olfactory discrimination. J Neurosci, 24, 8354–65.Google Scholar
Eriksson, P. S., Perfilieva, E., Bjork-Eriksson, T., et al. (1998) Neurogenesis in the adult human hippocampus. Nat Med, 4, 1313–17.Google Scholar
Fananas, L., Moral, P. & Bertranpetit, J. (1990) Quantitative dermatoglyphics in schizophrenia: study of family history subgroups. Hum Biol, 62, 421–7.Google Scholar
Féron, F., Perry, C., Hirning, M., et al. (1999) Altered adhesion, proliferation and death in neural cultures from adults with schizophrenia. Schizophr Res, 40, 211–18.Google Scholar
Féron, F., Perry, C., McGrath, J. J., et al. (1998) New techniques for biopsy and culture of human olfactory epithelial neurons. Arch Otolaryngol Head Neck Surg, 124, 861–6.Google Scholar
Galli, R., Gritti, A., Bonfanti, L., et al. (2003) Neural stem cells: an overview. Circ Res, 92, 598–608.Google Scholar
Garcia-Verdugo, J. M., Doetsch, F., Wichterle, H., et al. (1998) Architecture and cell types of the adult subventricular zone: in search of the stem cells. J Neurobiol, 36, 234–48.Google Scholar
Gheusi, G., Cremer, H., McLean, H., et al. (2000) Importance of newly generated neurons in the adult olfactory bulb for odor discrimination. Proc Natl Acad Sci USA, 97, 1823–8.Google Scholar
Giachino, C., Galbiati, M., Fasolo, A., et al. (2003) Neurogenesis in the subependymal layer of the adult rat: a role for neuroactive derivatives of progesterone. Ann NY Acad Sci, 335–9.Google Scholar
Gleeson, J. G., Lin, P. T., Flanagan, L. A., et al. (1999) Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron, 23, 257–71.Google Scholar
Gothelf, D., Frisch, A., Munitz, H., et al. (1997) Velocardiofacial manifestations and microdeletions in schizophrenic inpatients. Am J Med Genet, 72, 455–61.Google Scholar
Gottesman, II & Gould, T. D. (2003) The endophenotype concept in psychiatry: etymology and strategic intentions. Am J Psychiatry, 160, 636–45.Google Scholar
Gould, E. (1999) Serotonin and hippocampal neurogenesis. Neuropsychopharmacology, 21, 46S–51S.Google Scholar
Graziadei, P. P. C. & Monti Graziadei, G. A. (1978) The olfactory system: a model for the study of neurogenesis and axon regeneration in mammals. In Neuronal Plasticity (ed Cotman, C. W.), pp. 131–53. New York: Raven Press.
Green, M. F., Satz, P. & Christenson, C. (1994) Minor physical anomalies in schizophrenia patients, bipolar patients, and their siblings. Schizophr Bull, 20, 433–40.Google Scholar
Gross, R. E., Mehler, M. F., Mabie, P. C., et al. (1996) Bone morphogenetic proteins promote astroglial lineage commitment by mammalian subventricular zone progenitor cells. Neuron, 17, 595–606.Google Scholar
Hack, I., Bancila, M., Loulier, K., et al. (2002) Reelin is a detachment signal in tangential chain-migration during postnatal neurogenesis. Nat Neurosci, 5, 939–45.Google Scholar
Hakak, Y., Walker, J. R., Li, C., et al. (2001) Genome-wide expression analysis reveals dysregulation of myelination-related genes in chronic schizophrenia. Proc Natl Acad Sci USA, 98, 4746–51.Google Scholar
Helm, J. W. & German, R. Z. (1996) The epigenetic impact of weaning on craniofacial morphology during growth. J Exp Zool, 276, 243–53.Google Scholar
Hitoshi, S., Alexson, T., Tropepe, V., et al. (2002) Notch pathway molecules are essential for the maintenance, but not the generation, of mammalian neural stem cells. Genes Dev, 16, 846–58.Google Scholar
Hoglinger, G. U., Rizk, P., Muriel, M. P., et al. (2004) Dopamine depletion impairs precursor cell proliferation in Parkinson disease. Nat Neurosci, 7, 726–35.Google Scholar
Hu, H. & Rutishauser, U. (1996) A septum-derived chemorepulsive factor for migrating olfactory interneuron precursors. Neuron, 16, 933–40.Google Scholar
Jin, K., Peel, A. L., Mao, X. O., et al. (2004) Increased hippocampal neurogenesis in Alzheimer's disease. Proc Natl Acad Sci USA, 101, 343–7.Google Scholar
Johansson, C. B., Svensson, M., Wallstedt, L., et al. (1999) Neural stem cells in the adult human brain. Exp Cell Res, 253, 733–6.Google Scholar
Jones, P. & Murray, R. M. (1991) The genetics of schizophrenia is the genetics of neurodevelopment. Br J Psychiatry, 158, 615–23.Google Scholar
Kaplan, M. S. & Hinds, J. W. (1977) Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science, 197, 1092–4.Google Scholar
Kilpatrick, T. J. & Bartlett, P. F. (1993) Cloning and growth of multipotential neural precursors: requirements for proliferation and differentiation. Neuron, 10, 255–65.Google Scholar
Kim, T. E., Lee, H. S., Lee, Y. B., et al. (2003) Sonic hedgehog and FGF8 collaborate to induce dopaminergic phenotypes in the Nurr1-overexpressing neural stem cell. Biochem Biophys Res Commun, 305, 1040–48.Google Scholar
Kornack, D. R. & Rakic, P. (2001) The generation, migration, and differentiation of olfactory neurons in the adult primate brain. Proc Natl Acad Sci USA, 98, 4752–7.Google Scholar
Kuhn, H. G., Winkler, J., Kempermann, G., et al. (1997) Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. J Neurosci, 17, 5820–29.Google Scholar
Kukekov, V. G., Laywell, E. D., Suslov, O., et al. (1999) Multipotent stem/progenitor cells with similar properties arise from two neurogenic regions of adult human brain. Exp Neurol, 156, 333–44.Google Scholar
Lane, A., Kinsella, A., Murphy, P., et al. (1997) The anthropometric assessment of dysmorphic features in schizophrenia as an index of its developmental origins. Psychol Med, 27, 1155–64.Google Scholar
Lawrie, S. M. & Abukmeil, S. S. (1998) Brain abnormality in schizophrenia. A systematic and quantitative review of volumetric magnetic resonance imaging studies. Br J Psychiatry, 172, 110–20.Google Scholar
Leopold, D. A., Hummel, T., Schwob, J. E., et al. (2000) Anterior distribution of human olfactory epithelium. Laryngoscope, 110, 417–21.Google Scholar
Lim, D. A., Tramontin, A. D., Trevejo, J. M., et al. (2000) Noggin antagonizes BMP signaling to create a niche for adult neurogenesis. Neuron, 28, 713–26.Google Scholar
Lipska, B. & Weinberger, D. (2003) Animal models of schizophrenia. In Schizophrenia (ed Hirsch, S. & Weinberger, D.), pp. 388–402. Oxford: Blackwell.
Liu, Z. & Martin, L. J. (2003) Olfactory bulb core is a rich source of neural progenitor and stem cells in adult rodent and human. J Comp Neurol, 459, 368–91.Google Scholar
Lois, C. & Alvarez-Buylla, A. (1994) Long-distance neuronal migration in the adult mammalian brain. Science, 264, 1145–8.Google Scholar
Lois, C., Garcia-Verdugo, J. M. & Alvarez-Buylla, A. (1996) Chain migration of neuronal precursors. Science, 271, 978–81.Google Scholar
Luskin, M. B. (1993) Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron, 11, 173–89.Google Scholar
Luskin, M. B. & Boone, M. S. (1994) Rate and pattern of migration of lineally-related olfactory bulb interneurons generated postnatally in the subventricular zone of the rat. Chem Senses, 19, 695–714.Google Scholar
Lyon, M., Barr, C. E., Cannon, T. D., et al. (1989) Fetal neural development and schizophrenia. Schizophr Bull, 15, 149–61.Google Scholar
MacDonald, K. P. A., Murrell, W. G., Bartlett, P. F., et al. (1996) FGF2 promotes neuronal differentiation in explant cultures of adult and embryonic mouse olfactory epithelium. J Neurosci Res, 44, 27–39.Google Scholar
Mackay-Sim, A. (2003) Neurogenesis in the adult olfactory neuroepithelium. In Handbook of Olfaction and Gustation (ed Doty, R.), pp. 93–113. New York: Marcel Dekker.
Mackay-Sim, A. & Chuah, M. (2000) Neurotrophic factors in the primary olfactory pathway. Prog Neurobiol, 62, 527–59.Google Scholar
Mahadik, S. P., Mukherjee, S., Wakade, C. G., et al. (1994) Decreased adhesiveness and altered cellular distribution of fibronectin in fibroblasts from schizophrenic patients. Psychiatry Res, 53, 87–97.Google Scholar
Mandairon, N., Sacquet, J., Jourdan, F., et al. (2006) Long-term fate and distribution of newborn cells in the adult mouse olfactory bulb: Influences of olfactory deprivation. Neuroscience, 141, 443–51.Google Scholar
Manji, H. K. & Duman, R. S. (2001) Impairments of neuroplasticity and cellular resilience in severe mood disorders: implications for the development of novel therapeutics. Psychopharmacol Bull, 35, 5–49.Google Scholar
Manji, H. K., Moore, G. J. & Chen, G. (2000) Clinical and preclinical evidence for the neurotrophic effects of mood stabilizers: implications for the pathophysiology and treatment of manic-depressive illness. Biol Psychiatry, 48, 740–54.Google Scholar
Mason, H. A., Ito, S. & Corfas, G. (2001) Extracellular signals that regulate the tangential migration of olfactory bulb neuronal precursors: inducers, inhibitors, and repellents. J Neurosci, 21, 7654–63.Google Scholar
McGrath, J., El-Saadi, O., Grim, V., et al. (2002) Minor physical anomalies and quantitative measures of the head and face in patients with psychosis. Arch Gen Psychiatry, 59, 458–64.Google Scholar
McGrath, J. & Murray, R. (2003) Risk factors for schizophrenia: from conception to birth. In Schizophrenia (eds Hirsch, S. & Weinberger, D. R.), pp. 232–50. Oxford: Blackwell.
McGrath, J. J., Feron, F. P., Burne, T. H., et al. (2003) The neurodevelopmental hypothesis of schizophrenia: a review of recent developments. Ann Med, 35, 86–93.Google Scholar
Mellor, C. S. (1992) Dermatoglyphic evidence of fluctuating asymmetry in schizophrenia. Br J Psychiatry, 160, 467–72.Google Scholar
Mercer, A., Ronnholm, H., Holmberg, J., et al. (2004) PACAP promotes neural stem cell proliferation in adult mouse brain. J Neurosci Res, 76, 205–15.Google Scholar
Miller, J. P. & German, R. Z. (1999) Protein malnutrition affects the growth trajectories of the craniofacial skeleton in rats. J Nutr, 129, 2061–9.Google Scholar
Mirnics, K., Middleton, F. A., Marquez, A., et al. (2000) Molecular characterization of schizophrenia viewed by microarray analysis of gene expression in prefrontal cortex. Neuron, 28, 53–67.Google Scholar
Miyamae, Y., Nakamura, Y., Kashiwagi, Y., et al. (1998) Altered adhesion efficiency and fibronectin content in fibroblasts from schizophrenic patients. Psychiatry Clin Neurosci, 52, 345–52.Google Scholar
Morshead, C. M., Reynolds, B. A., Craig, C. G., et al. (1994) Neural stem cells in adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells. Neuron, 13, 1071–82.Google Scholar
Murrell, W., Bushell, G. R., Livesey, J., et al. (1996) Neurogenesis in adult human. Neuroreport, 7, 1189–94.Google Scholar
Newman, M. P., Feron, F. & Mackay-Sim, A. (2000) Growth factor regulation of neurogenesis in adult olfactory epithelium. Neuroscience, 99, 343–50.Google Scholar
Nopoulos, P., Torres, I., Flaum, M., et al. (1995) Brain morphology in first-episode schizophrenia. Am J Psychiatry, 152, 1721–3.Google Scholar
Nunes, M. C., Roy, N. S., Keyoung, H. M., et al. (2003) Identification and isolation of multipotential neural progenitor cells from the subcortical white matter of the adult human brain. Nat Med, 9, 439–47.Google Scholar
Pagano, S. F., Impagnatiello, F., Girelli, M., et al. (2000) Isolation and characterization of neural stem cells from the adult human olfactory bulb. Stem Cells, 18, 295–300.Google Scholar
Pencea, V., Bingaman, K. D., Freedman, L. J., et al. (2001) Neurogenesis in the subventricular zone and rostral migratory stream of the neonatal and adult primate forebrain. Exp Neurol, 172, 1–16.Google Scholar
Peretto, P., Merighi, A., Fasolo, A., et al. (1999) The subependymal layer in rodents: a site of structural plasticity and cell migration in the adult mammalian brain. Brain Res Bull, 49, 221–43.Google Scholar
Perry, C., Mackay-Sim, A., Feron, F., et al. (2002) Olfactory neural cells: an untapped diagnostic and therapeutic resource. The 2000 Ogura Lecture. Laryngoscope, 112, 603–7.Google Scholar
Pincus, D. W., Harrison-Restelli, C., Barry, J., et al. (1997) In vitro neurogenesis by adult human epileptic temporal neocortex. Clin Neurosurg, 44, 17–25.Google Scholar
Pixley, S. K. (1992) The olfactory nerve contains two populations of glia, identified both in vivo and in vitro. Glia, 5, 269–84.Google Scholar
Reynolds, B. A. & Weiss, S. (1992) Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science, 255, 1707–10.Google Scholar
Richards, L. J., Kilpatrick, T. J. & Bartlett, P. F. (1992) De novo generation of neuronal cells from the adult mouse brain. Proc Natl Acad Sci USA, 89, 8591–5.Google Scholar
Ronnett, G. V., Leopold, D., Cai, X., et al. (2003) Olfactory biopsies demonstrate a defect in neuronal development in Rett's syndrome. Ann Neurol, 54, 206–18.Google Scholar
Rosa, A., Fananas, L., Bracha, H. S., et al. (2000) Congenital dermatoglyphic malformations and psychosis: a twin study. Am J Psychiatry, 157, 1511–13.Google Scholar
Rousselot, P., Lois, C. & Alvarez-Buylla, A. (1995) Embryonic (PSA) N-CAM reveals chains of migrating neuroblasts between the lateral ventricle and the olfactory bulb of adult mice. J Comp Neurol, 351, 51–61.Google Scholar
Roy, N. S., Wang, S., Jiang, L., et al. (2000) In vitro neurogenesis by progenitor cells isolated from the adult human hippocampus. Nat Med, 6, 271–7.Google Scholar
Saghatelyan, A., Chevigny, A., Schachner, M., et al. (2004) Tenascin-R mediates activity-dependent recruitment of neuroblasts in the adult mouse forebrain. Nat Neurosci, 7, 347–56.Google Scholar
Sanai, N., Tramontin, A. D., Quinones-Hinojosa, A., et al. (2004) Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature, 427, 740–44.Google Scholar
Shimazaki, T., Shingo, T. & Weiss, S. (2001) The ciliary neurotrophic factor/leukemia inhibitory factor/gp130 receptor complex operates in the maintenance of mammalian forebrain neural stem cells. J Neurosci, 21, 7642–53.Google Scholar
Shingo, T., Gregg, C., Enwere, E., et al. (2003) Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin. Science, 299, 117–20.Google Scholar
Shingo, T., Sorokan, S. T., Shimazaki, T., et al. (2001) Erythropoietin regulates the in vitro and in vivo production of neuronal progenitors by mammalian forebrain neural stem cells. J Neurosci, 21, 9733–43.Google Scholar
Shou, J., Rim, P. C. & Calof, A. L. (1999) BMPs inhibit neurogenesis by a mechanism involving degradation of a transcription factor. Nat Neurosci, 2, 339–45.Google Scholar
Sperber, G. (2001) Craniofacial Development. Hamilton, Ontario: Dekker.
Thorogood, P., Smith, L., Nicol, A., et al. (1982) Effects of vitamin A on the behaviour of migratory neural crest cells in vitro. J Cell Sci, 57, 331–50.Google Scholar
Turetsky, B. I., Moberg, P. J., Yousem, D. M., et al. (2000) Reduced olfactory bulb volume in patients with schizophrenia. Am J Psychiatry, 157, 828–30.Google Scholar
Os, J., Woodruff, P. W., Fananas, L., et al. (2000) Association between cerebral structural abnormalities and dermatoglyphic ridge counts in schizophrenia. Compr Psychiatry, 41, 380–84.Google Scholar
Vawter, M. P., Barrett, T., Cheadle, C., et al. (2001) Application of cDNA microarrays to examine gene expression differences in schizophrenia. Brain Res Bull, 55, 641–50.Google Scholar
Vescovi, A. L., Reynolds, B. A., Fraser, D. D., et al. (1993) bFGF regulates the proliferative fate of unipotent (neuronal) and bipotent (neuronal/astroglial) EGF-generated CNS progenitor cells. Neuron, 11, 951–66.Google Scholar
Waddington, J. L., Lane, A., Larkin, C., et al. (1999) The neurodevelopmental basis of schizophrenia: clinical clues from cerebro-craniofacial dysmorphogenesis, and the roots of a lifetime trajectory of disease. Biol Psychiatry, 46, 31–9.Google Scholar
Wagner, J. P., Black, I. B. & DiCicco-Bloom, E. (1999) Stimulation of neonatal and adult brain neurogenesis by subcutaneous injection of basic fibroblast growth factor. J Neurosci, 19, 6006–16.Google Scholar
Wakade, C. G., Mahadik, S. P., Waller, J. L., et al. (2002) Atypical neuroleptics stimulate neurogenesis in adult rat brain. J Neurosci Res, 69, 72–9.Google Scholar
Weinberger, D. (1995) Schizophrenia as a neurodevelopmental disorder. In Schizophrenia (ed Weinberger, D.), pp. 293–323. Oxford: Blackwell Science Ltd.
Weinberger, D. & Marenco, S. (2003) Schizophrenia as a neurodevelopmental disorder. In Schizophrenia (eds Hirsch, S. & Weinberger, D.), pp. 326–48. Oxford:Blackwell.
Wolozin, B., Lesch, P., Lebovics, R., et al. (1993) Olfactory neuroblasts from Alzheimer donors: studies on APP processing and cell regulation. Biol Psychiatry, 34, 824–38.Google Scholar
Wolozin, B., Sunderland, T., Zheng, B. B., et al. (1992) Continuous culture of neuronal cells from adult human olfactory epithelium. J Mol Neurosci, 3, 137–46.Google Scholar
Wright, I. C., Rabe-Hesketh, S., Woodruff, P. W., et al. (2000) Meta-analysis of regional brain volumes in schizophrenia. Am J Psychiatry, 157, 16–25.Google Scholar
Wu, W., Wong, K., Chen, J., et al. (1999) Directional guidance of neuronal migration in the olfactory system by the protein Slit. Nature, 400, 331–6.Google Scholar
Zaidel, D. W. (1999) Regional differentiation of neuron morphology in human left and right hippocampus: comparing normal to schizophrenia. Int J Psychophysiol, 34, 187–96.Google Scholar
Zucker, A. & Wiegand, D. (1988) Freud, Fliess, and the nasogenital reflex: did a look into the nose let us see the mind?Otolaryngol Head Neck Surg, 98, 319–22.Google Scholar

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×