Skip to main content
Top
Published in: Journal of Neural Transmission 1/2013

Open Access 01-01-2013 | Basic Neurosciences, Genetics and Immunology - Original Article

Increased cell proliferation in the rat anterior cingulate cortex following neonatal hypoxia: relevance to schizophrenia

Authors: Evelin L. Schaeffer, Franziska Kühn, Angelika Schmitt, Wagner F. Gattaz, Oliver Gruber, Thomas Schneider-Axmann, Peter Falkai, Andrea Schmitt

Published in: Journal of Neural Transmission | Issue 1/2013

Login to get access

Abstract

As a consequence of obstetric complications, neonatal hypoxia has been discussed as an environmental factor in the pathophysiology of schizophrenia. However, the biological consequences of hypoxia are unclear. The neurodevelopmental hypothesis of schizophrenia suggests that the onset of abnormal brain development and neuropathology occurs perinatally, whereas symptoms of the disease appear in early adulthood. In our animal model of chronic neonatal hypoxia, we have detected behavioral alterations resembling those known from schizophrenia. Disturbances in cell proliferation possibly contribute to the pathophysiology of this disease. In the present study, we used postnatal rats to investigate cell proliferation in several brain areas following neonatal hypoxia. Rats were repeatedly exposed to hypoxia (89 % N2, 11 % O2) from postnatal day (PD) 4–8. We then evaluated cell proliferation on PD 13 and 39, respectively. These investigations were performed in the anterior cingulate cortex (ACC), caudate-putamen (CPU), dentate gyrus, and subventricular zone. Rats exposed to hypoxia exhibited increased cell proliferation in the ACC at PD 13, normalizing at PD 39. In other brain regions, no alterations have been detected. Additionally, hypoxia-treated rats showed decreased CPU volume at PD 13. The results of the present study on the one hand support the assumption of chronic hypoxia influencing transient cell proliferation in the ACC, and on the other hand reveal normalization during ageing.
Literature
go back to reference Altman J, Bayer SA (1990) Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods. J Comp Neurol 301:365–381PubMedCrossRef Altman J, Bayer SA (1990) Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods. J Comp Neurol 301:365–381PubMedCrossRef
go back to reference Asami T, Bouix S, Whitford TJ, Shenton ME, Salisbury DF, McCarley RW (2012) Longitudinal loss of gray matter volume in patients with first-episode schizophrenia: DARTEL automated analysis and ROI validation. Neuroimage 59:986–996PubMedCrossRef Asami T, Bouix S, Whitford TJ, Shenton ME, Salisbury DF, McCarley RW (2012) Longitudinal loss of gray matter volume in patients with first-episode schizophrenia: DARTEL automated analysis and ROI validation. Neuroimage 59:986–996PubMedCrossRef
go back to reference Becker A, Peters B, Schroeder H, Mann T, Huether G, Grecksch G (2003) Ketamine-induced changes in rat behaviour: a possible animal model of schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry 27:687–700PubMedCrossRef Becker A, Peters B, Schroeder H, Mann T, Huether G, Grecksch G (2003) Ketamine-induced changes in rat behaviour: a possible animal model of schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry 27:687–700PubMedCrossRef
go back to reference Bédard A, Parent A (2004) Evidence of newly generated neurons in the human olfactory bulb. Brain Res Dev Brain Res 151:159–168PubMedCrossRef Bédard A, Parent A (2004) Evidence of newly generated neurons in the human olfactory bulb. Brain Res Dev Brain Res 151:159–168PubMedCrossRef
go back to reference Benes FM, Bird ED (1987) An analysis of the arrangement of neurons in the cingulate cortex of schizophrenic patients. Arch Gen Psychiatry 44(7):608–616 Benes FM, Bird ED (1987) An analysis of the arrangement of neurons in the cingulate cortex of schizophrenic patients. Arch Gen Psychiatry 44(7):608–616
go back to reference Benes FM, Davidson J, Bird ED (1986) Quantitative cytoarchitectural studies of the cerebral cortex of schizophrenics. Arch Gen Psychiatry 43(1):31–35 Benes FM, Davidson J, Bird ED (1986) Quantitative cytoarchitectural studies of the cerebral cortex of schizophrenics. Arch Gen Psychiatry 43(1):31–35
go back to reference Bernstein HG, Becker A, Keilhoff G, Spilker C, Gorczyca A, Braunewell KH et al (2003) Brain region-specific changes in the expression of calcium sensor proteins after repeated application of ketamine to rats. Neurosci Lett 339:95–98PubMedCrossRef Bernstein HG, Becker A, Keilhoff G, Spilker C, Gorczyca A, Braunewell KH et al (2003) Brain region-specific changes in the expression of calcium sensor proteins after repeated application of ketamine to rats. Neurosci Lett 339:95–98PubMedCrossRef
go back to reference Blaise SA, Nédélec E, Alberto JM, Schroeder H, Audonnet S, Bossenmeyer-Pourié C, Guéant JL, Daval JL (2009) Short hypoxia could attenuate the adverse effects of hyperhomocysteinemia on the developing rat brain by inducing neurogenesis. Exp Neurol 216:231–238PubMedCrossRef Blaise SA, Nédélec E, Alberto JM, Schroeder H, Audonnet S, Bossenmeyer-Pourié C, Guéant JL, Daval JL (2009) Short hypoxia could attenuate the adverse effects of hyperhomocysteinemia on the developing rat brain by inducing neurogenesis. Exp Neurol 216:231–238PubMedCrossRef
go back to reference Braff DL, Grillon C, Geyer MA (1992) Gating and habituation of the startle reflex in schizophrenic patients. Arch Gen Psychiatry 49:206–215PubMedCrossRef Braff DL, Grillon C, Geyer MA (1992) Gating and habituation of the startle reflex in schizophrenic patients. Arch Gen Psychiatry 49:206–215PubMedCrossRef
go back to reference Burns KA, Ayoub AE, Breunig JJ et al (2007) Nestin-CreER mice reveal DNA synthesis by nonapoptotic neurons following cerebral ischemia–hypoxia. Cereb Cortex 17:2585–2592PubMedCrossRef Burns KA, Ayoub AE, Breunig JJ et al (2007) Nestin-CreER mice reveal DNA synthesis by nonapoptotic neurons following cerebral ischemia–hypoxia. Cereb Cortex 17:2585–2592PubMedCrossRef
go back to reference Cannon TD, Rosso IM, Bearden CE, Sanchez LE, Hadley T (1999) A prospective cohort study of neurodevelopmental processes in the genesis and epigenesis of schizophrenia. Dev Psychopathol 11:467–485PubMedCrossRef Cannon TD, Rosso IM, Bearden CE, Sanchez LE, Hadley T (1999) A prospective cohort study of neurodevelopmental processes in the genesis and epigenesis of schizophrenia. Dev Psychopathol 11:467–485PubMedCrossRef
go back to reference Cannon TD, Van Erp TG, Rosso IM, Huttunen M, Lonnqvist J, Pirkola T, Salonen O, Valanne L, Poutanen VP, Standertskjold-Nordenstam CG (2002) Fetal hypoxia and structural brain abnormalities in schizophrenic patients, their siblings, and controls. Arch Gen Psychiatry 59:35–41PubMedCrossRef Cannon TD, Van Erp TG, Rosso IM, Huttunen M, Lonnqvist J, Pirkola T, Salonen O, Valanne L, Poutanen VP, Standertskjold-Nordenstam CG (2002) Fetal hypoxia and structural brain abnormalities in schizophrenic patients, their siblings, and controls. Arch Gen Psychiatry 59:35–41PubMedCrossRef
go back to reference Chua SE, Cheung C, Cheung V, Tsang JT, Chen EY, Wong JC, Cheung JP, Yip L, Tai KS, Suckling J, McAlonan GM (2007) Cerebral grey, white matter and CSF in never-medicated, first-episode schizophrenia. Schizophr Res 89:12–21PubMedCrossRef Chua SE, Cheung C, Cheung V, Tsang JT, Chen EY, Wong JC, Cheung JP, Yip L, Tai KS, Suckling J, McAlonan GM (2007) Cerebral grey, white matter and CSF in never-medicated, first-episode schizophrenia. Schizophr Res 89:12–21PubMedCrossRef
go back to reference Corson PW, Nopoulos P, Andreasen NC, Heckel D, Arndt S (1999) Caudate size in first-episode neuroleptic-naive schizophrenic patients measured using an artificial neural network. Biol Psychiatry 46:712–720PubMedCrossRef Corson PW, Nopoulos P, Andreasen NC, Heckel D, Arndt S (1999) Caudate size in first-episode neuroleptic-naive schizophrenic patients measured using an artificial neural network. Biol Psychiatry 46:712–720PubMedCrossRef
go back to reference Dalman C, Thomas HV, David AS, Gentz J, Lewis G, Allebeck P (2001) Signs of asphyxia at birth and risk of schizophrenia. Population-based case-control study. Br J Psychiatry 179:403–408PubMedCrossRef Dalman C, Thomas HV, David AS, Gentz J, Lewis G, Allebeck P (2001) Signs of asphyxia at birth and risk of schizophrenia. Population-based case-control study. Br J Psychiatry 179:403–408PubMedCrossRef
go back to reference Daval JL, Pourié G, Grojean S, Lièvre V, Strazielle C, Blaise S, Vert P (2004) Neonatal hypoxia triggers transient apoptosis followed by neurogenesis in the rat CA1 hippocampus. Pediatr Res 55:561–567PubMedCrossRef Daval JL, Pourié G, Grojean S, Lièvre V, Strazielle C, Blaise S, Vert P (2004) Neonatal hypoxia triggers transient apoptosis followed by neurogenesis in the rat CA1 hippocampus. Pediatr Res 55:561–567PubMedCrossRef
go back to reference Ehninger D, Kempermann G (2008) Neurogenesis in the adult hippocampus. Cell Tissue Res 331:243–250PubMedCrossRef Ehninger D, Kempermann G (2008) Neurogenesis in the adult hippocampus. Cell Tissue Res 331:243–250PubMedCrossRef
go back to reference Fagel DM, Ganat Y, Silbereis J, Ebbitt T, Stewart W, Zhang H, Ment LR, Vaccarino FM (2006) Cortical neurogenesis enhanced by chronic perinatal hypoxia. Exp Neurol 199:77–91PubMedCrossRef Fagel DM, Ganat Y, Silbereis J, Ebbitt T, Stewart W, Zhang H, Ment LR, Vaccarino FM (2006) Cortical neurogenesis enhanced by chronic perinatal hypoxia. Exp Neurol 199:77–91PubMedCrossRef
go back to reference Fendt M, Lex A, Falkai P, Henn FA, Schmitt A (2008) Behavioural alterations in rats following neonatal hypoxia and effects of clozapine: implications for schizophrenia. Pharmacopsychiatry 41:138–145PubMedCrossRef Fendt M, Lex A, Falkai P, Henn FA, Schmitt A (2008) Behavioural alterations in rats following neonatal hypoxia and effects of clozapine: implications for schizophrenia. Pharmacopsychiatry 41:138–145PubMedCrossRef
go back to reference Fornito A, Yücel M, Wood SJ, Adamson C, Velakoulis D, Saling MM, McGorry PD, Pantelis C (2008) Surface-based morphometry of the anterior cingulate cortex in first episode schizophrenia. Hum Brain Mapp 29:478–489PubMedCrossRef Fornito A, Yücel M, Wood SJ, Adamson C, Velakoulis D, Saling MM, McGorry PD, Pantelis C (2008) Surface-based morphometry of the anterior cingulate cortex in first episode schizophrenia. Hum Brain Mapp 29:478–489PubMedCrossRef
go back to reference Glenthoj A, Glenthoj BY, Mackeprang T, Pagsberg AK, Hemmingsen RP, Jernigan TL, Baaré WF (2007) Basal ganglia volumes in drug-naive first-episode schizophrenia patients before and after short-term treatment with either a typical or an atypical antipsychotic drug. Psychiatry Res 154:199–208PubMedCrossRef Glenthoj A, Glenthoj BY, Mackeprang T, Pagsberg AK, Hemmingsen RP, Jernigan TL, Baaré WF (2007) Basal ganglia volumes in drug-naive first-episode schizophrenia patients before and after short-term treatment with either a typical or an atypical antipsychotic drug. Psychiatry Res 154:199–208PubMedCrossRef
go back to reference Gould E, Reeves AJ, Graziano MS, Gross CG (1999) Neurogenesis in the neocortex of adult primates. Science 286:548–552PubMedCrossRef Gould E, Reeves AJ, Graziano MS, Gross CG (1999) Neurogenesis in the neocortex of adult primates. Science 286:548–552PubMedCrossRef
go back to reference Gratzner HG (1982) Monoclonal antibody to 5-bromo- and 5-iododeoxyuridine: a new reagent for detection of DNA replication. Science 218:474–475PubMedCrossRef Gratzner HG (1982) Monoclonal antibody to 5-bromo- and 5-iododeoxyuridine: a new reagent for detection of DNA replication. Science 218:474–475PubMedCrossRef
go back to reference Gundersen HJ, Bagger P, Bendtsen TF et al (1988) The new stereological tools: disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. APMIS 96:857–881PubMedCrossRef Gundersen HJ, Bagger P, Bendtsen TF et al (1988) The new stereological tools: disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. APMIS 96:857–881PubMedCrossRef
go back to reference Ikonomidou C, Mosinger JL, Salles KS, Labruyere J, Olney JW (1989) Sensitivity of the developing rat brain to hypobaric/ischemic damage parallels sensitivity to N-methyl-aspartate neurotoxicity. J Neurosci 9:2809–2818PubMed Ikonomidou C, Mosinger JL, Salles KS, Labruyere J, Olney JW (1989) Sensitivity of the developing rat brain to hypobaric/ischemic damage parallels sensitivity to N-methyl-aspartate neurotoxicity. J Neurosci 9:2809–2818PubMed
go back to reference Jayatissa MN, Henningsen K, Nikoajsen G et al (2010) A reduced number of hippocampal granule cells does not associate with an anhedonia-like phenotype in a rat chronic stress model of depression. Stress 13:95–105PubMedCrossRef Jayatissa MN, Henningsen K, Nikoajsen G et al (2010) A reduced number of hippocampal granule cells does not associate with an anhedonia-like phenotype in a rat chronic stress model of depression. Stress 13:95–105PubMedCrossRef
go back to reference Job DE, Whalley HC, McConnell S, Glabus M, Johnstone EC, Lawrie SM (2002) Structural gray matter differences between first-episode schizophrenics and normal controls using voxel-based morphometry. Neuroimage 17:880–889PubMedCrossRef Job DE, Whalley HC, McConnell S, Glabus M, Johnstone EC, Lawrie SM (2002) Structural gray matter differences between first-episode schizophrenics and normal controls using voxel-based morphometry. Neuroimage 17:880–889PubMedCrossRef
go back to reference Kaspárek T, Prikryl R, Mikl M, Schwarz D, Cesková E, Krupa P (2007) Prefrontal but not temporal grey matter changes in males with first-episode schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry 31:151–157PubMedCrossRef Kaspárek T, Prikryl R, Mikl M, Schwarz D, Cesková E, Krupa P (2007) Prefrontal but not temporal grey matter changes in males with first-episode schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry 31:151–157PubMedCrossRef
go back to reference Katchanow J, Harms C, Gertz K et al (2001) Mild cerebral ischemia induces loss of cyclin-dependent kinase inhibitors and activation of cell cycle machinery before delayed neuronal cell death. J Neuroscience 21:5045–5053 Katchanow J, Harms C, Gertz K et al (2001) Mild cerebral ischemia induces loss of cyclin-dependent kinase inhibitors and activation of cell cycle machinery before delayed neuronal cell death. J Neuroscience 21:5045–5053
go back to reference Keilhoff G, Becker A, Grecksch G, Wolf G, Bernstein HG (2004a) Repeated application of ketamine to rats induces changes in the hippocampal expression of parvalbumin, nNOS and cFOS similar to those found in human schizophrenia. Neuroscience 126:591–598PubMedCrossRef Keilhoff G, Becker A, Grecksch G, Wolf G, Bernstein HG (2004a) Repeated application of ketamine to rats induces changes in the hippocampal expression of parvalbumin, nNOS and cFOS similar to those found in human schizophrenia. Neuroscience 126:591–598PubMedCrossRef
go back to reference Keilhoff G, Bernstein HG, Becker A, Grecksch G, Wolf G (2004b) Increased neurogenesis in a rat ketamine model of schizophrenia. Biol Psychiatry 56:317–322PubMedCrossRef Keilhoff G, Bernstein HG, Becker A, Grecksch G, Wolf G (2004b) Increased neurogenesis in a rat ketamine model of schizophrenia. Biol Psychiatry 56:317–322PubMedCrossRef
go back to reference Kodama M, Fuijoka T, Duman RS (2004) Chronic olanzapine or fluoxetine administration increases cell proliferation in hippocampus and prefrontal cortex of adult rat. Biol Psychiatry 56(8):570–580PubMedCrossRef Kodama M, Fuijoka T, Duman RS (2004) Chronic olanzapine or fluoxetine administration increases cell proliferation in hippocampus and prefrontal cortex of adult rat. Biol Psychiatry 56(8):570–580PubMedCrossRef
go back to reference Kuan C-Y, Schloemer AJ, Lu A et al (2004) Hypoxia-ischemia induces DNA synthesis without cell proliferation in dying neurons in adult rodent brain. Neurobiol Dis 24:10763–10772 Kuan C-Y, Schloemer AJ, Lu A et al (2004) Hypoxia-ischemia induces DNA synthesis without cell proliferation in dying neurons in adult rodent brain. Neurobiol Dis 24:10763–10772
go back to reference Kuhn HG, Dickinson-Anson H, Gage FH (1996) Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16:2027–2033PubMed Kuhn HG, Dickinson-Anson H, Gage FH (1996) Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16:2027–2033PubMed
go back to reference Lederbogen F, Kirsch P, Haddad L, Streit F, Tost H, Schuch P, Wüst S, Pruessner JC, Rietschel M, Deuschle M, Meyer-Lindenberg A (2011) City living and urban upbringing affect neural social stress processing in humans. Nature 474(7352):498–501 Lederbogen F, Kirsch P, Haddad L, Streit F, Tost H, Schuch P, Wüst S, Pruessner JC, Rietschel M, Deuschle M, Meyer-Lindenberg A (2011) City living and urban upbringing affect neural social stress processing in humans. Nature 474(7352):498–501
go back to reference Lieberman J, Chakos M, Wu H, Alvir J, Hoffman E, Robinson D, Bilder R (2001) Longitudinal study of brain morphology in first episode schizophrenia. Biol Psychiatry 49:487–499PubMedCrossRef Lieberman J, Chakos M, Wu H, Alvir J, Hoffman E, Robinson D, Bilder R (2001) Longitudinal study of brain morphology in first episode schizophrenia. Biol Psychiatry 49:487–499PubMedCrossRef
go back to reference Lui S, Deng W, Huang X, Jiang L, Ma X, Chen H, Zhang T, Li X, Li D, Zou L, Tang H, Zhou XJ, Mechelli A, Collier DA, Sweeney JA, Li T, Gong Q (2009) Association of cerebral deficits with clinical symptoms in antipsychotic-naive first-episode schizophrenia: an optimized voxel-based morphometry and resting state functional connectivity study. Am J Psychiatry 166:196–205PubMedCrossRef Lui S, Deng W, Huang X, Jiang L, Ma X, Chen H, Zhang T, Li X, Li D, Zou L, Tang H, Zhou XJ, Mechelli A, Collier DA, Sweeney JA, Li T, Gong Q (2009) Association of cerebral deficits with clinical symptoms in antipsychotic-naive first-episode schizophrenia: an optimized voxel-based morphometry and resting state functional connectivity study. Am J Psychiatry 166:196–205PubMedCrossRef
go back to reference Madsen TM, Yeh DD, Valentine GW, Duman RS (2005) Electroconvulsive seizure treatment increases cell proliferation in rat frontal cortex. Neuropsychopharmacology 30(1):27–34PubMedCrossRef Madsen TM, Yeh DD, Valentine GW, Duman RS (2005) Electroconvulsive seizure treatment increases cell proliferation in rat frontal cortex. Neuropsychopharmacology 30(1):27–34PubMedCrossRef
go back to reference Manning EE, Ransome MI, Burrows EL, Hannan AJ (2012) Increased adult hippocampal neurogenesis and abnormal migration of adult-born granule neurons is associated with hippocampal-specific cognitive deficits in phospholipase C-β1 knockout mice. Hippocampus 22:309–319PubMedCrossRef Manning EE, Ransome MI, Burrows EL, Hannan AJ (2012) Increased adult hippocampal neurogenesis and abnormal migration of adult-born granule neurons is associated with hippocampal-specific cognitive deficits in phospholipase C-β1 knockout mice. Hippocampus 22:309–319PubMedCrossRef
go back to reference McNeil TF, Cantor-Graae E, Ismail B (2000a) Obstetric complications and congenital malformation in schizophrenia. Brain Res Brain Res Rev 31:166–178PubMedCrossRef McNeil TF, Cantor-Graae E, Ismail B (2000a) Obstetric complications and congenital malformation in schizophrenia. Brain Res Brain Res Rev 31:166–178PubMedCrossRef
go back to reference McNeil TF, Cantor-Graae E, Weinberger DR (2000b) Relationship of obstetric complications and differences in size of brain structures in monozygotic twin pairs discordant for schizophrenia. Am J Psychiatry 157:203–212PubMedCrossRef McNeil TF, Cantor-Graae E, Weinberger DR (2000b) Relationship of obstetric complications and differences in size of brain structures in monozygotic twin pairs discordant for schizophrenia. Am J Psychiatry 157:203–212PubMedCrossRef
go back to reference McOmish CE, Burrows E, Howard M, Scarr E, Kim D, Shin HS, Dean B, van den Buuse M, Hannan AJ (2008a) Phospholipase Cbeta1 knockout mice exhibit endophenotypes modeling schizophrenia which are rescued by environmental enrichment and clozapine administration. Mol Psychiatry 13:661–672PubMedCrossRef McOmish CE, Burrows E, Howard M, Scarr E, Kim D, Shin HS, Dean B, van den Buuse M, Hannan AJ (2008a) Phospholipase Cbeta1 knockout mice exhibit endophenotypes modeling schizophrenia which are rescued by environmental enrichment and clozapine administration. Mol Psychiatry 13:661–672PubMedCrossRef
go back to reference McOmish CE, Burrows EL, Howard M, Hannan AJ (2008b) PLCbeta1 knockout mice as a model of disrupted cortical development and plasticity: behavioral endophenotypes and dysregulation of RGS4 gene expression. Hippocampus 18:824–834PubMedCrossRef McOmish CE, Burrows EL, Howard M, Hannan AJ (2008b) PLCbeta1 knockout mice as a model of disrupted cortical development and plasticity: behavioral endophenotypes and dysregulation of RGS4 gene expression. Hippocampus 18:824–834PubMedCrossRef
go back to reference Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates. 2nd edn. Academic Press, San Diego Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates. 2nd edn. Academic Press, San Diego
go back to reference Pencea V, Bingaman KD, Wiegand SJ, Luskin MB (2001) Infusion of brain-derived neurotrophic factor into the lateral ventricle of the adult rat leads to new neurons in the parenchyma of the striatum, septum, thalamus, and hypothalamus. J Neurosci 21:6706–6717PubMed Pencea V, Bingaman KD, Wiegand SJ, Luskin MB (2001) Infusion of brain-derived neurotrophic factor into the lateral ventricle of the adult rat leads to new neurons in the parenchyma of the striatum, septum, thalamus, and hypothalamus. J Neurosci 21:6706–6717PubMed
go back to reference Pourié G, Blaise S, Trabalon M, Nédélec E, Guéant JL, Daval JL (2006) Mild, non-lesioning transient hypoxia in the newborn rat induces delayed brain neurogenesis associated with improved memory scores. Neuroscience 140:1369–1379PubMedCrossRef Pourié G, Blaise S, Trabalon M, Nédélec E, Guéant JL, Daval JL (2006) Mild, non-lesioning transient hypoxia in the newborn rat induces delayed brain neurogenesis associated with improved memory scores. Neuroscience 140:1369–1379PubMedCrossRef
go back to reference Reif A, Fritzen S, Finger M, Strobel A, Lauer M, Schmitt A, Lesch KP (2006) Neural stem cell proliferation is decreased in schizophrenia, but not in depression. Mol Psychiatry 11(5):514–522PubMedCrossRef Reif A, Fritzen S, Finger M, Strobel A, Lauer M, Schmitt A, Lesch KP (2006) Neural stem cell proliferation is decreased in schizophrenia, but not in depression. Mol Psychiatry 11(5):514–522PubMedCrossRef
go back to reference Schmitt A, Fendt M, Zink M, Ebert U, Starke M, Berthold M, Herb A, Petroianu G, Falkai P, Henn FA (2007) Altered NMDA receptor expression and behavior following postnatal hypoxia: potential relevance to schizophrenia. J Neural Transm 114:239–248PubMedCrossRef Schmitt A, Fendt M, Zink M, Ebert U, Starke M, Berthold M, Herb A, Petroianu G, Falkai P, Henn FA (2007) Altered NMDA receptor expression and behavior following postnatal hypoxia: potential relevance to schizophrenia. J Neural Transm 114:239–248PubMedCrossRef
go back to reference Schmitz C (1998) Variation of fractionator estimates and its prediction. Anat Embryol (Berl) 198:371–397CrossRef Schmitz C (1998) Variation of fractionator estimates and its prediction. Anat Embryol (Berl) 198:371–397CrossRef
go back to reference Schmitz C, Hof PR (2000) Recommendations for straightforward and rigorous methods of counting neurons based on a computer simulation approach. J Chem Neuroanat 20:93–114PubMedCrossRef Schmitz C, Hof PR (2000) Recommendations for straightforward and rigorous methods of counting neurons based on a computer simulation approach. J Chem Neuroanat 20:93–114PubMedCrossRef
go back to reference Shapiro EM, Gonzalez-Perez O, Manuel García-Verdugo J, Alvarez-Buylla A, Koretsky AP (2006) Magnetic resonance imaging of the migration of neuronal precursors generated in the adult rodent brain. Neuroimage 32:1150–1157PubMedCrossRef Shapiro EM, Gonzalez-Perez O, Manuel García-Verdugo J, Alvarez-Buylla A, Koretsky AP (2006) Magnetic resonance imaging of the migration of neuronal precursors generated in the adult rodent brain. Neuroimage 32:1150–1157PubMedCrossRef
go back to reference Sommer JU, Schmitt A, Heck M, Schaeffer EL, Fendt M, Zink M, Nieselt K, Symons S, Petroianu G, Lex A, Herrera-Marschitz M, Spanagel R, Falkai P, Gebicke-Haerter PJ (2010) Differential expression of presynaptic genes in a rat model of postnatal hypoxia: relevance to schizophrenia. Eur Arch Psychiatry Clin Neurosci 260(Suppl 2):S81–S89PubMedCrossRef Sommer JU, Schmitt A, Heck M, Schaeffer EL, Fendt M, Zink M, Nieselt K, Symons S, Petroianu G, Lex A, Herrera-Marschitz M, Spanagel R, Falkai P, Gebicke-Haerter PJ (2010) Differential expression of presynaptic genes in a rat model of postnatal hypoxia: relevance to schizophrenia. Eur Arch Psychiatry Clin Neurosci 260(Suppl 2):S81–S89PubMedCrossRef
go back to reference Sterio DC (1984) The unbiased estimation of number and sizes of arbitrary particles using the disector. J Microsc 134:127–136PubMedCrossRef Sterio DC (1984) The unbiased estimation of number and sizes of arbitrary particles using the disector. J Microsc 134:127–136PubMedCrossRef
go back to reference Van den Buuse M, Garner B, Koch M (2003) Neurodevelopmental animal models of schizophrenia: effects on prepulse inhibition. Curr Mol Med 3:459–471PubMedCrossRef Van den Buuse M, Garner B, Koch M (2003) Neurodevelopmental animal models of schizophrenia: effects on prepulse inhibition. Curr Mol Med 3:459–471PubMedCrossRef
go back to reference Van Erp TG, Saleh PA, Rosso IM, Huttunen M, Lönnqvist J, Pirkola T, Salonen O, Valanne L, Poutanen VP, Standertskjöld-Nordenstam CG, Cannon TD (2002) Contributions of genetic risk and fetal hypoxia to hippocampal volume in patients with schizophrenia or schizoaffective disorder, their unaffected siblings, and healthy unrelated volunteers. Am J Psychiatry 159:1514–1520PubMedCrossRef Van Erp TG, Saleh PA, Rosso IM, Huttunen M, Lönnqvist J, Pirkola T, Salonen O, Valanne L, Poutanen VP, Standertskjöld-Nordenstam CG, Cannon TD (2002) Contributions of genetic risk and fetal hypoxia to hippocampal volume in patients with schizophrenia or schizoaffective disorder, their unaffected siblings, and healthy unrelated volunteers. Am J Psychiatry 159:1514–1520PubMedCrossRef
go back to reference Verdoux H, Geddes JR, Takei N, Lawrie SM, Bovet P, Eagles JM, Heun R, McCreadie RG, McNeil TF, O’Callaghan E, Stober G, Willinger MU, Wright P, Murray RM (1997) Obstetric complications and age at onset in schizophrenia: an international collaborative meta-analysis of individual patient data. Am J Psychiatry 154:1220–1227PubMed Verdoux H, Geddes JR, Takei N, Lawrie SM, Bovet P, Eagles JM, Heun R, McCreadie RG, McNeil TF, O’Callaghan E, Stober G, Willinger MU, Wright P, Murray RM (1997) Obstetric complications and age at onset in schizophrenia: an international collaborative meta-analysis of individual patient data. Am J Psychiatry 154:1220–1227PubMed
go back to reference Watson DR, Anderson JM, Bai F, Barrett SL, McGinnity TM, Mulholland CC, Rushe TM, Cooper SJ (2012) A voxel based morphometry study investigating brain structural changes in first episode psychosis. Behav Brain Res 227:91–99PubMedCrossRef Watson DR, Anderson JM, Bai F, Barrett SL, McGinnity TM, Mulholland CC, Rushe TM, Cooper SJ (2012) A voxel based morphometry study investigating brain structural changes in first episode psychosis. Behav Brain Res 227:91–99PubMedCrossRef
go back to reference Weinberger DR (1996) On the plausibility of “the neurodevelopmental hypothesis” of schizophrenia. Neuropsychopharmacology 14:1–11CrossRef Weinberger DR (1996) On the plausibility of “the neurodevelopmental hypothesis” of schizophrenia. Neuropsychopharmacology 14:1–11CrossRef
go back to reference West MJ (1999) Stereological methods for estimating the total number of neurons and synapses: issues of precision and bias. Trends Neurosci 22:51–61PubMedCrossRef West MJ (1999) Stereological methods for estimating the total number of neurons and synapses: issues of precision and bias. Trends Neurosci 22:51–61PubMedCrossRef
go back to reference West MJ, Slomianka L, Gundersen HJ (1991) Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482–497PubMedCrossRef West MJ, Slomianka L, Gundersen HJ (1991) Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482–497PubMedCrossRef
go back to reference Witthaus H, Kaufmann C, Bohner G, Ozgürdal S, Gudlowski Y, Gallinat J, Ruhrmann S, Brüne M, Heinz A, Klingebiel R, Juckel G (2009) Gray matter abnormalities in subjects at ultra-high risk for schizophrenia and first-episode schizophrenic patients compared to healthy controls. Psychiatry Res 173:163–169PubMedCrossRef Witthaus H, Kaufmann C, Bohner G, Ozgürdal S, Gudlowski Y, Gallinat J, Ruhrmann S, Brüne M, Heinz A, Klingebiel R, Juckel G (2009) Gray matter abnormalities in subjects at ultra-high risk for schizophrenia and first-episode schizophrenic patients compared to healthy controls. Psychiatry Res 173:163–169PubMedCrossRef
go back to reference Yamashima T, Tonchev AB, Yukie M (2007) Adult hippocampal neurogenesis in rodents and primates: endogenous, enhanced, and engrafted. Rev Neurosci 18:67–82PubMed Yamashima T, Tonchev AB, Yukie M (2007) Adult hippocampal neurogenesis in rodents and primates: endogenous, enhanced, and engrafted. Rev Neurosci 18:67–82PubMed
Metadata
Title
Increased cell proliferation in the rat anterior cingulate cortex following neonatal hypoxia: relevance to schizophrenia
Authors
Evelin L. Schaeffer
Franziska Kühn
Angelika Schmitt
Wagner F. Gattaz
Oliver Gruber
Thomas Schneider-Axmann
Peter Falkai
Andrea Schmitt
Publication date
01-01-2013
Publisher
Springer Vienna
Published in
Journal of Neural Transmission / Issue 1/2013
Print ISSN: 0300-9564
Electronic ISSN: 1435-1463
DOI
https://doi.org/10.1007/s00702-012-0859-y

Other articles of this Issue 1/2013

Journal of Neural Transmission 1/2013 Go to the issue