Skip to main content
main-content
Erschienen in: Brain Structure and Function 1/2018

29.08.2017 | Original Article

Chronic stress targets adult neurogenesis preferentially in the suprapyramidal blade of the rat dorsal dentate gyrus

verfasst von: Nuno D. Alves, Patrícia Patrício, Joana S. Correia, António Mateus-Pinheiro, Ana R. Machado-Santos, Eduardo Loureiro-Campos, Mónica Morais, João M. Bessa, Nuno Sousa, Luísa Pinto

Erschienen in: Brain Structure and Function | Ausgabe 1/2018

Einloggen, um Zugang zu erhalten

Abstract

The continuous generation of new neurons and glial cells in the adult hippocampal dentate gyrus (DG) represents an important form of adult neuroplasticity, involved in normal brain function and behavior but also associated with the etiopathogenesis and treatment of psychiatric disorders. Despite the large number of studies addressing cell genesis along the septotemporal axis, data on the anatomical gradients of cytogenesis along the DG transverse axis is scarce, especially after exposure to stress. As such, in this study we characterized both basal proliferation and survival of adult-born neural cells along the transverse axis of the rat dorsal DG, and after stress exposure. In basal conditions, both proliferating cells and newborn neurons and glial cells were preferentially located at the subgranular zone and suprapyramidal blade. Exposure to chronic stress induced an overall decrease in the generation of adult-born neural cells and, more specifically, produced a regional-specific decrease in the survival of adult-born neurons at the suprapyramidal blade. No particular region-specific alterations were observed on surviving adult-born glial cells. This work reveals, for the first time, a distinct survival profile of adult-born neural cells, neurons and glial cells, among the transverse axis of the DG, in both basal and stress conditions. Our results unveil that adult-born neurons are preferentially located in the suprapyramidal blade and suggest a regional-specific impact of chronic stress in this blade with potential repercussions for its functional significance.
Anhänge
Nur mit Berechtigung zugänglich
Literatur
Zurück zum Zitat Ambrogini P et al (2000) Spatial learning affects immature granule cell survival in adult rat dentate gyrus. Neurosci Lett 286:21–24 CrossRefPubMed Ambrogini P et al (2000) Spatial learning affects immature granule cell survival in adult rat dentate gyrus. Neurosci Lett 286:21–24 CrossRefPubMed
Zurück zum Zitat Biebl M, Cooper CM, Winkler J, Kuhn HG (2000) Analysis of neurogenesis and programmed cell death reveals a self-renewing capacity in the adult rat brain. Neurosci Lett 291:17–20 CrossRefPubMed Biebl M, Cooper CM, Winkler J, Kuhn HG (2000) Analysis of neurogenesis and programmed cell death reveals a self-renewing capacity in the adult rat brain. Neurosci Lett 291:17–20 CrossRefPubMed
Zurück zum Zitat Cameron HA, McKay RD (2001) Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol 435:406–417 CrossRefPubMed Cameron HA, McKay RD (2001) Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol 435:406–417 CrossRefPubMed
Zurück zum Zitat Choi YS, Cho KO, Kim SY (2007) Asymmetry in enhanced neurogenesis in the rostral dentate gyrus following kainic acid-induced status epilepticus in adult rats. Arch Pharm Res 30:646–652 CrossRefPubMed Choi YS, Cho KO, Kim SY (2007) Asymmetry in enhanced neurogenesis in the rostral dentate gyrus following kainic acid-induced status epilepticus in adult rats. Arch Pharm Res 30:646–652 CrossRefPubMed
Zurück zum Zitat Chowdhury GM, Fujioka T, Nakamura S (2000) Induction and adaptation of Fos expression in the rat brain by two types of acute restraint stress. Brain Res Bull 52:171–182 CrossRefPubMed Chowdhury GM, Fujioka T, Nakamura S (2000) Induction and adaptation of Fos expression in the rat brain by two types of acute restraint stress. Brain Res Bull 52:171–182 CrossRefPubMed
Zurück zum Zitat de Bruin JP, Sanchez-Santed F, Heinsbroek RP, Donker A, Postmes P (1994) A behavioural analysis of rats with damage to the medial prefrontal cortex using the Morris water maze: evidence for behavioural flexibility, but not for impaired spatial navigation. Brain Res 652:323–333 CrossRefPubMed de Bruin JP, Sanchez-Santed F, Heinsbroek RP, Donker A, Postmes P (1994) A behavioural analysis of rats with damage to the medial prefrontal cortex using the Morris water maze: evidence for behavioural flexibility, but not for impaired spatial navigation. Brain Res 652:323–333 CrossRefPubMed
Zurück zum Zitat Desmond NL, Levy WB (1985) Granule cell dendritic spine density in the rat hippocampus varies with spine shape and location. Neurosci Lett 54:219–224 CrossRefPubMed Desmond NL, Levy WB (1985) Granule cell dendritic spine density in the rat hippocampus varies with spine shape and location. Neurosci Lett 54:219–224 CrossRefPubMed
Zurück zum Zitat Kempermann G, Gast D, Kronenberg G, Yamaguchi M, Gage FH (2003) Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development 130:391–399 CrossRefPubMed Kempermann G, Gast D, Kronenberg G, Yamaguchi M, Gage FH (2003) Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development 130:391–399 CrossRefPubMed
Zurück zum Zitat Lee JC, Yau SY, Lee TM, Lau BW, So KF (2016) Voluntary wheel running reverses the decrease in subventricular zone neurogenesis caused by corticosterone. Cell Transplant 25:1979–1986 CrossRefPubMed Lee JC, Yau SY, Lee TM, Lau BW, So KF (2016) Voluntary wheel running reverses the decrease in subventricular zone neurogenesis caused by corticosterone. Cell Transplant 25:1979–1986 CrossRefPubMed
Zurück zum Zitat Mateus-Pinheiro A et al (2016) AP2gamma controls adult hippocampal neurogenesis and modulates cognitive, but not anxiety or depressive-like behavior. Mol Psychiatry. doi: 10.​1038/​mp.​2016.​169 Mateus-Pinheiro A et al (2016) AP2gamma controls adult hippocampal neurogenesis and modulates cognitive, but not anxiety or depressive-like behavior. Mol Psychiatry. doi: 10.​1038/​mp.​2016.​169
Zurück zum Zitat Morris R (1984) Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 11:47–60 CrossRefPubMed Morris R (1984) Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 11:47–60 CrossRefPubMed
Zurück zum Zitat Nieto-Estevez V, Oueslati-Morales CO, Li L, Pickel J, Morales AV, Vicario-Abejon C (2016) Brain insulin-like growth factor-I directs the transition from stem cells to mature neurons during postnatal/adult hippocampal neurogenesis. Stem Cells 34:2194–2209. doi: 10.​1002/​stem.​2397 CrossRefPubMed Nieto-Estevez V, Oueslati-Morales CO, Li L, Pickel J, Morales AV, Vicario-Abejon C (2016) Brain insulin-like growth factor-I directs the transition from stem cells to mature neurons during postnatal/adult hippocampal neurogenesis. Stem Cells 34:2194–2209. doi: 10.​1002/​stem.​2397 CrossRefPubMed
Zurück zum Zitat Nollet M, Gaillard P, Tanti A, Girault V, Belzung C, Leman S (2012) Neurogenesis-independent antidepressant-like effects on behavior and stress axis response of a dual orexin receptor antagonist in a rodent model of depression. Neuropsychopharmacology 37:2210–2221. doi: 10.​1038/​npp.​2012.​70 CrossRefPubMedPubMedCentral Nollet M, Gaillard P, Tanti A, Girault V, Belzung C, Leman S (2012) Neurogenesis-independent antidepressant-like effects on behavior and stress axis response of a dual orexin receptor antagonist in a rodent model of depression. Neuropsychopharmacology 37:2210–2221. doi: 10.​1038/​npp.​2012.​70 CrossRefPubMedPubMedCentral
Zurück zum Zitat O’Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Clarendon Press, Oxford O’Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Clarendon Press, Oxford
Zurück zum Zitat Schousboe A, Waagepetersen HS (2006) Glial modulation of GABAergic and glutamat ergic neurotransmission. Curr Top Med Chem 6:929–934 CrossRefPubMed Schousboe A, Waagepetersen HS (2006) Glial modulation of GABAergic and glutamat ergic neurotransmission. Curr Top Med Chem 6:929–934 CrossRefPubMed
Zurück zum Zitat Seri B, Garcia-Verdugo JM, McEwen BS, Alvarez-Buylla A (2001) Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 21:7153–7160 PubMed Seri B, Garcia-Verdugo JM, McEwen BS, Alvarez-Buylla A (2001) Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 21:7153–7160 PubMed
Zurück zum Zitat Smith MA, Makino S, Kvetnansky R, Post RM (1995) Stress and glucocorticoids affect the expression of brain-derived neurotrophic factor and neurotrophin-3 mRNAs in the hippocampus. J Neurosci 15:1768–1777 PubMed Smith MA, Makino S, Kvetnansky R, Post RM (1995) Stress and glucocorticoids affect the expression of brain-derived neurotrophic factor and neurotrophin-3 mRNAs in the hippocampus. J Neurosci 15:1768–1777 PubMed
Zurück zum Zitat Sousa N, Almeida OF, Holsboer F, Paula-Barbosa MM, Madeira MD (1998) Maintenance of hippocampal cell numbers in young and aged rats submitted to chronic unpredictable stress. Comparison with the effects of corticosterone treatment. Stress 2:237–249 CrossRefPubMed Sousa N, Almeida OF, Holsboer F, Paula-Barbosa MM, Madeira MD (1998) Maintenance of hippocampal cell numbers in young and aged rats submitted to chronic unpredictable stress. Comparison with the effects of corticosterone treatment. Stress 2:237–249 CrossRefPubMed
Zurück zum Zitat Toyoda A, Iio W, Goto T, Koike H, Tsukahara T (2014) Differential expression of genes encoding neurotrophic factors and their receptors along the septal-temporal axis of the rat hippocampus. Anim Sci J 85:986–993. doi: 10.​1111/​asj.​12268 CrossRefPubMed Toyoda A, Iio W, Goto T, Koike H, Tsukahara T (2014) Differential expression of genes encoding neurotrophic factors and their receptors along the septal-temporal axis of the rat hippocampus. Anim Sci J 85:986–993. doi: 10.​1111/​asj.​12268 CrossRefPubMed
Zurück zum Zitat Tsankova NM, Berton O, Renthal W, Kumar A, Neve RL, Nestler EJ (2006) Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action. Nat Neurosci 9:519–525. doi: 10.​1038/​nn1659 CrossRefPubMed Tsankova NM, Berton O, Renthal W, Kumar A, Neve RL, Nestler EJ (2006) Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action. Nat Neurosci 9:519–525. doi: 10.​1038/​nn1659 CrossRefPubMed
Zurück zum Zitat Ueki T et al (2003) A novel secretory factor, Neurogenesin-1, provides neurogenic environmental cues for neural stem cells in the adult hippocampus. J Neurosci 23:11732–11740 PubMed Ueki T et al (2003) A novel secretory factor, Neurogenesin-1, provides neurogenic environmental cues for neural stem cells in the adult hippocampus. J Neurosci 23:11732–11740 PubMed
Zurück zum Zitat Vinogradova OS (1995) Expression, control, and probable functional significance of the neuronal theta-rhythm. Prog Neurobiol 45:523–583 CrossRefPubMed Vinogradova OS (1995) Expression, control, and probable functional significance of the neuronal theta-rhythm. Prog Neurobiol 45:523–583 CrossRefPubMed
Zurück zum Zitat Wyss JM, Swanson LW, Cowan WM (1979) Evidence for an input to the molecular layer and the stratum granulosum of the dentate gyrus from the supramammillary region of the hypothalamus. Anat Embryol (Berl) 156:165–176 CrossRef Wyss JM, Swanson LW, Cowan WM (1979) Evidence for an input to the molecular layer and the stratum granulosum of the dentate gyrus from the supramammillary region of the hypothalamus. Anat Embryol (Berl) 156:165–176 CrossRef
Zurück zum Zitat Youngblood BD, Zhou J, Smagin GN, Ryan DH, Harris RB (1997) Sleep deprivation by the “flower pot” technique and spatial reference memory. Physiol Behav 61:249–256 CrossRefPubMed Youngblood BD, Zhou J, Smagin GN, Ryan DH, Harris RB (1997) Sleep deprivation by the “flower pot” technique and spatial reference memory. Physiol Behav 61:249–256 CrossRefPubMed
Metadaten
Titel
Chronic stress targets adult neurogenesis preferentially in the suprapyramidal blade of the rat dorsal dentate gyrus
verfasst von
Nuno D. Alves
Patrícia Patrício
Joana S. Correia
António Mateus-Pinheiro
Ana R. Machado-Santos
Eduardo Loureiro-Campos
Mónica Morais
João M. Bessa
Nuno Sousa
Luísa Pinto
Publikationsdatum
29.08.2017
Verlag
Springer Berlin Heidelberg
Erschienen in
Brain Structure and Function / Ausgabe 1/2018
Print ISSN: 1863-2653
Elektronische ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-017-1490-3

Weitere Artikel der Ausgabe 1/2018

Brain Structure and Function 1/2018 Zur Ausgabe

Neu im Fachgebiet Neurologie

Newsletter

Bestellen Sie unseren kostenlosen Newsletter Update Neurologie und bleiben Sie gut informiert – ganz bequem per eMail.