Prenatal Stress Inhibits Hippocampal Neurogenesis but Spares Olfactory Bulb Neurogenesis

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Belnoue, Laure ^a,b   Grosjean, Noelle ^a,b   Ladevèze, Elodie ^a,b   Abrous, Djoher Nora ^a,b   Koehl, Muriel ^a,b  

^a INSTITUT FRANÇOIS MAGENDIE   (France)

^b UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT ANIMAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN DEVELOPMENT; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DENTATE GYRUS; FEMALE; HIPPOCAMPUS; MALE; MOUSE; NONHUMAN; OLFACTORY BULB; OLFACTORY DISCRIMINATION; OLFACTORY MEMORY; PRENATAL STRESS; PROGENY; SHORT TERM MEMORY;

ANIMALS; FEMALE; GESTATIONAL AGE; HIPPOCAMPUS; MEMORY, SHORT-TERM; MICE; NEUROGENESIS; ODORS; OLFACTORY BULB; OLFACTORY PERCEPTION; PREGNANCY; STRESS, PHYSIOLOGICAL;

EID: 84883229740     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0072972     Document Type: Article

References (59)

1. Abrous DN, Koehl M, Le Moal M, (2005) Adult neurogenesis: from precursors to network and physiology. Physiol Rev 85: 523-569.
2. Ming GL, Song H, (2011) Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 70: 687-702.
3. Lledo PM, Merkle FT, Alvarez-Buylla A, (2008) Origin and function of olfactory bulb interneuron diversity. Trends Neurosci 31: 392-400.
4. Mandairon N, Sacquet J, Jourdan F, Didier A, (2006) Long-term fate and distribution of newborn cells in the adult mouse olfactory bulb: Influences of olfactory deprivation. Neuroscience 141: 443-451.
5. Petreanu L, Alvarez-Buylla A, (2002) Maturation and death of adult-born olfactory bulb granule neurons: role of olfaction. J Neurosci 22: 6106-6113.
6. Yamaguchi M, Mori K, (2005) Critical period for sensory experience-dependent survival of newly generated granule cells in the adult mouse olfactory bulb. Proc Natl Acad Sci U S A 102: 9697-9702.
7. 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.
8. Koehl M, Abrous DN, (2011) A new chapter in the field of memory: adult hippocampal neurogenesis. Eur J Neurosci 33: 1101-1114.
9. Dupret D, Fabre A, Dobrossy MD, Panatier A, Rodriguez JJ, et al. (2007) Spatial learning depends on both the addition and removal of new hippocampal neurons. PLoS Biol 5: e214.
10. Tronel S, Belnoue L, Grosjean N, Revest JM, Piazza PV, et al. (2010) Adult-born neurons are necessary for extended contextual discrimination. Hippocampus.
11. Clelland CD, Choi M, Romberg C, Clemenson GD Jr, Fragniere A, et al. (2009) A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 325: 210-213.
12. Nakashiba T, Cushman JD, Pelkey KA, Renaudineau S, Buhl DL, et al. (2012) Young dentate granule cells mediate pattern separation, whereas old granule cells facilitate pattern completion. Cell 149: 188-201.
13. Breton-Provencher V, Lemasson M, Peralta MR III, Saghatelyan A, (2009) Interneurons produced in adulthood are required for the normal functioning of the olfactory bulb network and for the execution of selected olfactory behaviors. J Neurosci 29: 15245-15257.
14. Moreno MM, Linster C, Escanilla O, Sacquet J, Didier A, et al. (2009) Olfactory perceptual learning requires adult neurogenesis. Proc Natl Acad Sci U S A.
15. Lazarini F, Mouthon MA, Gheusi G, de CF, Olivo-Marin JC, et al. (2009) Cellular and behavioral effects of cranial irradiation of the subventricular zone in adult mice. PLoS ONE 4: e7017.
16. Alonso M, Lepousez G, Sebastien W, Bardy C, Gabellec MM, et al. (2012) Activation of adult-born neurons facilitates learning and memory. Nat Neurosci 15: 897-904.
17. Belnoue L, Grosjean N, Abrous DN, Koehl M, (2011) A critical time window for the recruitment of bulbar newborn neurons by olfactory discrimination learning. J Neurosci 31: 1010-1016.
18. Mouret A, Lepousez G, Gras J, Gabellec MM, Lledo PM, (2009) Turnover of newborn olfactory bulb neurons optimizes olfaction. J Neurosci 29: 12302-12314.
19. Korosi A, Naninck EF, Oomen CA, Schouten M, Krugers H, et al. (2012) Early-life stress mediated modulation of adult neurogenesis and behavior. Behav Brain Res 227: 400-409.
20. Fumagalli F, Molteni R, Racagni G, Riva MA, (2007) Stress during development: Impact on neuroplasticity and relevance to psychopathology. Prog Neurobiol 81: 197-217.
21. Koehl M, Lemaire V, Le Moal M, Abrous DN, (2009) Age-dependent effect of prenatal stress on hippocampal cell proliferation in female rats. Eur J Neurosci 29: 635-640.
22. Lemaire V, Koehl M, Le MM, Abrous DN, (2000) Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc Natl Acad Sci U S A 97: 11032-11037.
23. Coe CL, Kramer M, Czeh B, Gould E, Reeves AJ, et al. (2003) Prenatal stress diminishes neurogenesis in the dentate gyrus of juvenile rhesus monkeys. Biol Psychiatry 54: 1025-1034.
24. Zuena AR, Mairesse J, Casolini P, Cinque C, Alema GS, et al. (2008) Prenatal restraint stress generates two distinct behavioral and neurochemical profiles in male and female rats. PLoS One 3: e2170.
25. Rayen I, van den Hove DL, Prickaerts J, Steinbusch HW, Pawluski JL, (2011) Fluoxetine during development reverses the effects of prenatal stress on depressive-like behavior and hippocampal neurogenesis in adolescence. PLoS One 6: e24003.
26. Mandyam CD, Crawford EF, Eisch AJ, Rivier CL, Richardson HN, (2008) Stress experienced in utero reduces sexual dichotomies in neurogenesis, microenvironment, and cell death in the adult rat hippocampus. Dev Neurobiol 68: 575-589.
27. Vallee M, MacCari S, Dellu F, Simon H, Le Moal M, et al. (1999) Long-term effects of prenatal stress and postnatal handling on age-related glucocorticoid secretion and cognitive performance: a longitudinal study in the rat. Eur J Neurosci 11: 2906-2916.
28. Son GH, Geum D, Chung S, Kim EJ, Jo JH, et al. (2006) Maternal stress produces learning deficits associated with impairment of NMDA receptor-mediated synaptic plasticity. J Neurosci 26: 3309-3318.
29. Schulz KM, Pearson JN, Neeley EW, Berger R, Leonard S, et al. (2011) Maternal stress during pregnancy causes sex-specific alterations in offspring memory performance, social interactions, indices of anxiety, and body mass. Physiol Behav 104: 340-347.
30. Van Waes V, Enache M, Zuena A, Mairesse J, Nicoletti F, et al. (2009) Ethanol attenuates spatial memory deficits and increases mGlu1a receptor expression in the hippocampus of rats exposed to prenatal stress. Alcohol Clin Exp Res 33: 1346-1354.
31. Salomon S, Bejar C, Schorer-Apelbaum D, Weinstock M, (2011) Corticosterone mediates some but not other behavioural changes induced by prenatal stress in rats. J Neuroendocrinol 23: 118-128.
32. Hinds JW, (1968) Autoradiographic study of histogenesis in the mouse olfactory bulb. I. Time of origin of neurons and neuroglia. J Comp Neurol 134: 287-304.
33. Kitraki E, Alexis MN, Papalopoulou M, Stylianopoulou F, (1996) Glucocorticoid receptor gene expression in the embryonic rat brain. Neuroendocrinology 63: 305-317.
34. Koehl M, van der Veen R, Gonzales D, Piazza PV, Abrous DN, (2012) Interplay of maternal care and genetic influences in programming adult hippocampal neurogenesis. Biol Psychiatry 72: 282-289.
35. Morgan CP, Bale TL, (2011) Early prenatal stress epigenetically programs dysmasculinization in second-generation offspring via the paternal lineage. J Neurosci 31: 11748-11755.
36. Lucassen PJ, Bosch OJ, Jousma E, Kromer SA, Andrew R, et al. (2009) Prenatal stress reduces postnatal neurogenesis in rats selectively bred for high, but not low, anxiety: possible key role of placental 11beta-hydroxysteroid dehydrogenase type 2. Eur J Neurosci 29: 97-103.
37. Bustamante C, Henriquez R, Medina F, Reinoso C, Vargas R, et al. (2013) Maternal exercise during pregnancy ameliorates the postnatal neuronal impairments induced by prenatal restraint stress in mice. Int J Dev Neurosci 31: 267-273.
38. Bodyak N, Slotnick B, (1999) Performance of mice in an automated olfactometer: odor detection, discrimination and odor memory. Chem Senses 24: 637-645.
39. Koehl M, Meerlo P, Gonzales D, Rontal A, Turek FW, et al. (2008) Exercise-induced promotion of hippocampal cell proliferation requires beta-endorphin. FASEB J 22: 2253-2262.
40. Plumpe T, Ehninger D, Steiner B, Klempin F, Jessberger S, et al. (2006) Variability of doublecortin-associated dendrite maturation in adult hippocampal neurogenesis is independent of the regulation of precursor cell proliferation. BMC Neurosci 7: 77.
41. Walker TL, Yasuda T, Adams DJ, Bartlett PF, (2007) The doublecortin-expressing population in the developing and adult brain contains multipotential precursors in addition to neuronal-lineage cells. J Neurosci 27: 3734-3742.
42. Akers KG, Kushner SA, Leslie AT, Clarke L, van der Kooy D, et al. (2011) Fetal alcohol exposure leads to abnormal olfactory bulb development and impaired odor discrimination in adult mice. Mol Brain 4: 29.
43. Bayer LE, Kakumanu S, Mactutus CF, Booze RM, Strupp BJ, (2002) Prenatal cocaine exposure alters sensitivity to the effects of idazoxan in a distraction task. Behav Brain Res 133: 185-196.
44. Mouret A, Gheusi G, Gabellec MM, de CF, Olivo-Marin JC, et al. (2008) Learning and survival of newly generated neurons: when time matters. J Neurosci 28: 11511-11516.
45. Rochefort C, Gheusi G, Vincent JD, Lledo PM, (2002) Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J Neurosci 22: 2679-2689.
46. Veyrac A, Sacquet J, Nguyen V, Marien M, Jourdan F, et al. (2009) Novelty determines the effects of olfactory enrichment on memory and neurogenesis through noradrenergic mechanisms. Neuropsychopharmacology 34: 786-795.
47. Racekova E, Lievajova K, Danko J, Martoncikova M, Flesarova S, et al. (2009) Maternal separation induced alterations of neurogenesis in the rat rostral migratory stream. Cell Mol Neurobiol 29: 811-819.
48. Kippin TE, Cain SW, Masum Z, Ralph MR, (2004) Neural stem cells show bidirectional experience-dependent plasticity in the perinatal mammalian brain. J Neurosci 24: 2832-2836.
49. Darnaudery M, Perez-Martin M, Belizaire G, Maccari S, Garcia-Segura LM, (2006) Insulin-like growth factor 1 reduces age-related disorders induced by prenatal stress in female rats. Neurobiol Aging 27: 119-127.
50. Brown J, Cooper-Kuhn CM, Kempermann G, Van Praag H, Winkler J, et al. (2003) Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. Eur J Neurosci 17: 2042-2046.
51. Koehl M, Sawamoto K, Parent JM, Alvarez-Buylla A, editors. Neurogenesis in the adult brain II.
52. Wong EY, Herbert J, (2005) Roles of mineralocorticoid and glucocorticoid receptors in the regulation of progenitor proliferation in the adult hippocampus. Eur J Neurosci 22: 785-792.
53. Schoenfeld TJ, Gould E, (2012) Stress, stress hormones, and adult neurogenesis. Exp Neurol 233: 12-21.
54. Hitoshi S, Maruta N, Higashi M, Kumar A, Kato N, et al. (2007) Antidepressant drugs reverse the loss of adult neural stem cells following chronic stress. J Neurosci Res 85: 3574-3585.
55. Lau WM, Qiu G, Helmeste DM, Lee TM, Tang SW, et al. (2007) Corticosteroid decreases subventricular zone cell proliferation, which could be reversed by paroxetine. Restor Neurol Neurosci 25: 17-23.
56. Duric V, McCarson KE, (2006) Persistent pain produces stress-like alterations in hippocampal neurogenesis and gene expression. J Pain 7: 544-555.
57. Montaron MF, Petry KG, Rodriguez JJ, Marinelli M, Aurousseau C, et al. (1999) Adrenalectomy increases neurogenesis but not PSA-NCAM expression in aged dentate gyrus. Eur J Neurosci 11: 1479-1485.
58. Dupret D, Revest JM, Koehl M, Ichas F, De GF, et al. (2008) Spatial relational memory requires hippocampal adult neurogenesis. PLoS ONE 3: e1959.
59. Sahay A, Wilson DA, Hen R, (2011) Pattern separation: a common function for new neurons in hippocampus and olfactory bulb. Neuron 70: 582-588.