Perinatal fluoxetine increases hippocampal neurogenesis and reverses the lasting effects of pre-gestational stress on serum corticosterone, but not on maternal behavior, in the rat dam
Gemmel, M.; Harmeyer, D.; Bögi, E.et al.
2018 • In Behavioural Brain Research, 339, p. 222-231
Perinatal fluoxetine increases hippocampal neurogenesis and reverses the lasting effects of pre-gestational stress on serum corticosterone, but not on maternal behavior, in the rat dam.pdf
CIRM - Centre Interdisciplinaire de Recherche sur le Médicament - ULiège
Disciplines :
Pharmacy, pharmacology & toxicology
Author, co-author :
Gemmel, M.; Department of Biological Sciences, Ohio University, Athens, OH, United States
Harmeyer, D.; Department of Biological Sciences, Ohio University, Athens, OH, United States
Bögi, E.; Institute of Experimental Pharmacology and Toxicology, Slovak Academy of Sciences, Department of Reproductive Toxicology, Bratislava, Slovakia
Fillet, Marianne ; Université de Liège - ULiège > Département de pharmacie > Analyse des médicaments
Hill, L. A.; Department of Cellular and Physiological Sciences, Faculty of Medicine, The University of British Columbia, Vancouver, Canada
Hammond, G. L.; Department of Cellular and Physiological Sciences, Faculty of Medicine, The University of British Columbia, Vancouver, Canada
Charlier, T. D.; Institut de Recherche en Sante, Environnement et Travail (Irset), Institut National de la Santé et de la Recherche Médicale U1085, Université de Rennes 1, Rennes, France
Pawluski, Jodi L.; Institut de Recherche en Sante, Environnement et Travail (Irset), Institut National de la Santé et de la Recherche Médicale U1085, Université de Rennes 1, Rennes, France
Language :
English
Title :
Perinatal fluoxetine increases hippocampal neurogenesis and reverses the lasting effects of pre-gestational stress on serum corticosterone, but not on maternal behavior, in the rat dam
Pawluski, J.L., Lonstein, J.S., Fleming, A.S., The neurobiology of postpartum anxiety and depression. Trends Neurosci. 40:2 (2017), 106–120.
Gemmel, M., Bögi, E., Ragan, C., Hazlett, M., Dubovicky, M., Van den Hove, D.L., Oberlander, T.F., Charlier, T.D., Pawluski, J.L., Perinatal selective serotonin reuptake inhibitor medication (SSRI) effects on social behaviors, neurodevelopment and the epigenome. Neurosci. Biobehav. Rev., 2017 Epub ahead of print.
Glover, M., Clinton, S., Of rodents and humans: a comparative review of the neurobehavioral effects of early life SSRI exposure in preclinical and clinical research. Int. J. Dev. Neurosci. 51 (2016), 50–72.
Huang, Y., Xu, H., Li, H., Yang, H., Chen, Y., Shi, X., Pre-gestational stress reduces the ratio of 5-HIAA to 5-HT and the expression of 5-HT1A receptor and serotonin transporter in the brain of foetal rat. BMC Neurosci., 13, 2012, 22.
Field, T., Psychologically depressed parents. Bornstein, M., (eds.) Handbook of Parenting, 1995, L. Erlbaum Associates, New Jersey.
Field, T., Healy, B., Goldstein, M., Guthertz, M., Behavior-state matching and synchrony in mother-infant interactions of nondepressed versus depressed dyads. Dev. Psychobiol. 26:1 (1990), 7–14.
Fleming, A.S., Ruble, D.N., Flett, G.L., Shaul, D., Postpartum adjustment in first-time mothers: relations between mood, maternal attitudes and mother-infant interactions’. Dev. Psychobiol. 24 (1988), 71–81.
Brummelte, S., Pawluski, J.L., Galea, L.A., High post-partum levels of corticosterone given to dams influence postnatal hippocampal cell proliferation and behavior of offspring: a model of post-partum stress and possible depression. Horm. Behav. 50:3 (2006), 370–382.
Belnoue, L., Malvaut, S., Ladeveze, E., Abrous, D.N., Koehl, M., Plasticity in the olfactory bulb of the maternal mouse is prevented by gestational stress. Sci. Rep., 6, 2016, 37615.
Champagne, F.A., Meaney, M.J., Stress during gestation alters postpartum maternal care and the development of the offspring in a rodent model. Biol. Psychiatry 59:12 (2006), 1227–1235.
Haim, A., Sherer, M., Leuner, B., Gestational stress induces persistent depressive-like behavior and structural modifications within the postpartum nucleus accumbens. Eur. J. Neurosci. 40:12 (2014), 3766–3773.
Hillerer, K.M., Neumann, I.D., Slattery, D.A., From stress to postpartum mood and anxiety disorders: how chronic peripartum stress can impair maternal adaptations. Neuroendocrinology 95:1 (2012), 22–38.
Moses-Kolko, E.L., Horner, M.S., Phillips, M.L., Hipwell, A.E., Swain, J.E., In search of neural endophenotypes of postpartum psychopathology and disrupted maternal caregiving. J. Neuroendocrinol. 26:10 (2014), 665–684.
Pawluski, J.L., Csaszar, E., Savage, E., Martinez-Claros, M., Steinbusch, H.W., van den Hove, D., Effects of stress early in gestation on hippocampal neurogenesis and glucocorticoid receptor density in pregnant rats. Neuroscience 290 (2015), 379–388.
Pawluski, J.L., van den Hove, D.L., Rayen, I., Prickaerts, J., Steinbusch, H.W., Stress and the pregnant female: impact on hippocampal cell proliferation, but not affective-like behaviors. Horm. Behav. 59:4 (2011), 572–580.
Maghsoudi, N., Ghasemi, R., Ghaempanah, Z., Ardekani, A.M., Nooshinfar, E., Tahzibi, A., Effect of chronic restraint stress on HPA axis activity and expression of BDNF and Trkb in the hippocampus of pregnant rats: possible contribution in depression during pregnancy and postpartum period. Basic Clin. Neurosci. 5:2 (2014), 131–137.
Pawluski, J.L., Valenca, A., Santos, A.I., Costa-Nunes, J.P., Steinbusch, H.W., Strekalova, T., Pregnancy or stress decrease complexity of CA3 pyramidal neurons in the hippocampus of adult female rats. Neuroscience 227 (2012), 201–210.
Hillerer, K.M., Neumann, I.D., Couillard-Despres, S., Aigner, L., Slattery, D.A., Lactation-induced reduction in hippocampal neurogenesis is reversed by repeated stress exposure. Hippocampus 24:6 (2014), 673–683.
Brummelte, S., Galea, L.A., Chronic corticosterone during pregnancy and postpartum affects maternal care, cell proliferation and depressive-like behavior in the dam. Horm. Behav. 58:8 (2010), 769–779.
Workman, J.L., Brummelte, S., Galea, L.A., Postpartum corticosterone administration reduces dendritic complexity and increases the density of mushroom spines of hippocampal CA3 arbours in dams. J. Neuroendocrinol. 25:2 (2013), 119–130.
Lemaire, V., Billard, J.M., Dutar, P., George, O., Piazza, P.V., Epelbaum, J., Le Moal, M., Mayo, W., Motherhood-induced memory improvement persists across lifespan in rats but is abolished by a gestational stress. Eur. J. Neurosci. 23:12 (2006), 3368–3374.
Dranovsky, A., Hen, R., Hippocampal neurogenesis: regulation by stress and antidepressants. Biol. Psychiatry 59:12 (2006), 1136–1143.
Eisch, A.J., Cameron, H.A., Encinas, J.M., Meltzer, L.A., Ming, G.L., Overstreet-Wadiche, L.S., Adult neurogenesis, mental health, and mental illness: hope or hype?. J. Neurosci. 28:46 (2008), 11785–11791.
Eisch, A.J., Petrik, D., Depression and hippocampal neurogenesis: a road to remission?. Science 338:6103 (2012), 72–75.
Pawluski, J.L., Galea, L.A., Reproductive experience alters hippocampal neurogenesis during the postpartum period in the dam. Neuroscience 149:1 (2007), 53–67.
Leuner, B., Glasper, E.R., Gould, E., Parenting and plasticity. Trends Neurosci. 33:10 (2010), 465–473.
Pawluski, J.L., Galea, L.A., Hippocampal morphology is differentially affected by reproductive experience in the mother. J. Neurobiol. 66:1 (2006), 71–81.
Leuner, B., Sabihi, S., The birth of new neurons in the maternal brain: hormonal regulation and functional implications. Front. Neuroendocrinol. 41 (2016), 99–113.
Charlton, R.A., Jordan, S., Pierini, A., Garne, E., Neville, A.J., Hansen, A.V., Gini, R., Thayer, D., Tingay, K., Puccini, A., Bos, H.J., Nybo Andersen, A.M., Sinclair, M., Dolk, H., de Jong-van den Berg, L.T., Selective serotonin reuptake inhibitor prescribing before, during and after pregnancy: a population-based study in six European regions. BJOG 122:7 (2015), 1010–1020.
Cooper, W.O., Willy, M.E., Pont, S.J., Ray, W.A., Increasing use of antidepressants in pregnancy. Am. J. Obstet. Gynecol., 196(6), 2007, 544 e1-5.
Oberlander, T.F., Warburton, W., Misri, S., Aghajanian, J., Hertzman, C., Neonatal outcomes after prenatal exposure to selective serotonin reuptake inhibitor antidepressants and maternal depression using population-based linked health data. Arch. Gen. Psychiatry 63:8 (2006), 898–906.
Zoega, H., Kieler, H., Norgaard, M., Furu, K., Valdimarsdottir, U., Brandt, L., Haglund, B., Use of SSRI and SNRI antidepressants during pregnancy: a population-based study from Denmark, Iceland, Norway and Sweden. PLoS One, 10(12), 2015, e0144474.
Barden, N., Reul, J.M., Holsboer, F., Do antidepressants stabilize mood through actions on the hypothalamic-pituitary-adrenocortical system?. Trends Neurosci. 18:1 (1995), 6–11.
Santarelli, L., Saxe, M., Gross, C., Surget, A., Battaglia, F., Dulawa, S., Weisstaub, N., Lee, J., Duman, R., Arancio, O., Belzung, C., Hen, R., Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301:5634 (2003), 805–809.
Malberg, J.E., Duman, R.S., Cell proliferation in adult hippocampus is decreased by inescapable stress: reversal by fluoxetine treatment. Neuropsychopharmacology 28:9 (2003), 1562–1571.
Weikum, W.M., Mayes, L.C., Grunau, R.E., Brain, U., Oberlander, T.F., The impact of prenatal serotonin reuptake inhibitor (SRI) antidepressant exposure and maternal mood on mother-infant interactions at 3 months of age. Infant Behav. Dev. 36:4 (2013), 485–493.
Logsdon, M.C., Wisner, K., Hanusa, B.H., Does maternal role functioning improve with antidepressant treatment in women with postpartum depression?. J. Womens Health (Larchmt) 18:1 (2009), 85–90.
McFarland, J., Salisbury, A.L., Battle, C.L., Hawes, K., Halloran, K., Lester, B.M., Major depressive disorder during pregnancy and emotional attachment to the fetus. Arch. Womens Ment. Health 14:5 (2011), 425–434.
Johns, J.M., Joyner, P.W., McMurray, M.S., Elliott, D.L., Hofler, V.E., Middleton, C.L., Knupp, K., Greenhill, K.W., Lomas, L.M., Walker, C.H., The effects of dopaminergic/serotonergic reuptake inhibition on maternal behavior, maternal aggression, and oxytocin in the rat. Pharmacol. Biochem. Behav. 81:4 (2005), 769–785.
Workman, J.L., Gobinath, A.R., Kitay, N.F., Chow, C., Brummelte, S., Galea, L.A., Parity modifies the effects of fluoxetine and corticosterone on behavior, stress reactivity, and hippocampal neurogenesis. Neuropharmacology 105 (2016), 443–453.
Pawluski, J., Charlier, T., Fillet, M., Houbart, V., Crispin, H., Steinbusch, H., van den Hove, D., Chronic fluoxetine treatment and maternal adversity differentially alter neurobehavioral outcomes in the rat dam. Behav. Brain Res. 228:1 (2012), 159–168.
Gemmel, M., Rayen, I., van Donkelaar, E., Loftus, T., Steinbusch, H.W., Kokras, N., Dalla, C., Pawluski, J.L., Gestational stress and fluoxetine treatment differentially affect plasticity, methylation and serotonin levels in the PFC and hippocampus of rat dams. Neuroscience 327 (2016), 32–43.
Huang, Y., Shi, X., Xu, H., Yang, H., Chen, T., Chen, S., Chen, X., Chronic unpredictable stress before pregnancy reduce the expression of brain-derived neurotrophic factor and N-methyl-D-aspartate receptor in hippocampus of offspring rats associated with impairment of memory. Neurochem. Res. 35:7 (2010), 1038–1049.
Martin, A.L., Brown, R.E., The lonely mouse: verification of a separation-induced model of depression in female mice. Behav. Brain Res. 207:1 (2010), 196–207.
McEwen, B.S., Glucocorticoids, depression, and mood disorders: structural remodeling in the brain. Metabolism 54:5 Suppl. 1 (2005), 20–23.
Ennaceur, A., Delacour, J., A new one-trial test for neurobiological studies of memory in rats. 1: Behavioral data. Behav. Brain Res. 31:1 (1988), 47–59.
Macbeth, A.H., Gautreaux, C., Luine, V.N., Pregnant rats show enhanced spatial memory, decreased anxiety, and altered levels of monoaminergic neurotransmitters. Brain Res. 1241 (2008), 136–147.
Prut, L., Belzung, C., The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur. J. Pharmacol. 463:1–3 (2003), 3–33.
Gemmel, M., Hazlett, M., Bogi, E., De Lacalle, S., Hill, L.A., Kokras, N., Hammond, G.L., Dalla, C., Charlier, T.D., Pawluski, J.L., Perinatal fluoxetine effects on social play, the HPA system, and hippocampal plasticity in pre-adolescent male and female rats: interactions with pre-gestational maternal stress. Psychoneuroendocrinology 84 (2017), 159–171.
Pawluski, J.L., van Donkelaar, E., Abrams, Z., Houbart, V., Fillet, M., Steinbusch, H.W., Charlier, T.D., Fluoxetine dose and administration method differentially affect hippocampal plasticity in adult female rats. Neural Plast., 2014, 2014, 123026.
Knaepen, L., Rayen, I., Charlier, T.D., Fillet, M., Houbart, V., van Kleef, M., Steinbusch, H.W., Patijn, J., Tibboel, D., Joosten, E.A., Pawluski, J.L., Developmental fluoxetine exposure normalizes the long-term effects of maternal stress on post-operative pain in Sprague-Dawley rat offspring. PLoS One, 8(2), 2013, e57608.
Corbett, A., McGowin, A., Sieber, S., Flannery, T., Sibbitt, B., A method for reliable voluntary oral administration of a fixed dosage (mg/kg) of chronic daily medication to rats. Lab. Anim. 46:4 (2012), 318–324.
Pawluski, J.L., Rayen, I., Niessen, N.A., Kristensen, S., van Donkelaar, E.L., Balthazart, J., Steinbusch, H.W., Charlier, T.D., Developmental fluoxetine exposure differentially alters central and peripheral measures of the HPA system in adolescent male and female offspring. Neuroscience 220 (2012), 131–141.
Houbart, V., Servais, A.C., Charlier, T.D., Pawluski, J.L., Abts, F., Fillet, M., A validated microfluidics-based LC-chip-MS/MS method for the quantitation of fluoxetine and norfluoxetine in rat serum. Electrophoresis 33:22 (2012), 3370–3379.
Pawluski, J.L., Charlier, T.D., Lieblich, S.E., Hammond, G.L., Galea, L.A., Reproductive experience alters corticosterone and CBG levels in the rat dam. Physiol. Behav. 96:1 (2009), 108–114.
Hammond, G.L., Lahteenmaki, P.L., A versatile method for the determination of serum cortisol binding globulin and sex hormone binding globulin binding capacities. Clin. Chim. Acta 132:1 (1983), 101–110.
Pawluski, J.L., Rayen, I., Niessen, N.A., Kristensen, S., Donkelaar, E.L.v., Balthazart, J., Steinbusch, H.W., Charlier, T.D., Developmental fluoxetine exposure differentially alters central and peripheral measures of the HPA system in adolescent male and female offspring. Neuroscience 220 (2012), 131–141.
Rayen, I., Gemmel, M., Pauley, G., Steinbusch, H.W., Pawluski, J.L., Developmental exposure to SSRIs, in addition to maternal stress, has long-term sex-dependent effects on hippocampal plasticity. Psychopharmacology (Berl) 232:7 (2015), 1231–1244.
Rayen, I., van den Hove, D.L., Prickaerts, J., Steinbusch, H.W., Pawluski, J.L., Fluoxetine during development reverses the effects of prenatal stress on depressive-like behavior and hippocampal neurogenesis in adolescence. PLoS One, 6(9), 2011, e24003.
Hillerer, K.M., Reber, S.O., Neumann, I.D., Slattery, D.A., Exposure to chronic pregnancy stress reverses peripartum-associated adaptations: implications for postpartum anxiety and mood disorders. Endocrinology 152:10 (2011), 3930–3940.
Dalla, C., Antoniou, K., Kokras, N., Drossopoulou, G., Papathanasiou, G., Bekris, S., Daskas, S., Papadopoulou-Daifoti, Z., Sex differences in the effects of two stress paradigms on dopaminergic neurotransmission. Physiol. Behav. 93:3 (2008), 595–605.
Dalla, C., Antoniou, K., Drossopoulou, G., Xagoraris, M., Kokras, N., Sfikakis, A., Papadopoulou-Daifoti, Z., Chronic mild stress impact: are females more vulnerable?. Neuroscience 135:3 (2005), 703–714.
Geraghty, A.C., Kaufer, D., Glucocorticoid regulation of reproduction. Adv. Exp. Med. Biol. 872 (2015), 253–278.
Rivier, C., Rivest, S., Effect of stress on the activity of the hypothalamic-pituitary-gonadal axis: peripheral and central mechanisms. Biol. Reprod. 45:4 (1991), 523–532.
Toufexis, D., Rivarola, M.A., Lara, H., Viau, V., Stress and the reproductive axis. J. Neuroendocrinol. 26:9 (2014), 573–586.
Dobson, H., Ghuman, S., Prabhakar, S., Smith, R., A conceptual model of the influence of stress on female reproduction. Reproduction 125:2 (2003), 151–163.
Keen-Rhinehart, E., Michopoulos, V., Toufexis, D.J., Martin, E.I., Nair, H., Ressler, K.J., Davis, M., Owens, M.J., Nemeroff, C.B., Wilson, M.E., Continuous expression of corticotropin-releasing factor in the central nucleus of the amygdala emulates the dysregulation of the stress and reproductive axes. Mol. Psychiatry 14:1 (2009), 37–50.
Baker, S.L., Kentner, A.C., Konkle, A.T., Santa-Maria Barbagallo, L., Bielajew, C., Behavioral and physiological effects of chronic mild stress in female rats. Physiol. Behav. 87:2 (2006), 314–322.
Gonzalez, A.S., Rodriguez Echandia, E.L., Cabrera, R., Foscolo, M.R., Neonatal chronic stress induces subsensitivity to chronic stress in adult rats: II. Effects on estrous cycle in females. Physiol. Behav. 56:3 (1994), 591–595.
Li, X.F., Hu, M.H., Li, S.Y., Geach, C., Hikima, A., Rose, S., Greenwood, M.P., Greenwood, M., Murphy, D., Poston, L., Lightman, S.L., O'Byrne, K.T., Overexpression of corticotropin releasing factor in the central nucleus of the amygdala advances puberty and disrupts reproductive cycles in female rats. Endocrinology 155:10 (2014), 3934–3944.
Frye, C.A., Orecki, Z.A., Prenatal stress alters reproductive responses of rats in behavioral estrus and paced mating of hormone-primed rats. Horm. Behav. 42:4 (2002), 472–483.
Gonzalez Jatuff, A.S., Berastegui, M., Rodriguez, C.I., Rodriguez Echandia, E.L., Permanent and transient effects of repeated preweaning stress on social and sexual behaviors of rats. Stress 3:2 (1999), 97–106.
Heinrichs, S.C., Min, H., Tamraz, S., Carmouche, M., Boehme, S.A., Vale, W.W., Anti-sexual and anxiogenic behavioral consequences of corticotropin-releasing factor overexpression are centrally mediated. Psychoneuroendocrinology 22:4 (1997), 215–224.
Uphouse, L., Selvamani, A., Lincoln, C., Morales, L., Comeaux, D., Mild restraint reduces the time hormonally primed rats spend with sexually active males. Behav. Brain Res. 157:2 (2005), 343–350.
Yoon, H., Chung, W.S., Park, Y.Y., Cho, I.H., Effects of stress on female rat sexual function. Int. J. Impot. Res. 17:1 (2005), 33–38.
deCatanzaro, D., Macniven, E., Psychogenic pregnancy disruptions in mammals. Neurosci. Biobehav. Rev. 16:1 (1992), 43–53.
Pawluski, J.L., Charlier, T.D., Fillet, M., Houbart, V., Crispin, H.T., Steinbusch, H.W., van den Hove, D.L., Chronic fluoxetine treatment and maternal adversity differentially alter neurobehavioral outcomes in the rat dam. Behav. Brain Res. 228:1 (2012), 159–168.
Belovicova, K., Bogi, E., Koprdova, R., Ujhazy, E., Mach, M., Dubovicky, M., Effects of venlafaxine and chronic unpredictable stress on behavior and hippocampal neurogenesis of rat dams. Neuro Endocrinol. Lett. 38:1 (2017), 19–26.
Alenina, N., Kikic, D., Todiras, M., Mosienko, V., Qadri, F., Plehm, R., Boye, P., Vilianovitch, L., Sohr, R., Tenner, K., Hortnagl, H., Bader, M., Growth retardation and altered autonomic control in mice lacking brain serotonin. Proc. Natl. Acad. Sci. U. S. A. 106:25 (2009), 10332–10337.
Keer, S.E., Stern, J.M., Dopamine receptor blockade in the nucleus accumbens inhibits maternal retrieval and licking, but enhances nursing behavior in lactating rats. Physiol. Behav. 67:5 (1999), 659–669.
Zhao, C., Li, M., c-Fos identification of neuroanatomical sites associated with haloperidol and clozapine disruption of maternal behavior in the rat. Neuroscience 166:4 (2010), 1043–1055.
Kohl, J., Autry, A.E., Dulac, C., The neurobiology of parenting: a neural circuit perspective. Bioessays 39:1 (2017), 1–11.
Holschbach, M.A., Lonstein, J.S., Motherhood and infant contact regulate neuroplasticity in the serotonergic midbrain dorsal raphe. Psychoneuroendocrinology 76 (2017), 97–106.
Darnaudery, M., Dutriez, I., Viltart, O., Morley-Fletcher, S., Maccari, S., Stress during gestation induces lasting effects on emotional reactivity of the dam rat. Behav. Brain Res. 153:1 (2004), 211–216.
Bodnar, T.S., Hill, L.A., Taves, M.D., Yu, W., Soma, K.K., Hammond, G.L., Weinberg, J., Colony-specific differences in endocrine and immune responses to an inflammatory challenge in female Sprague Dawley rats. Endocrinology 156:12 (2015), 4604–4617.
Hill, L.A., Bodnar, T.S., Weinberg, J., Hammond, G.L., Corticosteroid-binding globulin is a biomarker of inflammation onset and severity in female rats. J. Endocrinol. 230:2 (2016), 215–225.
Fleming, A.S., Steiner, M., Corter, C., Cortisol, hedonics, and maternal responsiveness in human mothers. Horm. Behav. 32 (1997), 85–98.
Graham, M.D., Rees, S.L., Steiner, M., Fleming, A.S., The effects of adrenalectomy and corticosterone replacement on maternal memory in postpartum rats. Horm. Behav. 49:3 (2006), 353–361.
Rees, S.L., Panesar, S., Steiner, M., Fleming, A.S., The effects of adrenalectomy and corticosterone replacement on induction of maternal behavior in the virgin female rat. Horm. Behav. 49:3 (2006), 337–345.
Rees, S.L., Panesar, S., Steiner, M., Fleming, A.S., The effects of adrenalectomy and corticosterone replacement on maternal behavior in the postpartum rat. Horm. Behav. 46:4 (2004), 411–419.
Ragan, C.M., Lonstein, J.S., Differential postpartum sensitivity to the anxiety-modulating effects of offspring contact is associated with innate anxiety and brainstem levels of dopamine beta-hydroxylase in female laboratory rats. Neuroscience 256 (2014), 433–444.
Pawluski, J.L., Brummelte, S., Barha, C.K., Crozier, T.M., Galea, L.A., Effects of steroid hormones on neurogenesis in the hippocampus of the adult female rodent during the estrous cycle, pregnancy, lactation and aging. Front. Neuroendocrinol. 30:3 (2009), 343–357.
Malberg, J.E., Eisch, A.J., Nestler, E.J., Duman, R.S., Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J. Neurosci. 20:24 (2000), 9104–9110.
O'Leary, O.F., Cryan, J.F., A ventral view on antidepressant action: roles for adult hippocampal neurogenesis along the dorsoventral axis. Trends Pharmacol. Sci. 35:12 (2014), 675–687.
Tanti, A., Belzung, C., Neurogenesis along the septo-temporal axis of the hippocampus: are depression and the action of antidepressants region-specific?. Neuroscience 252 (2013), 234–252.
Brown, H.K., Ray, J.G., Wilton, A.S., Lunsky, Y., Gomes, T., Vigod, S.N., Association between serotonergic antidepressant use during pregnancy and autism spectrum disorder in children. JAMA 317:15 (2017), 1544–1552.
Mezzacappa, A., Lasica, P.A., Gianfagna, F., Cazas, O., Hardy, P., Falissard, B., Sutter-Dallay, A.L., Gressier, F., Risk for autism spectrum disorders according to period of prenatal antidepressant exposure: a systematic review and meta-analysis. JAMA Pediatr. 171:6 (2017), 555–563.
