Gonadal hormone modulation of hippocampal neurogenesis in the adult
Abstract
Gonadal hormones modulate neurogenesis in the dentate gyrus (DG) of adult rodents in complex ways. Estradiol, the most potent estrogen, initially enhances and subsequently suppresses cell proliferation in the dentate gryus of adult female rodents. Much less is known about how estradiol modulates neurogenesis in the adult male rodent; however, recent evidence suggests that estradiol may have a moderate effect on cell proliferation but enhances cell survival in the DG of newly synthesized cells but only when estradiol is administered during a specific stage in the cell maturation cycle in the adult male rodent. Testosterone likely plays a role in adult neurogenesis, although there have been no direct studies to address this. However, pilot studies from our laboratory suggest that testosterone up‐regulates cell survival but not cell proliferation in the DG of adult male rats. Progesterone appears to attenuate the estradiol‐induced enhancement of cell proliferation. Neurosteroids such as allopregnalone decrease neurogenesis in adult rodents, while pregnancy and motherhood differentially regulate adult neurogenesis in the adult female rodent. Very few studies have investigated the effects of gonadal hormones on male rodents; however, studies have indicated that there is a gender difference in the response to hormone‐regulated hippocampal neurogenesis in the adult. Clearly, more work needs to be done to elucidate the effects of gonadal hormones on neurogenesis in the DG of both male and female rodents. © 2006 Wiley‐Liss Inc.
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Steroid hormones exert trophic effects on the amygdala and hippocampus.
“and steroid hormones exert trophic effects on the amygdala and hippocampus (Galea et al. 2006;Zhang et al. 2008).”
From Puberty influences medial temporal lobe and cortical gray matter maturation differently in boys than girls matched for sexual maturity (2011) · cites this paper as Galea et al. 2006
Cites
Gould, E., McEwen, B. S., Tanapat, P., Galea, L. A. M., & Fuchs, E. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-07-02492.1997 · Cited by 1,496 · see citing works
Self-citationGould, E., Tanapat, P., McEwen, B. S., Flügge, G., & Fuchs, E. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.6.3168 · Cited by 1,395 · see citing works
Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons
Woolley, C., Gould, E., Frankfurt, M., & McEwen, B. (1990) · Journal of Neuroscience · doi:10.1523/jneurosci.10-12-04035.1990 · Cited by 1,107 · see citing works
Tanapat, P., Hastings, N. B., Reeves, A. J., & Gould, E. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-14-05792.1999 · Cited by 978 · see citing works
Lee, J., Duan, W., & Mattson, M. P. (2002) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2002.01085.x · Cited by 975 · see citing works
Source of Estrogen Production in Postmenopausal Women1
GRODIN, J. M., SIITERI, P. K., & MACDONALD, P. C. (1973) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-36-2-207 · Cited by 959 · see citing works
VEGF links hippocampal activity with neurogenesis, learning and memory
Cao, L., Jiao, X., Zuzga, D. S., Liu, Y., Fong, D. M., Young, D., & During, M. J. (2004) · Nature Genetics · doi:10.1038/ng1395 · Cited by 850 · see citing works
Coordinated Interaction of Neurogenesis and Angiogenesis in the Adult Songbird Brain
Louissaint, A., Rao, S., Leventhal, C., & Goldman, S. A. (2002) · Neuron · doi:10.1016/s0896-6273(02)00722-5 · Cited by 735 · see citing works
Pregnancy-Stimulated Neurogenesis in the Adult Female Forebrain Mediated by Prolactin
Shingo, T., Gregg, C., Enwere, E. K., Fujikawa, H., Hassam, R., Geary, C. L., Cross, J. C., & Weiss, S. (2003) · Science · doi:10.1126/science.1076647 · Cited by 711 · see citing works
(1997) · PubMed · Cited by 643 · see citing works
Sexual differentiation of the vertebrate nervous system
Morris, J. A., Jordan, C. L., & Breedlove, S. M. (2004) · Nature Neuroscience · doi:10.1038/nn1325 · Cited by 627 · see citing works
Toran‐Allerand, C. D., Guan, X., MacLusky, N. J., Horváth, T. L., Diano, S., Singh, M., Connolly, E. S., Nethrapalli, I. S., & Tinnikov, A. A. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-19-08391.2002 · Cited by 547 · see citing works
Drug Transporters in the Central Nervous System: Brain Barriers and Brain Parenchyma Considerations
Lee, G. S., Dallas, S., Hong, M., & Bendayan, R. (2001) · Pharmacological Reviews · doi:10.1016/s0031-6997(24)01513-8 · Cited by 540 · see citing works
Neurotrophic and Neuroprotective Actions of Estrogens and Their Therapeutic Implications
Lee, S. H., & McEwen, B. S. (2001) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.41.1.569 · Cited by 533 · see citing works
Subordination stress: Behavioral, brain, and neuroendocrine correlates
Blanchard, D. C., Sakai, R. R., McEwen, B. S., Weiss, S. Μ., & Blanchard, R. J. (1993) · Behavioural Brain Research · doi:10.1016/0166-4328(93)90096-9 · Cited by 484 · see citing works
HEMSELL, D. L., GRODIN, J. M., BRENNER, P. F., SIITERI, P. K., & MACDONALD, P. C. (1974) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-38-3-476 · Cited by 444 · see citing works
Concas, A., Mostallino, M. C., Porcu, P., Follesa, P., Barbaccia, M. L., Trabucchi, M., Purdy, R. H., Grisenti, P., & Biggio, G. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.22.13284 · Cited by 422 · see citing works
García‐Segura, L. M., Wozniak, A., Azcoitia, Í., Rodríguez, J., Hutchison, R. E., & Hutchison, J. B. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00340-6 · Cited by 376 · see citing works
Czéh, B., Welt, T., Fischer, A., Erhardt, A., Schmitt, W. B., Müller, M. B., Toschi, N., Fuchs, E., & Keck, M. E. (2002) · Biological Psychiatry · doi:10.1016/s0006-3223(02)01457-9 · Cited by 370 · see citing works
Weill-Engerer, S., David, J.-P., Sazdovitch, V., Liere, P., Eychenne, B., Pianos, A., Schumacher, M., Delacourte, A., Baulieu, E.-E., & Akwa, Y. (2002) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-020878 · Cited by 333 · see citing works
Origin of Estrogen in Normal Men and in Women with Testicular Feminization*
MacDonald, P. C., Madden, J. D., Brenner, P. F., Wilson, J. D., & Siiteri, P. K. (1979) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-49-6-905 · Cited by 320 · see citing works
Karishma, K. K., & Herbert, J. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.02099.x · Cited by 297 · see citing works
Kerr, J. E., Allore, R., Beck, S. G., & Handa, R. J. (1995) · Endocrinology · doi:10.1210/endo.136.8.7628354 · Cited by 296 · see citing works
Vallée, M., Mayo, W., Darnaudéry, M., Corpechot, C., Young, J., Koehl, M., Moal, M. L., Baulieu, É.-É., Röbel, P., & Simon, H. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.26.14865 · Cited by 294 · see citing works
Galea, L. A. M., & McEwen, B. S. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00345-5 · Cited by 276 · see citing works
Self-citationTanapat, P., Hastings, N. B., & Gould, E. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20385 · Cited by 270 · see citing works
BDNF Mediates the Effects of Testosterone on the Survival of New Neurons in an Adult Brain
Rasika, S., Álvarez-Buylla, A., & Nottebohm, F. (1999) · Neuron · doi:10.1016/s0896-6273(00)80678-9 · Cited by 270 · see citing works
Wang, J. M., Johnston, P. B., Ball, B. G., & Brinton, R. D. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.4520-04.2005 · Cited by 261 · see citing works
Estrogen-Receptor-Dependent Regulation of Neural Stem Cell Proliferation and Differentiation
Brännvall, K. (2002) · Molecular and Cellular Neuroscience · doi:10.1006/mcne.2002.1194 · Cited by 240 · see citing works
Hormonal basis during pregnancy for the onset of maternal behavior in the rat
Rosenblatt, J. S. (1988) · Psychoneuroendocrinology · doi:10.1016/0306-4530(88)90005-4 · Cited by 227 · see citing works
Rasika, S., Nottebohm, F., & Álvarez-Buylla, A. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.17.7854 · Cited by 227 · see citing works
Serotonin mediates oestrogen stimulation of cell proliferation in the adult dentate gyrus
Banasr, M., Héry, M., Brezun, J. M., & Daszuta, A. (2001) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01763.x · Cited by 226 · see citing works
Birth, migration, incorporation, and death of vocal control neurons in adult songbirds
Álvarez-Buylla, A., & Kirn, J. R. (1997) · Journal of Neurobiology · doi:10.1002/(sici)1097-4695(19971105)33:5 · Cited by 208 · see citing works
Hormonal Correlates of Agonistic Behavior in Adult Male Rats
Schuurman, T. (1980) · Progress in brain research · doi:10.1016/s0079-6123(08)60079-5 · Cited by 201 · see citing works
Vallée, M., Mayo, W., & Moal, M. L. (2001) · Brain Research Reviews · doi:10.1016/s0165-0173(01)00135-7 · Cited by 198 · see citing works
Ormerod, B. K., Lee, T. T.-Y., & Galea, L. A. M. (2003) · Journal of Neurobiology · doi:10.1002/neu.10181 · Cited by 183 · see citing works
Self-citationDominance Hierarchy Influences Adult Neurogenesis in the Dentate Gyrus: Figure 1.
Kozorovitskiy, Y., & Gould, E. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.0345-04.2004 · Cited by 179 · see citing works
Ormerod, B. K., & Galea, L. A. M. (2001) · Neuroscience · doi:10.1016/s0306-4522(00)00474-7 · Cited by 163 · see citing works
Self-citationSuzuki, M., Wright, L. S., Marwah, P., Lardy, H. A., & Svendsen, C. N. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0307325101 · Cited by 152 · see citing works
Bimonte-Nelson, H., Singleton, R., Nelson, M., Eckman, C., Barber, J., Scott, T. Y., & Granholm, A. (2003) · Experimental Neurology · doi:10.1016/s0014-4886(03)00061-x · Cited by 148 · see citing works
Social stress in laboratory rats: hormonal responses and immune cell distribution
Stefanski, V. (2000) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(99)00066-9 · Cited by 137 · see citing works
19‐Nortestosterone influences neural stem cell proliferation and neurogenesis in the rat brain
Brännvall, K., Bogdanović, N., Korhonen, L., & Lindholm, D. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.03942.x · Cited by 127 · see citing works
Ormerod, B. K., Lee, T. T. ‐., & Galea, L. A. M. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.06.039 · Cited by 125 · see citing works
Self-citationPérez‐Martín, M., Azcoitia, Í., Trejo, J. L., Sierra, A., & García‐Segura, L. M. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02830.x · Cited by 121 · see citing works
Age-dependent susceptibility of adult hippocampal cell proliferation to chronic psychosocial stress
Simon, M., Czéh, B., & Fuchs, E. (2005) · Brain Research · doi:10.1016/j.brainres.2005.05.006 · Cited by 99 · see citing works
Pravosudov, V. V., Mendoza, S. P., & Clayton, N. S. (2003) · Hormones and Behavior · doi:10.1016/s0018-506x(03)00119-3 · Cited by 98 · see citing works
Zhang, L., Li, B. S., Ma, W., Barker, J. L., Chang, Y. H., Zhao, W., & Rubinow, D. R. (2002) · Molecular Brain Research · doi:10.1016/s0169-328x(01)00315-1 · Cited by 95 · see citing works
Self-citationPregnenolone sulfate enhances neurogenesis and PSA-NCAM in young and aged hippocampus
Mayo, W., Lemaire, V., Malaterre, J., Rodriguez, J. J., Cayre, M., Stewart, M. G., Kharouby, M., Rougon, G. N., Moal, M. L., Piazza, P. V., et al. (2004) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2004.03.013 · Cited by 90 · see citing works
Galea, L. A. M., Perrot-Sinal, T. S., Kavaliers, M., & Ossenkopp, K. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01100-2 · Cited by 90 · see citing works
Self-citationNeurogenesis in adult canary telencephalon is independent of gonadal hormone levels
Brown, S., Johnson, F., & Bottjer, S. W. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-05-02024.1993 · Cited by 88 · see citing works
Isgor, C., & Watson, S. J. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.05.008 · Cited by 87 · see citing works
Non-nuclear estrogen receptor ? and ? in the hippocampus of male and female rats
Kalita, K. B., Szymczak, S., & Kaczmarek, L. (2005) · Hippocampus · doi:10.1002/hipo.20066 · Cited by 83 · see citing works
Newly proliferated cells in the adult male amygdala are affected by gonadal steroid hormones
Fowler, C. D., Freeman, M. E., & Wang, Z. (2003) · Journal of Neurobiology · doi:10.1002/neu.10273 · Cited by 79 · see citing works
Blurton-Jones, M. M., Kuan, P. N., & Tuszynski, M. H. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10989 · Cited by 75 · see citing works
Ormerod, B. K., & Galea, L. A. M. (2003) · Neuroscience Letters · doi:10.1016/s0304-3940(03)00546-9 · Cited by 73 · see citing works
Self-citationAbsil, P., Pinxten, R., Balthazart, J., & Eens, M. (2003) · Behavioural Brain Research · doi:10.1016/s0166-4328(03)00006-8 · Cited by 59 · see citing works
Wood, C. E. (2004) · Journal of the Society for Gynecologic Investigation · doi:10.1016/j.jsgi.2004.10.011 · Cited by 58 · see citing works
Витальевич, П. В., & Omanska-Klusek, A. (2004) · Journal of Neurobiology · doi:10.1002/neu.20065 · Cited by 57 · see citing works
Orikasa, C., McEwen, B. S., Hayashi, H., Sakuma, Y., & Hayashi, S. (2000) · Developmental Brain Research · doi:10.1016/s0165-3806(00)00016-x · Cited by 51 · see citing works
Darnaudéry, M., Pallarés, M., Piazza, P., Moal, M. L., & Mayo, W. (2002) · Brain Research · doi:10.1016/s0006-8993(02)03166-9 · Cited by 49 · see citing works
Nagy, A. I., Ormerod, B. K., Mazzucco, C., & Galea, L. A. M. (2005) · Drug Development Research · doi:10.1002/ddr.20053 · Cited by 33 · see citing works
Self-citationGender Differences in Psychiatric Illness and Treatments
Gold, J. H. (1998) · The Journal of Nervous and Mental Disease · doi:10.1097/00005053-199812000-00005 · Cited by 33 · see citing works
Androgens and Androgen Receptor
Chang, C. (2002) · Springer US · doi:10.1007/978-1-4615-1161-8 · Cited by 13 · see citing works
Stevenson, T. J., Ge, B., Hampson, E., Arckens, L., & MacDougall‐Shackleton, S. A. (2005) · Hormones and Behavior · Cited by 3 · see citing works
Day, H. E. W., Curran, E. J., Watson, S. J., & Akil, H. (1999) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19991011)413:1
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Ridding, M. C., & Ziemann, U. (2010) · The Journal of Physiology · doi:10.1113/jphysiol.2010.190314 · Cited by 787 · see citing works
Sex Differences in Traumatic Brain Injury: What We Know and What We Should Know
Gupte, R. P., Brooks, W. M., Vukas, R. R., Pierce, J. D., & Harris, J. L. (2019) · Journal of Neurotrauma · doi:10.1089/neu.2018.6171 · Cited by 533 · see citing works
Sex differences in anxiety and depression: Role of testosterone
McHenry, J. A., Carrier, N., Hull, E. M., & Kabbaj, M. (2013) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2013.09.001 · Cited by 505 · see citing works
Neurogenesis in the embryonic and adult brain: same regulators, different roles
Urbán, N., & Guillemot, F. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00396 · Cited by 493 · see citing works
Sex Differences and the Impact of Steroid Hormones on the Developing Human Brain
Neufang, S., Specht, K., Hausmann, M., Güntürkün, O., Herpertz‐Dahlmann, B., Fink, G. R., & Konrad, K. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhn100 · Cited by 421 · see citing works
Uncovering the mechanisms of estrogen effects on hippocampal function
Spencer-Segal, J. L., Waters, E. M., Romeo, R. D., Wood, G. E., Milner, T. A., & McEwen, B. S. (2007) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2007.08.006 · Cited by 415 · see citing works
Rodríguez, J. J., Jones, V. C., Tabuchi, M., Allan, S. M., Knight, E. M., LaFerla, F. M., Oddo, S., & Verkhratsky, A. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002935 · Cited by 377 · see citing works
Gender Differences in the Effects of Prenatal Stress on Brain Development and Behaviour
Weinstock, M. (2007) · Neurochemical Research · doi:10.1007/s11064-007-9339-4 · Cited by 349 · see citing works
Pawluski, J. L., Brummelte, S., Barha, C. K., Crozier, T. M., & Galea, L. A. M. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2009.03.007 · Cited by 306 · see citing works
Self-citationSpritzer, M. D., & Galea, L. A. M. (2007) · Developmental Neurobiology · doi:10.1002/dneu.20457 · Cited by 277 · see citing works
Self-citationBramen, J. E., Hranilovich, J. A., Dahl, R. E., Forbes, E. E., Chen, J., Toga, A. W., Dinov, I. D., Worthman, C. M., & Sowell, E. R. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq137 · Cited by 266 · see citing works
Neuroactive steroids: State of the art and new perspectives
Melcangi, R. C., García‐Segura, L. M., & Mensah‐Nyagan, A. G. (2007) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-007-7403-5 · Cited by 232 · see citing works
Gender Differences in Human Brain: A Review
Zaidi, Z. F. (2010) · The Open Anatomy Journal · doi:10.2174/1877609401002010037 · Cited by 229 · see citing works
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Garcia‐Segura, L. M. (2008) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01713.x · Cited by 209 · see citing works
Reproductive experience alters hippocampal neurogenesis during the postpartum period in the dam
Pawluski, J. L., & Galea, L. A. M. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.07.031 · Cited by 209 · see citing works
Self-citationOpposite effects of early maternal deprivation on neurogenesis in male versus female rats
Oomen, C. A., Girardi, C. E. N., Cahyadi, R., Verbeek, E. C., Krugers, H., Joëls, M., & Lucassen, P. J. (2009) · PLoS ONE · doi:10.1371/journal.pone.0003675 · Cited by 190 · see citing works
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Barha, C. K., & Galea, L. A. M. (2010) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2010.01.006 · Cited by 188 · see citing works
Self-citationDiotel, N., Charlier, T. D., d’Hellencourt, C. L., Couret, D., Trudeau, V. L., Cano‐Nicolau, J., Meilhac, O., Kah, O., & Pellegrini, E. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00084 · Cited by 188 · see citing works
Hippocampal volume and functional connectivity changes during the female menstrual cycle
Lisofsky, N., Mårtensson, J., Eckert, A., Lindenberger, U., Gallinat, J., & Kühn, S. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2015.06.012 · Cited by 185 · see citing works
A developmental sex difference in hippocampal neurogenesis is mediated by endogenous oestradiol
Bowers, J. M., Waddell, J., & McCarthy, M. M. (2010) · Biology of Sex Differences · doi:10.1186/2042-6410-1-8 · Cited by 181 · see citing works
Rayen, I., van den Hove, D., Prickaerts, J., Steinbusch, H. W. M., & Pawluski, J. L. (2011) · PLoS ONE · doi:10.1371/journal.pone.0024003 · Cited by 175 · see citing works
Self-citationStress and adolescent hippocampal neurogenesis: diet and exercise as cognitive modulators
Hueston, C. M., Cryan, J. F., & Nolan, Y. M. (2017) · Translational Psychiatry · doi:10.1038/tp.2017.48 · Cited by 171 · see citing works
Wainwright, S. R., & Galea, L. A. M. (2013) · Neural Plasticity · doi:10.1155/2013/805497 · Cited by 164 · see citing works
Self-citationNeurogenesis in Alzheimer’s disease
Rodriguez, J. J., & Verkhratsky, A. (2011) · Journal of Anatomy · doi:10.1111/j.1469-7580.2011.01343.x · Cited by 163 · see citing works
Effects of estradiol in adult neurogenesis and brain repair in zebrafish
Diotel, N., Vaillant, C., Gabbero, C., Mironov, S., Fostier, A., Guéguen, M., Anglade, I., Kah, O., & Pellegrini, E. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.04.003 · Cited by 160 · see citing works
Okamoto, M., Hojo, Y., Inoue, K., Matsui, T., Kawato, S., McEwen, B. S., & Soya, H. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1210023109 · Cited by 157 · see citing works
Witte, A. V., Savli, M., Holik, A., Kasper, S. F., & Lanzenberger, R. R. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2009.09.046 · Cited by 152 · see citing works
Tuscher, J. J., Luine, V., Frankfurt, M., & Frick, K. M. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.3135-15.2016 · Cited by 149 · see citing works
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Melcangi, R. C., Panzica, G., & García‐Segura, L. M. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.06.024 · Cited by 143 · see citing works
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Lagace, D. C., Fischer, S. J., & Eisch, A. J. (2007) · Hippocampus · doi:10.1002/hipo.20265 · Cited by 139 · see citing works
Music facilitate the neurogenesis, regeneration and repair of neurons.
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Activity Dependency and Aging in the Regulation of Adult NeurogenesisPreprint
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Brain plasticity and recovery from early cortical injury
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The birth of new neurons in the maternal brain: Hormonal regulation and functional implications
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Green, A. D., & Galea, L. A. M. (2008) · Hormones and Behavior · doi:10.1016/j.yhbeh.2008.02.023 · Cited by 109 · see citing works
Self-citationKikusui, T., Ichikawa, S., & Mori, Y. (2009) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2008.12.009 · Cited by 108 · see citing works
Aromatase, brain sexualization and plasticity: the fish paradigm
Page, Y. L., Diotel, N., Vaillant, C., Pellegrini, E., Anglade, I., Mérot, Y., & Kah, O. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07519.x · Cited by 103 · see citing works
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Sotiropoulos, I., Cerqueira, J., Catania, C., Takashima, A., Sousa, N., & Almeida, O. F. X. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.05.007 · Cited by 101 · see citing works
Roughton, K., Kalm, M., & Blomgren, K. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08197.x · Cited by 100 · see citing works
Aromatase distribution in the monkey temporal neocortex and hippocampus
Yagüe, J. G., Wang, A. C., Janssen, W. G. M., Hof, P. R., García‐Segura, L. M., Azcoitia, Í., & Morrison, J. H. (2008) · Brain Research · doi:10.1016/j.brainres.2008.02.061 · Cited by 96 · see citing works
Adult Hippocampal Neurogenesis in Natural Populations of MammalsPreprint
Amrein, I. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a021295 · Cited by 96 · see citing works
Carrier, N., & Kabbaj, M. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.03.001 · Cited by 92 · see citing works
Brain microglia express steroid-converting enzymes in the mouse
Gottfried‐Blackmore, A., Sierra, A., Jellinck, P. H., McEwen, B. S., & Bulloch, K. (2008) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2007.12.013 · Cited by 90 · see citing works
Estrogen effects on cognition and hippocampal transcription in middle-aged mice
Aenlle, K. K., Kumar, A., Cui, L., Jackson, T. C., & Foster, T. C. (2007) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2007.09.004 · Cited by 90 · see citing works
Mandyam, C. D., Crawford, E. F., Eisch, A. J., RIVIER, C. L., & Richardson, H. N. (2008) · Developmental Neurobiology · doi:10.1002/dneu.20600 · Cited by 89 · see citing works
Harburg, G. C., Hall, F. S., Harrist, A. V., Sora, I., Uhl, G. R., & Eisch, A. J. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2006.09.018 · Cited by 87 · see citing works
Testosterone and social isolation influence adult neurogenesis in the dentate gyrus of male rats
Spritzer, M. D., Ibler, E., Inglis, W., & Curtis, M. G. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.08.034 · Cited by 81 · see citing works
Self-citationThe Impact of Estradiol on Neurogenesis and Cognitive Functions in Alzheimer’s Disease
Negah, S. S., Hajali, V., Moradi, H. R., & Gorji, A. (2019) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-019-00733-0 · Cited by 83 · see citing works
Arias, C., Zepeda, A., Hernández‐Ortega, K., Leal‐Galicia, P., Lojero, C., & Camacho‐Arroyo, I. (2008) · Hormones and Behavior · doi:10.1016/j.yhbeh.2008.10.016 · Cited by 83 · see citing works
Decreased proliferation of hippocampal progenitor cells in APPswe/PS1dE9 transgenic mice
Taniuchi, N., Niidome, T., Goto, Y., Akaike, A., Kihara, T., & Sugimoto, H. (2007) · Neuroreport · doi:10.1097/wnr.0b013e3282f1c9e9 · Cited by 79 · see citing works
Barker, J. M., & Galea, L. A. M. (2009) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2009.05.008 · Cited by 78 · see citing works
Self-citationPhysiological control of elaborate male courtship: Female choice for neuromuscular systems
Fusani, L., Barske, J., Day, L. B., Fuxjager, M. J., & Schlinger, B. A. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.07.017 · Cited by 78 · see citing works
Burkitt, J., Widman, D., & Saucier, D. M. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.03.007 · Cited by 76 · see citing works
ÖZAÇMAK, V. H., & Sayan, H. (2009) · Physiological Research · doi:10.33549/physiolres.931647 · Cited by 75 · see citing works
Sex steroids and the dentate gyrus
Hajszán, T., Milner, T. A., & Leranth, C. (2007) · Progress in brain research · doi:10.1016/s0079-6123(07)63023-4 · Cited by 73 · see citing works
Changes in Hippocampal Plasticity in Depression and Therapeutic Approaches Influencing These Changes
Xu, W., Yao, X., Zhao, F., Zhao, H., Cheng, Z., Yang, W., Cui, R., Xu, S., & Li, B. (2020) · Neural Plasticity · doi:10.1155/2020/8861903 · Cited by 73 · see citing works
Barker, J. M., Boonstra, R., & Wojtowicz, J. M. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07823.x · Cited by 72 · see citing works
Self-citationNonclassical Progesterone Signalling Molecules in the Nervous System
Petersen, S. L., Intlekofer, K. A., Moura-Conlon, P. J., Brewer, D. N., del Pino, J., & Lopez, J. A. (2013) · Journal of Neuroendocrinology · doi:10.1111/jne.12060 · Cited by 72 · see citing works
Bryan, K. J., Mudd, J. C., Richardson, S. L., Chang, J., Lee, H., Zhu, X., Smith, M. A., & Casadesús, G. (2009) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2009.06502.x · Cited by 70 · see citing works
Calingasan, N. Y., Ho, D. J., Wille, E. J., Campagna, M. V., Ruan, J., Dumont, M., Yang, L., Shi, Q., Gibson, G. E., & Beal, M. F. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.02.071 · Cited by 69 · see citing works
Gomes, F. G. N., Fernandes, J., Campos, D. V., Cassilhas, R. C., Viana, G. M., D’Almeida, V., Rêgo, M. K. D. M., Buainain, P. I., Cavalheiro, É. A., & Arida, R. M. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.08.009 · Cited by 69 · see citing works
Hauger, R. L., Saelzler, U. G., Pagadala, M. S., & Panizzon, M. S. (2022) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-022-09767-0 · Cited by 68 · see citing works
Steroid modulation of neurogenesis: Focus on radial glial cells in zebrafish
Pellegrini, E., Diotel, N., Vaillant, C., Maria, R. P., Guéguen, M., Nasri, A., Cano‐Nicolau, J., & Kah, O. (2015) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2015.06.011 · Cited by 66 · see citing works
Neuroprotective effects of estradiol in hippocampal neurons and glia of middle age mice
Saravia, F., Beauquis, J., Pietranera, L., & Nicola, A. F. D. (2007) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2007.02.012 · Cited by 67 · see citing works
Douet, V., Chang, L., Cloak, C., & Ernst, T. (2013) · Brain Imaging and Behavior · doi:10.1007/s11682-013-9260-1 · Cited by 65 · see citing works
Gemmel, M., Bögi, E., Ragan, C. M., Hazlett, M. F., Dubovický, M., van den Hove, D., Oberlander, T. F., Charlier, T. D., & Pawluski, J. L. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.04.023 · Cited by 65 · see citing works
Self-citationCrozier, J. C., Wang, L., Huettel, S. A., & De Bellis, M. D. (2014) · Development and Psychopathology · doi:10.1017/s095457941400008x · Cited by 64 · see citing works
Pletzer, B., Winkler-Crepaz, K., & Hillerer, K. (2023) · Frontiers in neuroendocrinology (Print) · doi:10.1016/j.yfrne.2023.101060 · Cited by 52 · see citing works
Pup exposure elicits hippocampal cell proliferation in the prairie vole
Ruscio, M. G., Sweeny, T. D., Hazelton, J. L., Suppatkul, P., Boothe, E., & Carter, C. S. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.08.028 · Cited by 62 · see citing works
Hippocampal Gene Expression Is Highly Responsive to Estradiol Replacement in Middle-Aged Female Rats
Sárvári, M., Kalló, I., Hrabovszky, E., Solymosi, N., Rodolosse, A., Vastagh, C., Auer, H., & Liposits, Z. (2015) · Endocrinology · doi:10.1210/en.2015-1109 · Cited by 60 · see citing works
Seiger, R., Hahn, A., Hummer, A., Kranz, G., Ganger, S., Woletz, M., Kraus, C., Sladky, R., Kautzky, A., Kasper, S., et al. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.09.028 · Cited by 55 · see citing works
Aromatase expression in the normal and epileptic human hippocampus
Yagüe, J. G., Azcoitia, Í., DeFelipe, J., García‐Segura, L. M., & Muñoz, A. (2009) · Brain Research · doi:10.1016/j.brainres.2009.09.111 · Cited by 58 · see citing works
Marín, R., & Díaz, M. L. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00128 · Cited by 58 · see citing works
Mouriec, K., Pellegrini, E., Anglade, I., Menuet, A., Adrio, F., Thieulant, M.-L., Pakdel, F., & Kah, O. (2007) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2007.10.030 · Cited by 58 · see citing works
Brock, O., Keller, M., Veyrac, A., Douhard, Q., & Bakker, J. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2009.12.050 · Cited by 57 · see citing works
The Effect of Testosterone on the Formation of Brain Structures
Filová, B., Ostatníková, D., Celec, P., & Hodosy, J. (2013) · Cells Tissues Organs · doi:10.1159/000345567 · Cited by 56 · see citing works
Rayen, I., Gemmel, M., Pauley, G., Steinbusch, H. W. M., & Pawluski, J. L. (2014) · Psychopharmacology · doi:10.1007/s00213-014-3758-0 · Cited by 55 · see citing works
Self-citationCurlik, D. M., DiFeo, G., & Shors, T. J. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00070 · Cited by 55 · see citing works
Temporal lobe epilepsy and the BDNF receptor, TrkB
McNamara, J. O., & Scharfman, H. E. (2010) · Epilepsia · doi:10.1111/j.1528-1167.2010.02832.x · Cited by 54 · see citing works
Estrogen activates Alzheimer's disease genes
Ratnakumar, A., Zimmerman, S. E., Jordan, B. A., & Mar, J. C. (2019) · Alzheimer s & Dementia Translational Research & Clinical Interventions · doi:10.1016/j.trci.2019.09.004 · Cited by 52 · see citing works
Effects of testosterone on orchiectomy-induced oxidative damage in the rat hippocampus
Meydan, S., Kuş, İ., Taş, U., Ögetürk, M., Sancakdar, E., Dabak, D. Ö., Zararsız, İ., & Sarsılmaz, M. (2010) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2010.07.006 · Cited by 53 · see citing works
Woon, F. L. M., & Hedges, D. W. (2010) · Hippocampus · doi:10.1002/hipo.20746 · Cited by 52 · see citing works
Endocrine and social regulation of adult neurogenesis in songbirds
Balthazart, J., & Ball, G. F. (2016) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2016.03.003 · Cited by 51 · see citing works
Sex differences in adult cell proliferation within the zebrafish (Danio rerio) cerebellum
Ampatzis, K., & Dermon, C. R. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05366.x · Cited by 52 · see citing works
Moyse, E., Segura, S., Liard, O., Mahaut, S., & Mechawar, N. (2008) · Current Stem Cell Research & Therapy · doi:10.2174/157488808785740334 · Cited by 51 · see citing works
Bless, E., Reddy, T., Acharya, K. D., Beltz, B., & Tetel, M. (2014) · Journal of neuroendocrinology · doi:10.1111/jne.12206 · Cited by 49 · see citing works
Brain Volumes, Cognitive Impairment, and Conjugated Equine Estrogens
Espeland, M. A., Tindle, H. A., Bushnell, C. A., Jaramillo, S. A., Kuller, L. H., Margolis, K. L., Mysiw, W. J., Maldjian, J. A., Melhem, E. R., Resnick, S. M., et al. (2009) · The Journals of Gerontology Series A · doi:10.1093/gerona/glp128 · Cited by 51 · see citing works
Manning, E. E., Ransome, M. I., Burrows, E. L., & Hannan, A. J. (2010) · Hippocampus · doi:10.1002/hipo.20900 · Cited by 47 · see citing works
Estrogens, hormone therapy, and hippocampal volume in postmenopausal women
Wnuk, A., Korol, D. L., & Erickson, K. I. (2012) · Maturitas · doi:10.1016/j.maturitas.2012.07.001 · Cited by 47 · see citing works
Balthazart, J., & Ball, G. F. (2014) · The Journal of Comparative Neurology · doi:10.1002/cne.23661 · Cited by 46 · see citing works
Diotel, N., Vaillant, C., Kah, O., & Pellegrini, E. (2015) · Gene Expression Patterns · doi:10.1016/j.gep.2015.11.003 · Cited by 46 · see citing works
Is there a neuroendocrinological rationale for testosterone as a therapeutic option in depression?
Ebinger, M., Sievers, C., Ivan, D., Schneider, H., & Stalla, G. K. (2008) · Journal of Psychopharmacology · doi:10.1177/0269881108092337 · Cited by 45 · see citing works
Regulation of adult hippocampal neurogenesis: relevance to depression
Vaidya, V. A., Fernandes, K. A., & Jha, S. (2007) · Expert Review of Neurotherapeutics · doi:10.1586/14737175.7.7.853 · Cited by 43 · see citing works
Temporal Lobe Epilepsy and the BDNF Receptor, TrkB
McNamara, J. O., & Scharfman, H. E. (2012) · Oxford University Press eBooks · doi:10.1093/med/9780199746545.003.0039 · Cited by 43 · see citing works
Bencker, C., Gschwandtner, L. P., Nayman, S., Grikšienė, R., Nguyen, B., Nater, U. M., Guennoun, R., Poromaa, I. S., Pletzer, B. A., Bixo, M., et al. (2024) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2024.101160 · Cited by 52 · see citing works
Pechenino, A. S., & Frick, K. M. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.09.017 · Cited by 42 · see citing works
Ho, S. W., Tsui, Y. T. C., Wong, T. T., Cheung, S. K.-K., Goggins, W. B., Yi, L. M., Cheng, K. K., & Baum, L. (2013) · Translational Neurodegeneration · doi:10.1186/2047-9158-2-24 · Cited by 42 · see citing works
- Authors
- Galea, L. A. M., Spritzer, M. D., Barker, J. M., & Pawluski, J. L.
- Affiliations
- University of British Columbia (CA)
- Corresponding author
- Galea, Liisa A.M.
- Venue
- Hippocampus
- Publisher
- Wiley
- Published
- 2006-01
- Volume
- 16
- Issue
- 3
- Pages
- 225-232
- ISSN
- 1050-9631 (ISSN-L)
- 1098-1063
- OpenAlex
- W1995175293
- Cited by
- 238
- References
- 66
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 5 · 2023: 3 · 2022: 8 · 2021: 5 · 2020: 7 · 2019: 10 · 2018: 6 · 2017: 7 · 2016: 14 · 2015: 13 · 2014: 17 · 2013: 17 · 2012: 22
- FWCI
- 1.45
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Hippocampus (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- gonadal hormones, adult neurogenesis, dentate gyrus, estradiol, testosterone, progesterone, neurosteroids, allopregnanolone, cell proliferation, cell survival, gender differences, pregnancy, motherhood, rodents
- MeSH terms
- Animals, Cell Differentiation, Female, Male, Neuronal Plasticity, Neurons, Reproduction, Sex Characteristics, Gonadal Steroid Hormones, Stem Cells, Dentate Gyrus, Cell Proliferation
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