[en] Testosterone aromatization into estrogens in the preoptic area (POA) is critical for the activation of male sexual behavior in many vertebrates. Yet, cellular mechanisms mediating actions of neuroestrogens on sexual behavior remain largely unknown. We investigated in male and female Japanese quail by dual-label fluorescent in situ hybridization (FISH) whether aromatase-positive (ARO) neurons express glutamic acid decarboxylase 67 (GAD67), the rate-limiting enzyme in GABA biosynthesis. AROcells and ARO cells double labeled with GAD67 (ARO-GAD67) were counted at standardized locations in the medial preoptic nucleus (POM) and the medial bed nucleus of the stria terminalis (BST) to produce three-dimensional distribution maps. Overall, males had more ARO cells than females in POM and BST. The numberof double-labeled ARO-GAD67 cells was also higher in males than in females and greatly varied as a function of the specific position in these nuclei. Significant sex differences were however present only in the most caudal part of POM.Although both ARO and GAD67 were expressed in the VMN, no colocalization between these markers was detected.Together, these data show that a high proportion of estrogen synthesizing neurons in POM and BST are inhibitory and the colocalization of GAD67 with AROexhibits a high degree of anatomical specificity as well as localized sex differences. The fact that many preoptic ARO neurons project to the periaqueductal gray in male quail suggests possible mechanisms through which locally produced estrogens could activate male sexual behavior.
Research center :
Giga-Neurosciences - ULiège
Disciplines :
Neurosciences & behavior
Author, co-author :
Cornil, Charlotte ; Université de Liège - ULiège > Neurosciences-Neuroendocrinology
Ball, Gregory F.
Balthazart, Jacques ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Département des sciences biomédicales et précliniques
Language :
English
Title :
Sexually differentiated and neuroanatomically specific co-expression of aromatase neurons and GAD67 in the male and female quail brain
Publication date :
2020
Journal title :
European Journal of Neuroscience
ISSN :
0953-816X
eISSN :
1460-9568
Publisher :
Blackwell, Oxford, United Kingdom
Volume :
52
Issue :
3
Pages :
2963-2981
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
NIH - National Institutes of Health [US-MD] F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE] ULiège - Université de Liège [BE]
Absil, P., Riters, L. V., & Balthazart, J. (2001). Preoptic aromatase cells project to the mesencephalic central gray in the male Japanese quail (Coturnix japonica). Hormones and Behavior, 40, 369–383. https://doi.org/10.1006/hbeh.2001.1702
Acconcia, F., Ascenzi, P., Bocedi, A., Spisni, E., Tomasi, V., Trentalance, A., … Marino, M. (2005). Palmitoylation-dependent estrogen receptor alpha membrane localization: Regulation by 17beta-estradiol. Molecular Biology of the Cell, 16, 231–237.
Adkins, E. K. (1975). Hormonal basis of sexual differentiation in the Japanese quail. Journal of Comparative and Physiological Psychology, 89, 61–71.
Aste, N., Panzica, G. C., Aimar, P., Viglietti-Panzica, C., Harada, N., Foidart, A., & Balthazart, J. (1994). Morphometric studies demonstrate that aromatase-immunoreactive cells are the main target of androgens and estrogens in the quail medial preoptic nucleus. Experimental Brain Research, 101, 241–252. https://doi.org/10.1007/BF00228744
Aste, N., Panzica, G. C., Viglietti-Panzica, C., & Balthazart, J. (1991). Effects of in ovo estradiol benzoate treatments on sexual behavior and size of neurons in the sexually dimorphic medial preoptic nucleus of Japanese quail. Brain Research Bulletin, 27, 713–720. https://doi.org/10.1016/0361-9230(91)90051-K
Ball, G. F., & Balthazart, J. (2010). Japanese quail as a model system for studying the neuroendocrine control of reproductive and social behaviors. ILAR Journal, 51, 310–325. https://doi.org/10.1093/ilar.51.4.310
Balthazart, J., Absil, P., Gérard, M., Appeltants, D., & Ball, G. F. (1998). Appetitive and consummatory male sexual behavior in Japanese quail are differentially regulated by subregions of the preoptic medial nucleus. Journal of Neuroscience, 18, 6512–6527.
Balthazart, J., Baillien, M., Cornil, C. A., & Ball, G. F. (2004). Preoptic aromatase modulates male sexual behavior: Slow and fast mechanisms of action. Physiology and Behavior, 83, 247–270. https://doi.org/10.1016/j.physbeh.2004.08.025
Balthazart, J., & Ball, G. F. (2006). Is brain estradiol a hormone or a neurotransmitter? Trends in Neurosciences, 29, 241–249. https://doi.org/10.1016/j.tins.2006.03.004
Balthazart, J., & Ball, G. F. (2007). Topography in the preoptic region: Differential regulation of appetitive and consummatory male sexual behaviors. Frontiers in Neuroendocrinology, 28, 161–178. https://doi.org/10.1016/j.yfrne.2007.05.003
Balthazart, J., & Ball, G. F. (2013). Brain aromatase, estrogens and behavior. New York, NY: Oxford University Press.
Balthazart, J., Foidart, A., Surlemont, C., & Harada, N. (1991). Neuroanatomical specificity in the co-localization of aromatase and estrogen receptors. Journal of Neurobiology, 22, 143–157. https://doi.org/10.1002/neu.480220205
Balthazart, J., Foidart, A., Surlemont, C., Vockel, A., & Harada, N. (1990). Distribution of aromatase in the brain of the Japanese quail, ring dove, and zebra finch: An immunocytochemical study. The Journal of Comparative Neurology, 301, 276–288. https://doi.org/10.1002/cne.903010210
Balthazart, J., Schumacher, M., & Ottinger, M. A. (1983). Sexual differences in the Japanese quail: Behavior, morphology and intracellular metabolism of testosterone. General and Comparative Endocrinology, 51, 191–207.
Balthazart, J., Surlemont, C., & Harada, N. (1992). Aromatase as a cellular marker of testosterone action in the preoptic area. Physiology and Behavior, 51, 395–409. https://doi.org/10.1016/0031-9384(92)90158-X
Balthazart, J., Tlemçani, O., & Harada, N. (1996). Localization of testosterone-sensitive and sexually dimorphic aromatase-immunoreactive cells in the quail preoptic area. Journal of Chemical Neuroanatomy, 11, 147–171. https://doi.org/10.1016/0891-0618(96)00149-4
Balthazart, J., Tlemçani, O., Harada, N., & Baillien, M. (2000). Ontogeny of aromatase and tyrosine hydroxylase activity and of aromatase-immunoreactive cells in the preoptic area of male and female Japanese quail. Journal of Neuroendocrinology, 12, 853–866.
Bayless, D. W., Yang, T., Mason, M. M., Susanto, A. A. T., Lobdell, A., & Shah, N. M. (2019). Limbic neurons shape sex recognition and social behavior in sexually naive males. Cell, 176, 1190–1205.e1120. https://doi.org/10.1016/j.cell.2018.12.041
Beyer, C., Green, S. J., Barker, P. J., Huskisson, N. S., & Hutchison, J. B. (1994). Aromatase-immunoreactivity is localised specifically in neurones in the developing mouse hypothalamus and cortex. Brain Research, 638, 203–210.
Bondar, G., Kuo, J., Hamid, N., & Micevych, P. (2009). Estradiol-induced estrogen receptor-alpha trafficking. The Journal of Neuroscience, 29, 15323–15330.
Brackett, N. L., Iuvone, P. M., & Edwards, D. A. (1986). Midbrain lesions, dopamine and male sexual behavior. Behavioral Brain Research, 20, 231–240. https://doi.org/10.1016/0166-4328(86)90006-9
Carere, C., Ball, G. F., & Balthazart, J. (2007). Sex differences in projections from preoptic area aromatase cells to the periaqueductal gray in Japanese quail. Journal of Comparative Neurology, 500, 894–907. https://doi.org/10.1002/cne.21210
Charlier, T. D., Harada, N., Balthazart, J., & Cornil, C. A. (2011). Human and quail aromatase activity is rapidly and reversibly inhibited by phosphorylating conditions. Endocrinology, 152, 4199–4210. https://doi.org/10.1210/en.2011-0119
Cornil, C. A. (2009). Rapid regulation of brain oestrogen synthesis: The behavioural roles of oestrogens and their fates. Journal of Neuroendocrinology, 21, 217–226. https://doi.org/10.1111/j.1365-2826.2009.01822.x
Cornil, C. A. (2018). On the role of brain aromatase in females: Why are estrogens produced locally when they are available systemically?. Journal of Comparative Physiology A, Neuroethology, Sensory, Neural, and Behavioral Physiology, 204, 31–49. https://doi.org/10.1007/s00359-017-1224-2
Cornil, C. A. (2019). The organization and activation of sexual behavior in quail. In M. Ludwig & G. Levkowitz (Eds.), Model animals in neuroendocrinology: From worm to mouse to man (pp. 464). Hoboken, NJ: Wiley.
Cornil, C. A., Ball, G. F., & Balthazart, J. (2015). The dual action of estrogen hypothesis. Trends in Neurosciences, 38, 408–416. https://doi.org/10.1016/j.tins.2015.05.004
Cornil, C. A., Leung, C. H., Pletcher, E. R., Naranjo, K. C., Blauman, S. J., & Saldanha, C. J. (2012). Acute and specific modulation of presynaptic aromatization in the vertebrate brain. Endocrinology, 153, 2562–2567. https://doi.org/10.1210/en.2011-2159
Cornil, C. A., Seutin, V., Motte, P., & Balthazart, J. (2004). Electrophysiological and neurochemical characterization of neurons of the medial preoptic area in Japanese quail (Coturnix japonica). Brain Research, 1029, 224–240. https://doi.org/10.1016/j.brainres.2004.09.047
de Bournonville, C., Dickens, M. J., Ball, G. F., Balthazart, J., & Cornil, C. A. (2013). Dynamic changes in brain aromatase activity following sexual interactions in males: Where, when and why? Psychoneuroendocrinology, 38, 789–799. https://doi.org/10.1016/j.psyneuen.2012.09.001
de Bournonville, C., Smolders, I., Van Eeckhaut, A., Ball, G. F., Balthazart, J., & Cornil, C. A. (2017). Glutamate released in the preoptic area during sexual behavior controls local estrogen synthesis in male quail. Psychoneuroendocrinology, 79, 49–58. https://doi.org/10.1016/j.psyneuen.2017.02.002
de Bournonville, M. P., de Bournonville, C., Ball, G. F., Balthazart, J., & Cornil, C. A. (2017). Rapid changes in preoptic estradiol concentration during male sexual behavior. Abstract. Society for Neuroscience, Washington DC, 67.04/HH10.
Dickens, M. J., Cornil, C. A., & Balthazart, J. (2011). Acute stress differentially affects aromatase activity in specific brain nuclei of adult male and female quail. Endocrinology, 152, 4242–4251. https://doi.org/10.1210/en.2011-1341
Dickens, M. J., de Bournonville, C., Balthazart, J., & Cornil, C. A. (2014). Relationships between rapid changes in local aromatase activity and estradiol concentrations in male and female quail brain. Hormones and Behavior, 65, 154–164. https://doi.org/10.1016/j.yhbeh.2013.12.011
Dominguez, J. M., Gil, M., & Hull, E. M. (2006). Preoptic glutamate facilitates male sexual behavior. The Journal of Neuroscience, 26, 1699–1703. https://doi.org/10.1523/JNEUROSCI.4176-05.2006
Foidart, A., de Clerck, A., Harada, N., & Balthazart, J. (1994). Aromatase-immunoreactive cells in the quail brain: Effects of testosterone and sex dimorphism. Physiology & Behavior, 55, 453–464. https://doi.org/10.1016/0031-9384(94)90100-7
Foidart, A., Reid, J., Absil, P., Yoshimura, N., Harada, N., & Balthazart, J. (1995). Critical re-examination of the distribution of aromatase-immunoreactive cells in the quail forebrain using antibodies raised against human placental aromatase and against the recombinant quail, mouse or human enzyme. Journal of Chemical Neuroanatomy, 8, 267–282. https://doi.org/10.1016/0891-0618(95)00054-B
Gahr, M., & Garcia-Segura, L. M. (1996). Testosterone-dependent increase of gap-junctions in HVC neurons of adult female canaries. Brain Research, 712, 69–73.
Garcia-Segura, L. M., Wozniak, A., Azcoitia, I., Rodriguez, J. R., Hutchison, R. E., & Hutchison, J. B. (1999). Aromatase expression by astrocytes after brain injury: Implications for local estrogen formation in brain repair. Neuroscience, 89, 567–578. https://doi.org/10.1016/S0306-4522(98)00340-6
Huang, G. Z., & Woolley, C. S. (2012). Estradiol acutely suppresses inhibition in the hippocampus through a sex-specific endocannabinoid and mGluR-dependent mechanism. Neuron, 74, 801–808. https://doi.org/10.1016/j.neuron.2012.03.035
Hull, E. M., Meisel, R. L., & Sachs, B. D. (2002). Male sexual behavior. In D. W. Pfaff, A. P. Arnold, A. M. Etgen, S. E. Fahrbach, & R. T. Rubin (Eds.), Hormones, brain and behavior (pp. 1–137). San Diego, CA: Academic Press.
Hull, E. M., & Rodriguez-Manzo, G. (2009). Male sexual behavior. In D. W. Pfaff, A. P. Arnold, A. M. Etgen, S. E. Fahrbach, & R. T. Rubin (Eds.), Hormones, brain and behavior (pp. 5–65). San Diego, CA: Academic Press.
Ikeda, M. Z., Krentzel, A. A., Oliver, T. J., Scarpa, G. B., & Remage-Healey, L. (2017). Clustered organization and region-specific identities of estrogen-producing neurons in the forebrain of Zebra Finches (Taeniopygia guttata). The Journal of Comparative Neurology, 525, 3636–3652.
Jeong, J. K., Burrows, K., Tremere, L. A., & Pinaud, R. (2011). Neurochemical organization and experience-dependent activation of estrogen-associated circuits in the songbird auditory forebrain. The European Journal of Neuroscience, 34, 283–291. https://doi.org/10.1111/j.1460-9568.2011.07743.x
Jeong, J. K., Terleph, T. A., Burrows, K., Tremere, L. A., & Pinaud, R. (2011). Expression and rapid experience-dependent regulation of type-A GABAergic receptors in the songbird auditory forebrain. Developmental Neurobiology, 71, 803–817. https://doi.org/10.1002/dneu.20896
Kramar, E. A., Chen, L. Y., Brandon, N. J., Rex, C. S., Liu, F., Gall, C. M., & Lynch, G. (2009). Cytoskeletal changes underlie estrogen’s acute effects on synaptic transmission and plasticity. Journal of Neuroscience, 29, 12982–12993. https://doi.org/10.1523/JNEUROSCI.3059-09.2009
Kuenzel, W. J., & Masson, M. (1988). A stereotaxic atlas of the brain of the chick (Gallus domesticus). Baltimore, MD: The Johns Hopkins University Press.
McEwen, B. S., & Milner, T. A. (2017). Understanding the broad influence of sex hormones and sex differences in the brain. Journal of Neuroscience Research, 95, 24–39.
Meddle, S. L., King, V. M., Follett, B. K., Wingfield, J. C., Ramenofsky, M., Foidart, A., & Balthazart, J. (1997). Copulation activates Fos-like immunoreactivity in the male quail forebrain. Behavioral Brain Research, 85, 143–159.
Mermelstein, P. G. (2009). Membrane-localised oestrogen receptor alpha and beta influence neuronal activity through activation of metabotropic glutamate receptors. Journal of Neuroendocrinology, 21, 257–262.
Morrell, J. I., Kelley, D. B., & Pfaff, D. W. (1975). Sex steroid binding in the brain of vertebrates. In K. M. Knigge, D. E. Scott, H. Kobayashi, S. Miura, & S. Ishii (Eds.), Brain-endocrine interactions II (pp. 230–256). Basel, Switzerland: Karger.
Murphy, A. Z., & Hoffman, G. E. (2001). Distribution of gonadal steroid receptor-containing neurons in the preoptic-periaqueductal gray-brainstem pathway: A potential circuit for the initiation of male sexual behavior. The Journal of Comparative Neurology, 438, 191–212. https://doi.org/10.1002/cne.1309
Murphy, A. Z., Rizvi, T. A., Ennis, M., & Shipley, M. T. (1999). The organization of preoptic-medullary circuits in the male rat: Evidence for interconnectivity of neural structures involved in reproductive behavior, antinociception and cardiovascular regulation. Neuroscience, 91, 1103–1116. https://doi.org/10.1016/S0306-4522(98)00677-0
Murphy, A. Z., Shupnik, M. A., & Hoffman, G. E. (1999). Androgen and estrogen (alpha) receptor distribution in the periaqueductal gray of the male rat. Hormones and Behavior, 36, 98–108.
Naftolin, F., Horvath, T. L., Jakab, R. L., Leranth, C., Harada, N., & Balthazart, J. (1996). Aromatase immunoreactivity in axon terminals of the vertebrate brain: An immunocytochemical study on quail, rat, monkey and human tissues. Neuroendocrinology, 63, 149–155. https://doi.org/10.1159/000126951
Naftolin, F., Ryan, K. J., Davies, I. J., Reddy, V. V., Flores, F., Petro, Z., … Wolin, L. (1975). The formation of estrogens by central neuroendocrine tissues. Recent Progress in Hormone Research, 31, 295–319.
Normandin, J. J., & Murphy, A. Z. (2008). Nucleus paragigantocellularis afferents in male and female rats: Organization, gonadal steroid receptor expression, and activation during sexual behavior. The Journal of Comparative Neurology, 508, 771–794. https://doi.org/10.1002/cne.21704
Oberlander, J. G., & Woolley, C. S. (2016). 17beta-estradiol acutely potentiates glutamatergic synaptic transmission in the hippocampus through distinct mechanisms in males and females. The Journal of Neuroscience, 36, 2677–2690.
O'Malley, B. W., & Tsai, M.-J. (1992). Molecular pathways of steroid receptor action. Biology of Reproduction, 46, 163–167.
Panzica, G. C., Viglietti-Panzica, C., & Balthazart, J. (1996). The sexually dimorphic medial preoptic nucleus of quail: A key brain area mediating steroid action on male sexual behavior. Frontiers in Neuroendocrinology, 17, 51–125. https://doi.org/10.1006/frne.1996.0002
Panzica, G., Viglietti-Panzica, C., Sanchez, F., Sante, P., & Balthazart, J. (1991). Effects of testosterone on a selected neuronal population within the preoptic sexually dimorphic nucleus of the Japanese quail. Journal of Comparative Neurology, 303, 443–456. https://doi.org/10.1002/cne.903030310
Peterson, R. S., Yarram, L., Schlinger, B. A., & Saldanha, C. J. (2005). Aromatase is pre-synaptic and sexually dimorphic in the adult zebra finch brain. Proceedings of the Royal Society B: Biological Sciences, 272, 2089–2096. https://doi.org/10.1098/rspb.2005.3181
Pfaff, D. W. (1976). The neuroanatomy of sex hormone receptors in the vertebrate brain. In T. C. Anand Kumar (Ed.), Neuroendocrine regulation of fertility (pp. 30–45). Basel, Switzerland: Karger.
Pfaff, D. W. (1980). Estrogen and brain function. New York, NY: Springer-Verlag.
Pfaff, D., & Keiner, M. (1973). Atlas of estradiol-concentrating cells in the central nervous system of the female rat. The Journal of Comparative Neurology, 151, 121–158.
Qiu, J., Ronnekleiv, O. K., & Kelly, M. J. (2008). Modulation of hypothalamic neuronal activity through a novel G-protein-coupled estrogen membrane receptor. Steroids, 73(9-10), 985–991. https://doi.org/10.1016/j.steroids.2007.11.008
Revankar, C. M., Cimino, D. F., Sklar, L. A., Arterburn, J. B., & Prossnitz, E. R. (2005). A transmembrane intracellular estrogen receptor mediates rapid cell signalling. Science, 307, 1625–1630.
Rizvi, T. A., Ennis, M., & Shipley, M. T. (1992). Reciprocal connections between the medial preoptic area and the midbrain periaqueductal gray in rat: A WGA-HRP and PHA-L study. The Journal of Comparative Neurology, 315, 1–15. https://doi.org/10.1002/cne.903150102
Rizvi, T. A., Murphy, A. Z., Ennis, M., Behbehani, M. M., & Shipley, M. T. (1996). Medial preoptic area afferents to periaqueductal gray medullo-output neurons: A combined Fos and tract tracing study. Journal of Neuroscience, 16, 333–344. https://doi.org/10.1523/JNEUROSCI.16-01-00333.1996
Rohmann, K. N., Schlinger, B. A., & Saldanha, C. J. (2007). Subcellular compartmentalization of aromatase is sexually dimorphic in the adult zebra finch brain. Developmental Neurobiology, 67, 1–9. https://doi.org/10.1002/dneu.20303
Roselli, C. (2013). The distribution and regulation of aromatase in the mammalian brain: From mice to monkeys. In J. Balthazart, & G. F. Ball (Eds.), Brain aromatase, estrogens, and behavior (pp. 43–63). Oxford, New York, NY: Oxford University Press.
Sachs, B. D. (1967). Photoperiodic control of the cloacal gland of the Japanese quail. Science, 157, 201–203. https://doi.org/10.1126/science.157.3785.201
Saldanha, C. J., Remage-Healey, L., & Schlinger, B. A. (2011). Synaptocrine signaling: Steroid synthesis and action at the synapse. Endocrine Reviews, 32, 532–549. https://doi.org/10.1210/er.2011-0004
Saldanha, C. J., Remage-Healey, L., & Schlinger, B. (2013). Neuroanatomical distribution of aromatase in birds: Cellular and subcellular analyses. In J. Balthazart, & G. F. Ball (Eds.), Brain Aromatase, estrogens, and behavior (pp. 100–114). Oxford, New York, NY: Oxford University Press.
Saldanha, C. J., Tuerk, M. J., Kim, Y. H., Fernandes, A. O., Arnold, A. P., & Schlinger, B. A. (2000). Distribution and regulation of telencephalic aromatase expression in the zebra finch revealed with a specific antibody. The Journal of Comparative Neurology, 423, 619–630.
Schlinger, B. A., & Callard, G. V. (1989). Localization of aromatase in synaptosomal and microsomal subfractions of quail (Coturnix coturnix japonica) brain. Neuroendocrinology, 49, 434–441.
Seredynski, A. L., Balthazart, J., Ball, G. F., & Cornil, C. A. (2015). Estrogen receptor beta activation rapidly modulates male sexual motivation through the transactivation of metabotropic glutamate receptor 1a. The Journal of Neuroscience, 35, 13110–13123.
Seredynski, A. L., Balthazart, J., Christophe, V. J., Ball, G. F., & Cornil, C. A. (2013). Neuroestrogens rapidly regulate sexual motivation but not performance. Journal of Neuroscience, 33, 164–174. https://doi.org/10.1523/JNEUROSCI.2557-12.2013
Simerly, R. B., & Swanson, L. W. (1986). The organization of neural inputs to the medial preoptic nucleus of the rat. The Journal of Comparative Neurology, 246, 312–342.
Smejkalova, T., & Woolley, C. S. (2010). Estradiol acutely potentiates hippocampal excitatory synaptic transmission through a presynaptic mechanism. The Journal of Neuroscience, 30, 16137–16148. https://doi.org/10.1523/JNEUROSCI.4161-10.2010
Stanic, D., Dubois, S., Chua, H. K., Tonge, B., Rinehart, N., Horne, M. K., & Boon, W. C. (2014). Characterization of aromatase expression in the adult male and female mouse brain. I. Coexistence with oestrogen receptors alpha and beta, and androgen receptors. PLoS ONE, 9, e90451.
Taziaux, M., Cornil, C. A., Dejace, C., Arckens, L., Ball, G. F., & Balthazart, J. (2006). Neuroanatomical specificity in the expression of the immediate early gene c-fos following expression of appetitive and consummatory male sexual behaviour in Japanese quail. European Journal of Neuroscience, 23, 1869–1887.
Tsai, M. J., & O'Malley, B. W. (1994). Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Annual Review of Biochemistry, 63, 451–486. https://doi.org/10.1146/annurev.bi.63.070194.002315
Unger, E. K., Burke, K. J. Jr, Yang, C. F., Bender, K. J., Fuller, P. M., & Shah, N. M. (2015). Medial amygdalar aromatase neurons regulate aggression in both sexes. Cell Reports, 10, 453–462. https://doi.org/10.1016/j.celrep.2014.12.040
Voigt, C., Ball, G. F., & Balthazart, J. (2007). Neuroanatomical specificity of sex differences in expression of aromatase mRNA in the quail brain. Journal of Chemical Neuroanatomy, 33, 75–86. https://doi.org/10.1016/j.jchemneu.2006.12.004
Wong, M., & Moss, R. L. (1992). Long-term and short-term electrophysiological effects of estrogen on the synaptic properties of hippocampal CA1 neurons. Journal of Neuroscience, 12, 3217–3225. https://doi.org/10.1523/JNEUROSCI.12-08-03217.1992
Wu, M. V., Manoli, D. S., Fraser, E. J., Coats, J. K., Tollkuhn, J., Honda, S. I., … Shah, N. M. (2009). Estrogen masculinizes neural pathways and sex-specific behaviors. Cell, 139, 61–72. https://doi.org/10.1016/j.cell.2009.07.036
