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No of Pages 9 06 September 2019 ARTICLE IN PRESS Cheng Wang et al. Neuroscience 418(2019)XXx-XXX Montag C, Reuter M, Weber B, Markett S, Schoene-Bake JC (2012) Sahingoz M, Uguz F, Gezginc K(2011)Prevalence and related factors Individual differences in trait anxiety are associated with white ma of mood and anxiety disorders in a clinical sample of postmenopau- ter tract integrity in the left temporal lobe in healthy males but not en.PerspectPsychiatrCare47(4):213-219,https://doiorg/ femalesNeuroscience217:77-83,https://doi.org/10.101 10.11111744-61632010.00296 euroscience 2012.05.017 Schneider T, Popik P(2007)Attenuation of estrous cycle-dependent Mora S, Dussaubat N, Diaz-Veliz G (1996)Effects of the estrous cycle rble burying in female rats by acute treatment with progester and ovarian hormones on behavioral indices of anxiety in female d antidepressants. Psychoneuroendocrinology 32(6): 651-659 rats. Psychoneuroendocrinology 21(7): 609-620 tt ps: //doi. org/10.1016/j-psyneuen 2007.04.003 Nelson JF, Felicio LS, Randall PK, Sims C, Finch CE. (1982)A longitu. Seeman MV(1997)Psychopathology in women and men: focus on dinal study of estrous cyclicity in aging C57BL/6J mice: I cycle fre- malehormonesAmJPsychiatry154(12):1641-1647,https://doi o, quency, length and vaginal cytology. Biol Reprod 27(2): 327-339 og/10.1176ajp.154.12.1641 Nolen-Hoeksema S, Girgus JS.(1994)The emergence of gender differ- Seo D, Ahluwalia A, Potenza MN, Sinha R(2017)Gender differences nces in depression during adolescence. Psychol Bull 115(3):4 in neural correlates of stress-induced anxiety. J Neurosci Res 95 ODonnell P, Grace AA. (1995)Synaptic interactions among excitato Seo D, Jia Z, Lacadie CM, Tsou KA, Bergquist K, Sinha R(2011)Se afferents to nucleus accumbens neurons: hippocampal gating of differences in neural responses to stress and alcohol context frontal cortical input. J Neurosci 15(5 Pt 1): 3622-3639 0.1002 ceptor beta(ERbeta)messenger ribonucleic acid(mRNA)expres- Shah AA, Sjovold T, Treit D (2004)Inactivation of the medial prefrontal sion within the human forebrain: distinct distribution pattern to ERal cortex with the GABAa receptor agonist muscimol increases open. phamrna.JClinEndocrinolMetab85(10):3840-3846,https://doi. arm activity in the elevated plus-maze and attenuates shock-probe org/10.1210cem85.10.6913 buryinginratsBrainRes1028(1):112-115,https://doi.org/10.1016/ Padilla-Coreano N. Bolkan ss. Pierce M. Blackman DR. Hardin w brainres. 2004.08 061 Garcia-Garcia AL, Gordon JA(2016)Direct ventral hippocampa Shughrue PJ, Lane MV, Merchenthaler L(1997) Comparative distribu- ty-related neural activity and tion of estrogen receptor-alpha and-beta mRNA in the rat centra behaviorNeuron89(4):857-866,https://doi.org/10.1016 nervous system. J Comp Neurol 388(4): 507-525 neuron.2016.01.011 Stern CA, Do Monte FH, Gazarini L, Carobrez AP, Bertoglio LJ. (2010) Parfitt GM, Nguyen R, Bang JY, Aqrabawi AJ, Tran MM, Seo DK, Kim Activity in prelimbic cortex is required for adjusting the anxi JC(2017)Bidirectional control of anxiety-related behaviors in mice sponse level during the elevated plus-maze retest Neuroscience inputs arising from the ventral Hippocampus 170(1)214-22, https://doi.org/10.1016/j septum and medial prefrontal cortex. Neuropsychopharmacology neuroscience. 2010. 06.080 42(8):1715-1728,https://do.org10.1038np9.2017.56. Walf AA, Frye CA (2006)A review and update of mechanisms of estro- Paxinos G, Franklin K.B. J.(2001)The mouse brain in stereotaxic coor- gen in the hippocampus and amygdala for anxiety and depression dinates. 2nd ed. San Diego: Academic Press, 2001 behaviorNeuropsychopharmacology31(6):1097-1111,https://doi. Pikkarainen M, Ronkko S, Savander V, Insausti R, Pitkanen A(1999) org/10.1038/ sinpp.1301067 Projections from the lateral, basal, and accessory basal nuclei of Walf AA, Frye CA(2007) Estradiol decreases anxiety behavio the amygdala to the hippocampal formation in rat. J Comp Neurol hances inhibitory avoidance and gestational stress pr oppositeeffectsStress10(3):251-260,https://doi.org/10.1 Roca cA. schmidt PJ. Altemus M. Deuster P. Danaceau mA putnam 00958970701220416 K, Rubinow DR (2003)Differential menstrual cycle regulation of Zhang Y, Jiang YY, Shao S, Zhang C, Liu FY, Wan Y, Yi M. (2017)Inhi hypothalamic-pituitary-adrenal axis in women with premenstrual biting medial septal cholinergic neurons with DREADD alleviated yndrome and controls. J Clin Endocrinol Metab 88(7): 3057-3063 anxiety-likebehaviorsinmiceNeurosciLett638:139-144,https:// https://doi.org/10.1210/jc.2002-021570 ol. org/10.1016/ neale2016.12010 Rosen JB, Schulkin J(1998) From normal fear to pathological anxie Zheng J, Jiang YY, Xu LC, Ma LY, Liu FY, Cui S, Yi M. (2017)Adult hip. Psychol Rev 105(2): 325-350 pocampal neurogenesis along the dorsoventral axis contributes dif- Ruigrok AN, Salimi-Khorshidi G, Lai MC, Baron-Cohen S, Lombardo inhumanbrainstructureNeurosciBiobehavRev39:34-50,https:// 37(541464569con 57,https://doi.org/10.1523/jneuroscl3333- doi. org/10.1016/j. neubiorev. 2013. 12.004 16.2017. Received 25 March 2019) (Available online 25 August 2019)Montag C, Reuter M, Weber B, Markett S, Schoene-Bake JC. (2012) Individual differences in trait anxiety are associated with white matter tract integrity in the left temporal lobe in healthy males but not females. Neuroscience 217:77-83, https://doi.org/10.1016/j. neuroscience.2012.05.017. Mora S, Dussaubat N, Diaz-Veliz G. (1996) Effects of the estrous cycle and ovarian hormones on behavioral indices of anxiety in female rats. Psychoneuroendocrinology 21(7):609-620. Nelson JF, Felicio LS, Randall PK, Sims C, Finch CE. (1982) A longitudinal study of estrous cyclicity in aging C57BL/6J mice: I. cycle frequency, length and vaginal cytology. Biol Reprod 27(2):327-339. Nolen-Hoeksema S, Girgus JS. (1994) The emergence of gender differences in depression during adolescence. Psychol Bull 115(3):424- 443. O'Donnell P, Grace AA. (1995) Synaptic interactions among excitatory afferents to nucleus accumbens neurons: hippocampal gating of prefrontal cortical input. J Neurosci 15(5 Pt 1):3622-3639. Osterlund MK, Gustafsson JA, Keller E, Hurd YL. (2000) Estrogen receptor beta (ERbeta) messenger ribonucleic acid (mRNA) expression within the human forebrain: distinct distribution pattern to ERalpha mRNA. J Clin Endocrinol Metab 85(10):3840-3846, https://doi. org/10.1210/jcem.85.10.6913. Padilla-Coreano N, Bolkan SS, Pierce GM, Blackman DR, Hardin WD, Garcia-Garcia AL, Gordon JA. (2016) Direct ventral hippocampalprefrontal input is required for anxiety-related neural activity and behavior. Neuron 89(4):857-866, https://doi.org/10.1016/j. neuron.2016.01.011. Parfitt GM, Nguyen R, Bang JY, Aqrabawi AJ, Tran MM, Seo DK, Kim JC. (2017) Bidirectional control of anxiety-related behaviors in mice: role of inputs arising from the ventral Hippocampus to the lateral septum and medial prefrontal cortex. Neuropsychopharmacology 42(8):1715-1728, https://doi.org/10.1038/npp.2017.56. Paxinos G, Franklin K.B.J.. (2001) The mouse brain in stereotaxic coordinates. 2nd ed. San Diego: Academic Press, 2001. Pikkarainen M, Ronkko S, Savander V, Insausti R, Pitkanen A. (1999) Projections from the lateral, basal, and accessory basal nuclei of the amygdala to the hippocampal formation in rat. J Comp Neurol 403(2):229-260. Roca CA, Schmidt PJ, Altemus M, Deuster P, Danaceau MA, Putnam K, Rubinow DR. (2003) Differential menstrual cycle regulation of hypothalamic-pituitary-adrenal axis in women with premenstrual syndrome and controls. J Clin Endocrinol Metab 88(7):3057-3063, https://doi.org/10.1210/jc.2002-021570. Rosen JB, Schulkin J. (1998) From normal fear to pathological anxiety. Psychol Rev 105(2):325-350. Ruigrok AN, Salimi-Khorshidi G, Lai MC, Baron-Cohen S, Lombardo MV, Tait RJ, Suckling J. (2014) A meta-analysis of sex differences in human brain structure. Neurosci Biobehav Rev 39:34-50, https:// doi.org/10.1016/j.neubiorev.2013.12.004. Sahingoz M, Uguz F, Gezginc K. (2011) Prevalence and related factors of mood and anxiety disorders in a clinical sample of postmenopausal women. Perspect Psychiatr Care 47(4):213-219, https://doi.org/ 10.1111/j.1744-6163.2010.00296.x. Schneider T, Popik P. (2007) Attenuation of estrous cycle-dependent marble burying in female rats by acute treatment with progesterone and antidepressants. Psychoneuroendocrinology 32(6):651-659, https://doi.org/10.1016/j.psyneuen.2007.04.003. Seeman MV. (1997) Psychopathology in women and men: focus on female hormones. Am J Psychiatry 154(12):1641-1647, https://doi. org/10.1176/ajp.154.12.1641. Seo D, Ahluwalia A, Potenza MN, Sinha R. (2017) Gender differences in neural correlates of stress-induced anxiety. J Neurosci Res 95 (1–2):115-125, https://doi.org/10.1002/jnr.23926. Seo D, Jia Z, Lacadie CM, Tsou KA, Bergquist K, Sinha R. (2011) Sex differences in neural responses to stress and alcohol context cues. Hum Brain Mapp 32(11):1998-2013, https://doi.org/10.1002/ hbm.21165. Shah AA, Sjovold T, Treit D. (2004) Inactivation of the medial prefrontal cortex with the GABAA receptor agonist muscimol increases openarm activity in the elevated plus-maze and attenuates shock-probe burying in rats. Brain Res 1028(1):112-115, https://doi.org/10.1016/ j.brainres.2004.08.061. Shughrue PJ, Lane MV, Merchenthaler I. (1997) Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. J Comp Neurol 388(4):507-525. Stern CA, Do Monte FH, Gazarini L, Carobrez AP, Bertoglio LJ. (2010) Activity in prelimbic cortex is required for adjusting the anxiety response level during the elevated plus-maze retest. Neuroscience 170(1):214-222, https://doi.org/10.1016/j. neuroscience.2010.06.080. Walf AA, Frye CA. (2006) A review and update of mechanisms of estrogen in the hippocampus and amygdala for anxiety and depression behavior. Neuropsychopharmacology 31(6):1097-1111, https://doi. org/10.1038/sj.npp.1301067. Walf AA, Frye CA. (2007) Estradiol decreases anxiety behavior and enhances inhibitory avoidance and gestational stress produces opposite effects. Stress 10(3):251-260, https://doi.org/10.1080/ 00958970701220416. Zhang Y, Jiang YY, Shao S, Zhang C, Liu FY, Wan Y, Yi M. (2017) Inhibiting medial septal cholinergic neurons with DREADD alleviated anxiety-like behaviors in mice. Neurosci Lett 638:139-144, https:// doi.org/10.1016/j.neulet.2016.12.010. Zheng J, Jiang YY, Xu LC, Ma LY, Liu FY, Cui S, Yi M. (2017) Adult hippocampal neurogenesis along the dorsoventral axis contributes differentially to environmental enrichment combined with voluntary exercise in alleviating chronic inflammatory pain in mice. J Neurosci 37(15):4145-4157, https://doi.org/10.1523/JNEUROSCI.3333- 16.2017. (Received 25 March 2019) (Available online 25 August 2019) Cheng Wang et al. / Neuroscience 418 (2019) xxx–xxx 9 NSC 19240 No of Pages 9 06 September 2019