Cahill L. Why sex matters for neuroscience. Nat Rev Neurosci. 2006;7:477–84.
Article
CAS
Google Scholar
McCarthy MM, Arnold AP, Ball GF, Blaustein JD, De Vries GJ. Sex differences in the brain: the not so inconvenient truth. J Neurosci. 2012;32:2241–7.
Article
Google Scholar
Seney ML, Sibille E. Sex differences in mood disorders: perspectives from humans and rodent models. Biol Sex Differ. 2014;5:17.
Article
Google Scholar
Abel KM, Drake R, Goldstein JM. Sex differences in schizophrenia. Int Rev Psychiatry. 2010;22:417–28.
Article
Google Scholar
Alonso J, Angermeyer MC, Bernert S, Bruffaerts R, Brugha TS, Bryson H, et al. Prevalence of mental disorders in Europe: results from the European Study of the Epidemiology of Mental Disorders (ESEMeD) project. Acta Psychiatr Scand. 2004;109:21–7.
Article
Google Scholar
Breslau N, Davis GC, Andreski P, Peterson EL, Schultz LR. Sex differences in posttraumatic stress disorder. Arch Gen Psychiatry. 1997;54:1044–8.
Article
CAS
Google Scholar
McLean CP, Asnaani A, Litz BT, Hofmann SG. Gender differences in anxiety disorders: prevalence, course of illness, comorbidity and burden of illness. J Psychiatry Res. 2011;45:1027–35.
Article
Google Scholar
Aleman A, Kahn RS, Selten J-P. Sex differences in the risk of schizophrenia. Arch Gen Psychiatry. 2003;60:565.
Article
Google Scholar
Arnett AB, Pennington BF, Willcutt EG, DeFries JC, Olson RK. Sex differences in ADHD symptom severity. J Child Psychol Psychiatry. 2015;56:632–9.
Article
Google Scholar
Goldstein JM, Tsuang MT, Faraone SV. Gender and schizophrenia: implications for understanding the heterogeneity of the illness. Psychiatry Res. 1989;28:243–53.
Article
CAS
Google Scholar
Kaczkurkin AN, Raznahan A, Satterthwaite TD. Sex differences in the developing brain: insights from multimodal neuroimaging. Neuropsychopharmacology. 2019;44:71–85.
Article
Google Scholar
Morris JA, Jordan CL, Breedlove SM. Sexual differentiation of the vertebrate nervous system. Nat Neurosci. 2004;7:1034–9.
Article
CAS
Google Scholar
Simerly RB. Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Annu Rev Neurosci. 2002;25:507–36.
Article
CAS
Google Scholar
Bangasser DA, Cuarenta A. Sex differences in anxiety and depression: circuits and mechanisms. Nat Rev Neurosci. 2021;22:674–84.
Article
CAS
Google Scholar
de Vries GJ, Södersten P. Sex differences in the brain: the relation between structure and function. Horm Behav. 2009;55:589–96.
Article
Google Scholar
Buck J, Manion MTC, Zhang W, Glasper ER, Wang KH. Comparative anatomical analysis of dopamine systems in Mus musculus and Peromyscus californicus. Brain Struct Funct. 2022;227:2219–27.
Article
CAS
Google Scholar
Campi KL, Jameson CE, Trainor BC. Sexual dimorphism in the brain of the monogamous California mouse (Peromyscus californicus). Brain Behav Evol. 2013;81:236–49.
Article
Google Scholar
Gorski RA, Gordon JH, Shryne JE, Southam AM. Evidence for a morphological sex difference within the medial preoptic area of the rat brain. Brain Res. 1978;148:333–46.
Article
CAS
Google Scholar
Simerly RB, Swanson LW, Gorski RA. The distribution of monoaminergic cells and fibers in a periventricular preoptic nucleus involved in the control of gonadotropin release: immunohistochemical evidence for a dopaminergic sexual dimorphism. Brain Res. 1985;330:55–64.
Article
CAS
Google Scholar
Cooke BM, Woolley CS. Sexually dimorphic synaptic organization of the medial amygdala. J Neurosci. 2005;25:10759–67.
Article
CAS
Google Scholar
Johnson RT, Breedlove SM, Jordan CL. Sex differences and laterality in astrocyte number and complexity in the adult rat medial amygdala. J Comp Neurol. 2008;511:599–609.
Article
Google Scholar
VanRyzin JW, Marquardt AE, Argue KJ, Vecchiarelli HA, Ashton SE, Arambula SE, et al. Microglial phagocytosis of newborn cells is induced by endocannabinoids and sculpts sex differences in juvenile rat social play. Neuron. 2019;102:435-449.e6.
Article
CAS
Google Scholar
Wu MV, Manoli DS, Fraser EJ, Coats JK, Tollkuhn J, Honda S-I, et al. Estrogen masculinizes neural pathways and sex-specific behaviors. Cell. 2009;139:61–72.
Article
CAS
Google Scholar
Shansky RM. Sex differences in amygdala structure and function: from rodents to humans. Handb Behav Neurosci. 2000;26:275–84.
Article
Google Scholar
Forlano PM, Woolley CS. Quantitative analysis of pre- and postsynaptic sex differences in the nucleus accumbens. J Comp Neurol. 2010;518:1330–48.
CAS
Google Scholar
Kolb B, Stewart J. Sex-related differences in dendritic branching of cells in the prefrontal cortex of rats. J Neuroendocrinol. 1991;3:95–9.
Article
CAS
Google Scholar
Mitsushima D, Yamada K, Takase K, Funabashi T, Kimura F. Sex differences in the basolateral amygdala: the extracellular levels of serotonin and dopamine, and their responses to restraint stress in rats. Eur J Neurosci. 2006;24:3245–54.
Article
Google Scholar
Williams OOF, Coppolino M, George SR, Perreault ML. Sex differences in dopamine receptors and relevance to neuropsychiatric disorders. Brain Sci. 2021;11:1199.
Article
CAS
Google Scholar
Locklear MN, Cohen AB, Jone A, Kritzer MF. Sex differences distinguish intracortical glutamate receptor-mediated regulation of extracellular dopamine levels in the prefrontal cortex of adult rats. Cereb Cortex. 2014;26:599.
Google Scholar
Ernst M, Fudge JL. A developmental neurobiological model of motivated behavior: anatomy, connectivity and ontogeny of the triadic nodes. Neurosci Biobehav Rev. 2009;33:367–82.
Article
Google Scholar
Russo SJ, Nestler EJ. The brain reward circuitry in mood disorders. Nat Rev Neurosci. 2013;14:609–25.
Article
CAS
Google Scholar
Trainor BC. Stress responses and the mesolimbic dopamine system: social contexts and sex differences. Horm Behav. 2011;60:457–69.
Article
CAS
Google Scholar
Chaudhury D, Walsh JJ, Friedman AK, Juarez B, Ku SM, Koo JW, et al. Rapid regulation of depression-related behaviours by control of midbrain dopamine neurons. Nature. 2013;493:532–6.
Article
CAS
Google Scholar
Lammel S, Hetzel A, Häckel O, Jones I, Liss B, Roeper J. Unique properties of mesoprefrontal neurons within a dual mesocorticolimbic dopamine system. Neuron. 2008;57:760–73.
Article
CAS
Google Scholar
Lutas A, Kucukdereli H, Alturkistani O, Carty C, Sugden AU, Fernando K, et al. State-specific gating of salient cues by midbrain dopaminergic input to basal amygdala. Nat Neurosci. 2019;22:1820–33.
Article
CAS
Google Scholar
Tye KM, Mirzabekov JJ, Warden MR, Ferenczi EA, Tsai H-C, Finkelstein J, et al. Dopamine neurons modulate neural encoding and expression of depression-related behaviour. Nature. 2013;493:537–41.
Article
CAS
Google Scholar
Howes OD, Kambeitz J, Kim E, Stahl D, Slifstein M, Abi-Dargham A, et al. The nature of dopamine dysfunction in schizophrenia and what this means for treatment. Arch Gen Psychiatry. 2012;69:776–86.
Article
CAS
Google Scholar
Volkow ND, Wang G-J, Kollins SH, Wigal TL, Newcorn JH, Telang F, et al. Evaluating dopamine reward pathway in ADHD: clinical implications. JAMA. 2009;302:1084–91.
Article
CAS
Google Scholar
Janak PH, Tye KM. From circuits to behaviour in the amygdala. Nature. 2015;517:284–92.
Article
CAS
Google Scholar
Roozendaal B, McEwen BS, Chattarji S. Stress, memory and the amygdala. Nat Rev Neurosci. 2009;10:423–33.
Article
CAS
Google Scholar
Swanson LW, Petrovich GD. What is the amygdala? Trends Neurosci. 1998;21:323–31.
Article
CAS
Google Scholar
Beyeler A, Namburi P, Glober GF, Simonnet C, Calhoon GG, Conyers GF, et al. Divergent routing of positive and negative information from the amygdala during memory retrieval. Neuron. 2016;90:348–61.
Article
CAS
Google Scholar
Gore F, Schwartz EC, Brangers BC, Aladi S, Stujenske JM, Likhtik E, et al. Neural representations of unconditioned stimuli in basolateral amygdala mediate innate and learned responses. Cell. 2015;162:134–45.
Article
CAS
Google Scholar
Kim J, Zhang X, Muralidhar S, LeBlanc SA, Tonegawa S. Basolateral to central amygdala neural circuits for appetitive behaviors. Neuron. 2017;93:1464-1479.e5.
Article
CAS
Google Scholar
Zhang X, Guan W, Yang T, Furlan A, Xiao X, Yu K, et al. Genetically identified amygdala-striatal circuits for valence-specific behaviors. Nat Neurosci. 2021;24:1586–600.
Article
CAS
Google Scholar
Beier KT, Steinberg EE, DeLoach KE, Xie S, Miyamichi K, Schwarz L, et al. Circuit architecture of VTA dopamine neurons revealed by systematic input–output mapping. Cell. 2015;162:622–34.
Article
CAS
Google Scholar
Lerner TN, Shilyansky C, Davidson TJ, Evans KE, Beier KT, Zalocusky KA, et al. Intact-brain analyses reveal distinct information carried by SNc dopamine subcircuits. Cell. 2015;162:635–47.
Article
CAS
Google Scholar
Poulin J-F, Caronia G, Hofer C, Cui Q, Helm B, Ramakrishnan C, et al. Mapping projections of molecularly defined dopamine neuron subtypes using intersectional genetic approaches. Nat Neurosci. 2018;21:1260–71.
Article
CAS
Google Scholar
Morel C, Montgomery SE, Li L, Durand-de Cuttoli R, Teichman EM, Juarez B, et al. Midbrain projection to the basolateral amygdala encodes anxiety-like but not depression-like behaviors. Nat Commun. 2022;13:1532.
Article
CAS
Google Scholar
Tang W, Kochubey O, Kintscher M, Schneggenburger R. A VTA to basal amygdala dopamine projection contributes to signal salient somatosensory events during fear learning. J Neurosci. 2020;40:3969–80.
Article
Google Scholar
Aransay A, Rodríguez-López C, García-Amado M, Clascáand F, Prensa L. Long-range projection neurons of the mouse ventral tegmental area: a single-cell axon tracing analysis. Front Neuroanat. 2015;9:59.
Article
Google Scholar
Walsh JJ, Han MH. The heterogeneity of ventral tegmental area neurons: projection functions in a mood-related context. Neuroscience. 2014;282C:101–8.
Article
Google Scholar
Gong S, Doughty M, Harbaugh CR, Cummins A, Hatten ME, Heintz N, et al. Targeting Cre recombinase to specific neuron populations with bacterial artificial chromosome constructs. J Neurosci. 2007;27:9817–23.
Article
CAS
Google Scholar
Franklin KBJ, Paxinos G. Paxinos and Franklin’s The mouse brain in stereotaxic coordinates. 4th ed. Amsterdam: Academic Press; 2013.
Google Scholar
Byers SL, Wiles MV, Dunn SL, Taft RA. Mouse estrous cycle identification tool and images. PLoS ONE. 2012;7:1–5.
Article
Google Scholar
Mastwal S, Ye Y, Ren M, Jimenez DV, Martinowich K, Gerfen CR, et al. Phasic dopamine neuron activity elicits unique mesofrontal plasticity in adolescence. J Neurosci. 2014;34:9484–96.
Article
Google Scholar
Sato Y, Nakajima S, Shiraga N, Atsumi H, Yoshida S, Koller T, et al. Three-dimensional multi-scale line filter for segmentation and visualization of curvilinear structures in medical images. Med Image Anal. 1998;2:143–68.
Article
CAS
Google Scholar
Ye Y, Liu Q, Zhang W, Mastwal S, Wang KH. Developmental exposure to psychostimulant primes activity-dependent gene induction in frontal cortex. Dev Neurobiol. 2019;79:96–108.
CAS
Google Scholar
Marr D, Hildreth E. Theory of edge detection. Proc R Soc Lond B Biol Sci. 1980;207:187–217.
Article
CAS
Google Scholar
Wang KH, Majewska A, Schummers J, Farley B, Hu C, Sur M, et al. In vivo two-photon imaging reveals a role of arc in enhancing orientation specificity in visual cortex. Cell. 2006;126:389–402.
Article
CAS
Google Scholar
Ye Y, Mastwal S, Cao VY, Ren M, Liu Q, Zhang W, et al. Dopamine is required for activity-dependent amplification of Arc mRNA in developing postnatal frontal cortex. Cereb Cortex. 2017;27:3600–8.
Google Scholar
Goldman-Rakic PS, Leranth C, Williams SM, Mons N, Geffard M. Dopamine synaptic complex with pyramidal neurons in primate cerebral cortex. Proc Natl Acad Sci. 1989;86:9015–9.
Article
CAS
Google Scholar
Sulzer D, Cragg SJ, Rice ME. Striatal dopamine neurotransmission: regulation of release and uptake. Basal Ganglia. 2016;6:123–48.
Article
Google Scholar
Oh SW, Harris JA, Ng L, Winslow B, Cain N, Mihalas S, et al. A mesoscale connectome of the mouse brain. Nature. 2014;508:207–14.
Article
CAS
Google Scholar
Wang X, Liu Y, Li X, Zhang Z, Yang H, Zhang Y, et al. Deconstruction of corticospinal circuits for goal-directed motor skills. Cell. 2017;171:440–55.
Article
CAS
Google Scholar
Manago F, Mereu M, Mastwal S, Mastrogiacomo R, Scheggia D, Emanuele M, et al. Genetic disruption of Arc/Arg3. 1 in mice causes alterations in dopamine and neurobehavioral phenotypes related to schizophrenia. Cell Rep. 2016;16:2116–28.
Article
CAS
Google Scholar
Patriarchi T, Cho JR, Merten K, Howe MW, Marley A, Xiong W-H, et al. Ultrafast neuronal imaging of dopamine dynamics with designed genetically encoded sensors. Science. 2018;360:eaat4422.
Article
Google Scholar
Sun F, Zeng J, Jing M, Zhou J, Feng J, Owen SF, et al. A Genetically encoded fluorescent sensor enables rapid and specific detection of dopamine in flies, fish, and mice. Cell. 2018;174:481-496.e19.
Article
CAS
Google Scholar
Blume SR, Freedberg M, Vantrease JE, Chan R, Padival M, Record MJ, et al. Sex- and estrus-dependent differences in rat basolateral amygdala. J Neurosci. 2017;37:10567–86.
Article
CAS
Google Scholar
Dalla C, Shors TJ. Sex differences in learning processes of classical and operant conditioning. Physiol Behav. 2009;97:229–38.
Article
CAS
Google Scholar
Day HLL, Reed MM, Stevenson CW. Sex differences in discriminating between cues predicting threat and safety. Neurobiol Learn Mem. 2016;133:196–203.
Article
Google Scholar
Denti A, Epstein A. Sex differences in the acquisition of two kinds of avoidance behavior in rats. Physiol Behav. 1972;8:611–5.
Article
CAS
Google Scholar
Maren S, De Oca B, Fanselow MS. Sex differences in hippocampal long-term potentiation (LTP) and Pavlovian fear conditioning in rats: positive correlation between LTP and contextual learning. Brain Res. 1994;661:25–34.
Article
CAS
Google Scholar
Pezze MA, Feldon J. Mesolimbic dopaminergic pathways in fear conditioning. Prog Neurobiol. 2004;74:301–20.
Article
CAS
Google Scholar
Urien L, Bauer EP. Sex differences in BNST and amygdala activation by contextual, cued, and unpredictable threats. Eneuro. 2022;9:ENEURO.0233-21.2021.
Article
Google Scholar
McCarthy MM, Arnold AP. Reframing sexual differentiation of the brain. Nat Neurosci. 2011;14:677–83.
Article
CAS
Google Scholar
Ahmed EI, Zehr JL, Schulz KM, Lorenz BH, Lydia L, Sisk CL. Pubertal hormones modulate the addition of new cells to sexually dimorphic brain regions. Nat Neurosci. 2009;11:995–7.
Article
Google Scholar
Bowers JM, Waddell J, McCarthy MM. A developmental sex difference in hippocampal neurogenesis is mediated by endogenous oestradiol. Biol Sex Differ. 2010;1:8.
Article
CAS
Google Scholar
Schwarz JM, Liang S-L, Thompson SM, McCarthy MM. Estradiol induces hypothalamic dendritic spines by enhancing glutamate release: a mechanism for organizational sex differences. Neuron. 2008;58:584–98.
Article
CAS
Google Scholar
Berger B, Gaspar P, Verney C. Dopaminergic innervation of the cerebral cortex: unexpected differences between rodents and primates. Trends Neurosci. 1991;14:21–7.
Article
CAS
Google Scholar
Brenhouse HC, Andersen SL. Developmental trajectories during adolescence in males and females: a cross-species understanding of underlying brain changes. Neurosci Biobehav Rev. 2011;35:1687–703.
Article
Google Scholar
Kalsbeek A, Voorn P, Buijs RM, Pool CW, Uylings HBM. Development of the dopaminergic innervation in the prefrontal cortex of the rat. J Comp Neurol. 1988;269:58–72.
Article
CAS
Google Scholar
Aubele T, Kaufman R, Montalmant F, Kritzer MF. Effects of gonadectomy and hormone replacement on a spontaneous novel object recognition task in adult male rats. Horm Behav. 2008;54:244–52.
Article
CAS
Google Scholar
Aubele T, Kritzer MF. Gonadectomy and hormone replacement affects in vivo basal extracellular dopamine levels in the prefrontal cortex but not motor cortex of adult male rats. Cereb Cortex. 2011;21:222–32.
Article
CAS
Google Scholar
Aubele T, Kritzer MF. Androgen influence on prefrontal dopamine systems in adult male rats: localization of cognate intracellular receptors in medial prefrontal projections to the ventral tegmental area and effects of gonadectomy and hormone replacement on glutamate-stimulated extracellular dopamine level. Cereb Cortex. 2012;22:1799–812.
Article
CAS
Google Scholar
Kritzer MF, Brewer A, Montalmant F, Davenport M, Robinson JK. Effects of gonadectomy on performance in operant tasks measuring prefrontal cortical function in adult male rats. Horm Behav. 2007;51:183–94.
Article
CAS
Google Scholar
Brooks DC, Coon VJS, Ercan CM, Xu X, Dong H, Levine JE, et al. Brain aromatase and the regulation of sexual activity in male mice. Endocrinology. 2020;161:bqaa137.
Article
Google Scholar
Simerly RB, Zee MC, Pendleton JW, Lubahn DB, Korach KS. Estrogen receptor-dependent sexual differentiation of dopaminergic neurons in the preoptic region of the mouse. Proc Natl Acad Sci. 1997;94:14077–82.
Article
CAS
Google Scholar
Becker JB, Chartoff E. Sex differences in neural mechanisms mediating reward and addiction. Neuropsychopharmacology. 2019;44:166–83.
Article
CAS
Google Scholar