Neurosteroids and the mesocorticolimbic system

Neuroscience & Biobehavioral Reviews - Tập 153 - Trang 105356 - 2023
Désirée R. Seib1, Daniel J. Tobiansky2, John Meitzen3, Stan B. Floresco1, Kiran K. Soma1
1Department of Psychology and Djavad Mowafaghian Centre for Brain Health, University of British Columbia, Vancouver, BC, Canada
2Department of Biology and Neuroscience Program, St. Mary’s College of Maryland, St. Mary’s City, MD, USA
3Department of Biological Sciences and Center for Human Health and the Environment, NC State University, Raleigh, NC, USA

Tài liệu tham khảo

Agis-Balboa, 2006, Characterization of brain neurons that express enzymes mediating neurosteroid biosynthesis, Proc. Natl. Acad. Sci., 103, 14602, 10.1073/pnas.0606544103 Almey, 2015, Estrogen receptors in the central nervous system and their implication for dopamine-dependent cognition in females, Horm. Behav., 74, 125, 10.1016/j.yhbeh.2015.06.010 Almey, 2022, Estrogen receptors observed at extranuclear neuronal sites and in glia in the nucleus accumbens core and shell of the female rat: Evidence for localization to catecholaminergic and GABAergic neurons, J. Comp. Neurol., 530, 2056, 10.1002/cne.25320 Andersen, 1997, Sex differences in dopamine receptor overproduction and elimination, NeuroReport, 8, 1495, 10.1097/00001756-199704140-00034 Andrew, 1972, Testosterone, search behaviour and persistence, Nature, 237, 343, 10.1038/237343a0 Aubele, 2011, 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, 21, 222, 10.1093/cercor/bhq083 Aubele, 2012, Cereb. Cortex, 22, 1799, 10.1093/cercor/bhr258 Aubele, 2008, Effects of gonadectomy and hormone replacement on a spontaneous novel object recognition task in adult male rats, Horm. Behav., 54, 244, 10.1016/j.yhbeh.2008.04.001 Balthazart, 1998, New insights into the regulation and function of brain estrogen synthase (aromatase), Trends Neurosci., 21, 243, 10.1016/S0166-2236(97)01221-6 Balthazart, 1994, Distribution and regulation of estrogen-2-hydroxylase in the quail brain, Brain Res. Bull., 35, 339, 10.1016/0361-9230(94)90111-2 Baulieu, 1998, Neurosteroids: a novel function of the brain, Psychoneuroendocrinology, 23, 963, 10.1016/S0306-4530(98)00071-7 Beatty, 1982, Stereotyped behavior elicited by amphetamine in the rat: Influences of the testes, Pharmacol. Biochem. Behav., 16, 565, 10.1016/0091-3057(82)90416-6 Becker, 1999, Gender differences in dopaminergic function in striatum and nucleus accumbens, Pharmacol. Biochem. Behav., 64, 803, 10.1016/S0091-3057(99)00168-9 Becker, 2019, Sex differences in neural mechanisms mediating reward and addiction, Neuropsychopharmacol, 44, 166, 10.1038/s41386-018-0125-6 Berger, 2002, Long-term effects of prenatal stress on dopamine and glutamate receptors in adult rat brain, Neurochem Res, 27, 1525, 10.1023/A:1021656607278 Brady, 2022, Sex-specific cholinergic regulation of dopamine release mechanisms through nicotinic receptors in the nucleus accumbens, Biol. Psychiatry, 91, S90, 10.1016/j.biopsych.2022.02.241 Brozoski, 1979, Cognitive deficit caused by regional depletion of dopamine in prefrontal cortex of rhesus monkey, Science, 205, 929, 10.1126/science.112679 Cabib, 1998, Stress promotes major changes in dopamine receptor densities within the mesoaccumbens and nigrostriatal systems, Neuroscience, 84, 193, 10.1016/S0306-4522(97)00468-5 Cao, 2018, Sex differences in medium spiny neuron excitability and glutamatergic synaptic input: heterogeneity across striatal regions and evidence for estradiol-dependent sexual differentiation, Front. Endocrinol., 9, 173, 10.3389/fendo.2018.00173 Celec, 2015, On the effects of testosterone on brain behavioral functions, Front. Neurosci., 9 Chavez, 2010, The effect of estrogen on dopamine and serotonin receptor and transporter levels in the brain: an autoradiography study, Brain Res., 1321, 51, 10.1016/j.brainres.2009.12.093 Cools, 2019, Chemistry of the adaptive mind: lessons from dopamine, Neuron, 104, 113, 10.1016/j.neuron.2019.09.035 Corpéchot, 1981, Characterization and measurement of dehydroepiandrosterone sulfate in rat brain, Proc. Natl. Acad. Sci., 78, 4704, 10.1073/pnas.78.8.4704 Cullity, 2019, Postnatal developmental trajectory of dopamine receptor 1 and 2 expression in cortical and striatal brain regions, J. Comp. Neurol., 527, 1039, 10.1002/cne.24574 Dazzi, 2002, Progesterone enhances ethanol-induced modulation of mesocortical dopamine neurons: antagonism by finasteride: Interaction of neurosteroids and ethanol, J. Neurochem., 83, 1103, 10.1046/j.1471-4159.2002.01218.x Dib, 2018, Neonatal programming with testosterone propionate reduces dopamine transporter expression in nucleus accumbens and methylphenidate-induced locomotor activity in adult female rats, Behav. Brain Res., 346, 80, 10.1016/j.bbr.2017.12.001 Dluzen, 1989, Effects of orchidectomy on nigro-striatal dopaminergic function: behavioral and physiological evidence, J. Neuroendocrinol., 1, 285, 10.1111/j.1365-2826.1989.tb00117.x Dornellas, 2021, Allopregnanolone Decreases Evoked Dopamine Release Differently in Rats by Sex and Estrous Stage, Front. Pharmacol., 11, 10.3389/fphar.2020.608887 Drzewiecki, 2021, Impact of pubertal onset on region‐specific Esr2 expression, J. Neuroendocrinol., 33 Duff, 2000, A beneficial effect of estrogen on working memory in postmenopausal women taking hormone replacement therapy, Horm. Behav., 38, 262, 10.1006/hbeh.2000.1625 Elgueta-Reyes, 2021, Neonatal programming with sex hormones: Effect on expression of dopamine D1 receptor and neurotransmitters release in nucleus accumbens in adult male and female rats, Eur. J. Pharmacol., 902, 10.1016/j.ejphar.2021.174118 Floresco, 2013, Prefrontal dopamine and behavioral flexibility: shifting from an “inverted-U” toward a family of functions, Front. Neurosci., 7, 62, 10.3389/fnins.2013.00062 Foidart, A., Harada, N., Balthazart, J., 1995. Aromatase-immunoreactive cells are present in mouse brain areas that are known to express high levels of aromatase activity. Cell and Tissue Research 280, 561–574. https://doi.org/DOI:10.1007/BF00318360. Giatti, 2019, Sex differences in the brain expression of steroidogenic molecules under basal conditions and after gonadectomy, J. Neuroendocrinol., 31, 10.1111/jne.12736 Gross, K.S., Mermelstein, P.G., 2020. Estrogen receptor signaling through metabotropic glutamate receptors, in: Vitamins and Hormones. Elsevier, pp. 211–232. https://doi.org/10.1016/bs.vh.2020.06.003. Gross, 2018, mGluR5 mediates dihydrotestosterone-induced nucleus accumbens structural plasticity, but not conditioned reward, Front. Neurosci., 12, 855, 10.3389/fnins.2018.00855 Haluk, 2009, Ventral striatal dopamine modulation of different forms of behavioral flexibility, Neuropsychopharmacol, 34, 2041, 10.1038/npp.2009.21 Harp, 2020, Sexual differentiation and substance use: a mini-review, Endocrinol. 161, bqaa129, 10.1210/endocr/bqaa129 Hasbi, 2020, Sex difference in dopamine D1-D2 receptor complex expression and signaling affects depression- and anxiety-like behaviors, Biol. Sex. Differ., 11, 8, 10.1186/s13293-020-00285-9 Hauger, 2020, Anabolic androgenic steroid dependence is associated with executive dysfunction, Drug Alcohol Depend., 208, 10.1016/j.drugalcdep.2020.107874 Henry, 1995, Prenatal stress in rats facilitates amphetamine-induced sensitization and induces long-lasting changes in dopamine receptors in the nucleus accumbens, Brain Res., 685, 179, 10.1016/0006-8993(95)00430-X Hernandez, 1994, Testosterone modulates mesolimbic dopaminergic activity in male rats, Neurosci. Lett., 171, 172, 10.1016/0304-3940(94)90632-7 Hill, 2014, Long-term effects of combined neonatal and adolescent stress on brain-derived neurotrophic factor and dopamine receptor expression in the rat forebrain, Biochim. Et. Biophys. Acta (BBA) - Mol. Basis Dis., 1842, 2126, 10.1016/j.bbadis.2014.08.009 Hojo, 2018, Neurosteroids in adult hippocampus of male and female rodents: biosynthesis and actions of sex steroids, Front. Endocrinol., 9, 183, 10.3389/fendo.2018.00183 Huijgens, 2021, Effects of gonadectomy and dihydrotestosterone on neuronal plasticity in motivation and reward related brain regions in the male rat, J. Neuroendocrinol., 33 Hutson, 2019, Estrogen receptor profiles across tissues from male and female Rattus norvegicus, Biol. Sex. Differ., 10, 4, 10.1186/s13293-019-0219-9 Hynes, 2020, Chemogenetic inhibition of dopaminergic projections to the nucleus accumbens has sexually dimorphic effects in the rat gambling task, Behav. Neurosci., 134, 309, 10.1037/bne0000372 Jenni, 2021, Medial orbitofrontal cortex dopamine D1/D2 receptors differentially modulate distinct forms of probabilistic decision-making, Neuropsychopharmacol, 46, 1240, 10.1038/s41386-020-00931-1 Jett, 2017, Deficits in cognitive flexibility induced by chronic unpredictable stress are associated with impaired glutamate neurotransmission in the rat medial prefrontal cortex, Neuroscience, 346, 284, 10.1016/j.neuroscience.2017.01.017 Kaasinen, 2001, Sex differences in extrastriatal dopamine D2-like receptors in the human brain, AJP, 158, 308, 10.1176/appi.ajp.158.2.308 Kokane, 2020, Sex differences and the role of estradiol in mesolimbic reward circuits and vulnerability to cocaine and opiate addiction, Front. Behav. Neurosci., 14, 74, 10.3389/fnbeh.2020.00074 Kopec, 2018, Microglial dopamine receptor elimination defines sex-specific nucleus accumbens development and social behavior in adolescent rats, Nat. Commun., 9, 3769, 10.1038/s41467-018-06118-z Krentzel, 2019, Estradiol rapidly modulates excitatory synapse properties in a sex- and region-specific manner in rat nucleus accumbens core and caudate-putamen, J. Neurophysiol., 122, 1213, 10.1152/jn.00264.2019 Krentzel, 2021, Estrogen receptor alpha, G‐protein coupled estrogen receptor 1, and aromatase: developmental, sex, and region‐specific differences across the rat caudate–putamen, nucleus accumbens core and shell, J. Comp. Neurol., 529, 786, 10.1002/cne.24978 Krentzel, 2022, The estrous cycle and 17β‐estradiol modulate the electrophysiological properties of rat nucleus accumbens core medium spiny neurons, J. Neuroendocrinol., 10.1111/jne.13122 Kritzer, 2003, Long-term gonadectomy affects the density of tyrosine hydroxylase- but not dopamine-β-hydroxylase-, choline acetyltransferase- or serotonin- immunoreactive axons in the medial prefrontal cortices of adult male rats, Cereb. Cortex, 13, 282, 10.1093/cercor/13.3.282 Kritzer, 2001, Gonadectomy impairs T-maze acquisition in adult male rats, Horm. Behav., 39, 167, 10.1006/hbeh.2001.1645 Kritzer, 2007, Effects of gonadectomy on performance in operant tasks measuring prefrontal cortical function in adult male rats, Horm. Behav., 51, 183, 10.1016/j.yhbeh.2006.07.005 Larkin, 2016, Modulation of risk/reward decision making by dopaminergic transmission within the basolateral amygdala, Psychopharmacology, 233, 121, 10.1007/s00213-015-4094-8 Lévesque, 1990, Effect of the rat estrous cycle at ovariectomy on striatal D-1 dopamine receptors, Brain Res. Bull., 24, 281, 10.1016/0361-9230(90)90216-M Liu, 2005, Cytochrome P450 17α hydroxylase/17,20 lyase (CYP17) function in cholesterol biosynthesis: identification of squalene monooxygenase (epoxidase) activity associated with CYP17 in Leydig cells, Mol. Endocrinol., 19, 1918, 10.1210/me.2004-0271 Locklear, 2017, Gonadectomy but not biological sex affects burst-firing in dopamine neurons of the ventral tegmental area and in prefrontal cortical neurons projecting to the ventral tegmentum in adult rats, Eur. J. Neurosci., 45, 106, 10.1111/ejn.13380 Lohani, 2018, Burst activation of dopamine neurons produces prolonged post-burst availability of actively released dopamine, Neuropsychopharmacol, 43, 2083, 10.1038/s41386-018-0088-7 Low, 2017, Tyramide signal amplification permits immunohistochemical analyses of androgen receptors in the rat prefrontal cortex, J. Histochem Cytochem, 65, 295, 10.1369/0022155417694870 Low, 2020, Effects of aging on testosterone and androgen receptors in the mesocorticolimbic system of male rats, Horm. Behav., 120, 10.1016/j.yhbeh.2020.104689 Luine, 2020, Estrogenic regulation of memory: the first 50 years, Horm. Behav., 121, 10.1016/j.yhbeh.2020.104711 Luo, 2020, Does GPER really function as a G protein-coupled estrogen receptor in vivo, Front. Endocrinol., 11, 148, 10.3389/fendo.2020.00148 MacLusky, 1986, Estrogen formation and binding in the cerebral cortex of the developing rhesus monkey, Proc. Natl. Acad. Sci., 83, 513, 10.1073/pnas.83.2.513 Maher, 2022, Ovarian hormones regulate nicotine consumption and accumbens glutamatergic plasticity in female rats, ENEURO 9, ENEURO, 0286–21, 2022 Micevych, 2008, Estradiol regulation of progesterone synthesis in the brain, Mol. Cell. Endocrinol., 290, 44, 10.1016/j.mce.2008.04.016 Miller, 2011, The molecular biology, biochemistry, and physiology of human steroidogenesis and its disorders, Endocr. Rev., 32, 81, 10.1210/er.2010-0013 Nicola, 2021, The prostate cancer therapy enzalutamide compared with abiraterone acetate/prednisone impacts motivation for exploration, spatial learning and alters dopaminergic transmission in aged castrated mice, Cancers, 13, 3518, 10.3390/cancers13143518 Nowend, 2001, D1 or D2 antagonism in nucleus accumbens core or dorsomedial shell suppresses lever pressing for food but leads to compensatory increases in chow consumption, Pharmacol. Biochem. Behav., 69, 373, 10.1016/S0091-3057(01)00524-X Oberlander, 2016, 17β-estradiol acutely potentiates glutamatergic synaptic transmission in the hippocampus through distinct mechanisms in males and females, J. Neurosci., 36, 2677, 10.1523/JNEUROSCI.4437-15.2016 Orsini, 2015, Neural mechanisms regulating different forms of risk-related decision-making: Insights from animal models, Neurosci. Biobehav. Rev., 58, 147, 10.1016/j.neubiorev.2015.04.009 Osawa, 1993, Multiple functions of aromatase and the active site structure; aromatase is the placental estrogen 2-hydroxylase, J. Steroid Biochem. Mol. Biol., 44, 469, 10.1016/0960-0760(93)90252-R Pallarés, 2013, Age-dependent effects of prenatal stress on the corticolimbic dopaminergic system development in the rat male offspring, Neurochem Res, 38, 2323, 10.1007/s11064-013-1143-8 Prado, 2017, Cholinergic circuits in cognitive flexibility, Neuroscience, 345, 130, 10.1016/j.neuroscience.2016.09.013 Proaño, 2020, Estradiol decreases medium spiny neuron excitability in female rat nucleus accumbens core, J. Neurophysiol., 123, 2465, 10.1152/jn.00210.2020 Proaño, 2020, Differential and synergistic roles of 17β-estradiol and progesterone in modulating adult female rat nucleus accumbens core medium spiny neuron electrophysiology, J. Neurophysiol., 123, 2390, 10.1152/jn.00157.2020 Purves-Tyson, 2014, Testosterone induces molecular changes in dopamine signaling pathway molecules in the adolescent male rat nigrostriatal pathway, PLoS One, 9, 10.1371/journal.pone.0091151 Quigley, 2021, Sex differences in vulnerability to addiction, Neuropharmacology, 187, 10.1016/j.neuropharm.2021.108491 Ragozzino, 2002, The effects of dopamine D1 receptor blockade in the prelimbic-infralimbic areas on behavioral flexibility, Learn. Mem., 9, 18, 10.1101/lm.45802 Rougé-Pont, 2002, The neurosteroid allopregnanolone increases dopamine release and dopaminergic response to morphine in the rat nucleus accumbens: neurosteroids and dopamine release, Eur. J. Neurosci., 16, 169, 10.1046/j.1460-9568.2002.02084.x Saldanha, 2011, Synaptocrine signaling: steroid synthesis and action at the synapse, Endocr. Rev., 32, 532, 10.1210/er.2011-0004 Salih, 2008, Regulation of catechol O-methyltransferase expression in granulosa cells: a potential role for follicular arrest in polycystic ovary syndrome, Fertil. Steril., 89, 1414, 10.1016/j.fertnstert.2007.04.020 Satta, 2018, Estrogen receptor β in the nucleus accumbens regulates the rewarding properties of cocaine in female mice, Int. J. Neuropsychopharmacol., 21, 382, 10.1093/ijnp/pyx118 Schendzielorz, 2011, Complex estrogenic regulation of catechol-o-methyltransferase (COMT) in rats, J. Physiol. Pharmacol., 62, 483 Schweimer, 2006, Dopamine D1 receptors in the anterior cingulate cortex regulate effort-based decision making, Learn. Mem., 13, 777, 10.1101/lm.409306 Shay, 2020, Changes in nucleus accumbens gene expression accompany sex-specific suppression of spontaneous physical activity in aromatase knockout mice, Horm. Behav., 121, 10.1016/j.yhbeh.2020.104719 Snyder, 2010, Multiple ERβ antisera label in ERβ knockout and null mouse tissues, J. Neurosci. Methods, 188, 226, 10.1016/j.jneumeth.2010.02.012 Song, 2019, Estradiol-induced potentiation of dopamine release in dorsal striatum following amphetamine administration requires estradiol receptors and mGlu5, ENEURO 6, ENEURO, 0446–18, 2019 de Souza Silva, 2009, Dopaminergic and serotonergic activity in neostriatum and nucleus accumbens enhanced by intranasal administration of testosterone, Eur. Neuropsychopharmacol., 19, 53, 10.1016/j.euroneuro.2008.08.003 Spritzer, 2008, Castration differentially affects spatial working and reference memory in male rats, Arch. Sex. Behav., 37, 19, 10.1007/s10508-007-9264-2 Surmeier, 2007, D1 and D2 dopamine-receptor modulation of striatal glutamatergic signaling in striatal medium spiny neurons, Trends Neurosci., 30, 228, 10.1016/j.tins.2007.03.008 Sze, 2021, Effects of prenatal stress on neuroactive steroid responses to acute stress in adult male and female rats, J. Neuroendocr., 33 Thiblin, 1999, Increased dopaminergic and 5-hydroxytryptaminergic activities in male rat brain following long-term treatment with anabolic androgenic steroids: Effect of anabolic androgenic steroids on monoamines, Br. J. Pharmacol., 126, 1301, 10.1038/sj.bjp.0702412 Thomas, 2018, ZIP9, a novel membrane androgen receptor and zinc transporter protein, Gen. Comp. Endocrinol., 257, 130, 10.1016/j.ygcen.2017.04.016 Thompson, 1979, “Persistence” in rats: effects of testosterone, Psychobiology, 7, 291, 10.3758/BF03326643 Tobiansky, D.J., Fuxjager, M.J., 2021. Neuroendocrine regulation of vocalizations and other sounds in nonsongbirds, in: Neuroendocrine Regulation of Animal Vocalization. Elsevier, pp. 315–326. https://doi.org/10.1016/B978–0-12–815160-0.00019–0. Tobiansky, 2016, Estradiol in the preoptic area regulates the dopaminergic response to cocaine in the nucleus accumbens, Neuropsychopharmacol, 41, 1897, 10.1038/npp.2015.360 Tobiansky, 2018, Testosterone and corticosterone in the mesocorticolimbic system of male rats: effects of gonadectomy and caloric restriction, Endocrinology, 159, 450, 10.1210/en.2017-00704 Tobiansky, 2020, Sucrose consumption alters steroid and dopamine signalling in the female rat brain, J. Endocrinol., 245, 231, 10.1530/JOE-19-0386 Tobiansky, 2021, Maternal sucrose consumption alters behaviour and steroids in adult rat offspring, J. Endocrinol., 251, 161, 10.1530/JOE-21-0166 Tomm, 2018, Effects of aging on executive functioning and mesocorticolimbic dopamine markers in male Fischer 344 × brown Norway rats, Neurobiol. Aging, 72, 134, 10.1016/j.neurobiolaging.2018.08.020 Tomm, 2022, Androgen synthesis inhibition increases behavioural flexibility and tyrosine hydroxylase in gonadectomized male rats, J. Neuroendocrinol., 10.1111/jne.13128 Walker, 2001, Sex differences in cocaine-stimulated motor behavior disparate effects of gonadectomy, Neuropsychopharmacology, 25, 118, 10.1016/S0893-133X(00)00248-7 Wallin, 2015, Anabolic–androgenic steroids impair set-shifting and reversal learning in male rats, Eur. Neuropsychopharmacol., 25, 583, 10.1016/j.euroneuro.2015.01.002 Wallin, 2015, Anabolic–androgenic steroids and decision making: probability and effort discounting in male rats, Psychoneuroendocrinology, 84, 10.1016/j.psyneuen.2015.03.023 Wallin-Miller, 2016, Anabolic-androgenic steroids decrease dendritic spine density in the nucleus accumbens of male rats, Neuroscience, 330, 72, 10.1016/j.neuroscience.2016.05.045 Westberry, 2012, Regulation of estrogen receptor alpha gene expression in the mouse prefrontal cortex during early postnatal development, Neurogenetics, 13, 159, 10.1007/s10048-012-0323-z Wood, 2020, Anabolic-androgenic steroid abuse and cognitive impairment: testosterone IMPAIRS biconditional task performance in male rats, Behav. Brain Res., 379, 10.1016/j.bbr.2019.112339 Xu, 2022, Neurosteroids: a novel promise for the treatment of stroke and post‐stroke complications, J. Neurochem., 160, 113, 10.1111/jnc.15503 Yoest, 2018, Rapid effects of ovarian hormones in dorsal striatum and nucleus accumbens, Horm. Behav., 104, 119, 10.1016/j.yhbeh.2018.04.002 Yoest, 2019, Oestradiol influences on dopamine release from the nucleus accumbens shell: sex differences and the role of selective oestradiol receptor subtypes, Br. J. Pharmacol., 176, 4136, 10.1111/bph.14531