{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,14]],"date-time":"2026-10-14T22:19:51Z","timestamp":1792016391895,"version":"4.4.0"},"reference-count":111,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2024,9,18]],"date-time":"2024-09-18T00:00:00Z","timestamp":1726617600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000026","name":"National Institute on Drug Abuse","doi-asserted-by":"publisher","award":["DA047265"],"award-info":[{"award-number":["DA047265"]}],"id":[{"id":"10.13039\/100000026","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000026","name":"National Institute on Drug Abuse","doi-asserted-by":"publisher","award":["DA049837"],"award-info":[{"award-number":["DA049837"]}],"id":[{"id":"10.13039\/100000026","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000026","name":"National Institute on Drug Abuse","doi-asserted-by":"publisher","award":["DA007237"],"award-info":[{"award-number":["DA007237"]}],"id":[{"id":"10.13039\/100000026","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Behav. Neurosci."],"abstract":"<jats:p>Disruptions in glutamate homeostasis within the mesolimbic reward circuitry may play a role in the pathophysiology of various reward related disorders such as major depressive disorders, anxiety, and substance use disorders. Clear sex differences have emerged in the rates and symptom severity of these disorders which may result from differing underlying mechanisms of glutamatergic signaling. Indeed, preclinical models have begun to uncover baseline sex differences throughout the brain in glutamate transmission and synaptic plasticity. Glutamatergic synaptic strength can be assessed by looking at morphological features of glutamatergic neurons including spine size, spine density, and dendritic branching. Likewise, electrophysiology studies evaluate properties of glutamatergic neurons to provide information of their functional capacity. In combination with measures of glutamatergic transmission, synaptic plasticity can be evaluated using protocols that induce long-term potentiation or long-term depression. This review will consider preclinical rodent literature directly comparing glutamatergic transmission and plasticity in reward related regions of males and females. Additionally, we will suggest which regions are exhibiting evidence for sexually dimorphic mechanisms, convergent mechanisms, or no sex differences in glutamatergic transmission and plasticity and highlight gaps in the literature for future investigation.<\/jats:p>","DOI":"10.3389\/fnbeh.2024.1455478","type":"journal-article","created":{"date-parts":[[2024,9,18]],"date-time":"2024-09-18T09:46:37Z","timestamp":1726652797000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":23,"title":["Sex differences in glutamate transmission and plasticity in reward related regions"],"prefix":"10.3389","volume":"18","author":[{"given":"Alyssa R.","family":"Kniffin","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lisa A.","family":"Briand","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2024,9,18]]},"reference":[{"key":"B1","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41539-019-0048-y","article-title":"Is plasticity of synapses the mechanism of long-term memory storage?","volume":"4","author":"Abraham","year":"2019","journal-title":"NPJ Sci. Learn."},{"key":"B2","doi-asserted-by":"publisher","first-page":"283","DOI":"10.1016\/j.brainresrev.2007.07.014","article-title":"Behavioral functions of the mesolimbic dopaminergic system: An affective neuroethological perspective.","volume":"56","author":"Alcaro","year":"2007","journal-title":"Brain Res. Rev."},{"key":"B3","doi-asserted-by":"crossref","first-page":"571","DOI":"10.1016\/0306-4522(89)90424-7","article-title":"The three-dimensional organization of the hippocampal formation: A review of anatomical data.","volume":"31","author":"Amaral","year":"1989","journal-title":"Neuroscience"},{"key":"B4","doi-asserted-by":"crossref","first-page":"550","DOI":"10.1016\/j.tins.2021.03.006","article-title":"Circuit organization of the rodent medial prefrontal cortex.","volume":"44","author":"Anastasiades","year":"2021","journal-title":"Trends Neurosci."},{"key":"B5","doi-asserted-by":"crossref","first-page":"244","DOI":"10.1037\/1064-1297.2.3.244","article-title":"Comparative epidemiology of dependence on tobacco, alcohol, controlled substances, and inhalants: Basic findings from the national comorbidity survey.","volume":"2","author":"Anthony","year":"1994","journal-title":"Exp. Clin. Psychopharmacol."},{"key":"B6","doi-asserted-by":"publisher","first-page":"131","DOI":"10.3389\/neuro.01.1.1.010.2007","article-title":"Ultrastructure of dendritic spines: Correlation between synaptic and spine morphologies.","volume":"1","author":"Arellano","year":"2007","journal-title":"Front. Neurosci."},{"key":"B7","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1016\/j.yhbeh.2015.04.016","article-title":"Signaling mechanisms mediating the regulation of synaptic plasticity and memory by estradiol.","volume":"74","author":"Arevalo","year":"2015","journal-title":"Horm. Behav."},{"key":"B8","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1016\/j.neulet.2009.11.076","article-title":"The density of Golgi-impregnated dendritic spines from adult rat posterodorsal medial amygdala neurons displays no evidence of hemispheric or dorsal\/ventral differences.","volume":"469","author":"Arpini","year":"2010","journal-title":"Neurosci. Lett."},{"key":"B9","doi-asserted-by":"crossref","DOI":"10.3390\/brainsci11030404","article-title":"Plasticity in the hippocampus, neurogenesis and drugs of abuse.","volume":"11","author":"Avchalumov","year":"2021","journal-title":"Brain Sci."},{"key":"B10","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1016\/0959-4388(94)90101-5","article-title":"Synaptic plasticity: LTP and LTD.","volume":"4","author":"Bear","year":"1994","journal-title":"Curr. Opin. Neurobiol."},{"key":"B11","doi-asserted-by":"publisher","first-page":"36","DOI":"10.1016\/j.yfrne.2007.07.003","article-title":"Sex differences in drug abuse.","volume":"29","author":"Becker","year":"2008","journal-title":"Front. Neuroendocrinol."},{"key":"B12","doi-asserted-by":"publisher","first-page":"759","DOI":"10.1002\/cne.25460","article-title":"Estrous cycle impacts on dendritic spine plasticity in rat nucleus accumbens core and shell and caudate\u2013putamen.","volume":"531","author":"Beeson","year":"2023","journal-title":"J. Comp. Neurol."},{"key":"B13","doi-asserted-by":"publisher","DOI":"10.3389\/fnins.2024.1348551","article-title":"The impact of estradiol on serotonin, glutamate, and dopamine systems.","volume":"18","author":"Bendis","year":"2024","journal-title":"Front. Neurosci."},{"key":"B14","doi-asserted-by":"publisher","DOI":"10.1101\/2020.10.09.332965","article-title":"Sex-specific maturational trajectory of endocannabinoid plasticity in the rat prefrontal cortex.","author":"Bernabeu","year":"2020","journal-title":"bioRxiv"},{"key":"B15","doi-asserted-by":"publisher","DOI":"10.3389\/fnana.2014.00123","article-title":"Structural plasticity: Mechanisms and contribution to developmental psychiatric disorders.","volume":"8","author":"Bernardinelli","year":"2014","journal-title":"Front. Neuroanat."},{"key":"B16","doi-asserted-by":"publisher","first-page":"10567","DOI":"10.1523\/JNEUROSCI.0758-17.2017","article-title":"Sex- and estrus-dependent differences in rat basolateral amygdala.","volume":"37","author":"Blume","year":"2017","journal-title":"J. Neurosci."},{"key":"B17","doi-asserted-by":"publisher","first-page":"2627","DOI":"10.1093\/cercor\/bhz265","article-title":"Sex-specific difference of hippocampal synaptic plasticity in response to sex neurosteroids.","volume":"30","author":"Brandt","year":"2020","journal-title":"Cereb. Cortex"},{"key":"B18","doi-asserted-by":"publisher","first-page":"212","DOI":"10.1016\/j.tips.2008.12.006","article-title":"Estrogen-induced plasticity from cells to circuits: Predictions for cognitive function.","volume":"30","author":"Brinton","year":"2009","journal-title":"Trends Pharmacol. Sci."},{"key":"B19","doi-asserted-by":"publisher","first-page":"1589","DOI":"10.1523\/JNEUROSCI.20-04-01589.2000","article-title":"Estrogen selectively regulates spine density within the dendritic arbor of rat ventromedial hypothalamic neurons.","volume":"20","author":"Calizo","year":"2000","journal-title":"J. Neurosci."},{"key":"B20","doi-asserted-by":"publisher","first-page":"242","DOI":"10.1016\/j.physbeh.2011.01.024","article-title":"Sex differences in synaptic plasticity in stress-responsive brain regions following chronic variable stress.","volume":"104","author":"Carvalho-Netto","year":"2011","journal-title":"Physiol. Behav."},{"key":"B21","doi-asserted-by":"publisher","DOI":"10.3389\/fncel.2014.00401","article-title":"The role of AMPA receptors in postsynaptic mechanisms of synaptic plasticity.","volume":"8","author":"Chater","year":"2014","journal-title":"Front. Cell. Neurosci."},{"key":"B22","doi-asserted-by":"crossref","DOI":"10.36255\/exonpublications.cerebralischemia.2021.hippocampus","article-title":"The Anatomy of the Hippocampus","author":"Chauhan","year":"2021","journal-title":"Cerebral ischemia"},{"key":"B23","doi-asserted-by":"publisher","first-page":"498","DOI":"10.1016\/j.yhbeh.2014.07.008","article-title":"Roles of testosterone and amygdaloid LTP induction in determining sex differences in fear memory magnitude.","volume":"66","author":"Chen","year":"2014","journal-title":"Horm. Behav."},{"key":"B24","doi-asserted-by":"publisher","first-page":"839","DOI":"10.1037\/\/0735-7044.97.6.839","article-title":"The hamster hippocampal slice: II. Neuroendocrine modulation.","volume":"97","author":"Chiaia","year":"1983","journal-title":"Behav. Neurosci."},{"key":"B25","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1038\/sj.npp.1301559","article-title":"Synaptic plasticity: Multiple forms, functions, and mechanisms.","volume":"33","author":"Citri","year":"2008","journal-title":"Neuropsychopharmacology"},{"key":"B26","doi-asserted-by":"publisher","first-page":"1127","DOI":"10.1159\/000531351","article-title":"Cocaine exposure increases excitatory synaptic transmission and intrinsic excitability in the basolateral amygdala in male and female rats and across the estrous cycle.","volume":"113","author":"Corbett","year":"2023","journal-title":"Neuroendocrinology"},{"key":"B27","doi-asserted-by":"publisher","DOI":"10.1242\/jcs.227793","article-title":"Sexual dimorphism, estrous cycle and laterality determine the intrinsic and synaptic properties of medial amygdala neurons in rat.","volume":"132","author":"Dalpian","year":"2019","journal-title":"J. Cell Sci."},{"key":"B28","doi-asserted-by":"publisher","first-page":"202","DOI":"10.1038\/nrn3444","article-title":"New insights into the classification and nomenclature of cortical GABAergic interneurons.","volume":"14","author":"DeFelipe","year":"2013","journal-title":"Nat. Rev. Neurosci."},{"key":"B29","doi-asserted-by":"publisher","DOI":"10.1111\/adb.13077","article-title":"Adolescent social isolation induced alterations in nucleus accumbens glutamate signalling.","volume":"27","author":"Deutschmann","year":"2022","journal-title":"Addict. Biol."},{"key":"B30","doi-asserted-by":"crossref","first-page":"758","DOI":"10.1002\/hbm.20903","article-title":"The neural correlates of sex differences in emotional reactivity and emotion regulation.","volume":"31","author":"Domes","year":"2010","journal-title":"Hum. Brain Mapp."},{"key":"B31","doi-asserted-by":"crossref","first-page":"361","DOI":"10.1002\/syn.21909","article-title":"Synaptic number changes in the medial prefrontal cortex across adolescence in male and female rats: A role for pubertal onset.","volume":"70","author":"Drzewiecki","year":"2016","journal-title":"Synapse"},{"key":"B32","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1016\/j.yhbeh.2006.10.001","article-title":"Androgen receptors are required for full masculinization of the ventromedial hypothalamus (VMH) in rats.","volume":"51","author":"Dugger","year":"2007","journal-title":"Horm. Behav."},{"key":"B33","doi-asserted-by":"publisher","first-page":"329","DOI":"10.1002\/cne.1106","article-title":"Influence of sex and estrus cycle on the sexual dimorphisms of the hypothalamic ventromedial nucleus: Stereological evaluation and Golgi study.","volume":"432","author":"Dulce Madeira","year":"2001","journal-title":"J. Comp. Neurol."},{"key":"B34","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1146\/annurev-psych-010213-115159","article-title":"The nucleus accumbens: An interface between cognition, emotion, and action.","volume":"66","author":"Floresco","year":"2015","journal-title":"Annu. Rev. Psychol."},{"key":"B35","doi-asserted-by":"publisher","first-page":"1330","DOI":"10.1002\/cne.22279","article-title":"Quantitative analysis of pre-and postsynaptic sex differences in the nucleus accumbens.","volume":"518","author":"Forlano","year":"2010","journal-title":"J. Comp. Neurol."},{"key":"B36","doi-asserted-by":"publisher","first-page":"1532","DOI":"10.1016\/j.psyneuen.2012.12.022","article-title":"The effects of exogenous progesterone on drug craving and stress arousal in cocaine dependence: Impact of gender and cue type.","volume":"38","author":"Fox","year":"2013","journal-title":"Psychoneuroendocrinology"},{"key":"B37","doi-asserted-by":"publisher","first-page":"905","DOI":"10.1037\/0735-7044.120.4.905","article-title":"Estradiol\u2019s effects on learning and neuronal morphology vary with route of administration.","volume":"120","author":"Garza-Meilandt","year":"2006","journal-title":"Behav. Neurosci."},{"key":"B38","doi-asserted-by":"crossref","first-page":"218","DOI":"10.1016\/j.bcp.2007.06.039","article-title":"Glutamatergic substrates of drug addiction and alcoholism.","volume":"75","author":"Gass","year":"2008","journal-title":"Biochem. Pharmacol."},{"key":"B39","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1016\/j.neubiorev.2020.03.010","article-title":"Sex differences in the glutamate system: Implications for addiction.","volume":"113","author":"Giacometti","year":"2020","journal-title":"Neurosci. Biobehav. Rev."},{"key":"B40","doi-asserted-by":"publisher","first-page":"276","DOI":"10.1016\/j.neuropharm.2013.04.032","article-title":"Rapid, transient synaptic plasticity in addiction.","volume":"76","author":"Gipson","year":"2014","journal-title":"Neuropharmacology"},{"key":"B41","doi-asserted-by":"crossref","first-page":"333","DOI":"10.1016\/0006-8993(78)90723-0","article-title":"Evidence for a morphological sex difference within the medial preoptic area of the rat brain.","volume":"148","author":"Gorski","year":"1978","journal-title":"Brain Res."},{"key":"B42","doi-asserted-by":"publisher","first-page":"905","DOI":"10.1159\/000531148","article-title":"Sex hormones, neurosteroids, and glutamatergic neurotransmission: A review of the literature.","volume":"113","author":"Goyette","year":"2023","journal-title":"Neuroendocrinology"},{"key":"B43","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1038\/s41386-018-0153-2","article-title":"Sex differences in psychiatric disorders: What we can learn from sex chromosome aneuploidies.","volume":"44","author":"Green","year":"2019","journal-title":"Neuropsychopharmacology"},{"key":"B44","doi-asserted-by":"publisher","first-page":"10817","DOI":"10.1073\/pnas.0903603106","article-title":"Development regulates a switch between post- and presynaptic strengthening in response to activity deprivation.","volume":"106","author":"Han","year":"2009","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B45","doi-asserted-by":"publisher","first-page":"1723","DOI":"10.1523\/JNEUROSCI.0820-14.2015","article-title":"Opioid receptor-dependent sex differences in synaptic plasticity in the hippocampal mossy fiber pathway of the adult rat.","volume":"35","author":"Harte-Hargrove","year":"2015","journal-title":"J. Neurosci. Off. J. Soc. Neurosci."},{"key":"B46","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1038\/s41386-018-0167-9","article-title":"Sex differences in the hypothalamic\u2013pituitary\u2013adrenal axis\u2019 response to stress: An important role for gonadal hormones.","volume":"44","author":"Heck","year":"2019","journal-title":"Neuropsychopharmacology"},{"key":"B47","doi-asserted-by":"publisher","DOI":"10.3389\/fncom.2013.00045","article-title":"Theoretical models of synaptic short term plasticity.","volume":"7","author":"Hennig","year":"2013","journal-title":"Front. Comput. Neurosci."},{"key":"B48","doi-asserted-by":"crossref","first-page":"880","DOI":"10.1038\/35104061","article-title":"Dentritic spines: Structure, dynamics and regulation.","volume":"2","author":"Hering","year":"2001","journal-title":"Nat. Rev. Neurosci."},{"key":"B49","doi-asserted-by":"publisher","DOI":"10.1101\/2023.10.18.562844","article-title":"Sexual differences in neuronal and synaptic properties across subregions of the mouse insular cortex.","author":"Iezzi","year":"2023","journal-title":"bioRxiv"},{"key":"B50","doi-asserted-by":"publisher","first-page":"179","DOI":"10.1002\/neu.10200","article-title":"Effects of neonatal gonadal steroids on adult CA3 pyramidal neuron dendritic morphology and spatial memory in rats.","volume":"55","author":"Isgor","year":"2003","journal-title":"J. Neurobiol."},{"key":"B51","first-page":"1552","article-title":"Latent sex differences in molecular signaling that underlies excitatory synaptic potentiation in the hippocampus.","volume":"39","author":"Jain","year":"2019","journal-title":"J. Neurosci."},{"key":"B52","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuint.2023.105570","article-title":"Comprehensive analysis of sex differences in the function and ultrastructure of hippocampal presynaptic terminals.","volume":"169","author":"Kim","year":"2023","journal-title":"Neurochem. Int."},{"key":"B53","doi-asserted-by":"publisher","DOI":"10.1186\/s13293-023-00537-4","article-title":"Sex differences in pre- and post-synaptic glutamate signaling in the nucleus accumbens core.","volume":"14","author":"Knouse","year":"2023","journal-title":"Biol. Sex Differ."},{"key":"B54","doi-asserted-by":"crossref","DOI":"10.1186\/s13293-022-00468-6","article-title":"Sex differences in the medial prefrontal cortical glutamate system.","volume":"13","author":"Knouse","year":"2022","journal-title":"Biol. Sex Differ."},{"key":"B55","doi-asserted-by":"publisher","DOI":"10.3389\/fncel.2015.00015","article-title":"Plasticity in the prefrontal cortex of adult rats.","volume":"9","author":"Kolb","year":"2015","journal-title":"Front. Cell. Neurosci."},{"key":"B56","doi-asserted-by":"publisher","first-page":"95","DOI":"10.1111\/j.1365-2826.1991.tb00245.x","article-title":"Sex-related differences in dendritic branching of cells in the prefrontal cortex of rats.","volume":"3","author":"Kolb","year":"1991","journal-title":"J. Neuroendocrinol."},{"key":"B57","first-page":"216","article-title":"Androgen effects on neural plasticity.","volume":"2","author":"Kuwahara","year":"2021","journal-title":"Androgens"},{"key":"B58","doi-asserted-by":"publisher","first-page":"147","DOI":"10.1016\/0304-3940(95)12129-r","article-title":"Sexually dimorphic contribution from the fornix to the ventromedial hypothalamic nucleus: A quantitative electron microscopic study.","volume":"200","author":"Larriva-Sahd","year":"1995","journal-title":"Neurosci. Lett."},{"key":"B59","doi-asserted-by":"crossref","first-page":"495","DOI":"10.1523\/JNEUROSCI.4516-03.2004","article-title":"Androgens increase spine synapse density in the ca1 hippocampal subfield of ovariectomized female rats.","volume":"24","author":"Leranth","year":"2004","journal-title":"J. Neurosci."},{"key":"B60","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1007\/978-3-030-81147-1_4","article-title":"The Brain\u2019s reward system in health and disease.","volume":"1344","author":"Lewis","year":"2021","journal-title":"Adv. Exp. Med. Biol."},{"key":"B61","doi-asserted-by":"publisher","first-page":"1561","DOI":"10.1021\/acschemneuro.3c00062","article-title":"Current best practices for analysis of dendritic spine morphology and number in neurodevelopmental disorder research.","volume":"14","author":"Li","year":"2023","journal-title":"ACS Chem. Neurosci."},{"key":"B62","doi-asserted-by":"publisher","DOI":"10.3389\/fpsyt.2018.00767","article-title":"Glutamatergic dysfunction and glutamatergic compounds for major psychiatric disorders: Evidence from clinical neuroimaging studies.","volume":"9","author":"Li","year":"2019","journal-title":"Front. Psychiatry"},{"key":"B63","doi-asserted-by":"publisher","DOI":"10.3389\/fnana.2018.00084","article-title":"Cell-type-specific afferent innervation of the nucleus accumbens core and shell.","volume":"12","author":"Li","year":"2018","journal-title":"Front. Neuroanat."},{"key":"B64","doi-asserted-by":"crossref","DOI":"10.1186\/s13041-020-00583-8","article-title":"Sex difference in synaptic plasticity in the anterior cingulate cortex of adult mice.","volume":"13","author":"Liu","year":"2020","journal-title":"Mol. Brain"},{"key":"B65","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuroscience.2022.06.002","article-title":"Androgens enhance recognition memory and dendritic spine density in the hippocampus and prefrontal cortex of ovariectomized female rats.","author":"Luine","year":"2022","journal-title":"Neuroscience"},{"key":"B66","doi-asserted-by":"crossref","DOI":"10.1101\/cshperspect.a005710","article-title":"NMDA receptor-dependent long-term potentiation and long-term depression (LTP\/LTD).","volume":"4","author":"L\u00fcscher","year":"2012","journal-title":"Cold Spring Harb. Perspect. Biol."},{"key":"B67","doi-asserted-by":"publisher","first-page":"4154","DOI":"10.1210\/en.2004-0477","article-title":"Effects of dehydroepiandrosterone and flutamide on hippocampal CA1 spine synapse density in male and female rats: Implications for the role of androgens in maintenance of hippocampal structure.","volume":"145","author":"MacLusky","year":"2004","journal-title":"Endocrinology"},{"key":"B68","doi-asserted-by":"crossref","first-page":"537","DOI":"10.1007\/BF00227079","article-title":"Sexual dimorphism in the mossy fiber synapses of the rat hippocampus.","volume":"87","author":"Madeira","year":"1991","journal-title":"Exp. Brain Res."},{"key":"B69","doi-asserted-by":"crossref","DOI":"10.1038\/srep12511","article-title":"Basolateral amygdala rapid glutamate release encodes an outcome-specific representation vital for reward-predictive cues to selectively invigorate reward-seeking actions.","volume":"5","author":"Malvaez","year":"2015","journal-title":"Sci. Rep."},{"key":"B70","doi-asserted-by":"publisher","first-page":"177","DOI":"10.1016\/0304-3940(95)11869-x","article-title":"Sexually dimorphic perforant path long-term potentiation (LTP) in urethane-anesthetized rats.","volume":"196","author":"Maren","year":"1995","journal-title":"Neurosci. Lett."},{"key":"B71","doi-asserted-by":"crossref","first-page":"7548","DOI":"10.1523\/JNEUROSCI.15-11-07548.1995","article-title":"Synaptic plasticity in the basolateral amygdala induced by hippocampal formation stimulation in vivo.","volume":"15","author":"Maren","year":"1995","journal-title":"J. Neurosci. Off. J. Soc. Neurosci."},{"key":"B72","doi-asserted-by":"crossref","first-page":"579","DOI":"10.1016\/S0197-4580(02)00004-0","article-title":"Aging and sex influence the anatomy of the rat anterior cingulate cortex.","volume":"23","author":"Markham","year":"2002","journal-title":"Neurobiol. Aging"},{"key":"B73","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1016\/j.pnpbp.2012.12.012","article-title":"Synaptic plasticity in depression: Molecular, cellular and functional correlates.","volume":"43","author":"Marsden","year":"2013","journal-title":"Prog. Neuropsychopharmacol. Biol. Psychiatry"},{"key":"B74","doi-asserted-by":"publisher","first-page":"232","DOI":"10.1159\/000124445","article-title":"Male-female difference in synaptic organization of the ventromedial nucleus of the hypothalamus in the rat.","volume":"42","author":"Matsumoto","year":"2008","journal-title":"Neuroendocrinology"},{"key":"B75","doi-asserted-by":"publisher","first-page":"177","DOI":"10.1016\/j.neulet.2010.10.017","article-title":"Measurements of neuron soma size and density in rat dorsal striatum, nucleus accumbens core and nucleus accumbens shell: Differences between striatal region and brain hemisphere, but not sex.","volume":"487","author":"Meitzen","year":"2011","journal-title":"Neurosci. Lett."},{"key":"B76","doi-asserted-by":"crossref","first-page":"3112","DOI":"10.3390\/biom5043112","article-title":"Overview of glutamatergic dysregulation in central pathologies.","volume":"5","author":"Miladinovic","year":"2015","journal-title":"Biomolecules"},{"key":"B77","doi-asserted-by":"publisher","first-page":"1420","DOI":"10.1021\/acschemneuro.5b00096","article-title":"Gender differences in spatial learning, synaptic activity, and long-term potentiation in the hippocampus in rats: Molecular mechanisms.","volume":"6","author":"Monfort","year":"2015","journal-title":"ACS Chem. Neurosci."},{"key":"B78","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1016\/j.tics.2007.08.013","article-title":"The amygdala, reward and emotion.","volume":"11","author":"Murray","year":"2007","journal-title":"Trends Cogn. Sci."},{"key":"B79","doi-asserted-by":"publisher","DOI":"10.1016\/j.pharmthera.2020.107797","article-title":"Cocaine use disorder: A look at metabotropic glutamate receptors and glutamate transporters.","volume":"221","author":"Niedzielska-Andres","year":"2021","journal-title":"Pharmacol. Ther."},{"key":"B80","doi-asserted-by":"publisher","DOI":"10.3389\/fncel.2020.00268","article-title":"Sex differences in dendritic spine formation in the hippocampus and animal behaviors in a mouse model of hyperthyroidism.","volume":"14","author":"Niiyama","year":"2020","journal-title":"Front. Cell. Neurosci."},{"key":"B81","doi-asserted-by":"publisher","first-page":"31","DOI":"10.1016\/0006-8993(81)90029-9","article-title":"Sexual dimorphism in synaptic organization in the amygdala and its dependence on neonatal hormone environment.","volume":"212","author":"Nishizuka","year":"1981","journal-title":"Brain Res."},{"key":"B82","article-title":"Sex differences in dendritic spine density and morphology in auditory and visual cortices in adolescence and adulthood.","volume":"10","author":"Parker","year":"2020","journal-title":"Sci. Rep."},{"key":"B83","doi-asserted-by":"publisher","first-page":"3039","DOI":"10.1111\/ejn.15168","article-title":"Medial prefrontal cortical control of reward- and aversion-based behavioral output: Bottom-up modulation.","volume":"53","author":"Pastor","year":"2021","journal-title":"Eur. J. Neurosci."},{"key":"B84","doi-asserted-by":"publisher","DOI":"10.1523\/ENEURO.0401-18.2018","article-title":"Methamphetamine self-administration elicits sex-related changes in postsynaptic glutamate transmission in the prefrontal cortex.","volume":"6","author":"Pena-Bravo","year":"2019","journal-title":"eNeuro"},{"key":"B85","doi-asserted-by":"crossref","first-page":"124","DOI":"10.1016\/j.brainresrev.2010.09.001","article-title":"Prefrontal cortex and drug abuse vulnerability: Translation to prevention and treatment interventions.","volume":"65","author":"Perry","year":"2011","journal-title":"Brain Res. Rev."},{"key":"B86","doi-asserted-by":"publisher","DOI":"10.1002\/phy2.185","article-title":"Modulatory role of androgenic and estrogenic neurosteroids in determining the direction of synaptic plasticity in the CA1 hippocampal region of male rats.","volume":"1","author":"Pettorossi","year":"2013","journal-title":"Physiol. Rep."},{"key":"B87","doi-asserted-by":"publisher","first-page":"189","DOI":"10.1016\/0165-3806(91)90131-2","article-title":"Stereological analysis of the hypothalamic ventromedial nucleus: II. Hormone-induced changes in the synaptogenic pattern.","volume":"61","author":"Pozzo Miller","year":"1991","journal-title":"Dev. Brain Res."},{"key":"B88","doi-asserted-by":"publisher","first-page":"1356","DOI":"10.1152\/jn.00263.2018","article-title":"Estrous cycle-induced sex differences in medium spiny neuron excitatory synaptic transmission and intrinsic excitability in adult rat nucleus accumbens core.","volume":"120","author":"Proa\u00f1o","year":"2018","journal-title":"J. Neurophysiol."},{"key":"B89","doi-asserted-by":"publisher","first-page":"289","DOI":"10.1016\/B978-0-12-801942-9.00012-4","article-title":"Chapter 12 - role of the prefrontal cortex in addictive disorders","author":"Renard","year":"2017","journal-title":"The cerebral cortex in neurodegenerative and neuropsychiatric disorders"},{"key":"B90","doi-asserted-by":"publisher","first-page":"137","DOI":"10.1016\/j.neurobiolaging.2007.05.006","article-title":"Age-related dendritic hypertrophy and sexual dimorphism in rat basolateral amygdala.","volume":"30","author":"Rubinow","year":"2009","journal-title":"Neurobiol. Aging"},{"key":"B91","doi-asserted-by":"publisher","DOI":"10.1186\/s12993-021-00184-y","article-title":"Sex differences in spatial learning and memory and hippocampal long-term potentiation at perforant pathway-dentate gyrus (PP-DG) synapses in Wistar rats.","volume":"17","author":"Safari","year":"2021","journal-title":"Behav. Brain Funct."},{"key":"B92","doi-asserted-by":"crossref","first-page":"1333","DOI":"10.1016\/S0022-5347(05)67773-7","article-title":"ALTERED SYNAPTIC TRANSMISSION IN THE HIPPOCAMPUS OF THE CASTRATED MALE MOUSE IS REVERSED BY TESTOSTERONE REPLACEMENT.","volume":"163","author":"Sakata","year":"2000","journal-title":"J. Urol."},{"key":"B93","doi-asserted-by":"publisher","first-page":"205","DOI":"10.1007\/978-3-030-19898-5_9","article-title":"The mouse hypothalamus","author":"Schr\u00f6der","year":"2020","journal-title":"Neuroanatomy of the mouse: An introduction"},{"key":"B94","year":"2013","journal-title":"Reward circuit - an overview."},{"key":"B95","doi-asserted-by":"publisher","first-page":"365","DOI":"10.1159\/000125915","article-title":"Estrogen increases spine density in ventromedial hypothalamic neurons of peripubertal rats.","volume":"54","author":"Segarra","year":"2008","journal-title":"Neuroendocrinology"},{"key":"B96","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-021-96846-y","article-title":"Differences in synaptic vesicle pool behavior between male and female hippocampal cultured neurons.","volume":"11","author":"Sertel","year":"2021","journal-title":"Sci. Rep."},{"key":"B97","doi-asserted-by":"crossref","first-page":"517","DOI":"10.1016\/S0306-4522(01)00490-0","article-title":"Sex differences in hippocampal slice excitability: Role of testosterone.","volume":"109","author":"Smith","year":"2002","journal-title":"Neuroscience"},{"key":"B98","doi-asserted-by":"publisher","first-page":"353","DOI":"10.1016\/0006-8993(87)90634-2","article-title":"Progesterone alters GABA and glutamate responsiveness: A possible mechanism for its anxiolytic action.","volume":"400","author":"Smith","year":"1987","journal-title":"Brain Res."},{"key":"B99","doi-asserted-by":"crossref","first-page":"1578","DOI":"10.1016\/j.neuropsychologia.2012.03.011","article-title":"Sex differences in brain activation to emotional stimuli: A meta-analysis of neuroimaging studies.","volume":"50","author":"Stevens","year":"2012","journal-title":"Neuropsychologia"},{"key":"B100","doi-asserted-by":"publisher","first-page":"244","DOI":"10.1093\/cercor\/bhw388","article-title":"Age- and sex-dependent impact of repeated social stress on intrinsic and synaptic excitability of the rat prefrontal cortex.","volume":"27","author":"Urban","year":"2017","journal-title":"Cereb. Cortex"},{"key":"B101","doi-asserted-by":"crossref","first-page":"2829","DOI":"10.1523\/JNEUROSCI.13-07-02829.1993","article-title":"Glutamate neurons in hypothalamus regulate excitatory transmission.","volume":"13","author":"van den Pol","year":"1993","journal-title":"J. Neurosci."},{"key":"B102","doi-asserted-by":"publisher","first-page":"7935","DOI":"10.1523\/JNEUROSCI.0801-18.2018","article-title":"Memory-related synaptic plasticity is sexually dimorphic in rodent hippocampus.","volume":"38","author":"Wang","year":"2018","journal-title":"J. Neurosci."},{"key":"B103","doi-asserted-by":"publisher","first-page":"363","DOI":"10.1016\/j.neuroscience.2015.06.008","article-title":"Prenatal chronic mild stress induces depression-like behavior and sex-specific changes in regional glutamate receptor expression patterns in adult rats.","volume":"301","author":"Wang","year":"2015","journal-title":"Neuroscience"},{"key":"B104","doi-asserted-by":"publisher","first-page":"26","DOI":"10.1016\/0006-8993(95)01059-9","article-title":"LTP varies across the estrous cycle: Enhanced synaptic plasticity in proestrus rats.","volume":"703","author":"Warren","year":"1995","journal-title":"Brain Res."},{"key":"B105","doi-asserted-by":"publisher","DOI":"10.3389\/fnmol.2018.00197","article-title":"Sex differences in psychiatric disease: A focus on the glutamate system.","volume":"11","author":"Wickens","year":"2018","journal-title":"Front. Mol. Neurosci."},{"key":"B106","doi-asserted-by":"crossref","DOI":"10.1523\/ENEURO.0147-15.2016","article-title":"No evidence for sex differences in the electrophysiological properties and excitatory synaptic input onto nucleus accumbens shell medium spiny neurons.","volume":"3","author":"Willett","year":"2016","journal-title":"eNeuro"},{"key":"B107","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1007\/s00429-011-0353-6","article-title":"Ultrastructural analysis of sex differences in nucleus accumbens synaptic connectivity.","volume":"217","author":"Wissman","year":"2012","journal-title":"Brain Struct. Funct."},{"key":"B108","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1016\/j.neuropharm.2011.04.002","article-title":"Sex differences and effects of cocaine on excitatory synapses in the nucleus accumbens.","volume":"61","author":"Wissman","year":"2011","journal-title":"Neuropharmacology"},{"key":"B109","doi-asserted-by":"crossref","first-page":"4035","DOI":"10.1523\/JNEUROSCI.10-12-04035.1990","article-title":"Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons.","volume":"10","author":"Woolley","year":"1990","journal-title":"J. Neurosci."},{"key":"B110","doi-asserted-by":"publisher","first-page":"831","DOI":"10.1210\/me.2002-0314","article-title":"Estrogen enhances depolarization-induced glutamate release through activation of phosphatidylinositol 3-kinase and mitogen-activated protein kinase in cultured hippocampal neurons.","volume":"17","author":"Yokomaku","year":"2003","journal-title":"Mol. Endocrinol."},{"key":"B111","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1111\/j.1749-6632.1999.tb09264.x","article-title":"Functional-anatomical implications of the nucleus accumbens core and shell subterritories.","volume":"877","author":"Zahm","year":"1999","journal-title":"Ann. N. Y. Acad. Sci."}],"container-title":["Frontiers in Behavioral Neuroscience"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fnbeh.2024.1455478\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,9,18]],"date-time":"2024-09-18T09:46:52Z","timestamp":1726652812000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fnbeh.2024.1455478\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,9,18]]},"references-count":111,"alternative-id":["10.3389\/fnbeh.2024.1455478"],"URL":"https:\/\/doi.org\/10.3389\/fnbeh.2024.1455478","relation":{},"ISSN":["1662-5153"],"issn-type":[{"value":"1662-5153","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,9,18]]},"article-number":"1455478"}}