{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,18]],"date-time":"2026-08-18T15:59:09Z","timestamp":1787068749648,"version":"build-2736575974"},"reference-count":45,"publisher":"Elsevier BV","license":[{"start":{"date-parts":[[2021,10,1]],"date-time":"2021-10-01T00:00:00Z","timestamp":1633046400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2021,10,1]],"date-time":"2021-10-01T00:00:00Z","timestamp":1633046400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"},{"start":{"date-parts":[[2021,7,13]],"date-time":"2021-07-13T00:00:00Z","timestamp":1626134400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"}],"content-domain":{"domain":["clinicalkey.com","clinicalkey.com.au","clinicalkey.es","clinicalkey.fr","clinicalkey.jp","elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Neurobiology of Disease"],"published-print":{"date-parts":[[2021,10]]},"DOI":"10.1016\/j.nbd.2021.105448","type":"journal-article","created":{"date-parts":[[2021,7,16]],"date-time":"2021-07-16T05:16:59Z","timestamp":1626412619000},"page":"105448","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":10,"special_numbering":"C","title":["Serotonin drives striatal synaptic plasticity in a sex-related manner"],"prefix":"10.1016","volume":"158","author":[{"given":"Federica","family":"Campanelli","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gioia","family":"Marino","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Noemi","family":"Barsotti","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Giuseppina","family":"Natale","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Valeria","family":"Calabrese","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Antonella","family":"Cardinale","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Veronica","family":"Ghiglieri","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Giacomo","family":"Maddaloni","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alessandro","family":"Usiello","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paolo","family":"Calabresi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Massimo","family":"Pasqualetti","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Barbara","family":"Picconi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.nbd.2021.105448_bb0005","doi-asserted-by":"crossref","first-page":"10332","DOI":"10.1073\/pnas.0810793106","article-title":"Growth retardation and altered autonomic control in mice lacking brain serotonin","volume":"106","author":"Alenina","year":"2009","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"10.1016\/j.nbd.2021.105448_bb0010","doi-asserted-by":"crossref","first-page":"17921","DOI":"10.1523\/JNEUROSCI.2664-12.2012","article-title":"Rebalance of striatal NMDA\/AMPA receptor ratio underlies the reduced emergence of dyskinesia during D2-like dopamine agonist treatment in experimental Parkinson\u2019s disease","volume":"32","author":"Bagetta","year":"2012","journal-title":"J. Neurosci."},{"key":"10.1016\/j.nbd.2021.105448_bb0015","doi-asserted-by":"crossref","first-page":"4372","DOI":"10.1210\/endo.137.10.8828498","article-title":"Steroid regulation of estrogen and progestin receptor messenger ribonucleic acid in monkey hypothalamus and pituitary","volume":"137","author":"Bethea","year":"1996","journal-title":"Endocrinology"},{"key":"10.1016\/j.nbd.2021.105448_bb0020","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1006\/frne.2001.0225","article-title":"Diverse actions of ovarian steroids in the serotonin neural system","volume":"23","author":"Bethea","year":"2002","journal-title":"Front. Neuroendocrinol."},{"key":"10.1016\/j.nbd.2021.105448_bb0025","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0035538","article-title":"Mouse estrous cycle identification tool and images","volume":"7","author":"Byers","year":"2012","journal-title":"PLoS One"},{"key":"10.1016\/j.nbd.2021.105448_bb0030","doi-asserted-by":"crossref","first-page":"929","DOI":"10.1111\/j.1460-9568.1992.tb00119.x","article-title":"Long-term potentiation in the striatum is unmasked by removing the voltage-dependent magnesium block of NMDA receptor channels","volume":"4","author":"Calabresi","year":"1992","journal-title":"Eur. J. Neurosci."},{"key":"10.1016\/j.nbd.2021.105448_bb0035","doi-asserted-by":"crossref","first-page":"674","DOI":"10.1111\/jnc.13280","article-title":"Tph2 gene deletion enhances amphetamine-induced hypermotility: effect of 5-HT restoration and role of striatal noradrenaline release","volume":"135","author":"Carli","year":"2015","journal-title":"J. Neurochem."},{"key":"10.1016\/j.nbd.2021.105448_bb0040","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1016\/0278-5846(88)90061-9","article-title":"A regional study of sex differences in rat brain serotonin","volume":"12","author":"Carlsson","year":"1988","journal-title":"Prog. Neuro-Psychopharmacol. Biol. Psychiatry"},{"key":"10.1016\/j.nbd.2021.105448_bb0045","doi-asserted-by":"crossref","first-page":"1819","DOI":"10.1093\/brain\/awm082","article-title":"Dopamine released from 5-HT terminals is the cause of L-DOPA-induced dyskinesia in parkinsonian rats","volume":"130","author":"Carta","year":"2007","journal-title":"Brain"},{"key":"10.1016\/j.nbd.2021.105448_bb0050","doi-asserted-by":"crossref","first-page":"801","DOI":"10.1016\/j.neuron.2018.04.008","article-title":"Serotonergic signaling controls input-specific synaptic plasticity at striatal circuits","volume":"98","author":"Cavaccini","year":"2018","journal-title":"Neuron"},{"key":"10.1016\/j.nbd.2021.105448_bb0055","doi-asserted-by":"crossref","first-page":"3575","DOI":"10.1152\/jn.1999.82.6.3575","article-title":"Unilateral dopamine denervation blocks corticostriatal LTP","volume":"82","author":"Centonze","year":"1999","journal-title":"J. Neurophysiol."},{"key":"10.1016\/j.nbd.2021.105448_bb0060","doi-asserted-by":"crossref","first-page":"106","DOI":"10.1016\/j.biopsych.2014.04.002","article-title":"Derangement of Ras-guanine nucleotide-releasing factor 1 (Ras-GRF1) and extracellular signal-regulated kinase (ERK) dependent striatal plasticity in L-DOPA-induced dyskinesia","volume":"77","author":"Cerovic","year":"2015","journal-title":"Biol. Psychiatry"},{"key":"10.1016\/j.nbd.2021.105448_bb0065","doi-asserted-by":"crossref","first-page":"8165","DOI":"10.1523\/JNEUROSCI.1816-05.2005","article-title":"Genotype-dependent activity of tryptophan hydroxylase-2 determines the response to citalopram in a mouse model of depression","volume":"25","author":"Cervo","year":"2005","journal-title":"J. Neurosci."},{"key":"10.1016\/j.nbd.2021.105448_bb0070","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1016\/j.pneurobio.2016.03.004","article-title":"Serotonergic modulation of the activity of mesencephalic dopaminergic systems: therapeutic implications","volume":"151","author":"De Deurwaerdere","year":"2017","journal-title":"Prog. Neurobiol."},{"key":"10.1016\/j.nbd.2021.105448_bb0075","doi-asserted-by":"crossref","first-page":"238","DOI":"10.1038\/nm.4050","article-title":"Synaptic plasticity and depression: new insights from stress and rapid-acting antidepressants","volume":"22","author":"Duman","year":"2016","journal-title":"Nat. Med."},{"key":"10.1016\/j.nbd.2021.105448_bb0080","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1016\/0006-8993(96)00006-6","article-title":"A subgroup of dorsal raphe serotonergic neurons in the cat is strongly activated during oral-buccal movements","volume":"716","author":"Fornal","year":"1996","journal-title":"Brain Res."},{"key":"10.1016\/j.nbd.2021.105448_bb0085","doi-asserted-by":"crossref","first-page":"10933","DOI":"10.1038\/srep10933","article-title":"Rhes influences striatal cAMP\/PKA-dependent signaling and synaptic plasticity in a gender-sensitive fashion","volume":"5","author":"Ghiglieri","year":"2015","journal-title":"Sci. Rep."},{"key":"10.1016\/j.nbd.2021.105448_bb0090","doi-asserted-by":"crossref","first-page":"5442","DOI":"10.1523\/JNEUROSCI.22-13-05442.2002","article-title":"A third vesicular glutamate transporter expressed by cholinergic and serotoninergic neurons","volume":"22","author":"Gras","year":"2002","journal-title":"J. Neurosci."},{"key":"10.1016\/j.nbd.2021.105448_bb0095","doi-asserted-by":"crossref","first-page":"815","DOI":"10.1016\/S0306-4522(02)00026-X","article-title":"Neuromodulatory transmitter systems in the cortex and their role in cortical plasticity","volume":"111","author":"Gu","year":"2002","journal-title":"Neuroscience"},{"key":"10.1016\/j.nbd.2021.105448_bb0100","doi-asserted-by":"crossref","first-page":"26","DOI":"10.3389\/neuro.08.026.2009","article-title":"Living in a dangerous world: the shaping of behavioral profile by early environment and 5-HTT genotype","volume":"3","author":"Heiming","year":"2009","journal-title":"Front. Behav. Neurosci."},{"key":"10.1016\/j.nbd.2021.105448_bb0105","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1016\/0006-8993(90)90535-J","article-title":"Immunohistochemical demonstration of glutaminase in catecholaminergic and serotoninergic neurons of rat brain","volume":"507","author":"Kaneko","year":"1990","journal-title":"Brain Res."},{"key":"10.1016\/j.nbd.2021.105448_bb0110","doi-asserted-by":"crossref","first-page":"1223","DOI":"10.1038\/npp.2015.270","article-title":"Chronic enhancement of serotonin facilitates excitatory transcranial direct current stimulation-induced neuroplasticity","volume":"41","author":"Kuo","year":"2016","journal-title":"Neuropsychopharmacology"},{"key":"10.1016\/j.nbd.2021.105448_bb0115","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1016\/j.neuron.2012.09.013","article-title":"Serotonin in the modulation of neural plasticity and networks: implications for neurodevelopmental disorders","volume":"76","author":"Lesch","year":"2012","journal-title":"Neuron"},{"key":"10.1016\/j.nbd.2021.105448_bb0120","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1385\/ENDO:11:3:257","article-title":"Ovarian steroid action on tryptophan hydroxylase protein and serotonin compared to localization of ovarian steroid receptors in midbrain of guinea pigs","volume":"11","author":"Lu","year":"1999","journal-title":"Endocrine"},{"key":"10.1016\/j.nbd.2021.105448_bb0125","doi-asserted-by":"crossref","first-page":"110","DOI":"10.1016\/j.nbd.2004.01.007","article-title":"A model of L-DOPA-induced dyskinesia in 6-hydroxydopamine lesioned mice: relation to motor and cellular parameters of nigrostriatal function","volume":"16","author":"Lundblad","year":"2004","journal-title":"Neurobiol. Dis."},{"key":"10.1016\/j.nbd.2021.105448_bb0130","doi-asserted-by":"crossref","first-page":"202","DOI":"10.3389\/fncel.2017.00202","article-title":"Development of serotonergic fibers in the post-natal mouse brain","volume":"11","author":"Maddaloni","year":"2017","journal-title":"Front. Cell. Neurosci."},{"key":"10.1016\/j.nbd.2021.105448_bb0135","doi-asserted-by":"crossref","first-page":"11847","DOI":"10.1038\/s41598-018-30291-2","article-title":"Serotonin depletion causes valproate-responsive manic-like condition and increased hippocampal neuroplasticity that are reversed by stress","volume":"8","author":"Maddaloni","year":"2018","journal-title":"Sci. Rep."},{"key":"10.1016\/j.nbd.2021.105448_bb0140","doi-asserted-by":"crossref","first-page":"2336","DOI":"10.1093\/brain\/awp194","article-title":"Impairment of bidirectional synaptic plasticity in the striatum of a mouse model of DYT1 dystonia: role of endogenous acetylcholine","volume":"132","author":"Martella","year":"2009","journal-title":"Brain"},{"key":"10.1016\/j.nbd.2021.105448_bb0145","doi-asserted-by":"crossref","first-page":"7402","DOI":"10.1523\/JNEUROSCI.6250-10.2011","article-title":"Serotonin induces long-term depression at corticostriatal synapses","volume":"31","author":"Mathur","year":"2011","journal-title":"J. Neurosci."},{"key":"10.1016\/j.nbd.2021.105448_bb0150","doi-asserted-by":"crossref","first-page":"1106","DOI":"10.1038\/mp.2012.128","article-title":"Lack of brain serotonin affects postnatal development and serotonergic neuronal circuitry formation","volume":"18","author":"Migliarini","year":"2013","journal-title":"Mol. Psychiatry"},{"key":"10.1016\/j.nbd.2021.105448_bb0155","doi-asserted-by":"crossref","first-page":"3218","DOI":"10.1021\/acschemneuro.8b00655","article-title":"Fluoxetine induces morphological rearrangements of serotonergic fibers in the hippocampus","volume":"10","author":"Nazzi","year":"2019","journal-title":"ACS Chem. Neurosci."},{"key":"10.1016\/j.nbd.2021.105448_bb0160","doi-asserted-by":"crossref","first-page":"545","DOI":"10.1016\/0306-4522(92)90401-M","article-title":"Serotonin-, substance P- and glutamate\/aspartate-like immunoreactivities in medullo-spinal pathways of rat and primate","volume":"48","author":"Nicholas","year":"1992","journal-title":"Neuroscience"},{"key":"10.1016\/j.nbd.2021.105448_bb0165","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1016\/j.pbb.2017.05.001","article-title":"Organization of dopamine and serotonin system: anatomical and functional mapping of monosynaptic inputs using rabies virus","volume":"174","author":"Ogawa","year":"2018","journal-title":"Pharmacol. Biochem. Behav."},{"key":"10.1016\/j.nbd.2021.105448_bb0170","doi-asserted-by":"crossref","first-page":"774","DOI":"10.1016\/j.neuron.2015.10.007","article-title":"Multi-scale molecular deconstruction of the serotonin neuron system","volume":"88","author":"Okaty","year":"2015","journal-title":"Neuron"},{"key":"10.1016\/j.nbd.2021.105448_bb0175","doi-asserted-by":"crossref","first-page":"374","DOI":"10.1002\/cne.902290308","article-title":"Glutamate- and GABA-containing neurons in the mouse and rat brain, as demonstrated with a new immunocytochemical technique","volume":"229","author":"Ottersen","year":"1984","journal-title":"J. Comp. Neurol."},{"key":"10.1016\/j.nbd.2021.105448_bb0180","doi-asserted-by":"crossref","first-page":"14182","DOI":"10.1523\/JNEUROSCI.2149-10.2010","article-title":"Distinct levels of dopamine denervation differentially alter striatal synaptic plasticity and NMDA receptor subunit composition","volume":"30","author":"Paille","year":"2010","journal-title":"J. Neurosci."},{"key":"10.1016\/j.nbd.2021.105448_bb0185","doi-asserted-by":"crossref","DOI":"10.3390\/ijms20225729","article-title":"An association of serotonin with pain disorders and its modulation by estrogens","volume":"20","author":"Paredes","year":"2019","journal-title":"Int. J. Mol. Sci."},{"key":"10.1016\/j.nbd.2021.105448_bb0190","doi-asserted-by":"crossref","first-page":"501","DOI":"10.1038\/nn1040","article-title":"Loss of bidirectional striatal synaptic plasticity in L-DOPA-induced dyskinesia","volume":"6","author":"Picconi","year":"2003","journal-title":"Nat. Neurosci."},{"key":"10.1016\/j.nbd.2021.105448_bb0195","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1016\/j.biochi.2018.11.016","article-title":"Serotonergic neurotransmission manipulation for the understanding of brain development and function: learning from Tph2 genetic models","volume":"161","author":"Pratelli","year":"2019","journal-title":"Biochimie"},{"key":"10.1016\/j.nbd.2021.105448_bb0200","doi-asserted-by":"crossref","DOI":"10.1523\/ENEURO.0376-16.2017","article-title":"Perturbation of serotonin homeostasis during adulthood affects serotonergic neuronal circuitry","volume":"4","author":"Pratelli","year":"2017","journal-title":"eNeuro"},{"key":"10.1016\/j.nbd.2021.105448_bb0205","doi-asserted-by":"crossref","first-page":"676","DOI":"10.1038\/nmeth.2019","article-title":"Fiji: an open-source platform for biological-image analysis","volume":"9","author":"Schindelin","year":"2012","journal-title":"Nat. Methods"},{"key":"10.1016\/j.nbd.2021.105448_bb0210","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1515\/tnsci-2016-0007","article-title":"The serotonergic system and cognitive function","volume":"7","author":"Svob Strac","year":"2016","journal-title":"Transl. Neurosci."},{"key":"10.1016\/j.nbd.2021.105448_bb0215","doi-asserted-by":"crossref","first-page":"296","DOI":"10.1139\/jpn.0431","article-title":"Glutamate co-transmission as an emerging concept in monoamine neuron function","volume":"29","author":"Trudeau","year":"2004","journal-title":"J. Psychiatry Neurosci."},{"key":"10.1016\/j.nbd.2021.105448_bb0220","doi-asserted-by":"crossref","first-page":"1128","DOI":"10.1016\/j.celrep.2019.01.014","article-title":"Dorsal raphe dual serotonin-glutamate neurons drive reward by establishing excitatory synapses on VTA mesoaccumbens dopamine neurons","volume":"26","author":"Wang","year":"2019","journal-title":"Cell Rep."},{"key":"10.1016\/j.nbd.2021.105448_bb0225","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1126\/science.1097540","article-title":"Tryptophan hydroxylase-2 controls brain serotonin synthesis","volume":"305","author":"Zhang","year":"2004","journal-title":"Science"}],"container-title":["Neurobiology of Disease"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0969996121001972?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0969996121001972?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2025,10,19]],"date-time":"2025-10-19T05:26:54Z","timestamp":1760851614000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0969996121001972"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,10]]},"references-count":45,"alternative-id":["S0969996121001972"],"URL":"https:\/\/doi.org\/10.1016\/j.nbd.2021.105448","relation":{},"ISSN":["0969-9961"],"issn-type":[{"value":"0969-9961","type":"print"}],"subject":[],"published":{"date-parts":[[2021,10]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Serotonin drives striatal synaptic plasticity in a sex-related manner","name":"articletitle","label":"Article Title"},{"value":"Neurobiology of Disease","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.nbd.2021.105448","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2021 Published by Elsevier Inc.","name":"copyright","label":"Copyright"}],"article-number":"105448"}}