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Each year, over 50 million individuals worldwide suffer from TBI, and this leads to a number of acute and chronic health issues. These include affective and cognitive impairment, as well as an increased risk of alcohol and drug use. The dopaminergic system, a key component of reward circuitry, has been linked to alcohol and other substance use disorders, and previous research indicates that TBI can induce plasticity within this system. Understanding how TBI modifies the dopaminergic system may offer insights into the heightened substance use and reward-seeking behavior following TBI. The hippocampus, a critical component of the reward circuit, is responsible for encoding and integrating the spatial and salient aspects of rewarding stimuli. This study explored TBI-related changes in neuronal D2 receptor expression within the hippocampus, examining the hypothesis that sex differences exist in both baseline hippocampal D2 receptor expression and its response to TBI. Utilizing D2-expressing tdTomato transgenic male and female mice, we implemented either a sham injury or the lateral fluid percussion injury (FPI) model of TBI and subsequently performed a region-specific quantification of D2 expression in the hippocampus. The results show that male mice exhibit higher baseline hippocampal D2 expression compared to female mice. Additionally, there was a significant interaction effect between sex and injury on the expression of D2 in the hippocampus, particularly in regions of the dentate gyrus. Furthermore, TBI led to significant reductions in hippocampal D2 expression in male mice, while female mice remained mostly unaffected. These results suggest that hippocampal D2 expression varies between male and female mice, with the female dopaminergic system demonstrating less susceptibility to TBI-induced plasticity.<\/jats:p>","DOI":"10.3390\/ijms242216084","type":"journal-article","created":{"date-parts":[[2023,11,8]],"date-time":"2023-11-08T07:02:05Z","timestamp":1699426925000},"page":"16084","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":12,"title":["Sex-Specific and Traumatic Brain Injury Effects on Dopamine Receptor Expression in the Hippocampus"],"prefix":"10.3390","volume":"24","author":[{"given":"Jaclyn","family":"Iannucci","sequence":"first","affiliation":[{"name":"Department of Neuroscience and Experimental Therapeutics, Texas A&M University School of Medicine, Bryan, TX 77807, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0008-4839-9918","authenticated-orcid":false,"given":"Katherine","family":"O\u2019Neill","sequence":"additional","affiliation":[{"name":"Department of Biological Science, Texas A&M University, College Station, TX 77843, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xuehua","family":"Wang","sequence":"additional","affiliation":[{"name":"Department of Neuroscience and Experimental Therapeutics, Texas A&M University School of Medicine, Bryan, TX 77807, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sanjib","family":"Mukherjee","sequence":"additional","affiliation":[{"name":"Department of Neuroscience and Experimental Therapeutics, Texas A&M University School of Medicine, Bryan, TX 77807, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jun","family":"Wang","sequence":"additional","affiliation":[{"name":"Department of Neuroscience and Experimental Therapeutics, Texas A&M University School of Medicine, Bryan, TX 77807, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8368-1854","authenticated-orcid":false,"given":"Lee A.","family":"Shapiro","sequence":"additional","affiliation":[{"name":"Department of Neuroscience and Experimental Therapeutics, Texas A&M University School of Medicine, Bryan, TX 77807, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,11,8]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1080","DOI":"10.3171\/2017.10.JNS17352","article-title":"Estimating the global incidence of traumatic brain injury","volume":"130","author":"Dewan","year":"2018","journal-title":"J. Neurosurg."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1","DOI":"10.15585\/mmwr.ss6609a1","article-title":"Traumatic Brain Injury-Related Emergency Department Visits, Hospitalizations, and Deaths\u2014United States, 2007 and 2013","volume":"66","author":"Taylor","year":"2017","journal-title":"MMWR Surveill. Summ."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1016\/j.neubiorev.2017.03.015","article-title":"Factors affecting increased risk for substance use disorders following traumatic brain injury: What we can learn from animal models","volume":"77","author":"Merkel","year":"2017","journal-title":"Neurosci. Biobehav. Rev."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1016\/j.neubiorev.2016.01.005","article-title":"Alcohol abuse after traumatic brain injury: Experimental and clinical evidence","volume":"62","author":"Weil","year":"2016","journal-title":"Neurosci. Biobehav. Rev."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"324","DOI":"10.1097\/HTR.0b013e3181a712aa","article-title":"Psychiatric disorders following traumatic brain injury: Their nature and frequency","volume":"24","author":"Ponsford","year":"2009","journal-title":"J. Head Trauma Rehabil."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1186\/1755-7682-3-24","article-title":"Dopaminergic reward system: A short integrative review","volume":"3","author":"Stamelou","year":"2010","journal-title":"Int. Arch. Med."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"152","DOI":"10.3389\/fncir.2013.00152","article-title":"Dopamine signaling in reward-related behaviors","volume":"7","author":"Baik","year":"2013","journal-title":"Front. Neural Circuits"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1016\/S0165-0173(98)00019-8","article-title":"What is the role of dopamine in reward: Hedonic impact, reward learning, or incentive salience?","volume":"28","author":"Berridge","year":"1998","journal-title":"Brain Res. Rev."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"641","DOI":"10.1001\/archneur.61.5.641","article-title":"The neurobiology of dopamine signaling","volume":"61","author":"Girault","year":"2004","journal-title":"Arch. Neurol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"236","DOI":"10.1093\/cercor\/bht218","article-title":"Risk-taking behavior: Dopamine D2\/D3 receptors, feedback, and frontolimbic activity","volume":"25","author":"Kohno","year":"2015","journal-title":"Cereb. Cortex"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"12982","DOI":"10.1523\/JNEUROSCI.5587-12.2013","article-title":"Dopamine modulates risk-taking as a function of baseline sensation-seeking trait","volume":"33","author":"Norbury","year":"2013","journal-title":"J. Neurosci. Off. J. Soc. Neurosci."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1152\/jn.1998.80.1.1","article-title":"Predictive reward signal of dopamine neurons","volume":"80","author":"Schultz","year":"1998","journal-title":"J. Neurophysiol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1593","DOI":"10.1126\/science.275.5306.1593","article-title":"A neural substrate of prediction and reward","volume":"275","author":"Schultz","year":"1997","journal-title":"Science"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"918","DOI":"10.1016\/j.biopsych.2016.05.016","article-title":"Distinct Synaptic Strengthening of the Striatal Direct and Indirect Pathways Drives Alcohol Consumption","volume":"81","author":"Cheng","year":"2017","journal-title":"Biol. Psychiatry"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"715","DOI":"10.1126\/science.2903550","article-title":"Cellular and molecular mechanisms of drug dependence","volume":"242","author":"Koob","year":"1988","journal-title":"Science"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"498","DOI":"10.1016\/j.neuropharm.2013.06.031","article-title":"Imaging addiction: D2 receptors and dopamine signaling in the striatum as biomarkers for impulsivity","volume":"76 Pt B","author":"Trifilieff","year":"2014","journal-title":"Neuropharmacology"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1016\/j.neuropharm.2008.05.022","article-title":"Imaging dopamine\u2019s role in drug abuse and addiction","volume":"56","author":"Volkow","year":"2009","journal-title":"Neuropharmacology"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"569","DOI":"10.1111\/adb.12512","article-title":"Dopamine D1 or D2 receptor-expressing neurons in the central nervous system","volume":"23","author":"Wei","year":"2018","journal-title":"Addict. Biol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"797","DOI":"10.1093\/brain\/awx357","article-title":"Dopaminergic abnormalities following traumatic brain injury","volume":"141","author":"Jenkins","year":"2018","journal-title":"Brain J. Neurol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"693404","DOI":"10.3389\/fnins.2021.693404","article-title":"Role of the Dopaminergic System in the Striatum and Its Association With Functional Recovery or Rehabilitation After Brain Injury","volume":"15","year":"2021","journal-title":"Front. Neurosci."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"14835","DOI":"10.1073\/pnas.1616515114","article-title":"Dopamine release from the locus coeruleus to the dorsal hippocampus promotes spatial learning and memory","volume":"113","author":"Kempadoo","year":"2016","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1152\/jn.1992.67.1.145","article-title":"Responses of monkey dopamine neurons during learning of behavioral reactions","volume":"67","author":"Ljungberg","year":"1992","journal-title":"J. Neurophysiol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"272","DOI":"10.1093\/cercor\/10.3.272","article-title":"Reward processing in primate orbitofrontal cortex and basal ganglia","volume":"10","author":"Schultz","year":"2000","journal-title":"Cereb. Cortex"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"483","DOI":"10.1038\/nrn1406","article-title":"Dopamine, learning and motivation","volume":"5","author":"Wise","year":"2004","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"2483","DOI":"10.1007\/s00213-013-3414-0","article-title":"Opposing roles of prelimbic and infralimbic dopamine in conditioned cue and place preference","volume":"231","author":"Hayen","year":"2014","journal-title":"Psychopharmacology"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1016\/0091-3057(89)90499-1","article-title":"The effects of selective dopamine D1 or D2 receptor antagonists on the establishment of agonist-induced place conditioning in rats","volume":"33","author":"Hoffman","year":"1989","journal-title":"Pharmacol. Biochem. Behav."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1152\/physrev.1998.78.1.189","article-title":"Dopamine receptors: From structure to function","volume":"78","author":"Missale","year":"1998","journal-title":"Physiol. Rev."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1178","DOI":"10.1177\/0963689717714341","article-title":"Dexamethasone Attenuates the Enhanced Rewarding Effects of Cocaine Following Experimental Traumatic Brain Injury","volume":"26","author":"Merkel","year":"2017","journal-title":"Cell Transpl. Transplant."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1089\/neu.2015.4275","article-title":"Adolescent Traumatic Brain Injury Induces Chronic Mesolimbic Neuroinflammation with Concurrent Enhancement in the Rewarding Effects of Cocaine in Mice during Adulthood","volume":"34","author":"Merkel","year":"2017","journal-title":"J. Neurotrauma"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1016\/j.drugalcdep.2015.08.016","article-title":"Sex differences in dopamine binding and modafinil conditioned place preference in mice","volume":"155","author":"Bernardi","year":"2015","journal-title":"Drug Alcohol. Depend."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"112333","DOI":"10.1016\/j.bbr.2019.112333","article-title":"Reward and immune responses in adolescent females following experimental traumatic brain injury","volume":"379","author":"Cannella","year":"2020","journal-title":"Behav. Brain Res."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"895","DOI":"10.1089\/neu.2015.3953","article-title":"Juvenile Traumatic Brain Injury Increases Alcohol Consumption and Reward in Female Mice","volume":"33","author":"Weil","year":"2016","journal-title":"J. Neurotrauma"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"28","DOI":"10.3389\/fnsyn.2019.00028","article-title":"Gradient of Expression of Dopamine D2 Receptors Along the Dorso-Ventral Axis of the Hippocampus","volume":"11","author":"Dubovyk","year":"2019","journal-title":"Front. Synaptic Neurosci."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"2187","DOI":"10.1093\/cercor\/bhaa354","article-title":"Dopamine D2R is Required for Hippocampal-dependent Memory and Plasticity at the CA3-CA1 Synapse","volume":"31","author":"Espadas","year":"2021","journal-title":"Cereb. Cortex"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1643","DOI":"10.1016\/j.neuroimage.2006.11.008","article-title":"Memory and frontal lobe functions; possible relations with dopamine D2 receptors in the hippocampus","volume":"34","author":"Takahashi","year":"2007","journal-title":"Neuroimage"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1038\/npp.1994.27","article-title":"Dopamine receptor gene expression in the human medial temporal lobe","volume":"10","author":"Grandy","year":"1994","journal-title":"Neuropsychopharmacol. Off. Publ. Am. Coll. Neuropsychopharmacol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1016\/0006-8993(91)91456-B","article-title":"Localization of dopamine D3 receptor mRNA in the rat brain using in situ hybridization histochemistry: Comparison with dopamine D2 receptor mRNA","volume":"564","author":"Bouthenet","year":"1991","journal-title":"Brain Res."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"2199","DOI":"10.1002\/hipo.22044","article-title":"Characterization of dopamine D1 and D2 receptor-expressing neurons in the mouse hippocampus","volume":"22","author":"Gangarossa","year":"2012","journal-title":"Hippocampus"},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Williams, O.O.F., Coppolino, M., George, S.R., and Perreault, M.L. (2021). Sex Differences in Dopamine Receptors and Relevance to Neuropsychiatric Disorders. Brain Sci., 11.","DOI":"10.3390\/brainsci11091199"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1186\/s40478-014-0143-5","article-title":"Traumatic brain injury causes selective, CD74-dependent peripheral lymphocyte activation that exacerbates neurodegeneration","volume":"2","author":"Tobin","year":"2014","journal-title":"Acta Neuropathol. Commun."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"28","DOI":"10.3389\/fneur.2013.00028","article-title":"Increased seizure susceptibility in mice 30\u2009days after fluid percussion injury","volume":"4","author":"Mukherjee","year":"2013","journal-title":"Front. Neurol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"578","DOI":"10.1002\/cne.23851","article-title":"Evolution of the mammalian dentate gyrus","volume":"524","author":"Hevner","year":"2016","journal-title":"J. Comp. Neurol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/0014-4886(65)90121-4","article-title":"Time of neuron origin in the hippocampal region. An autoradiographic study in the mouse","volume":"11","author":"Angevine","year":"1965","journal-title":"Exp. Neurol. Suppl."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"541","DOI":"10.1007\/BF00236032","article-title":"Evidence that late-generated granule cells do not simply replace earlier formed neurons in the rat dentate gyrus","volume":"62","author":"Crespo","year":"1986","journal-title":"Exp. Brain Res."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"4479","DOI":"10.1002\/cne.22489","article-title":"A distinctive layering pattern of mouse dentate granule cells is generated by developmental and adult neurogenesis","volume":"518","author":"Mathews","year":"2010","journal-title":"J. Comp. Neurol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1002\/cne.901960109","article-title":"The time of origin of neurons in the hippocampal region of the rhesus monkey","volume":"196","author":"Rakic","year":"1981","journal-title":"J. Comp. Neurol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1002\/cne.901590202","article-title":"An autoradiographic study of the time of origin and the pattern of granule cell migration in the dentate gyrus of the rat","volume":"159","author":"Schlessinger","year":"1975","journal-title":"J. Comp. Neurol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"e63352","DOI":"10.7554\/eLife.63352","article-title":"Local circuit allowing hypothalamic control of hippocampal area CA2 activity and consequences for CA1","volume":"10","author":"Robert","year":"2021","journal-title":"eLife"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1038\/nn.3614","article-title":"Cell type-specific genetic and optogenetic tools reveal hippocampal CA2 circuits","volume":"17","author":"Kohara","year":"2014","journal-title":"Nat. Neurosci."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1559","DOI":"10.1016\/j.neuron.2022.01.028","article-title":"A direct lateral entorhinal cortex to hippocampal CA2 circuit conveys social information required for social memory","volume":"110","author":"Leroy","year":"2022","journal-title":"Neuron"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1016\/j.neuron.2010.08.042","article-title":"Spatial representation along the proximodistal axis of CA1","volume":"68","author":"Henriksen","year":"2010","journal-title":"Neuron"},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Stephan, H., von M\u00f6llendorff, W., and Bargmann, W. (1975). Handbuch der Mikroskopischen Anatomie des Menschen. Bd. 4, Nervensystem: Teil 9. Allocortex, Springer.","DOI":"10.1007\/978-3-642-80890-6"},{"key":"ref_53","doi-asserted-by":"crossref","unstructured":"Park, S.B., Lim, H.Y., Lee, E.Y., Yoo, S.W., Jung, H.S., Lee, E., Sun, W., and Lee, I. (2022). The fasciola cinereum subregion of the hippocampus is important for the acquisition of visual contextual memory. Prog. Neurobiol., 210.","DOI":"10.1016\/j.pneurobio.2022.102217"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"591","DOI":"10.1002\/cne.901740404","article-title":"Commissural connections of the dentate area in the rat","volume":"174","author":"Laurberg","year":"1977","journal-title":"J. Comp. Neurol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1002\/cne.901610107","article-title":"Crossed pathways from the entorhinal area to the fascia dentata. I. Normal in rabbits","volume":"161","author":"Zimmer","year":"1975","journal-title":"J. Comp. Neurol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"2129","DOI":"10.1523\/JNEUROSCI.3812-11.2012","article-title":"Weak and Nondiscriminative Responses to Conspecifics in the Rat Hippocampus","volume":"32","author":"Rao","year":"2012","journal-title":"J. Neurosci."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1002\/cne.901460206","article-title":"Projection of the lateral part of the entorhinal area to the hippocampus and fascia dentata","volume":"146","year":"1972","journal-title":"J. Comp. Neurol."},{"key":"ref_58","doi-asserted-by":"crossref","unstructured":"Geddes, R.I., Peterson, B.L., Stein, D.G., and Sayeed, I. (2016). Progesterone Treatment Shows Benefit in Female Rats in a Pediatric Model of Controlled Cortical Impact Injury. PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0146419"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"332","DOI":"10.1006\/exnr.2001.7820","article-title":"Regional vulnerability after traumatic brain injury: Gender differences in mice that overexpress human copper, zinc superoxide dismutase","volume":"172","author":"Igarashi","year":"2001","journal-title":"Exp. Neurol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"1423","DOI":"10.1002\/glia.23171","article-title":"Sexual dimorphism in the inflammatory response to traumatic brain injury","volume":"65","author":"Villapol","year":"2017","journal-title":"Glia"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1016\/j.expneurol.2017.07.004","article-title":"Comparable impediment of cognitive function in female and male rats subsequent to daily administration of haloperidol after traumatic brain injury","volume":"296","author":"Free","year":"2017","journal-title":"Exp. Neurol."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"1547","DOI":"10.1111\/j.1460-9568.2005.03995.x","article-title":"The neuroprotective effect of progesterone after traumatic brain injury in male mice is independent of both the inflammatory response and growth factor expression","volume":"21","author":"Jones","year":"2005","journal-title":"Eur. J. Neurosci."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"695","DOI":"10.3171\/jns.2005.103.4.0695","article-title":"Effect of atorvastatin on spatial memory, neuronal survival, and vascular density in female rats after traumatic brain injury","volume":"103","author":"Qu","year":"2005","journal-title":"J. Neurosurg."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1007\/s10863-014-9585-5","article-title":"Progesterone protects mitochondrial function in a rat model of pediatric traumatic brain injury","volume":"47","author":"Robertson","year":"2015","journal-title":"J. Bioenerg. Biomembr."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"1179069519844020","DOI":"10.1177\/1179069519844020","article-title":"Sex Differences in Animal Models of Traumatic Brain Injury","volume":"13","author":"Rubin","year":"2019","journal-title":"J. Exp. Neurosci."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"1017","DOI":"10.1016\/S0014-4886(03)00389-3","article-title":"The importance of gender on the beneficial effects of posttraumatic hypothermia","volume":"184","author":"Suzuki","year":"2003","journal-title":"Exp. Neurol."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1016\/j.bbr.2016.10.045","article-title":"Sex-dependent changes in neuronal morphology and psychosocial behaviors after pediatric brain injury","volume":"319","author":"Semple","year":"2017","journal-title":"Behav. Brain Res."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1016\/j.conb.2018.08.009","article-title":"Neuromodulation of hippocampal long-term synaptic plasticity","volume":"54","author":"Mellor","year":"2019","journal-title":"Curr. Opin. Neurobiol."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1002\/brb3.35","article-title":"Brain Circuits of Methamphetamine Place Reinforcement Learning: The Role of the Hippocampus-VTA Loop","volume":"2","author":"Keleta","year":"2012","journal-title":"Brain Behav."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"703","DOI":"10.1016\/j.neuron.2005.05.002","article-title":"The hippocampal-VTA loop: Controlling the entry of information into long-term memory","volume":"46","author":"Lisman","year":"2005","journal-title":"Neuron"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"803574","DOI":"10.3389\/fnbeh.2021.803574","article-title":"Bidirectional Regulation of Hippocampal Synaptic Plasticity and Modulation of Cumulative Spatial Memory by Dopamine D2-Like Receptors","volume":"15","author":"Caragea","year":"2021","journal-title":"Front. Behav. Neurosci."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"16366","DOI":"10.1073\/pnas.1004108107","article-title":"D1 and D2 dopamine receptors in separate circuits cooperate to drive associative long-term potentiation in the prefrontal cortex","volume":"107","author":"Xu","year":"2010","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1016\/j.bbr.2012.02.050","article-title":"Role of D1\/D2 dopamine receptors in the CA1 region of the rat hippocampus in the rewarding effects of morphine administered into the ventral tegmental area","volume":"231","author":"Esmaeili","year":"2012","journal-title":"Behav. Brain Res."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1007\/s002130000569","article-title":"Conditioned place preference: What does it add to our preclinical understanding of drug reward?","volume":"153","author":"Bardo","year":"2000","journal-title":"Psychopharmacology"},{"key":"ref_75","unstructured":"Carr, G.D., Fibiger, H.C., and Phillips, A.G. (1989). Conditioned Place Preference as a Measure of Drug Reward, Oxford University Press."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"138","DOI":"10.1016\/j.neulet.2013.03.001","article-title":"Intrahippocampal administration of D2 but not D1 dopamine receptor antagonist suppresses the expression of conditioned place preference induced by morphine in the ventral tegmental area","volume":"541","author":"Haghparast","year":"2013","journal-title":"Neurosci. Lett."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1016\/j.lfs.2006.09.013","article-title":"Dorsal hippocampal dopamine receptors are involved in mediating ethanol state-dependent memory","volume":"80","author":"Rezayof","year":"2007","journal-title":"Life Sci."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"1986","DOI":"10.1038\/s41593-019-0524-y","article-title":"A ventral CA1 to nucleus accumbens core engram circuit mediates conditioned place preference for cocaine","volume":"22","author":"Zhou","year":"2019","journal-title":"Nat. Neurosci."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"394","DOI":"10.1016\/j.bbr.2016.06.061","article-title":"D1- and D2-like dopamine receptors in the CA1 region of the hippocampus are involved in the acquisition and reinstatement of morphine-induced conditioned place preference","volume":"312","author":"Assar","year":"2016","journal-title":"Behav. Brain Res."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1016\/j.neures.2010.02.001","article-title":"Blockade of dorsal hippocampal dopamine receptors inhibits state-dependent learning induced by cannabinoid receptor agonist in mice","volume":"67","author":"Zarrindast","year":"2010","journal-title":"Neurosci. Res."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"981","DOI":"10.1016\/j.neubiorev.2009.03.011","article-title":"Persistent cognitive dysfunction after traumatic brain injury: A dopamine hypothesis","volume":"33","author":"Bales","year":"2009","journal-title":"Neurosci. Biobehav. Rev."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"2547","DOI":"10.1182\/blood-2016-11-753202","article-title":"Depletion of coagulation factor XII ameliorates brain pathology and cognitive impairment in Alzheimer disease mice","volume":"129","author":"Chen","year":"2017","journal-title":"Blood"},{"key":"ref_83","first-page":"2616","article-title":"The potential roles of dopamine in traumatic brain injury: A preclinical and clinical update","volume":"11","author":"Lan","year":"2019","journal-title":"Am. J. Transl. Res."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"546775","DOI":"10.3389\/fneur.2020.546775","article-title":"Sex, Drugs, and TBI: The Role of Sex in Substance Abuse Related to Traumatic Brain Injuries","volume":"11","author":"Oliverio","year":"2020","journal-title":"Front. Neurol."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"501","DOI":"10.1037\/neu0000074","article-title":"A comparison of adult outcomes for males compared to females following pediatric traumatic brain injury","volume":"29","author":"Scott","year":"2015","journal-title":"Neuropsychology"},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"907552","DOI":"10.3389\/fnbeh.2022.907552","article-title":"Ovarian Steroids Mediate Sex Differences in Alcohol Reward After Brain Injury in Mice","volume":"16","author":"Oliverio","year":"2022","journal-title":"Front. Behav. Neurosci."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1007\/7854_2010_93","article-title":"Females are more vulnerable to drug abuse than males: Evidence from preclinical studies and the role of ovarian hormones","volume":"8","author":"Anker","year":"2011","journal-title":"Curr. Top. Behav. Neurosci."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"829","DOI":"10.1016\/j.addbeh.2011.03.013","article-title":"Characteristics and correlates of men and women with prescription opioid dependence","volume":"36","author":"Back","year":"2011","journal-title":"Addict. Behav."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1016\/S0193-953X(05)70074-5","article-title":"Gender differences in substance use disorders","volume":"22","author":"Brady","year":"1999","journal-title":"Psychiatr. Clin. N. Am."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"672","DOI":"10.1016\/j.neuropharm.2003.11.017","article-title":"Sex differences in cocaine-induced behavioral responses, pharmacokinetics, and monoamine levels","volume":"46","author":"Festa","year":"2004","journal-title":"Neuropharmacology"},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"140","DOI":"10.1016\/j.pbb.2006.12.018","article-title":"Sex differences in (+)-amphetamine- and (+)-methamphetamine-induced behavioral response in male and female Sprague-Dawley rats","volume":"86","author":"McMillan","year":"2007","journal-title":"Pharmacol. Biochem. Behav."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"2947","DOI":"10.1007\/s00213-021-05910-y","article-title":"Vulnerability factors for mephedrone-induced conditioned place preference in rats-the impact of sex differences, social-conditioning and stress","volume":"238","author":"Wronikowska","year":"2021","journal-title":"Psychopharmacology"},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"108785","DOI":"10.1016\/j.drugalcdep.2021.108785","article-title":"Effects of the GluN2B-selective antagonist Ro 63-1908 on acquisition and expression of methamphetamine conditioned place preference in male and female rats","volume":"225","author":"Yates","year":"2021","journal-title":"Drug Alcohol. Depend."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"214","DOI":"10.1016\/S0006-8993(03)02346-1","article-title":"Sex differences in the conditioned rewarding effects of cocaine","volume":"970","author":"Russo","year":"2003","journal-title":"Brain Res."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.pbb.2014.07.016","article-title":"Single trial nicotine conditioned place preference in pre-adolescent male and female rats","volume":"125","author":"Edwards","year":"2014","journal-title":"Pharmacol. Biochem. Behav."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"258","DOI":"10.1038\/s41586-018-0740-8","article-title":"Reward behaviour is regulated by the strength of hippocampus-nucleus accumbens synapses","volume":"564","author":"LeGates","year":"2018","journal-title":"Nature"},{"key":"ref_97","doi-asserted-by":"crossref","unstructured":"Newell-Rogers, M.K., Rogers, S.K., Tobin, R.P., Mukherjee, S., and Shapiro, L.A. (2020). Antagonism of Macrophage Migration Inhibitory Factory (MIF) after Traumatic Brain Injury Ameliorates Astrocytosis and Peripheral Lymphocyte Activation and Expansion. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21207448"},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1016\/j.neuro.2022.04.001","article-title":"Neurogenesis and chronic neurobehavioral outcomes are partially improved by vagus nerve stimulation in a mouse model of Gulf War illness","volume":"90","author":"Iannucci","year":"2022","journal-title":"Neurotoxicology"},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1016\/S0079-6123(07)63001-5","article-title":"The dentate gyrus: Fundamental neuroanatomical organization (dentate gyrus for dummies)","volume":"163","author":"Amaral","year":"2007","journal-title":"Prog. Brain Res."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.brainresrev.2007.05.002","article-title":"Spatial organization of direct hippocampal field CA1 axonal projections to the rest of the cerebral cortex","volume":"56","author":"Cenquizca","year":"2007","journal-title":"Brain Res. Rev."},{"key":"ref_101","doi-asserted-by":"crossref","unstructured":"Ramon y Cajal, S. (1995). Histology of the Nervous System of Man and Vertebrates [English Translation], Oxford University Press.","DOI":"10.1093\/oso\/9780195074017.001.0001"},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"101950","DOI":"10.1016\/j.nicl.2019.101950","article-title":"Dopamine D2\/D3 receptor abnormalities after traumatic brain injury and their relationship to post-traumatic depression","volume":"24","author":"Jolly","year":"2019","journal-title":"Neuroimage Clin."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/22\/16084\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T21:19:24Z","timestamp":1760131164000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/22\/16084"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,11,8]]},"references-count":102,"journal-issue":{"issue":"22","published-online":{"date-parts":[[2023,11]]}},"alternative-id":["ijms242216084"],"URL":"https:\/\/doi.org\/10.3390\/ijms242216084","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,11,8]]}}}