Adaptor protein complex 2 in the orbitofrontal cortex predicts alcohol use disorder.
Journal
Molecular psychiatry
ISSN: 1476-5578
Titre abrégé: Mol Psychiatry
Pays: England
ID NLM: 9607835
Informations de publication
Date de publication:
07 Sep 2023
07 Sep 2023
Historique:
received:
25
05
2023
accepted:
23
08
2023
revised:
17
08
2023
medline:
8
9
2023
pubmed:
8
9
2023
entrez:
7
9
2023
Statut:
aheadofprint
Résumé
Alcohol use disorder (AUD) is a life-threatening disease characterized by compulsive drinking, cognitive deficits, and social impairment that continue despite negative consequences. The inability of individuals with AUD to regulate drinking may involve functional deficits in cortical areas that normally balance actions that have aspects of both reward and risk. Among these, the orbitofrontal cortex (OFC) is critically involved in goal-directed behavior and is thought to maintain a representation of reward value that guides decision making. In the present study, we analyzed post-mortem OFC brain samples collected from age- and sex-matched control subjects and those with AUD using proteomics, bioinformatics, machine learning, and reverse genetics approaches. Of the 4,500+ total unique proteins identified in the proteomics screen, there were 47 proteins that differed significantly by sex that were enriched in processes regulating extracellular matrix and axonal structure. Gene ontology enrichment analysis revealed that proteins differentially expressed in AUD cases were involved in synaptic and mitochondrial function, as well as transmembrane transporter activity. Alcohol-sensitive OFC proteins also mapped to abnormal social behaviors and social interactions. Machine learning analysis of the post-mortem OFC proteome revealed dysregulation of presynaptic (e.g., AP2A1) and mitochondrial proteins that predicted the occurrence and severity of AUD. Using a reverse genetics approach to validate a target protein, we found that prefrontal Ap2a1 expression significantly correlated with voluntary alcohol drinking in male and female genetically diverse mouse strains. Moreover, recombinant inbred strains that inherited the C57BL/6J allele at the Ap2a1 interval consumed higher amounts of alcohol than those that inherited the DBA/2J allele. Together, these findings highlight the impact of excessive alcohol consumption on the human OFC proteome and identify important cross-species cortical mechanisms and proteins that control drinking in individuals with AUD.
Identifiants
pubmed: 37679472
doi: 10.1038/s41380-023-02236-3
pii: 10.1038/s41380-023-02236-3
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : NIH HHS
ID : S10 OD025126
Pays : United States
Organisme : NEI NIH HHS
ID : P30 EY010572
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA069533
Pays : United States
Organisme : NIAAA NIH HHS
ID : R01 AA023288
Pays : United States
Organisme : NIAAA NIH HHS
ID : P50 AA010761
Pays : United States
Commentaires et corrections
Type : UpdateOf
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Collaborators GBDRF. Global burden of 87 risk factors in 204 countries and territories, 1990-2019: a systematic analysis for the Global Burden of Disease Study 2019. Lancet. 2020;396:1223–49.
doi: 10.1016/S0140-6736(20)30752-2
Spectrum N. Alcohol-related deaths continued to increase in 2021. vol. 15. National Institute of Alcohol Abuse and Alcoholism 2023.
Glantz MD, Bharat C, Degenhardt L, Sampson NA, Scott KM, Lim CCW, et al. The epidemiology of alcohol use disorders cross-nationally: Findings from the World Mental Health Surveys. Addict Behav. 2020;102:106128.
pubmed: 31865172
doi: 10.1016/j.addbeh.2019.106128
DSM-5. Diagnostic and statistical manual of mental disorders: DSM-5-TR. 5th ed. Text Revision DSM-5-TR edn. American Psychiatric Association: Arlington, VA, 2022.
Koob GF Anhedonia, Hyperkatifeia, and Negative Reinforcement in Substance Use Disorders. Curr Top Behav Neurosci 2022;58:147–65.
Badanich K, Mulholland P, Beckley J, Trantham-Davidson H, Woodward J. Ethanol reduces neuronal excitability of lateral orbitofrontal cortex neurons via a glycine receptor dependent mechanism. Neuropsycopharmacology. 2013;38:1176–88.
doi: 10.1038/npp.2013.12
Nimitvilai S, Lopez MF, Mulholland PJ, Woodward JJ. Chronic intermittent ethanol exposure enhances the excitability and synaptic plasticity of lateral orbitofrontal cortex neurons and induces a tolerance to the acute inhibitory actions of ethanol. Neuropsychopharmacology. 2016;41:1112–27.
pubmed: 26286839
doi: 10.1038/npp.2015.250
Cannady R, Nimitvilai-Roberts S, Jennings SD, Woodward JJ, Mulholland PJ Distinct Region- and Time-Dependent Functional Cortical Adaptations in C57BL/6J Mice after Short and Prolonged Alcohol Drinking. eNeuro 2020;7.
Moorman DE. The role of the orbitofrontal cortex in alcohol use, abuse, and dependence. Prog Neuropsychopharmacol Biol Psychiatry. 2018;87:85–107.
pubmed: 29355587
pmcid: 6072631
doi: 10.1016/j.pnpbp.2018.01.010
Shields CN, Gremel CM. Review of orbitofrontal cortex in alcohol dependence: a disrupted cognitive map? Alcohol, Clin Exp Res. 2020;44:1952–64.
pubmed: 32852095
doi: 10.1111/acer.14441
Hernandez JS, Moorman DE Orbitofrontal Cortex Encodes Preference for Alcohol. eNeuro 2020;7.
Jokisch D, Roser P, Juckel G, Daum I, Bellebaum C. Impairments in learning by monetary rewards and alcohol-associated rewards in detoxified alcoholic patients. Alcohol, Clin Exp Res. 2014;38:1947–54.
pubmed: 24930543
doi: 10.1111/acer.12460
Badanich KA, Fakih ME, Gurina TS, Roy EK, Hoffman JL, Uruena-Agnes AR et al. Reversal learning and experimenter-administered chronic intermittent ethanol exposure in male rats. Psychopharmacology 2016;233:3615–26.
Badanich K, Becker H, Woodward J. Effects of chronic intermittent ethanol exposure on orbitofrontal and medial prefrontal cortex-dependent behaviors in mice. Behav Neurosci. 2011;125:879–91.
pubmed: 22122149
pmcid: 3229192
doi: 10.1037/a0025922
McMurray MS, Amodeo LR, Roitman JD. Effects of voluntary alcohol intake on risk preference and behavioral flexibility during rat adolescence. PLoS One. 2014;9:e100697.
pubmed: 25007338
pmcid: 4090063
doi: 10.1371/journal.pone.0100697
Jedema HP, Carter MD, Dugan BP, Gurnsey K, Olsen AS, Bradberry CW. The acute impact of ethanol on cognitive performance in rhesus macaques. Cereb cortex. 2011;21:1783–91.
pubmed: 21148279
doi: 10.1093/cercor/bhq244
Renteria R, Baltz ET, Gremel CM. Chronic alcohol exposure disrupts top-down control over basal ganglia action selection to produce habits. Nat Commun. 2018;9:211.
pubmed: 29335427
pmcid: 5768774
doi: 10.1038/s41467-017-02615-9
Volkow ND, Wang GJ, Overall JE, Hitzemann R, Fowler JS, Pappas N, et al. Regional brain metabolic response to lorazepam in alcoholics during early and late alcohol detoxification. Alcohol, Clin Exp Res. 1997;21:1278–84.
pubmed: 9347090
doi: 10.1111/j.1530-0277.1997.tb04449.x
Myrick H, Anton RF, Li X, Henderson S, Drobes D, Voronin K, et al. Differential brain activity in alcoholics and social drinkers to alcohol cues: relationship to craving. Neuropsychopharmacol: Off Publ Am Coll Neuropsychopharmacol. 2004;29:393–402.
doi: 10.1038/sj.npp.1300295
Schacht JP, Yeongbin I, Hoffman M, Voronin KE, Book SW, Anton RF Effects of pharmacological and genetic regulation of COMT activity in alcohol use disorder: a randomized, placebo-controlled trial of tolcapone. Neuropsychopharmacol Offic Publ Am College Neuropsychopharmacol. 2022;47:1953–60.
Gioia DA, Woodward JJ. Altered activity of lateral orbitofrontal cortex neurons in mice following chronic intermittent ethanol exposure. eNeuro 2021;8.
Nimitvilai S, Uys JD, Woodward JJ, Randall PK, Ball LE, Williams RW, et al. Orbitofrontal neuroadaptations and cross-species synaptic biomarkers in heavy-drinking macaques. J Neurosci. 2017;37:3646–60.
pubmed: 28270566
pmcid: 5373140
doi: 10.1523/JNEUROSCI.0133-17.2017
Ongur D, Ferry AT, Price JL. Architectonic subdivision of the human orbital and medial prefrontal cortex. J Comp Neurol. 2003;460:425–49.
pubmed: 12692859
doi: 10.1002/cne.10609
Li J, Van Vranken JG, Pontano Vaites L, Schweppe DK, Huttlin EL, Etienne C, et al. TMTpro reagents: a set of isobaric labeling mass tags enables simultaneous proteome-wide measurements across 16 samples. Nat methods. 2020;17:399–404.
pubmed: 32203386
pmcid: 7302421
doi: 10.1038/s41592-020-0781-4
McAlister GC, Nusinow DP, Jedrychowski MP, Wuhr M, Huttlin EL, Erickson BK, et al. MultiNotch MS3 enables accurate, sensitive, and multiplexed detection of differential expression across cancer cell line proteomes. Anal Chem. 2014;86:7150–8.
pubmed: 24927332
pmcid: 4215866
doi: 10.1021/ac502040v
Eng JK, Jahan TA, Hoopmann MR. Comet: an open-source MS/MS sequence database search tool. Proteomics. 2013;13:22–24.
pubmed: 23148064
doi: 10.1002/pmic.201200439
Wilmarth PA, Riviere MA, David LL. Techniques for accurate protein identification in shotgun proteomic studies of human, mouse, bovine, and chicken lenses. J Ocul Biol Dis Info. 2009;2:223–34.
doi: 10.1007/s12177-009-9042-6
Chambers MC, Maclean B, Burke R, Amodei D, Ruderman DL, Neumann S, et al. A cross-platform toolkit for mass spectrometry and proteomics. Nat Biotechnol. 2012;30:918–20.
pubmed: 23051804
pmcid: 3471674
doi: 10.1038/nbt.2377
McDonald WH, Tabb DL, Sadygov RG, MacCoss MJ, Venable J, Graumann J, et al. MS1, MS2, and SQT-three unified, compact, and easily parsed file formats for the storage of shotgun proteomic spectra and identifications. Rapid Commun Mass Spectrom. 2004;18:2162–8.
pubmed: 15317041
doi: 10.1002/rcm.1603
Keller A, Nesvizhskii AI, Kolker E, Aebersold R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem. 2002;74:5383–92.
pubmed: 12403597
doi: 10.1021/ac025747h
Elias JE, Gygi SP. Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat methods. 2007;4:207–14.
pubmed: 17327847
doi: 10.1038/nmeth1019
Plubell DL, Wilmarth PA, Zhao Y, Fenton AM, Minnier J, Reddy AP, et al. Extended Multiplexing of Tandem Mass Tags (TMT) labeling reveals age and high fat diet specific proteome changes in mouse epididymal adipose tissue. Mol Cell Proteom: MCP. 2017;16:873–90.
pubmed: 28325852
doi: 10.1074/mcp.M116.065524
Perez-Riverol Y, Bai J, Bandla C, Garcia-Seisdedos D, Hewapathirana S, Kamatchinathan S, et al. The PRIDE database resources in 2022: a hub for mass spectrometry-based proteomics evidences. Nucleic Acids Res. 2022;50:D543–52.
pubmed: 34723319
doi: 10.1093/nar/gkab1038
Le Cao KA, Boitard S, Besse P. Sparse PLS discriminant analysis: biologically relevant feature selection and graphical displays for multiclass problems. BMC Bioinforma. 2011;12:253.
doi: 10.1186/1471-2105-12-253
McGuier NS, Rinker JA, Cannady R, Fulmer DB, Jones SR, Hoffman M, et al. Identification and validation of midbrain Kcnq4 regulation of heavy alcohol consumption in rodents. Neuropharmacology. 2018;138:10–19.
pubmed: 29775679
pmcid: 6054890
doi: 10.1016/j.neuropharm.2018.05.020
Padula AE, Griffin WC 3rd, Lopez MF, Nimitvilai S, Cannady R, McGuier NS, et al. KCNN genes that encode small-conductance Ca2+-Activated K+ channels influence alcohol and drug addiction. Neuropsychopharmacology. 2015;40:1928–39.
pubmed: 25662840
pmcid: 4839516
doi: 10.1038/npp.2015.42
Padula AE, Rinker JA, Lopez MF, Mulligan MK, Williams RW, Becker HC, et al. Bioinformatics identification and pharmacological validation of Kcnn3/K(Ca)2 channels as a mediator of negative affective behaviors and excessive alcohol drinking in mice. Transl psychiatry. 2020;10:414.
pubmed: 33247097
pmcid: 7699620
doi: 10.1038/s41398-020-01099-4
Rinker JA, Fulmer DB, Trantham-Davidson H, Smith ML, Williams RW, Lopez MF, et al. Differential potassium channel gene regulation in BXD mice reveals novel targets for pharmacogenetic therapies to reduce heavy alcohol drinking. Alcohol. 2017;58:33–45.
pubmed: 27432260
doi: 10.1016/j.alcohol.2016.05.007
McGuier NS, Griffin WC, 3rd, Gass JT, Padula AE, Chesler EJ, Mulholland PJ Kv7 channels in the nucleus accumbens are altered by chronic drinking and are targets for reducing alcohol consumption. Add Biol. 2015;21:1097–112.
Baker EJ, Jay JJ, Bubier JA, Langston MA, Chesler EJ. GeneWeaver: a web-based system for integrative functional genomics. Nucleic acids Res. 2012;40:D1067–76.
pubmed: 22080549
doi: 10.1093/nar/gkr968
Philip VM, Duvvuru S, Gomero B, Ansah TA, Blaha CD, Cook MN, et al. High-throughput behavioral phenotyping in the expanded panel of BXD recombinant inbred strains. Genes Brain Behav. 2010;9:129–59.
pubmed: 19958391
doi: 10.1111/j.1601-183X.2009.00540.x
Dickson PE, Miller MM, Calton MA, Bubier JA, Cook MN, Goldowitz D, et al. Systems genetics of intravenous cocaine self-administration in the BXD recombinant inbred mouse panel. Psychopharmacology. 2016;233:701–14.
pubmed: 26581503
doi: 10.1007/s00213-015-4147-z
Lopez MF, Miles MF, Williams RW, Becker HC. Variable effects of chronic intermittent ethanol exposure on ethanol drinking in a genetically diverse mouse cohort. Alcohol. 2017;58:73–82.
pubmed: 27793543
doi: 10.1016/j.alcohol.2016.09.003
Faul F, Erdfelder E, Lang AG, Buchner A. G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods. 2007;39:175–91.
pubmed: 17695343
doi: 10.3758/BF03193146
Leek JT, Johnson WE, Parker HS, Jaffe AE, Storey JD. The sva package for removing batch effects and other unwanted variation in high-throughput experiments. Bioinformatics. 2012;28:882–3.
pubmed: 22257669
pmcid: 3307112
doi: 10.1093/bioinformatics/bts034
Chen J, Bardes EE, Aronow BJ, Jegga AG. ToppGene Suite for gene list enrichment analysis and candidate gene prioritization. Nucleic Acids Res. 2009;37:W305–11.
pubmed: 19465376
pmcid: 2703978
doi: 10.1093/nar/gkp427
Cahill KM, Huo Z, Tseng GC, Logan RW, Seney ML. Improved identification of concordant and discordant gene expression signatures using an updated rank-rank hypergeometric overlap approach. Sci Rep. 2018;8:9588.
pubmed: 29942049
pmcid: 6018631
doi: 10.1038/s41598-018-27903-2
Uys JD, McGuier NS, Gass JT, Griffin WC 3rd, Ball LE, Mulholland PJ. Chronic intermittent ethanol exposure and withdrawal leads to adaptations in nucleus accumbens core postsynaptic density proteome and dendritic spines. Addict Biol. 2016;21:560–74.
pubmed: 25787124
doi: 10.1111/adb.12238
Kapoor M, Wang JC, Wetherill L, Le N, Bertelsen S, Hinrichs AL, et al. A meta-analysis of two genome-wide association studies to identify novel loci for maximum number of alcoholic drinks. Hum Genet. 2013;132:1141–51.
pubmed: 23743675
pmcid: 3776011
doi: 10.1007/s00439-013-1318-z
Grant JD, Agrawal A, Bucholz KK, Madden PA, Pergadia ML, Nelson EC, et al. Alcohol consumption indices of genetic risk for alcohol dependence. Biol psychiatry. 2009;66:795–800.
pubmed: 19576574
pmcid: 3077105
doi: 10.1016/j.biopsych.2009.05.018
Saccone NL, Kwon JM, Corbett J, Goate A, Rochberg N, Edenberg HJ, et al. A genome screen of maximum number of drinks as an alcoholism phenotype. Am J Med Genet. 2000;96:632–7.
pubmed: 11054770
doi: 10.1002/1096-8628(20001009)96:5<632::AID-AJMG8>3.0.CO;2-#
Schuckit MA, Smith TL, Danko GP, Bucholz KK, Agrawal A, Dick DM, et al. Predictors of subgroups based on maximum drinks per occasion over six years for 833 adolescents and young adults in COGA. J Stud Alcohol Drugs. 2014;75:24–34.
pubmed: 24411794
pmcid: 3893632
doi: 10.15288/jsad.2014.75.24
Wang X, Pandey AK, Mulligan MK, Williams EG, Mozhui K, Li Z, et al. Joint mouse-human phenome-wide association to test gene function and disease risk. Nat Commun. 2016;7:10464.
pubmed: 26833085
pmcid: 4740880
doi: 10.1038/ncomms10464
Caruana NJ, Stroud DA. The road to the structure of the mitochondrial respiratory chain supercomplex. Biochem Soc Trans. 2020;48:621–9.
pubmed: 32311046
pmcid: 7200630
doi: 10.1042/BST20190930
Qin L, Vetreno RP, Crews FT. NADPH oxidase and endoplasmic reticulum stress is associated with neuronal degeneration in orbitofrontal cortex of individuals with alcohol use disorder. Addiction Biol. 2023;28:e13262.
doi: 10.1111/adb.13262
Flatscher-Bader T, van der Brug M, Hwang JW, Gochee PA, Matsumoto I, Niwa S, et al. Alcohol-responsive genes in the frontal cortex and nucleus accumbens of human alcoholics. J Neurochem. 2005;93:359–70.
pubmed: 15816859
doi: 10.1111/j.1471-4159.2004.03021.x
Sokolov BP, Jiang L, Trivedi NS, Aston C. Transcription profiling reveals mitochondrial, ubiquitin and signaling systems abnormalities in postmortem brains from subjects with a history of alcohol abuse or dependence. J Neurosci Res. 2003;72:756–67.
pubmed: 12774316
doi: 10.1002/jnr.10631
Liu J, Lewohl JM, Dodd PR, Randall PK, Harris RA, Mayfield RD. Gene expression profiling of individual cases reveals consistent transcriptional changes in alcoholic human brain. J Neurochem. 2004;90:1050–8.
pubmed: 15312160
doi: 10.1111/j.1471-4159.2004.02570.x
Shang P, Lindberg D, Starski P, Peyton L, Hong SI, Choi S, et al. Chronic alcohol exposure induces aberrant mitochondrial morphology and inhibits respiratory capacity in the medial prefrontal cortex of mice. Front Neurosci. 2020;14:561173.
pubmed: 33192248
pmcid: 7646256
doi: 10.3389/fnins.2020.561173
Jung ME, Metzger DB. Aberrant histone acetylation promotes mitochondrial respiratory suppression in the brain of alcoholic rats. J Pharm Exp Ther. 2015;352:258–66.
doi: 10.1124/jpet.114.219311
Reddy VD, Padmavathi P, Kavitha G, Saradamma B, Varadacharyulu N. Alcohol-induced oxidative/nitrosative stress alters brain mitochondrial membrane properties. Mol Cell Biochem. 2013;375:39–47.
pubmed: 23212448
Vetreno RP, Qin L, Coleman LG Jr., Crews FT. Increased Toll-like Receptor-MyD88-NFkappaB-Proinflammatory neuroimmune signaling in the orbitofrontal cortex of humans with alcohol use disorder. Alcohol, Clin Exp Res. 2021;45:1747–61.
pubmed: 34415075
doi: 10.1111/acer.14669
Miguel-Hidalgo JJ, Overholser JC, Meltzer HY, Stockmeier CA, Rajkowska G. Reduced glial and neuronal packing density in the orbitofrontal cortex in alcohol dependence and its relationship with suicide and duration of alcohol dependence. Alcohol, Clin Exp Res. 2006;30:1845–55.
pubmed: 17067348
doi: 10.1111/j.1530-0277.2006.00221.x
Ruggiero A, Katsenelson M, Slutsky I. Mitochondria: new players in homeostatic regulation of firing rate set points. Trends Neurosci. 2021;44:605–18.
pubmed: 33865626
doi: 10.1016/j.tins.2021.03.002
Styr B, Gonen N, Zarhin D, Ruggiero A, Atsmon R, Gazit N, et al. Mitochondrial regulation of the hippocampal firing rate set point and seizure susceptibility. Neuron. 2019;102:1009–24.e1008.
pubmed: 31047779
pmcid: 6559804
doi: 10.1016/j.neuron.2019.03.045
Ponomarev I, Wang S, Zhang L, Harris RA, Mayfield RD. Gene coexpression networks in human brain identify epigenetic modifications in alcohol dependence. J Neurosci. 2012;32:1884–97.
pubmed: 22302827
pmcid: 3564514
doi: 10.1523/JNEUROSCI.3136-11.2012
Wolen AR, Phillips CA, Langston MA, Putman AH, Vorster PJ, Bruce NA, et al. Genetic dissection of acute ethanol responsive gene networks in prefrontal cortex: functional and mechanistic implications. PloS one. 2012;7:e33575.
pubmed: 22511924
pmcid: 3325236
doi: 10.1371/journal.pone.0033575
Lovinger DM. Presynaptic ethanol actions: potential roles in ethanol seeking. Handb Exp Pharm. 2018;248:29–54.
doi: 10.1007/164_2017_76
Le Berre AP. Emotional processing and social cognition in alcohol use disorder. Neuropsychology. 2019;33:808–21.
pubmed: 31448948
pmcid: 6711390
doi: 10.1037/neu0000572
Willis ML, Palermo R, Burke D, McGrillen K, Miller L. Orbitofrontal cortex lesions result in abnormal social judgements to emotional faces. Neuropsychologia. 2010;48:2182–7.
pubmed: 20399220
doi: 10.1016/j.neuropsychologia.2010.04.010
Watson KK, Platt ML. Social signals in primate orbitofrontal cortex. Curr Biol. 2012;22:2268–73.
pubmed: 23122847
pmcid: 3518589
doi: 10.1016/j.cub.2012.10.016
Azzi JC, Sirigu A, Duhamel JR. Modulation of value representation by social context in the primate orbitofrontal cortex. Proc Natl Acad Sci USA. 2012;109:2126–31.
pubmed: 22308343
pmcid: 3277550
doi: 10.1073/pnas.1111715109
Unger EK, Keller JP, Altermatt M, Liang R, Matsui A, Dong C, et al. Directed evolution of a selective and sensitive serotonin sensor via machine learning. Cell. 2020;183:1986–2002.e1926.
pubmed: 33333022
pmcid: 8025677
doi: 10.1016/j.cell.2020.11.040
Kuniishi H, Nakatake Y, Sekiguchi M, Yamada M. Adolescent social isolation induces distinct changes in the medial and lateral OFC-BLA synapse and social and emotional alterations in adult mice. Neuropsychopharmacol: Off Publ Am Coll Neuropsychopharmacol. 2022;47:1597–607.
doi: 10.1038/s41386-022-01358-6
Jennings JH, Kim CK, Marshel JH, Raffiee M, Ye L, Quirin S, et al. Interacting neural ensembles in orbitofrontal cortex for social and feeding behaviour. Nature. 2019;565:645–9.
pubmed: 30651638
pmcid: 6447429
doi: 10.1038/s41586-018-0866-8
Gautier M, Pabst A, Maurage P. Social decision making in severe alcohol use disorder: Scoping review and experimental perspectives. Alcohol, Clin Exp Res. 2021;45:1548–59.
pubmed: 34342010
doi: 10.1111/acer.14664
Charlet K, Schlagenhauf F, Richter A, Naundorf K, Dornhof L, Weinfurtner CE, et al. Neural activation during processing of aversive faces predicts treatment outcome in alcoholism. Addiction Biol. 2014;19:439–51.
doi: 10.1111/adb.12045
Bora E, Zorlu N. Social cognition in alcohol use disorder: a meta-analysis. Addiction. 2017;112:40–8.
pubmed: 27287050
doi: 10.1111/add.13486
Valmas MM, Mosher Ruiz S, Gansler DA, Sawyer KS, Oscar-Berman M. Social cognition deficits and associations with drinking history in alcoholic men and women. Alcohol, Clin Exp Res. 2014;38:2998–3007.
pubmed: 25581654
doi: 10.1111/acer.12566
Schmidt T, Roser P, Ze O, Juckel G, Suchan B, Thoma P. Cortical thickness and trait empathy in patients and people at high risk for alcohol use disorders. Psychopharmacology. 2017;234:3521–33.
pubmed: 28971228
doi: 10.1007/s00213-017-4741-3
Hulvershorn LA, Finn P, Hummer TA, Leibenluft E, Ball B, Gichina V, et al. Cortical activation deficits during facial emotion processing in youth at high risk for the development of substance use disorders. Drug Alcohol Depend. 2013;131:230–7.
pubmed: 23768841
pmcid: 3740548
doi: 10.1016/j.drugalcdep.2013.05.015
Hill SY, Kostelnik B, Holmes B, Goradia D, McDermott M, Diwadkar V, et al. fMRI BOLD response to the eyes task in offspring from multiplex alcohol dependence families. Alcohol, Clin Exp Res. 2007;31:2028–35.
pubmed: 18034695
doi: 10.1111/j.1530-0277.2007.00535.x
Hill SY, Wellman JL, Zezza N, Steinhauer SR, Sharma V, Holmes B Epigenetic Effects in HPA Axis Genes Associated with Cortical Thickness, ERP Components and SUD Outcome. Behav Sci (Basel) 2022;12:347.
Hill SY, Wang S, Kostelnik B, Carter H, Holmes B, McDermott M, et al. Disruption of orbitofrontal cortex laterality in offspring from multiplex alcohol dependence families. Biol Psychiatry. 2009;65:129–36.
pubmed: 18986649
doi: 10.1016/j.biopsych.2008.09.001
Xin J, Zhang Y, Tang Y, Yang Y. Brain differences between men and women: evidence from deep learning. Front Neurosci. 2019;13:185.
pubmed: 30906246
pmcid: 6418873
doi: 10.3389/fnins.2019.00185
Ritchie SJ, Cox SR, Shen X, Lombardo MV, Reus LM, Alloza C, et al. Sex differences in the adult human brain: evidence from 5216 UK biobank participants. Cereb Cortex. 2018;28:2959–75.
pubmed: 29771288
pmcid: 6041980
doi: 10.1093/cercor/bhy109
Batzdorf CS, Morr AS, Bertalan G, Sack I, Silva RV, Infante-Duarte C Sexual Dimorphism in Extracellular Matrix Composition and Viscoelasticity of the Healthy and Inflamed Mouse Brain. Biology (Basel) 2022;11:230.
Nazlee N, Waiter GD, Sandu AL. Age-associated sex and asymmetry differentiation in hemispheric and lobar cortical ribbon complexity across adulthood: A UK Biobank imaging study. Hum Brain Mapp. 2022;44:49–65.
pubmed: 36574599
pmcid: 9783444
doi: 10.1002/hbm.26076
Heilbronner SR, Haber SN. Frontal cortical and subcortical projections provide a basis for segmenting the cingulum bundle: implications for neuroimaging and psychiatric disorders. J Neurosci: Off J Soc Neurosci. 2014;34:10041–54.
doi: 10.1523/JNEUROSCI.5459-13.2014
Guo J, Bertalan G, Meierhofer D, Klein C, Schreyer S, Steiner B, et al. Brain maturation is associated with increasing tissue stiffness and decreasing tissue fluidity. Acta Biomater. 2019;99:433–42.
pubmed: 31449927
doi: 10.1016/j.actbio.2019.08.036
Arani A, Murphy MC, Glaser KJ, Manduca A, Lake DS, Kruse SA, et al. Measuring the effects of aging and sex on regional brain stiffness with MR elastography in healthy older adults. Neuroimage. 2015;111:59–64.
pubmed: 25698157
doi: 10.1016/j.neuroimage.2015.02.016
Sack I, Beierbach B, Wuerfel J, Klatt D, Hamhaber U, Papazoglou S, et al. The impact of aging and gender on brain viscoelasticity. Neuroimage. 2009;46:652–7.
pubmed: 19281851
doi: 10.1016/j.neuroimage.2009.02.040
Wuerfel J, Paul F, Beierbach B, Hamhaber U, Klatt D, Papazoglou S, et al. MR-elastography reveals degradation of tissue integrity in multiple sclerosis. Neuroimage. 2010;49:2520–5.
pubmed: 19539039
doi: 10.1016/j.neuroimage.2009.06.018
Mulholland PJ, Chandler LJ, Kalivas PW. Signals from the fourth dimension regulate drug relapse. Trends Neurosci. 2016;39:472–85.
pubmed: 27173064
pmcid: 4930682
doi: 10.1016/j.tins.2016.04.007
Lasek AW. Effects of ethanol on brain extracellular matrix: implications for alcohol use disorder. Alcohol, Clin Exp Res. 2016;40:2030–42.
pubmed: 27581478
doi: 10.1111/acer.13200
Kruyer A, Chioma VC, Kalivas PW. The opioid-addicted tetrapartite synapse. Biol Psychiatry. 2020;87:34–43.
pubmed: 31378302
doi: 10.1016/j.biopsych.2019.05.025
Seney ML, Kim SM, Glausier JR, Hildebrand MA, Xue X, Zong W, et al. Transcriptional alterations in dorsolateral prefrontal cortex and nucleus accumbens implicate neuroinflammation and synaptic remodeling in opioid use disorder. Biol Psychiatry. 2021;90:550–62.
pubmed: 34380600
pmcid: 8463497
doi: 10.1016/j.biopsych.2021.06.007
Sheedy D, Garrick T, Dedova I, Hunt C, Miller R, Sundqvist N, et al. An Australian Brain Bank: a critical investment with a high return! Cell Tissue Bank. 2008;9:205–16.
pubmed: 18543078
pmcid: 3391553
doi: 10.1007/s10561-008-9076-1