Cited by 23Neurotransmitter Receptor Influence on BehaviorPsychopathy, Forensic Psychiatry, Sexual OffendingNeuroendocrine regulation and behavior

Dysfunctional mesocortical dopamine circuit at pre-adolescence is associated to aggressive behavior in MAO-A hypomorphic mice exposed to early life stress

Open access
Frau, Roberto, Fanni, Silvia, Serra, Valeria, Simola, Nicola, Godar, Sean C., Traccis, Francesco, Devoto, Paola, Bortolato, Marco +1 more·2019·Neuropharmacology

Abstract

Aggressive behavior (AB) is a multifaceted disorder based on the interaction between genetic and environmental factors whose underlying mechanisms remain elusive. The best-characterized gene by environment (GxE) interaction for AB is the relationship between child neglect/abuse and low-activity alleles of the monoamine-oxidase A (MAOA) gene. MAOA oxidizes monoamines like serotonin and dopamine, whose aberrant signaling at discrete developmental ages plays a pivotal role in the ontogeny of AB. Here, we investigated the impact of this GxE on dopamine function at pre-adolescence by exposing hypomorphic MAOA (MAO Neo) mice to early life stress (ES) and by performing behavioral and ex vivo electrophysiological analyses in the ventral tegmental area (VTA) and the prefrontal cortex (PFC). MAOA Neo ES mouse dopamine neurons exhibited an enhanced post-synaptic responsiveness to excitatory inputs, aberrant plasticity in the PFC, and an AB. Systemic administration of the selective antagonist at dopamine D1 receptors SCH23390 fully restored PFC function and rescued AB. Collectively, these findings reveal that dysfunctional mesocortical dopamine signaling at pre-adolescence ties to AB in the MAOA Neo ES mouse, and identify dopamine D1 receptor as a molecular target to be exploited for an age-tailored therapy. This article is part of the Special Issue entitled 'The neuropharmacology of social behavior: from bench to bedside'.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.neuropharm.2019.01.032

Cites

8 of 8 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • In gene-by-environment studies, saline injections in combination with maternal separation increased aggression in MAOA hypomorphic, but not wild-type, mice when performed over the first week of life.

    “In gene-by-environment studies, saline injections in combination with maternal separation increased aggression in monoamine oxidase A (MAOA) hypomorphic, but not wild-type, mice when performed over the first week of life (Frau et al. 2019; Godar et al. 2019).”

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 84

  1. Anderson SW, Bechara A, Damasio H, Tranel D, Damasio AR, 1999. Impairment of social and moral behavior related to early damage in human prefrontal cortex. Nat. Neurosci 2, 1032– 1037. 10526345
  2. Balia C, Carucci S, Coghill D, Zuddas A, 2018. The pharmacological treatment of aggression in children and adolescents with conduct disorder. Do callous-unemotional traits modulate the efficacy of medication? Neurosci. Biobehav. Rev 91, 218– 238. 28137460
  3. Barria A, Malinow R, 2005. NMDA receptor subunit composition controls synaptic plasticity by regulating binding to CaMKII. Neuron 48, 289– 301. 16242409
  4. Bellone C, Mameli M, Luscher C, 2011. In utero exposure to cocaine delays postnatal synaptic maturation of glutamatergic transmission in the VTA. Nat. Neurosci 14, 1439– 1446. 21964489
  5. Blair RJ, 2013. The neurobiology of psychopathic traits in youths. Nat. Rev. Neurosci 14, 786– 799. 24105343 PMC4418507
  6. Blair RJR, 2017. Emotion-based learning systems and the development of morality. Cognition 167, 38– 45. 28395907 PMC5572654
  7. Booij J, de Bruin K, de Win MM, Lavini C, den Heeten GJ, Habraken JB, 2003. Imaging of striatal dopamine transporters in rat brain with single pinhole SPECT and co-aligned MRI is highly reproducible. Nucl. Med. Biol 30, 643– 649. 12900290
  8. Borre YE, O’Keeffe GW, Clarke G, Stanton C, Dinan TG, Cryan JF, 2014. Microbiota and neurodevelopmental windows: implications for brain disorders. Trends Mol. Med 20, 509– 518. 24956966
  9. Bortolato M, Chen K, Godar SC, Chen G, Wu W, Rebrin I, Farrell MR, Scott AL, Wellman CL, Shih JC, 2011. Social deficits and perseverative behaviors, but not overt aggression. In: MAO-A Hypomorphic Mice. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology, vol. 36. pp. 2674– 2688. PMC3230491 21832987
  10. Bortolato M, Godar SC, Melis M, Soggiu A, Roncada P, Casu A, Flore G, Chen K, Frau R, Urbani A, Castelli MP, Devoto P, Shih JC, 2012. NMDARs mediate the role of monoamine oxidase A in pathological aggression. J. Neurosci.: the official journal of the Society for Neuroscience 32, 8574– 8582. PMC3417343 22723698
  11. Brunner HG, Nelen M, Breakefield XO, Ropers HH, van Oost BA, 1993. Abnormal behavior associated with a point mutation in the structural gene for monoamine oxidase A. Science 262, 578– 580. 8211186
  12. Buckholtz JW, Meyer-Lindenberg A, 2008. MAOA and the neurogenetic architecture of human aggression. Trends Neurosci. 31, 120– 129. 18258310
  13. Burke JD, Loeber R, Birmaher B, 2002. Oppositional defiant disorder and conduct disorder: a review of the past 10 years, part II. J. Am. Acad. Child Adolesc. Psychiatr 41, 1275– 1293. 12410070
  14. Byrd AL, Manuck SB, 2014. MAOA, childhood maltreatment, and antisocial behavior: meta-analysis of a gene-environment interaction. Biol. Psychiatry 75, 9– 17. 23786983 PMC3858396
  15. Caspi A, McClay J, Moffitt TE, Mill J, Martin J, Craig IW, Taylor A, Poulton R, 2002. Role of genotype in the cycle of violence in maltreated children. Science 297, 851– 854. 12161658
  16. Checknita D, Maussion G, Labonte B, Comai S, Tremblay RE, Vitaro F, Turecki N, Bertazzo A, Gobbi G, Cote G, Turecki G, 2015. Monoamine oxidase A gene promoter methylation and transcriptional downregulation in an offender population with antisocial personality disorder. Br. J. Psychiatry: J. Ment. Sci 206, 216– 222. 25497297
  17. Choy O, Raine A, Hamilton RH, 2018. Stimulation of the prefrontal cortex reduces intentions to commit aggression: a randomized, double-blind, placebo-controlled, stratified, parallel-group trial. J. Neurosci.: the official journal of the Society for Neuroscience 38 (29), 6505– 6512. PMC6705949 29967006
  18. Comai S, Tau M, Gobbi G, 2012a. The psychopharmacology of aggressive behavior: a translational approach: part 1: neurobiology. J. Clin. Psychopharmacol 32, 83– 94. 22198449
  19. Comai S, Tau M, Pavlovic Z, Gobbi G, 2012b. The psychopharmacology of aggressive behavior: a translational approach: part 2: clinical studies using atypical anti-psychotics, anticonvulsants, and lithium. J. Clin. Psychopharmacol 32, 237– 260. 22367663
  20. Crick NR, Dodge KA, 1996. Social information-processing mechanisms in reactive and proactive aggression. Child Dev. 67, 993– 1002. 8706540
  21. Cui Y, Jin J, Zhang X, Xu H, Yang L, Du D, Zeng Q, Tsien JZ, Yu H, Cao X, 2011. Forebrain NR2B overexpression facilitating the prefrontal cortex long-term potentiation and enhancing working memory function in mice. PLoS One 6, e20312. 21655294 PMC3105019
  22. de Almeida RM, Ferrari PF, Parmigiani S, Miczek KA, 2005a. Escalated aggressive behavior: dopamine, serotonin and GABA. Eur. J. Pharmacol 526, 51– 64. 16325649
  23. de Almeida RM, Ferrari PF, Parmigiani S, Miczek KA, 2005b. Escalated aggressive behavior: dopamine, serotonin and GABA. Eur. J. Pharmacol 526, 51– 64. 16325649
  24. Ellis ML, Weiss B, Lochman JE, 2009. Executive functions in children: associations with aggressive behavior and appraisal processing. J. Abnorm. Child Psychol 37, 945– 956. 19408113 PMC3978175
  25. Fallon SJ, Williams-Gray CH, Barker RA, Owen AM, Hampshire A, 2013. Prefrontal dopamine levels determine the balance between cognitive stability and flexibility. Cerebr. Cortex 23, 361– 369. 22351648
  26. Farrington DP, 1990. Implications of criminal career research for the prevention of offending. J. Adolesc 13, 93– 113. 2387923
  27. Fergusson DM, Boden JM, Horwood LJ, Miller AL, Kennedy MA, 2011. MAOA, abuse exposure and antisocial behaviour: 30-year longitudinal study. Br. J. Psychiatry 198, 457– 463. 21628708 PMC3105117
  28. Flexner LB, Goodman RH, 1975. Studies on memory: inhibitors of protein synthesis also inhibit catecholamine synthesis. Proc. Natl. Acad. Sci. U.S.A 72, 4660– 4663. 1060144 PMC388783
  29. Gansler DA, Lee AK, Emerton BC, D’Amato C, Bhadelia R, Jerram M, Fulwiler C, 2011. Prefrontal regional correlates of self-control in male psychiatric patients: impulsivity facets and aggression. Psychiatr. Res 191, 16– 23. 21145213
  30. Godar SC, Fite PJ, McFarlin KM, Bortolato M, 2016. The role of monoamine oxidase A in aggression: current translational developments and future challenges. Progress in neuro-psychopharmacology & biological psychiatry 69, 90– 100. 26776902 PMC4865459
  31. Godar SC, Mosher Laura J., Melis Miriam, Scheggi Simona, Moench Kelly M., Strathman Hunter J., Jones Cori M., Wilkinson Brent, Devoto Paola, Frau Roberto, Pardu Alessandra, Gambarana Carla, DeMontis M Graziella, Fowler Stephen C., Shih Jean C., Coba Marcelo P., Wellman Cara L., Bortolato M, 2019 Feb 1. Gene-environment interactions in antisocial behavior are mediated by early-life 5-HT2A receptor activation. Neuropharmacology. 10.1016/j.neuropharm.2019.01.028. pii: S0028–3908(19)30028–0. PMC7578912 30716416 · DOI · Paper page
  32. Goldman-Rakic PS, 1996. The prefrontal landscape: implications of functional architecture for understanding human mentation and the central executive. Phil. Trans. Roy. Soc. Lond. B Biol. Sci 351, 1445– 1453. 8941956
  33. Goldman-Rakic PS, Muly EC 3rd, Williams GV, 2000. D(1) receptors in prefrontal cells and circuits. Brain research. Brain Res. Rev 31, 295– 301. 10719156
  34. Goldstein D, Hahn CS, Hasher L, Wiprzycka UJ, Zelazo PD, 2007. Time of day, intellectual performance, and behavioral problems in morning versus evening type Adolescents: is there a synchrony effect? Pers. Indiv. Differ 42, 431– 440. PMC1761650 17268574
  35. Gorodetsky E, Bevilacqua L, Carli V, Sarchiapone M, Roy A, Goldman D, Enoch MA, 2014. The interactive effect of MAOA-LPR genotype and childhood physical neglect on aggressive behaviors in Italian male prisoners. Genes Brain Behav. 13, 543– 549. 24805005 PMC4130458
  36. Grandjean J, Azzinnari D, Seuwen A, Sigrist H, Seifritz E, Pryce CR, Rudin M, 2016. Chronic psychosocial stress in mice leads to changes in brain functional connectivity and metabolite levels comparable to human depression. Neuroimage 142, 544– 552. 27520750
  37. Gregg TR, Siegel A, 2001. Brain structures and neurotransmitters regulating aggression in cats: implications for human aggression. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 25, 91– 140. 11263761
  38. Gunaydin LA, Grosenick L, Finkelstein JC, Kauvar IV, Fenno LE, Adhikari A, Lammel S, Mirzabekov JJ, Airan RD, Zalocusky KA, Tye KM, Anikeeva P, Malenka RC, Deisseroth K, 2014. Natural neural projection dynamics underlying social behavior. Cell 157, 1535– 1551. 24949967 PMC4123133
  39. Guo G, Ou XM, Roettger M, Shih JC, 2008. The VNTR 2 repeat in MAOA and delinquent behavior in adolescence and young adulthood: associations and MAOA promoter activity. Eur. J. Hum. Genet.: EJHG (Eur. J. Hum. Genet.) 16, 626– 634. 18212819 PMC2922855
  40. Halasz J, Toth M, Kallo I, Liposits Z, Haller J, 2006. The activation of prefrontal cortical neurons in aggression–a double labeling study. Behav. Brain Res 175, 166– 175. 16978716
  41. Hausknecht K, Haj-Dahmane S, Shen YL, Vezina P, Dlugos C, Shen RY, 2015. Excitatory Synaptic Function and Plasticity Is Persistently Altered in Ventral Tegmental Area Dopamine Neurons after Prenatal Ethanol Exposure, vol. 40. Neuropsychopharmacology: official publication of the American College of Neuropsychopharmacology, pp. 893– 905. 25284318 PMC4330503
  42. Henggeler SW, Sheidow AJ, 2003. Conduct disorder and delinquency. J. Marital Fam. Ther 29, 505– 522. 14593692
  43. Homayoun H, Jackson ME, Moghaddam B, 2005. Activation of metabotropic glutamate 2/3 receptors reverses the effects of NMDA receptor hypofunction on prefrontal cortex unit activity in awake rats. J. Neurophysiol 93, 1989– 2001. 15590730
  44. Huang YY, Cate SP, Battistuzzi C, Oquendo MA, Brent D, Mann JJ, 2004. An Association between a Functional Polymorphism in the Monoamine Oxidase a Gene Promoter, Impulsive Traits and Early Abuse Experiences, vol. 29. Neuropsychopharmacology: official publication of the American College of Neuropsychopharmacology, pp. 1498– 1505. 15150530
  45. Ironside M, Kumar P, Kang M, Pizzagalli D, 2018. Brain mechanisms mediating effects of stress on reward sensitivity. Current Opinion in Behavioral Sciences 22, 106– 113. 30349872 PMC6195323
  46. Jackson ME, Homayoun H, Moghaddam B, 2004. NMDA receptor hypofunction produces concomitant firing rate potentiation and burst activity reduction in the prefrontal cortex. Proc. Natl. Acad. Sci. U. S. A 101, 8467– 8472. 15159546 PMC420417
  47. Karere GM, Kinnally EL, Sanchez JN, Famula TR, Lyons LA, Capitanio JP, 2009. What is an “adverse” environment? Interactions of rearing experiences and MAOA genotype in rhesus monkeys. Biol. Psychiatry 65, 770– 777. 19103441 PMC2688474
  48. Kasanetz F, Deroche-Gamonet V, Berson N, Balado E, Lafourcade M, Manzoni O, Piazza PV, 2010. Transition to addiction is associated with a persistent impairment in synaptic plasticity. Science 328, 1709– 1712. 20576893
  49. Kasanetz F, Lafourcade M, Deroche-Gamonet V, Revest JM, Berson N, Balado E, Fiancette JF, Renault P, Piazza PV, Manzoni OJ, 2013. Prefrontal synaptic markers of cocaine addiction-like behavior in rats. Mol. Psychiatr 18, 729– 737. 22584869
  50. Kim-Cohen J, Caspi A, Taylor A, Williams B, Newcombe R, Craig IW, Moffitt TE, 2006. MAOA, maltreatment, and gene-environment interaction predicting children’s mental health: new evidence and a meta-analysis. Mol. Psychiatr 11, 903– 913. 16801953
  51. Lafourcade M, Elezgarai I, Mato S, Bakiri Y, Grandes P, Manzoni OJ, 2007. Molecular components and functions of the endocannabinoid system in mouse prefrontal cortex. PLoS One 2, e709. 17684555 PMC1933592
  52. Lahey BB, Loeber R, Burke J, Rathouz PJ, McBurnett K, 2002. Waxing and waning in concert: dynamic comorbidity of conduct disorder with other disruptive and emotional problems over 7 years among clinic-referred boys. J. Abnorm. Psychol 111, 556– 567. 12428769
  53. Lee AK, Jerram M, Fulwiler C, Gansler DA, 2011. Neural correlates of impulsivity factors in psychiatric patients and healthy volunteers: a voxel-based morphometry study. Brain imaging and behavior 5, 52– 64. 21210255
  54. Levy F, 2004. Synaptic Gating and ADHD: a Biological Theory of Comorbidity of ADHD and Anxiety, vol. 29. Neuropsychopharmacology: official publication of the American College of Neuropsychopharmacology, pp. 1589– 1596. 15114344
  55. Lewis BL, O’Donnell P, 2000. Ventral tegmental area afferents to the prefrontal cortex maintain membrane potential ‘up’ states in pyramidal neurons via D(1) dopamine receptors. Cerebr. Cortex 10, 1168– 1175. 11073866
  56. Lewis MD, Granic I, Lamm C, Zelazo PD, Stieben J, Todd RM, Moadab I, Pepler D, 2008. Changes in the neural bases of emotion regulation associated with clinical improvement in children with behavior problems. Dev. Psychopathol 20, 913– 939. 18606038
  57. Loeber R, Green SM, Lahey BB, Kalb L, 2000. Physical fighting in childhood as a risk factor for later mental health problems. J. Am. Acad. Child Adolesc. Psychiatr 39, 421– 428. 10761343
  58. Mason L, O’Sullivan N, Montaldi D, Bentall RP, El-Deredy W, 2014. Decision making and trait impulsivity in bipolar disorder are associated with reduced prefrontal regulation of striatal reward valuation. Brain: J. Neurol 137, 2346– 2355. PMC4107743 25009169
  59. Matsuda Y, Marzo A, Otani S, 2006. The presence of background dopamine signal converts long-term synaptic depression to potentiation in rat prefrontal cortex. J. Neurosci.: the official journal of the Society for Neuroscience 26, 4803– 4810. PMC6674173 16672653
  60. McAuliffe MD, Hubbard JA, Rubin RM, Morrow MT, Dearing KF, 2006. Reactive and proactive aggression: stability of constructs and relations to correlates. J. Genet. Psychol 167, 365– 382. 17645228
  61. Meyer-Lindenberg A, Buckholtz JW, Kolachana B, A RH, Pezawas L, Blasi G, Wabnitz A, Honea R, Verchinski B, Callicott JH, Egan M, Mattay V, Weinberger DR, 2006. Neural mechanisms of genetic risk for impulsivity and violence in humans. Proc. Natl. Acad. Sci. U.S.A 103, 6269– 6274. 16569698 PMC1458867
  62. Miller EK, Cohen JD, 2001. An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci 24, 167– 202. 11283309
  63. Olino TM, Seeley JR, Lewinsohn PM, 2010. Conduct disorder and psychosocial outcomes at age 30: early adult psychopathology as a potential mediator. J. Abnorm. Child Psychol 38, 1139– 1149. 20521096 PMC2952347
  64. Pignatelli M, Bonci A, 2015. Role of dopamine neurons in reward and aversion: a synaptic plasticity perspective. Neuron 86, 1145– 1157. 26050034
  65. Raine A, Lencz T, Bihrle S, LaCasse L, Colletti P, 2000. Reduced prefrontal gray matter volume and reduced autonomic activity in antisocial personality disorder. Arch. Gen. Psychiatr 57, 119– 127 discussion 128– 119. 10665614
  66. Rebello TJ, Yu Q, Goodfellow NM, Caffrey Cagliostro MK, Teissier A, Morelli E, Demireva EY, Chemiakine A, Rosoklija GB, Dwork AJ, Lambe EK, Gingrich JA, Ansorge MS, 2014. Postnatal day 2 to 11 constitutes a 5-HT-sensitive period impacting adult mPFC function. J. Neurosci.: the official journal of the Society for Neuroscience 34, 12379– 12393. PMC4160773 25209278
  67. Richter A, Richter S, Barman A, Soch J, Klein M, Assmann A, Libeau C, Behnisch G, Wustenberg T, Seidenbecher CI, Schott BH, 2013. Motivational salience and genetic variability of dopamine D2 receptor expression interact in the modulation of interference processing. Front. Hum. Neurosci 7, 250. 23760450 PMC3672681
  68. Rosell DR, Siever LJ, 2015. The neurobiology of aggression and violence. CNS Spectr. 20, 254– 279. 25936249
  69. Ruan H, Saur T, Yao WD, 2014. Dopamine-enabled anti-Hebbian timing-dependent plasticity in prefrontal circuitry. Front. Neural Circuits 8, 38. 24795571 PMC4005942
  70. Saal D, Dong Y, Bonci A, Malenka RC, 2003. Drugs of abuse and stress trigger a common synaptic adaptation in dopamine neurons. Neuron 37, 577– 582. 12597856
  71. Seguin JR, Arseneault L, Boulerice B, Harden PW, Tremblay RE, 2002. Response perseveration in adolescent boys with stable and unstable histories of physical aggression: the role of underlying processes. J. Child Psychol. Psychiatry Allied Discip 43, 481– 494. 12030594
  72. Seo D, Patrick CJ, Kennealy PJ, 2008. Role of serotonin and dopamine system interactions in the neurobiology of impulsive aggression and its comorbidity with other clinical disorders. Aggress. Violent Behav 13, 383– 395. 19802333 PMC2612120
  73. Shiner T, Symmonds M, Guitart-Masip M, Fleming SM, Friston KJ, Dolan RJ, 2015. Dopamine, salience, and response set shifting in prefrontal cortex. Cerebr. Cortex 25, 3629– 3639. PMC4585507 25246512
  74. Shohamy D, Myers CE, Grossman S, Sage J, Gluck MA, 2005. The role of dopamine in cognitive sequence learning: evidence from Parkinson’s disease. Behav. Brain Res 156, 191– 199. 15582105
  75. Simonoff E, Elander J, Holmshaw J, Pickles A, Murray R, Rutter M, 2004. Predictors of antisocial personality. Continuities from childhood to adult life. Br. J. Psychiatry: J. Ment. Sci 184, 118– 127. 14754823
  76. Stahl SM, 2009b. The prefrontal cortex is out of tune in attention-deficit/hyperactivity disorder. J. Clin. Psychiatr 70, 950– 951. 19653972
  77. Ungless MA, Whistler JL, Malenka RC, Bonci A, 2001. Single cocaine exposure in vivo induces long-term potentiation in dopamine neurons. Nature 411, 583– 587. 11385572
  78. Viding E, Frith U, 2006. Genes for susceptibility to violence lurk in the brain. Proc. Natl. Acad. Sci. U.S.A 103, 6085– 6086. 16606856 PMC1458834
  79. WA P, C v. d. M., W S, 2010. Dynamic coordination in brain and mind. In: von der Malsburg C, P.W., Singer W (Eds.), Dynamic Coordination in the Brain: from Neurons to Mind. MIT, Cambridge, MA, pp. 1– 25.
  80. Williams LM, Gatt JM, Kuan SA, Dobson-Stone C, Palmer DM, Paul RH, Song L, Costa PT, Schofield PR, Gordon E, 2009. A polymorphism of the MAOA gene is associated with emotional brain markers and personality traits on an antisocial index. Neuropsychopharmacology 34, 1797– 1809. 19194374
  81. Yang Y, Raine A, 2009. Prefrontal structural and functional brain imaging findings in antisocial, violent, and psychopathic individuals: a meta-analysis. Psychiatr. Res 174, 81– 88. PMC2784035 19833485
  82. Yu Q, Teixeira CM, Mahadevia D, Huang Y, Balsam D, Mann JJ, Gingrich JA, Ansorge MS, 2014a. Dopamine and serotonin signaling during two sensitive developmental periods differentially impact adult aggressive and affective behaviors in mice. Mol. Psychiatr 19, 688– 698. PMC4311886 24589889
  83. Yu Q, Teixeira CM, Mahadevia D, Huang YY, Balsam D, Mann JJ, Gingrich JA, Ansorge MS, 2014b. Optogenetic stimulation of DAergic VTA neurons increases aggression. Mol. Psychiatr 19, 635. 24847796
  84. Zuddas A, 2014. The poor outcome of conduct disorders: a need for innovative, more effective therapeutic interventions. Eur. Child Adolesc. Psychiatry 23, 515– 517. 24965799

Cited by

Sorted by citations

Authors
Frau, R., Fanni, S., Serra, V., Simola, N., Godar, S. C., Traccis, F., Devoto, P., Bortolato, M., & Melis, M.
Affiliations
  • University of Cagliari (IT)
  • University of Utah (US)
Corresponding author
Melis, Miriam
Venue
Neuropharmacology
Publisher
Elsevier BV
Published
2019-11
Volume
159
Pages
107517
ISSN
0028-3908 (ISSN-L)
OpenAlex
W2914981935
Cited by
23
References
8
Citations by year
2025: 4 · 2024: 3 · 2023: 5 · 2022: 2 · 2021: 2 · 2020: 4 · 2019: 3
FWCI
1.31
Type
journal article
Language
en
Open access
Locations
  • Neuropharmacology (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (publishedVersion)
  • UNICA IRIS Institutional Research Information System (University of Cagliari) (submittedVersion)
Funders
  • University of Cagliari (RICCAR 2017)
  • Region of Sardinia (L.R. 7 8/2007, RASSR32909, F72F16002850002)
  • National Institutes of Health (MH104603)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
  • Social Sciences › Psychology › Clinical Psychology › Psychopathy, Forensic Psychiatry, Sexual Offending
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Keywords
aggression, monoamine oxidase A, early life stress, gene-environment interaction, ventral tegmental area, prefrontal cortex, dopamine D1 receptor, synaptic plasticity, late childhood, child neglect and abuse
MeSH terms
Age Factors, Aggression, Animals, Animals, Newborn, Benzazepines, Dopamine, Male, Mice, Transgenic, Monoamine Oxidase, Nerve Net, Random Allocation, Stress, Psychological, Prefrontal Cortex, Receptors, Dopamine D1, Ventral Tegmental Area, Excitatory Postsynaptic Potentials, Mice, Mice, 129 Strain, Dopaminergic Neurons

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review