Stress, hypothalamic-pituitary-adrenal axis, hypothalamic-pituitary-gonadal axis, and aggression.

Aggression-related disorders Androgen system Glucocorticoids NeurobiologyTestosterone

Journal

Metabolic brain disease
ISSN: 1573-7365
Titre abrégé: Metab Brain Dis
Pays: United States
ID NLM: 8610370

Informations de publication

Date de publication:
31 Jul 2024
Historique:
received: 21 07 2023
accepted: 08 07 2024
medline: 31 7 2024
pubmed: 31 7 2024
entrez: 31 7 2024
Statut: aheadofprint

Résumé

This comprehensive review explores the intricate relationship between the hypothalamic-pituitary-adrenal (HPA) axis, the hypothalamic-pituitary-gonadal (HPG) axis, and aggression. It provides a detailed overview of the physiology and functioning of these axes, as well as the implications for aggressive behavior. The HPA axis, responsible for the stress response, is activated in response to various stressors and can influence aggressive behavior. Glucocorticoids, such as cortisol, play a crucial role in stress-induced activation of the HPA axis and have been implicated in aggressive tendencies. Chronic stress can dysregulate the HPA axis, leading to alterations in cortisol levels and potentially contributing to aggressive behavior. The HPG axis, particularly the androgen hormone testosterone, is also closely linked to aggression. Animal and human studies have consistently shown a positive association between testosterone levels and aggression. The androgen receptors in the brain's neural circuitry play a critical role in modulating aggressive behavior. Interactions between the HPA and HPG axes further contribute to the regulation of aggression. Feedback mechanisms and crosstalk between these axes provide a complex system for the modulation of both stress and reproductive functions, which can impact aggressive behavior. Additionally,the influence of stress on reproductive functions, particularly the role of androgens in stress-induced aggression, adds further complexity to this relationship. The review also discusses the future directions and implications for clinical interventions. Understanding the neurobiological mechanisms underlying aggression requires integrating molecular, cellular, and circuit-level approaches. Translational perspectives, including animal models and human studies, can bridge the gap between basic research and clinical applications. Finally, therapeutic strategies for aggression-related disorders are explored, highlighting the importance of targeted interventions based on a comprehensive understanding of the interactions between the HPA and HPG axes. In conclusion, this review provides a comprehensive overview of the physiological and neurobiological mechanisms underlying aggression, with a specific focus on the interplay between the HPA and HPG axes. By elucidating the complex interactions between stress, hormones, and aggressive behavior, this research paves the way for future investigations and potential therapeutic interventions for aggression-related disorders.

Identifiants

pubmed: 39083184
doi: 10.1007/s11011-024-01393-w
pii: 10.1007/s11011-024-01393-w
doi:

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024. The Author(s).

Références

Aikins AO, Nguyen DH, Paundralingga O, Farmer GE, Shimoura CG, Brock C, Cunningham JT (2021) Cardiovascular neuroendocrinology: emerging role for neurohypophyseal hormones in pathophysiology. Endocrinology 162(8). https://doi.org/10.1210/ENDOCR/BQAB082
Anacker C, Cattaneo A, Luoni A, Musaelyan K, Zunszain PA, Milanesi E, Rybka J, Berry A, Cirulli F, Thuret S, Price J, Riva MA, Gennarelli M, Pariante CM (2013) Glucocorticoid-related molecular signaling pathways regulating hippocampal neurogenesis. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology 38(5):872–883. https://doi.org/10.1038/NPP.2012.253
Albers HE (2012) The regulation of social recognition, social communication and aggression: Vasopressin in the social behavior neural network. Horm Behav 61(3):283–292. https://doi.org/10.1016/J.YHBEH.2011.10.007
doi: 10.1016/J.YHBEH.2011.10.007 pubmed: 22079778
Aujard F, Perret M (1998) Age-related effects on reproductive function and sexual competition in the male prosimian primate, Microcebus murinus. Physiol Behav 64(4):513–519. https://doi.org/10.1016/S0031-9384(98)00087-0
Ayres JS (2020) The biology of physiological health. Cell 181(2):250–269. https://doi.org/10.1016/J.CELL.2020.03.036
doi: 10.1016/J.CELL.2020.03.036 pubmed: 32302569
Balfour ME, Yu L, Coolen LM (2003) Sexual behavior and sex-associated environmental cues activate the mesolimbic system in male rats. Neuropsychopharmacol 2004 29:4(4):718–730. https://doi.org/10.1038/sj.npp.1300350
doi: 10.1038/sj.npp.1300350
Barsegyan A, Mirone G, Ronzoni G, Guo C, Song Q, van Kuppeveld D, Schut EHS, Atsak P, Teurlings S, McGaugh JL, Schubert D, Roozendaal B (2019) Glucocorticoid enhancement of recognition memory via basolateral amygdala-driven facilitation of prelimbic cortex interactions. Proc Natl Acad Sci USA 116(14):7077–7082. https://doi.org/10.1073/PNAS.1901513116/SUPPL_FILE/PNAS.1901513116.SAPP.PDF
doi: 10.1073/PNAS.1901513116/SUPPL_FILE/PNAS.1901513116.SAPP.PDF pubmed: 30877244
Batrinos ML (2012) Testosterone and aggressive behavior in man. Int J Endocrinol Metabolism 10(3):563. https://doi.org/10.5812/IJEM.3661
doi: 10.5812/IJEM.3661
Beech AR, Mitchell IJ (2005) A neurobiological perspective on attachment problems in sexual offenders and the role of selective serotonin re-uptake inhibitors in the treatment of such problems. Clin Psychol Rev 25(2):153–182. https://doi.org/10.1016/j.cpr.2004.10.002
Beit-Hallahmi B (1971) Sexual and aggressive fantasies in violent and non-violent prison inmates. J Pers Assess 35(4):326–330. https://doi.org/10.1080/00223891.1971.10119676
doi: 10.1080/00223891.1971.10119676 pubmed: 5566748
Bialy M, Bogacki-Rychlik W, Przybylski J, Zera T (2019) The sexual motivation of male rats as a tool in animal models of human health disorders. Front Behav Neurosci 13:257. https://doi.org/10.3389/FNBEH.2019.00257/BIBTEX
doi: 10.3389/FNBEH.2019.00257/BIBTEX pubmed: 31956302
Bickart KC, Hollenbeck MC, Barrett LF, Dickerson BC (2012) Intrinsic amygdala-cortical functional connectivity predicts social network size in humans. J Neurosci. https://doi.org/10.1523/JNEUROSCI.1599-12.2012
doi: 10.1523/JNEUROSCI.1599-12.2012 pubmed: 23077058
Binder EB, Nemeroff CB (2009) The CRF system, stress, depression and anxiety—insights from human genetic studies. Mol Psychiatry 2010 15(6):574–588. https://doi.org/10.1038/mp.2009.141
doi: 10.1038/mp.2009.141
Blanchard RJ, Blanchard DC, Takahashi T, Kelley MJ (1977) Attack and defensive behaviour in the albino rat. Anim Behav 25(PART 3):622–634. https://doi.org/10.1016/0003-3472(77)90113-0
Bock J, Wainstock T, Braun K, Segal M (2015) Stress in utero: prenatal programming of brain plasticity and cognition. Biol Psychiatry. https://doi.org/10.1016/j.biopsych.2015.02.036
Bornstein SR, Allolio B, Arlt W, Barthel A, Don-Wauchope A, Hammer GD, Husebye ES, Merke DP, Murad MH, Stratakis CA, Torpy DJ (2016) Diagnosis and Treatment of Primary Adrenal Insufficiency: An Endocrine Society Clinical Practice Guideline. J Clin Endocrinol Metab 101(2):364–389. https://doi.org/10.1210/jc.2015-1710
Bounoua N, Spielberg JM, Sadeh N (2022) Clarifying the synergistic effects of emotion dysregulation and inhibitory control on physical aggression. Hum Brain Mapp 43(17):5358–5369. https://doi.org/10.1002/HBM.26012
doi: 10.1002/HBM.26012 pubmed: 35838011
Brown GL, McGarvey EL, Shirtcliff EA, Keller A, Granger DA, Flavin K (2008) Salivary cortisol, dehydroepiandrosterone, and testosterone interrelationships in healthy young males: a pilot study with implications for studies of aggressive behavior. Psychiatry Res 159(1–2):67–76. https://doi.org/10.1016/J.PSYCHRES.2007.06.012
doi: 10.1016/J.PSYCHRES.2007.06.012 pubmed: 18314202
Brunton PJ (2013) Effects of maternal exposure to social stress during pregnancy: Consequences for mother and offspring. Reproduction 146(5):146–175. https://doi.org/10.1530/REP-13-0258
Bzdok D, Dunbar RIM (2020) The neurobiology of social distance. Trends Cogn Sci 24:717–733 Elsevier Ltd 9.  https://doi.org/10.1016/j.tics.2020.05.016
Cahill S, Chandola T, Hager R (2022) Genetic variants associated with resilience in human and animal studies. Front Psychiatry 13:840120. https://doi.org/10.3389/FPSYT.2022.840120/FULL
doi: 10.3389/FPSYT.2022.840120/FULL pubmed: 35669264 pmcid: 9163442
Calderon DP, Kilinc M, Maritan A, Banavar JR, Pfaff D (2016) Generalized CNS arousal: An elementary force within the vertebrate nervous system. Neurosci Biobehav Rev 68:167–176. https://doi.org/10.1016/j.neubiorev.2016.05.014
Campagne DM (2019) Stress and perceived social isolation (loneliness). Arch Gerontol Geriatr. https://doi.org/10.1016/j.archger.2019.02.007
Carré JM, Archer J (2018) Testosterone and human behavior: the role of individual and contextual variables. Curr Opin Psychol 19:149–153. https://doi.org/10.1016/J.COPSYC.2017.03.021
doi: 10.1016/J.COPSYC.2017.03.021 pubmed: 29279215
Chaudron Y, Pifferi F, Aujard F (2021) Overview of age-related changes in psychomotor and cognitive functions in a prosimian primate, the gray mouse lemur (Microcebus murinus): recent advances in risk factors and antiaging interventions. Am J Primatol 83(11):e23337. https://doi.org/10.1002/AJP.23337
doi: 10.1002/AJP.23337 pubmed: 34706117
Chester DS, DeWall CN, Derefinko KJ, Estus S, Lynam DR, Peters JR, Jiang Y (2016) Looking for reward in all the wrong places: dopamine receptor gene polymorphisms indirectly affect aggression through sensation-seeking. Soc Neurosci 11(5):487. https://doi.org/10.1080/17470919.2015.1119191
doi: 10.1080/17470919.2015.1119191 pubmed: 26592425
Chiappelli J, Savransky A, Ma Y, Gao S, Kvarta MD, Kochunov P, Slavich GM, Hong LE (2024) Impact of lifetime stressor exposure on neuroenergetics in schizophrenia spectrum disorders. Schizophr Res 269:58–63. https://doi.org/10.1016/j.schres.2024.04.027
Cizauskas CA, Turner WC, Pitts N, Getz WM (2015) Seasonal patterns of hormones, macroparasites, and microparasites in wild African ungulates: the interplay among stress, Reproduction, and Disease. PLoS One 10(4):e0120800. https://doi.org/10.1371/JOURNAL.PONE.0120800
doi: 10.1371/JOURNAL.PONE.0120800 pubmed: 25875647 pmcid: 4398380
Clark BJ, Prough RA, Klinge CM (2018) Mechanisms of Action of Dehydroepiandrosterone. Vitam Horm 108:29–73. https://doi.org/10.1016/bs.vh.2018.02.003
Coolen RL, Cambier JC, Spantidea PI, van Asselt E, Blok BFM (2021) Androgen receptors in areas of the spinal cord and brainstem: a study in adult male cats. J Anat 239(1):125–135. https://doi.org/10.1111/JOA.13407
doi: 10.1111/JOA.13407 pubmed: 33619726
Cunningham RL, Lumia AR, McGinnis MY (2012) Androgen receptors, sex behaviour, and aggression. Neuroendocrinology 96(2):131. https://doi.org/10.1159/000337663
Czoty PW, Gould RW, Nader MA (2009) Relationship between social rank and cortisol and testosterone concentrations in male cynomolgus monkeys (macaca fascicularis). J Neuroendocrinol 21(1):68–76. https://doi.org/10.1111/j.1365-2826.2008.01800.x
doi: 10.1111/j.1365-2826.2008.01800.x pubmed: 19094095
Dabbs JM, Morris R (1990) Testosterone, social class, and antisocial behavior in a sample of 4,462 men. Psychol Sci 1(3):209–211. https://doi.org/10.1111/j.1467-9280.1990.tb00200.x
Dabbs JM, Frady RL, Carr TS, Besch NF (1987) Saliva testosterone and criminal violence in young adult prison inmates. Psychosom Med 49(2):174–182. https://doi.org/10.1097/00006842-198703000-00007
doi: 10.1097/00006842-198703000-00007 pubmed: 3575604
Davey RA, Grossmann M (2016) Androgen receptor structure, function and Biology: from bench to bedside. Clin Biochem Rev 37(1):3
pubmed: 27057074
Deng Q, Zhang Z, Wu Y (2017) The pulsatility of ACTH secretion in the rat anterior pituitary cell perifusion system. Cell Physiol Biochem 41(1):154–162. https://doi.org/10.1159/000455984
doi: 10.1159/000455984
Deng K, Yang L, Xie J, Tang H, Wu GS, Luo HR (2019) Whole-brain mapping of projection from mouse lateral septal nucleus. Biology Open. https://doi.org/10.1242/bio.043554
doi: 10.1242/bio.043554 pubmed: 31208998
Denson TF, O’Dean SM, Blake KR, Beames JR (2018) Aggression in women: behavior, brain and hormones. Front Behav Neurosci 0:81. https://doi.org/10.3389/FNBEH.2018.00081
doi: 10.3389/FNBEH.2018.00081
Deuter CE, Duesenberg M, Hellmann-Regen J, Metz S, Roepke S, Wolf OT, Otte C, Wingenfeld K (2021) Psychosocial stress increases testosterone in patients with borderline personality disorder, post-traumatic stress disorder and healthy participants. Borderline Person Disord Emot Dysregulation 8(1):1–9. https://doi.org/10.1186/S40479-021-00145-X/FIGURES/1
doi: 10.1186/S40479-021-00145-X/FIGURES/1
Dismukes AR, Johnson MM, Vitacco MJ, Iturri F, Shirtcliff EA (2015) Coupling of the HPA and HPG axes in the context of early life adversity in incarcerated male adolescents. Dev Psychobiol 57(6):705. https://doi.org/10.1002/DEV.21231
doi: 10.1002/DEV.21231 pubmed: 25213098
Dunlap KD, Jashari D, Pappas KM (2011) Glucocorticoid receptor blockade inhibits brain cell addition and aggressive signaling in electric fish, Apteronotus leptorhynchus. Horm Behav 60(3):275. https://doi.org/10.1016/J.YHBEH.2011.06.001
doi: 10.1016/J.YHBEH.2011.06.001 pubmed: 21683080
Resmini E, Santos A, Gómez-Anson B, Vives Y, Pires P, Crespo I, Portella MJ, de Juan-Delago M, Barahona M-J, Webb SM (2012) Verbal and visual memory performance and hippocampal volumes, measured by 3-Tesla magnetic resonance imaging, in patients with Cushing’s syndrome. J Clin Endocrinol Metab 97(2):663–671.  https://doi.org/10.1210/JC.2011-2231
Edwards DA (1969) Early androgen stimulation and aggressive behavior in male and female mice. Physiol Behav 4(3):333–338. https://doi.org/10.1016/0031-9384(69)90185-1
doi: 10.1016/0031-9384(69)90185-1
Faught E, Vijayan MM (2018) The mineralocorticoid receptor is essential for stress axis regulation in zebrafish larvae. Sci Rep 2018 8(1):1–11. https://doi.org/10.1038/s41598-018-36681-w
doi: 10.1038/s41598-018-36681-w
Fedotova J, Akulova V, Pivina S, Dragasek J, Caprnda M, Kruzliak P (2017) Modifications of anxiety-like behavior in prenatally stressed male offspring with imbalance of androgens. Am J Translational Res 9(3):1448. /pmc/articles/PMC5376035/
Fernàndez-Castillo N, Cormand B (2016) Aggressive behavior in humans: genes and pathways identified through association studies. Am J Med Genet Part B: Neuropsychiatric Genet 171(5):676–696. https://doi.org/10.1002/AJMG.B.32419
doi: 10.1002/AJMG.B.32419
French JA, Mustoe AC, Cavanaugh J, Birnie AK (2013) The influence of androgenic steroid hormones on female aggression in ‘atypical’ mammals. Philos Trans R Soc B: Biol Sci 368(1631). https://doi.org/10.1098/RSTB.2013.0084
Fritz M, Soravia S-M, Dudeck M, Malli L, Fakhoury M (2023) Neurobiology of aggression—review of recent findings and relationship with alcohol and trauma. Biology 12(3):469. https://doi.org/10.3390/biology12030469
Gallo-Payet N, Martinez A, Lacroix A (2017) Editorial: ACTH Action in the Adrenal Cortex: from molecular biology to pathophysiology. Front Endocrinol 8:101. https://doi.org/10.3389/fendo.2017.00101
Ghasemi M, Navidhamidi M, Rezaei F, Azizikia A, Mehranfard N, Cognitive (2021) Affect Behav Neurosci 22(3):431–449. https://doi.org/10.3758/S13415-021-00973-Y
Gjerstad JK, Lightman SL, Spiga F (2018) Role of glucocorticoid negative feedback in the regulation of HPA axis pulsatility. Stress 21(5):403. https://doi.org/10.1080/10253890.2018.1470238
doi: 10.1080/10253890.2018.1470238 pubmed: 29764284 pmcid: 6220752
Godoy LD, Rossignoli MT, Delfino-Pereira P, Garcia-Cairasco N, Umeoka EH de L (2018) A comprehensive overview on stress neurobiology: basic concepts and clinical implications. Front Behav Neurosci 12:127. https://doi.org/10.3389/FNBEH.2018.00127
Goy RW, Bercovitch FB, McBrair MC (1988) Behavioral masculinization is independent of genital masculinization in prenatally androgenized female rhesus macaques. Horm Behav 22(4):552–571. https://doi.org/10.1016/0018-506X(88)90058-X
Hakamata Y, Komi S, Moriguchi Y, Izawa S, Motomura Y, Sato E, Mizukami S, Kim Y, Hanakawa T, Inoue Y, Tagaya H (2017) Amygdala-centred functional connectivity affects daily cortisol concentrations: a putative link with anxiety. Sci Rep 7(1). https://doi.org/10.1038/S41598-017-08918-7
Hales ST, Gannon TA (2019) Understanding sexual aggression in UK Male University students: an empirical assessment of prevalence and psychological risk factors. Orig Res Article Sex Abuse 0(0):1–27. https://doi.org/10.1177/10790632211051682
Handa RJ, Weiser MJ, Zuloaga DG (2009) A role for the androgen metabolite, 5α-androstane-3β,17β-Diol, in modulating oestrogen receptor β-Mediated regulation of hormonal stress reactivity. J Neuroendocrinol 21(4):351. https://doi.org/10.1111/J.1365-2826.2009.01840.X
Hawkley LC, Cole SW, Capitanio JP, Norman GJ, Cacioppo JT (2012) Effects of social isolation on glucocorticoid regulation in social mammals. Hormones Behav. https://doi.org/10.1016/j.yhbeh.2012.05.011
Heck AL, Handa RJ (2019) Sex differences in the hypothalamic–pituitary–adrenal axis’ response to stress: an important role for gonadal hormones. Neuropsychopharmacology 44(1):45. https://doi.org/10.1038/S41386-018-0167-9
doi: 10.1038/S41386-018-0167-9 pubmed: 30111811
Herman JP, McKlveen JM, Ghosal S, Kopp B, Wulsin A, Makinson R, Scheimann J, Myers B (2016) Regulation of the hypothalamic-pituitary-adrenocortical stress response. Compr Physiol 6(2):603–621. https://doi.org/10.1002/CPHY.C150015
doi: 10.1002/CPHY.C150015 pubmed: 27065163 pmcid: 4867107
Higham JP, Heistermann M, Maestripieri D (2013) The endocrinology of male rhesus macaque social and reproductive status: a test of the challenge and social stress hypotheses. Behav Ecol Sociobiol 67(1):19. https://doi.org/10.1007/S00265-012-1420-6
doi: 10.1007/S00265-012-1420-6 pubmed: 24634561 pmcid: 3950204
Hiller-Sturmhöfel S, Bartke A (1998) The Endocrine System: an overview. Alcohol Health Res World 22(3):153. /pmc/articles/PMC6761896/
Hines M, Constantinescu M, Spencer D (2015) Early androgen exposure and human gender development. Biology Sex Differences 6(1):3. https://doi.org/10.1186/S13293-015-0022-1
doi: 10.1186/S13293-015-0022-1
Hostinar CE, Sullivan RM, Gunnar MR (2014) Psychobiological mechanisms underlying the social buffering of the hypothalamic-pituitary-adrenocortical axis: a review of animal models and human studies across development. Psychol Bull. https://doi.org/10.1037/a0032671
doi: 10.1037/a0032671 pubmed: 23607429
Ip HF, van der Laan CM, Krapohl EML, Brikell I, Sánchez-Mora C, Nolte IM, Pourcain S, Bolhuis B, Palviainen K, Zafarmand T, Colodro-Conde H, Gordon L, Zayats S, Aliev T, Jiang F, Wang C, Saunders CA, Karhunen G, Hammerschlag V, Boomsma AR (2021) Genetic association study of childhood aggression across raters, instruments, and age. Transl Psychiatry 2021 11(1, 11):1–9. https://doi.org/10.1038/s41398-021-01480-x
doi: 10.1038/s41398-021-01480-x
Iwasa T, Matsuzaki T, Yano K, Irahara M (2017) Gonadotropin-inhibitory hormone plays roles in stress-induced reproductive dysfunction. Front Endocrinol 8(APR):62. https://doi.org/10.3389/FENDO.2017.00062/BIBTEX
doi: 10.3389/FENDO.2017.00062/BIBTEX
Jiang Y, Peng T, Gaur U, Silva M, Little P, Chen Z, Qiu W, Zhang Y, Zheng W (2019) Role of corticotropin releasing factor in the neuroimmune mechanisms of depression: examination of current pharmaceutical and herbal therapies. Front Cell Neurosci 0:290. https://doi.org/10.3389/FNCEL.2019.00290
doi: 10.3389/FNCEL.2019.00290
Kelley NJ, Gallucci A, Riva P, Romero Lauro LJ, Schmeichel BJ (2019) Stimulating self-regulation: a review of non-invasive brain stimulation studies of goal-directed behavior. Front Behav Neurosci 0:337. https://doi.org/10.3389/FNBEH.2018.00337
doi: 10.3389/FNBEH.2018.00337
Ketchesin KD, Stinnett GS, Seasholtz AF (2017) Corticotropin-releasing hormone-binding protein and stress: from invertebrates to humans. Stress (Amsterdam, Netherlands) 20(5):449–464. https://doi.org/10.1080/10253890.2017.1322575
KG B, G, M.-N., H G (2016) Early life stress accelerates behavioral and neural maturation of the hippocampus in male mice. Horm Behav 82:64–71. https://doi.org/10.1016/J.YHBEH.2016.04.010
doi: 10.1016/J.YHBEH.2016.04.010
Kirby ED, Muroy SE, Sun WG, Covarrubias D, Leong MJ, Barchas LA, Kaufer D (2013) Acute stress enhances adult rat hippocampal neurogenesis and activation of newborn neurons via secreted astrocytic FGF2. ELife 2013(2). https://doi.org/10.7554/ELIFE.00362
Knight EL, Morales PJ, Christian CB, Prasad S, Harbaugh WT, Mehta PH, Mayr U (2022) The Causal Effect of Testosterone on men’s competitive behavior is moderated by Basal Cortisol and cues to an opponent’s status: evidence for a context-dependent dual hormone hypothesis. J Personal Soc Psychol 123(4):693. https://doi.org/10.1037/PSPA0000305
doi: 10.1037/PSPA0000305
Koning A-SCAM, Buurstede JC, van Weert LTCM, Meijer OC (2019) Glucocorticoid and mineralocorticoid receptors in the brain: a transcriptional perspective. J Endocr Soc 3(10):1917–1930. https://doi.org/10.1210/JS.2019-00158
doi: 10.1210/JS.2019-00158 pubmed: 31598572
Kopin IJ, Eisenhofer G, Goldstein D (1988) Sympathoadrenal medullary system and stress. Adv Exp Med Biol 245:11–23. https://doi.org/10.1007/978-1-4899-2064-5_2
Koolhaas JM, Coppens CM, de Boer SF, Buwalda B, Meerlo P, Timmermans PJA (2013) The resident-intruder paradigm: a standardized test for aggression, violence and social stress. J Vis Exp: JoVE. https://doi.org/10.3791/4367
doi: 10.3791/4367 pubmed: 23852258
Kreuz LE, Rose RM (1972) Assessment of aggressive behavior and plasma testosterone in a young criminal population. Psychosom Med 34(4):321–332. https://doi.org/10.1097/00006842-197207000-00006
doi: 10.1097/00006842-197207000-00006 pubmed: 5074958
Kwak S, Joo WT, Youm Y, Chey J (2018) Social brain volume is associated with in-degree social network size among older adults. Proc R Soc B: Biol Sci. https://doi.org/10.1098/rspb.2017.2708
Lee JY, Cho KS (2013) Chemical castration for sexual offenders: Physicians’ views. J Korean Med Sci 28(2):171. https://doi.org/10.3346/JKMS.2013.28.2.171
doi: 10.3346/JKMS.2013.28.2.171 pubmed: 23401647
Lee AK, Tse FW, Tse A (2015) Arginine Vasopressin Potentiates the stimulatory action of CRH on Pituitary corticotropes via a protein kinase C–Dependent reduction of the background TREK-1 current. Endocrinology 156(10):3661–3672. https://doi.org/10.1210/EN.2015-1293
doi: 10.1210/EN.2015-1293 pubmed: 26248219
Lickley RA, Sebastian CL (2018) The neural basis of reactive aggression and its development in adolescence. Psychol Crime Law 24(3):313–333. https://doi.org/10.1080/1068316x.2017.1420187
Lindell SG, Yuan Q, Zhou Z, Goldman D, Thompson RC, Lopez JF, Suomi SJ, Higley D, J., Barr CS (2012) The serotonin transporter gene is a substrate for age and stress dependent epigenetic regulation in rhesus macaque brain: potential roles in genetic selection and gene × environment interactions. Dev Psychopathol 24(4):1391. https://doi.org/10.1017/S0954579412000788
doi: 10.1017/S0954579412000788 pubmed: 23062305
Liu J, Dietz K, Deloyht JM, Pedre X, Kelkar D, Kaur J, Vialou V, Lobo MK, Dietz DM, Nestler EJ, Dupree J, Casaccia P (2012) Impaired adult myelination in the prefrontal cortex of socially isolated mice. Nat Neurosci. https://doi.org/10.1038/nn.3263
doi: 10.1038/nn.3263 pubmed: 23263443
Liu L, Li J, Qing L, Yan M, Xiong G, Lian X, Hu L, Nie S (2021) Glucocorticoid receptor gene (NR3C1) is hypermethylated in adult males with aggressive behaviour. Int J Legal Med 135(1):43–51. https://doi.org/10.1007/S00414-020-02328-7
doi: 10.1007/S00414-020-02328-7 pubmed: 32577827
Loi M, Mossink JCL, Meerhoff GF, Blaauwen D, Lucassen JL, P. J., Joëls M (2017) Effects of early-life stress on cognitive function and hippocampal structure in female rodents. Neuroscience 342:101–119. https://doi.org/10.1016/J.NEUROSCIENCE.2015.08.024
doi: 10.1016/J.NEUROSCIENCE.2015.08.024 pubmed: 26297897
Lupien SJ, de Leon M, de Santi S, Convit A, Tarshish C, Nair NPV, Thakur M, McEwen BS, Hauger RL, Meaney MJ (1998) Cortisol levels during human aging predict hippocampal atrophy and memory deficits. Nat Neurosci 1(1):69–73. https://doi.org/10.1038/271
McCarty R, Horwatt K, Konarska M (1988) Chronic stress and sympathetic-adrenal medullary responsiveness. Soc Sci Med 26(3):333–341. https://doi.org/10.1016/0277-9536(88)90398-x
Madrid JE, Mandalaywala TM, Coyne SP, Ahloy-Dallaire J, Garner JP, Barr CS, Maestripieri D, Parker KJ (2018) Adaptive developmental plasticity in rhesus macaques: the serotonin transporter gene interacts with maternal care to affect juvenile social behaviour. Proc Royal Soc B: Biol Sci 285(1881). https://doi.org/10.1098/RSPB.2018.0541
Maggi R, Cariboni AM, Marelli MM, Moretti RM, Andrè V, Marzagalli M, Limonta P (2016) GnRH and GnRH receptors in the pathophysiology of the human female reproductive system. Hum Reprod Update 22(3):358–381. https://doi.org/10.1093/humupd/dmv059
Mbiydzenyuy NE, Hemmings SMJ, Qulu L (2022) Prenatal maternal stress and offspring aggressive behavior: intergenerational and transgenerational inheritance. Front Behav Neurosci 16:977416. https://doi.org/10.3389/FNBEH.2022.977416/BIBTEX
Miczek KA, Fish EW, De Bold JF (2003) Neurosteroids, GABAA receptors, and escalated aggressive behavior. Horm Behav 44(3):242–257. https://doi.org/10.1016/J.YHBEH.2003.04.002
Manes F, Sahakian B, Clark L, Rogers R, Antoun N, Aitken M, Robbins T (2002) Decision-making processes following damage to the prefrontal cortex. Brain 125(3):624–639. https://doi.org/10.1093/brain/awf049
Mark MD, Wollenweber P, Gesk A, Kösters K, Batzke K, Janoschka C, Maejima T, Han J, Deneris ES, Herlitze S (2019) RGS2 drives male aggression in mice via the serotonergic system. Commun Biol 2(1). https://doi.org/10.1038/S42003-019-0622-0
Martínez-Sanchis S, Salvador A, Moya-Albiol L, Ganzález-Bono E, Simón VM (1998) Effects of chronic treatment with testosterone propionate on aggression and hormonal levels in intact male mice. Psychoneuroendocrinology 23(3):275–293. https://doi.org/10.1016/S0306-4530(98)00005-5
McBurnett K, Lahey BB, Rathouz PJ, Loeber R (2000) Low salivary cortisol and persistent aggression in boys referred for disruptive behavior. Arch Gen Psychiatry 57(1):38–43. https://doi.org/10.1001/ARCHPSYC.57.1.38
doi: 10.1001/ARCHPSYC.57.1.38 pubmed: 10632231
Mechler K, Banaschewski T, Hohmann S, Häge A (2022) Evidence-based pharmacological treatment options for ADHD in children and adolescents. Pharmacol Ther 230:107940. https://doi.org/10.1016/J.PHARMTHERA.2021.107940
Mehta PH, Josephs RA (2010) Testosterone and cortisol jointly regulate dominance: evidence for a dual-hormone hypothesis. Horm Behav 58(5):898–906. https://doi.org/10.1016/J.YHBEH.2010.08.020
doi: 10.1016/J.YHBEH.2010.08.020 pubmed: 20816841
Meruelo AD, Timmins MA, Irwin MR, Coccaro EF (2023) Salivary cortisol awakening levels are reduced in human subjects with intermittent explosive disorder compared with controls. Psychoneuroendocrinology 151:106070. https://doi.org/10.1016/J.PSYNEUEN.2023.106070
Montoya ER, Terburg D, Bos PA, van Honk J (2012) Testosterone, cortisol, and serotonin as key regulators of social aggression: a review and theoretical perspective. Motivation Emot 36(1):65–73. https://doi.org/10.1007/S11031-011-9264-3/FIGURES/1
Morinan A, Leonard BE (1980) Some anatomical and physiological correlates of social isolation in the young rat. Physiol Behav. https://doi.org/10.1016/0031-9384(80)90265-6
Munley KM, Rendon NM, Demas GE (2018) Neural androgen synthesis and aggression: insights from a seasonally breeding rodent. Front Endocrinol 9(APR):136. https://doi.org/10.3389/FENDO.2018.00136/BIBTEX
Muñoz-Reyes JA, Polo P, Valenzuela N, Pavez P, Ramírez-Herrera O, Figueroa O, Rodriguez-Sickert C, Díaz D, Pita M (2020) The male warrior hypothesis: testosterone-related cooperation and aggression in the context of intergroup conflict. Sci Rep 10(1):1. https://doi.org/10.1038/s41598-019-57259-0
Murison R (2016) The neurobiology of stress. Neurosci Pain Stress Emot 29–49. https://doi.org/10.1016/B978-0-12-800538-5.00002-9
Murphy F, Nasa A, Cullinane D, Raajakesary K, Gazzaz A, Sooknarine V, Haines M, Roman E, Kelly L, O’Neill A, Cannon M, Roddy DW (2022) Childhood trauma, the HPA Axis and psychiatric illnesses: a targeted literature synthesis. Front Psychiatry 13:748372. https://doi.org/10.3389/FPSYT.2022.748372
Neumann ID, Veenema AH, Beiderbeck DI (2010) Aggression and anxiety: social context and neurobiological links. Front Behav Neurosci 4(MAR):12. https://doi.org/10.3389/FNBEH.2010.00012/BIBTEX
Nicolaides NC, Chrousos G, Kino T (2020) Glucocorticoid receptor. Encycl Endocr Dis 104–111. https://www.ncbi.nlm.nih.gov/books/NBK279171/
Nordman JC, Ma X, Gu Q, Potegal M, Li H, Kravitz AV, Li Z (2020) Potentiation of divergent medial amygdala pathways drives experience-dependent aggression escalation. J Neurosci 40(25):4858–4880. https://doi.org/10.1523/JNEUROSCI.0370-20.2020
Notari L, Kirton R, Mills DS (2022) Psycho-behavioural changes in dogs treated with corticosteroids: a clinical behaviour perspective. Anim 12(5):592. https://doi.org/10.3390/ANI12050592
O’donnell C, Demler TL, Trigoboff E (2022) Selective serotonin reuptake inhibitors (SSRIs) and their effect on patient aggression in adult patients in a state psychiatric facility: a retrospective analysis. Innov Clin Neurosci 19(1–3):33. /pmc/articles/PMC8970236/
Oliveira GA, Uceda S, Oliveira TF, Fernandes AC, Garcia-Marques T, Oliveira RF (2014) Testosterone response to competition in males is unrelated to opponent familiarity or threat appraisal. Front Psychol 5(NOV). https://doi.org/10.3389/FPSYG.2014.01240
Ong W-Y, Stohler CS, Herr DR (2019) Role of the prefrontal cortex in pain processing. Mol Neurobiol 56(2):1137. https://doi.org/10.1007/S12035-018-1130-9
Papargiris MM, Rivalland ETA, Hemsworth PH, Morrissey AD, Tilbrook AJ (2011) Acute and chronic stress-like levels of cortisol inhibit the oestradiol stimulus to induce sexual receptivity but have no effect on sexual attractivity or proceptivity in female sheep. Horm Behav 60(4):336–345. https://doi.org/10.1016/j.yhbeh.2011.06.008
Parihar VK, Hattiangady B, Kuruba R, Shuai B, Shetty AK (2011) Predictable chronic mild stress improves mood, hippocampal neurogenesis and memory. Mol Psychiatry 16(2):171–183. https://doi.org/10.1038/MP.2009.130
Pierce BN, Hemsworth PH, Rivalland ETA, Wagenmaker ER, Morrissey AD, Papargiris MM, Clarke IJ, Karsch FJ, Turner AI, Tilbrook AJ (2008) Psychosocial stress suppresses attractivity, proceptivity and pulsatile LH secretion in the ewe. Horm Behav 54(3):424–434. https://doi.org/10.1016/J.YHBEH.2008.04.005
Pierce BN, Stackpole CA, Breen KM, Clarke IJ, Karsch FJ, Rivalland ETA, Turner AI, Caddy DJ, Wagenmaker ER, Oakley AE, Tilbrook AJ (2009) Estradiol enables cortisol to act directly upon the pituitary to suppress pituitary responsiveness to GnRH in sheep. Neuroendocrinology 89(1):86–97. https://doi.org/10.1159/000151543
Rada RT, Laws DR, Kellner R (1976) Plasma testosterone levels in the rapist. Psychosom Med 38(4):257–268. https://doi.org/10.1097/00006842-197607000-00004
Rejeski WJ, Brubaker PH, Herb RA, Kaplan JR, Koritnik D (1988) Anabolic steroids and aggressive behavior in cynomolgus monkeys. J Behav Med 11(1):95–105. https://doi.org/10.1007/BF00846172/METRICS
Rider CV, Boekelheide K, Catlin N, Gordon CJ, Morata T, Selgrade MK, Sexton K, Simmons JE (2014) Cumulative risk: Toxicity and interactions of physical and chemical stressors. Toxicological Sciences: An Official Journal of the Society of Toxicology 137(1):3–11. https://doi.org/10.1093/toxsci/kft228
Rigney N, de Vries GJ, Petrulis A, Young LJ (2022) Oxytocin, vasopressin, and social behavior: from neural circuits to clinical opportunities. Endocrinology 163(9):bqac111. https://doi.org/10.1210/endocr/bqac111
Roper J, O'Carroll AM, Young W 3rd, Lolait S (2011) The vasopressin Avpr1b receptor: molecular and pharmacological studies. Stress 14(1):98–115. https://doi.org/10.3109/10253890.2010.512376
Sandnabba NK, Lagerspetz KMJ, Jensen E (1994) Effects of testosterone exposure and fighting experience on the aggressive behavior of female and male mice selectively bred for intermale aggression. Horm Behav 28(3):219–231. https://doi.org/10.1006/HBEH.1994.1019
Santi D, Crépieux P, Reiter E, Spaggiari G, Brigante G, Casarini L, Rochira V, Simoni M (2020) Follicle-Stimulating Hormone (FSH) action on spermatogenesis: a focus on physiological and therapeutic roles. J Clin Med 9(4). https://doi.org/10.3390/JCM9041014
Selye H (1936) A syndrome produced by diverse nocuous agents. Nature 1936 138(3479):32–32. https://doi.org/10.1038/138032a0
Senst L, Bains J (2014) Neuromodulators, stress and plasticity: a role for endocannabinoid signalling. J Exp Biol 217(1):102–108
doi: 10.1242/jeb.089730 pubmed: 24353209
Sheng JA, Bales NJ, Myers SA, Bautista AI, Roueinfar M, Hale TM, Handa RJ (2021a) The hypothalamic-pituitary-adrenal axis: development, programming actions of hormones, and maternal-fetal interactions. Front Behav Neurosci 14:256. https://doi.org/10.3389/FNBEH.2020.601939/BIBTEX
doi: 10.3389/FNBEH.2020.601939/BIBTEX
Sheng JA, Bales NJ, Myers SA, Bautista AI, Roueinfar M, Hale TM, Handa RJ (2021b) The hypothalamic-pituitary-adrenal axis: development, programming actions of hormones, and maternal-fetal interactions. Front Behav Neurosci 14. https://doi.org/10.3389/FNBEH.2020.601939
Siever LJ (2008) Neurobiology of aggression and violence. Am J Psychiatry 165(4):429. https://doi.org/10.1176/APPI.AJP.2008.07111774
doi: 10.1176/APPI.AJP.2008.07111774 pubmed: 18346997
Šimić G, Tkalčić M, Vukić V, Mulc D, Španić E, Šagud M, Olucha-Bordonau FE, Vukšić M, Hof PR (2021) Understanding emotions: origins and roles of the Amygdala. Biomolecules 11(6). https://doi.org/10.3390/BIOM11060823
Sladek CD, Somponpun SJ (2008) Estrogen receptors: their roles in regulation of vasopressin release for maintenance of fluid and electrolyte homeostasis. Front Neuroendocr 29(1):114–127. https://doi.org/10.1016/J.YFRNE.2007.08.005
Smagin DA, Park J-H, Michurina TV, Peunova N, Glass Z, Sayed K, Bondar NP, Kovalenko IN, Kudryavtseva NN, Enikolopov G (2015) Altered hippocampal neurogenesis and amygdalar neuronal activity in adult mice with repeated experience of aggression. Front NeuroSci 9(DEC):443. https://doi.org/10.3389/FNINS.2015.00443
Studer LH, Aylwin AS, Reddon JR (2005) Testosterone, sexual offense recidivism, and treatment effect among adult male sex offenders. Sex Abuse 17(2):171–181. https://doi.org/10.1177/107906320501700207
doi: 10.1177/107906320501700207 pubmed: 15974423
Surget A, Belzung C (2021) Adult hippocampal neurogenesis shapes adaptation and improves stress response: a mechanistic and integrative perspective. Mol Psychiatry 2021 27(1):403–421. https://doi.org/10.1038/s41380-021-01136-8
Takahashi A, Miczek KA (2014) Neurogenetics of aggressive behavior– studies in rodents. Curr Top Behav Neurosci 17:3. https://doi.org/10.1007/7854_2013_263
doi: 10.1007/7854_2013_263 pubmed: 24318936 pmcid: 4092042
Takahashi A, Quadros IM, de Almeida RMM, Miczek KA (2012) Behavioral and pharmacogenetics of aggressive behavior. Curr Top Behav Neurosci 12:73. https://doi.org/10.1007/7854_2011_191
Toufexis D, Rivarola MA, Lara H, Viau V (2014) Stress and the reproductive axis. J Neuroendocrinol 26(9):573. https://doi.org/10.1111/JNE.12179
Trifu SC, Tudor A, Radulescu I (2020) Aggressive behavior in psychiatric patients in relation to hormonal imbalance (review). Exp Ther Med 20(4):3483. https://doi.org/10.3892/ETM.2020.8974
Tsai SJ (2018) Critical Issues in BDNF Val66Met genetic studies of neuropsychiatric disorders. Front Mol Neurosci 11:156. https://doi.org/10.3389/fnmol.2018.00156
Tseligkaridou G, Egger ST, Spiller TR, Schneller L, Frauenfelder F, Vetter S, Seifritz E, Burrer A (2023) Relationship between antipsychotic medication and aggressive events in patients with a psychotic disorder hospitalized for treatment. BMC Psychiatry 23(1):1–10. https://doi.org/10.1186/S12888-023-04692-1/TABLES/4
doi: 10.1186/S12888-023-04692-1/TABLES/4
Tsigos C, Chrousos GP (2002) Hypothalamic-pituitary-adrenal axis, neuroendocrine factors and stress. J Psychosom Res. https://doi.org/10.1016/S0022-3999(02)00429-4
doi: 10.1016/S0022-3999(02)00429-4 pubmed: 12377295
Vaeroy H, Schneider F, Fetissov SO (2019) Neurobiology of Aggressive Behavior—Role of autoantibodies reactive with stress-related peptide hormones. Front Psychiatry. 10 https://doi.org/10.3389/FPSYT.2019.00872
doi: 10.3389/FPSYT.2019.00872 pubmed: 31866881
Vandael D, Gounko NV (2019) Corticotropin releasing factor-binding protein (CRF-BP) as a potential new therapeutic target in Alzheimer’s disease and stress disorders. Transl Psychiatry 9(1). https://doi.org/10.1038/S41398-019-0581-8
Van Erp AMM, Miczek KA (2000) Aggressive behavior, increased Accumbal dopamine, and decreased cortical serotonin in rats. J Neurosci 20(24):9320. https://doi.org/10.1523/JNEUROSCI.20-24-09320.2000
doi: 10.1523/JNEUROSCI.20-24-09320.2000 pubmed: 11125011
van Wingen G, Mattern C, Verkes RJ, Buitelaar J, Fernández G (2010) Testosterone reduces amygdala-orbitofrontal cortex coupling. Psychoneuroendocrinology 35(1):105–113. https://doi.org/10.1016/J.PSYNEUEN.2009.09.007
doi: 10.1016/J.PSYNEUEN.2009.09.007 pubmed: 19782476
Vasconcelos M, Stein DJ, Gallas-Lopes M, Landau L, de Almeida RMM (2020) Corticotropin-releasing factor receptor signaling and modulation: implications for stress response and resilience. Trends Psychiatry Psychother 42(2):195–206. https://doi.org/10.1590/2237-6089-2018-0027
Veer IM, Oei NYL, Spinhoven P, Van Buchem MA, Elzinga BM, Rombouts SARB (2012) Endogenous cortisol is associated with functional connectivity between the amygdala and medial prefrontal cortex. Psychoneuroendocrinology 37(7):1039–1047. https://doi.org/10.1016/J.PSYNEUEN.2011.12.001
doi: 10.1016/J.PSYNEUEN.2011.12.001 pubmed: 22204928
Viau V (2002) Functional cross-talk between the hypothalamic-pituitary-gonadal and -adrenal axes. J Neuroendocrinol 14(6):506–513. https://doi.org/10.1046/J.1365-2826.2002.00798.X
Viho EMG, Buurstede JC, Mahfouz A, Koorneef LL, van Weert LTCM, Houtman R, Hunt HJ, Kroon J, Meijer OC (2019) Corticosteroid action in the brain: the potential of selective receptor modulation. Neuroendocrinology 109(3):266–276. https://doi.org/10.1159/000499659
Volman I, von Borries AKL, Bulten BH, Verkes RJ, Toni I, Roelofs K (2016) Testosterone modulates altered prefrontal control of emotional actions in psychopathic offenders. ENeuro 3(1):52–60. https://doi.org/10.1523/eneuro.0107-15.2016
Westphal NJ, Seasholtz AF (2005) Gonadotropin-releasing hormone (GnRH) positively regulates corticotropin-releasing hormone-binding protein expression via multiple intracellular signaling pathways and a multipartite GnRH response element in alphaT3-1 cells. Mol Endocrinol 19(11):2780–2797. https://doi.org/10.1210/ME.2004-0519
Won E, Kim Y-K (2016) Stress, the autonomic nervous system, and the immune-kynurenine pathway in the etiology of depression. Curr Neuropharmacol 14(7):665. https://doi.org/10.2174/1570159X14666151208113006
Wong JS, Gravel J (2018) Do sex offenders have higher levels of testosterone? Results from a meta-analysis. Sexual Abuse: A Journal of Research and Treatment 30(2):147–168. https://doi.org/10.1177/1079063216637857
World Health Organization (2011) Chapter 6: sexual violence. World Report on Violence and Health
Wright P, Albarracin D, Brown RD, Li H, He G, Liu Y (2008) Dissociated responses in the amygdala and orbitofrontal cortex to bottom-up and top-down components of emotional evaluation. NeuroImage 39(2):894–902. https://doi.org/10.1016/J.NEUROIMAGE.2007.09.014
Zaman H, Sampson SJ, Beck ALS, Sharma T, Clay FJ, Spyridi S, Zhao S, Gillies D (2017) Benzodiazepines for psychosis-induced aggression or agitation. Cochrane Database Syst Rev 2017(12). https://doi.org/10.1002/14651858.CD003079.PUB4
Zhou JN, Fang H (2018) Transcriptional regulation of corticotropin-releasing hormone gene in stress response. IBRO Rep 5:137–146. https://doi.org/10.1016/J.IBROR.2018.08.003
Zitzmann M (2020) Testosterone, mood, behaviour and quality of life. Andrology 8(6):1598–1605. https://doi.org/10.1111/ANDR.12867
doi: 10.1111/ANDR.12867 pubmed: 32657051
Zuloaga DG, Heck AL, De Guzman RM, Handa RJ (2020) Roles for androgens in mediating the sex differences of neuroendocrine and behavioral stress responses. Biol Sex Differ 11(1):1–18. https://doi.org/10.1186/S13293-020-00319-2/FIGURES/2

Auteurs

Ngala Elvis Mbiydzenyuy (NE)

Basic Science Department, School of Medicine, Copperbelt University, P.O Box 71191, Ndola, Zambia.
Division of Medical Physiology, Biomedical Science Research Institute, Stellenbosch University, Private Bag X1, Matieland, 7602, Cape Town, South Africa.

Lihle-Appiah Qulu (LA)

Division of Medical Physiology, Biomedical Science Research Institute, Stellenbosch University, Private Bag X1, Matieland, 7602, Cape Town, South Africa. qulul@sun.ac.za.

Classifications MeSH