Scientific Papers

Sex influences the effects of social status on socioemotional behavior and serotonin neurochemistry in rhesus monkeys | Biology of Sex Differences


  • Mauvais-Jarvis F, Bairey Merz N, Barnes PJ, Brinton RD, Carrero JJ, DeMeo DL, et al. Sex and gender: modifiers of health, disease, and medicine. Lancet. 2020;396(10250):565–82. https://doi.org/10.1016/S0140-6736(20)31561-0.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Piccinelli M, Wilkinson G. Gender differences in depression. Critical review. Br J Psychiatry. 2000;177:486–92.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Altemus M, Sarvaiya N, Neill EC. Sex differences in anxiety and depression clinical perspectives. Front Neuroendocrinol. 2014;35(3):320–30. https://doi.org/10.1016/j.yfrne.2014.05.004.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kessler RC, McGonagle KA, Swartz M, Blazer DG, Nelson CB. Sex and depression in the National Comorbidity Survey. I: lifetime prevalence, chronicity and recurrence. J Affect Disord. 1993;29(2–3):85–96.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Kessler RC, McGonagle KA, Zhao S, Nelson CB, Hughes M, Eshleman S, et al. Lifetime and 12-month prevalence of DSM-III-R psychiatric disorders in the United States. Results from the National Comorbidity Survey. Arch Gen Psychiatry. 1994;51(1):8–19.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Werling DM, Geschwind DH. Sex differences in autism spectrum disorders. Curr Opin Neurol. 2013;26(2):146–53. https://doi.org/10.1097/WCO.0b013e32835ee548.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Shansky RM, Murphy AZ. Considering sex as a biological variable will require a global shift in science culture. Nat Neurosci. 2021;24(4):457–64. https://doi.org/10.1038/s41593-021-00806-8.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Bernstein IS, Gordon TP. The function of aggression in primate societies. Am Sci. 1974;62(3):304–11.

    CAS 
    PubMed 

    Google Scholar
     

  • Fernald RD. Communication about social status. Curr Opin Neurobiol. 2014;28:1–4. https://doi.org/10.1016/j.conb.2014.04.004.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Terranova JI, Ferris CF, Albers HE. Sex differences in the regulation of offensive aggression and dominance by arginine-vasopressin. Front Endocrinol (Lausanne). 2017;8:308. https://doi.org/10.3389/fendo.2017.00308.

    Article 
    PubMed 

    Google Scholar
     

  • Morrison KE, Bader LR, Clinard CT, Gerhard DM, Gross SE, Cooper MA. Maintenance of dominance status is necessary for resistance to social defeat stress in Syrian hamsters. Behav Brain Res. 2014;270:277–86. https://doi.org/10.1016/j.bbr.2014.05.041.

    Article 
    PubMed 

    Google Scholar
     

  • Morrison KE, Swallows CL, Cooper MA. Effects of dominance status on conditioned defeat and expression of 5-HT1A and 5-HT2A receptors. Physiol Behav. 2011;104(2):283–90. https://doi.org/10.1016/j.physbeh.2011.02.033.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Michopoulos V, Higgins M, Toufexis D, Wilson ME. Social subordination produces distinct stress-related phenotypes in female rhesus monkeys. Psychoneuroendocrinology. 2012;37(7):1071–85. https://doi.org/10.1016/j.psyneuen.2011.12.004.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Michopoulos V, Reding KM, Wilson ME, Toufexis D. Social subordination impairs hypothalamic-pituitary-adrenal function in female rhesus monkeys. Horm Behav. 2012;62(4):389–99. https://doi.org/10.1016/j.yhbeh.2012.07.014.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ravi M, Miller AH, Michopoulos V. The immunology of stress and the impact of inflammation on the brain and behavior. BJPsych Adv. 2021;27(Suppl 3):158–65. https://doi.org/10.1192/bja.2020.82.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Michopoulos V, Vester A, Neigh G. Posttraumatic stress disorder: a metabolic disorder in disguise? Exp Neurol. 2016;284(Pt B):220–9. https://doi.org/10.1016/j.expneurol.2016.05.038.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Terranova JI, Song Z, Larkin TE 2nd, Hardcastle N, Norvelle A, Riaz A, et al. Serotonin and arginine-vasopressin mediate sex differences in the regulation of dominance and aggression by the social brain. Proc Natl Acad Sci USA. 2016;113(46):13233–8. https://doi.org/10.1073/pnas.1610446113.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Chaouloff F, Berton O, Mormede P. Serotonin and stress. Neuropsychopharmacology. 1999;21(2 Suppl):28S-32S. https://doi.org/10.1016/S0893-133X(99)00008-1.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Drevets WC, Frank E, Price JC, Kupfer DJ, Greer PJ, Mathis C. Serotonin type-1A receptor imaging in depression. Nucl Med Biol. 2000;27(5):499–507.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Drevets WC, Thase ME, Moses-Kolko EL, Price J, Frank E, Kupfer DJ, et al. Serotonin-1A receptor imaging in recurrent depression: replication and literature review. Nucl Med Biol. 2007;34(7):865–77.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Jayamohananan H, Manoj Kumar MK, Aneesh TP. 5-HIAA as a potential biological marker for neurological and psychiatric disorders. Adv Pharm Bull. 2019;9(3):374–81. https://doi.org/10.15171/apb.2019.044.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lanzenberger RR, Mitterhauser M, Spindelegger C, Wadsak W, Klein N, Mien LK, et al. Reduced serotonin-1A receptor binding in social anxiety disorder. Biol Psychiatry. 2007;61(9):1081–9. https://doi.org/10.1016/j.biopsych.2006.05.022.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Neumeister A, Bain E, Nugent AC, Carson RE, Bonne O, Luckenbaugh DA, et al. Reduced serotonin type 1A receptor binding in panic disorder. J Neurosci. 2004;24(3):589–91. https://doi.org/10.1523/JNEUROSCI.4921-03.2004.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • O’Connell LA, Hofmann HA. The vertebrate mesolimbic reward system and social behavior network: a comparative synthesis. J Comp Neurol. 2011;519(18):3599–639. https://doi.org/10.1002/cne.22735.

    Article 
    PubMed 

    Google Scholar
     

  • Grieb ZA, Ross AP, McCann KE, Lee S, Welch M, Gomez MG, et al. Sex-dependent effects of social status on the regulation of arginine-vasopressin (AVP) V1a, oxytocin (OT), and serotonin (5-HT) 1A receptor binding and aggression in Syrian hamsters (Mesocricetus auratus). Horm Behav. 2021;127: 104878. https://doi.org/10.1016/j.yhbeh.2020.104878.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Summers CH, Korzan WJ, Lukkes JL, Watt MJ, Forster GL, Overli O, et al. Does serotonin influence aggression? Comparing regional activity before and during social interaction. Physiol Biochem Zool. 2005;78(5):679–94.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Eisenreich BR, Szalda-Petree A. Behavioral effects of fluoxetine on aggression and associative learning in Siamese fighting fish (Betta splendens). Behav Processes. 2015;121:37–42. https://doi.org/10.1016/j.beproc.2015.10.008.

    Article 
    PubMed 

    Google Scholar
     

  • Ricci LA, Melloni RH Jr. Repeated fluoxetine administration during adolescence stimulates aggressive behavior and alters serotonin and vasopressin neural development in hamsters. Behav Neurosci. 2012;126(5):640–53. https://doi.org/10.1037/a0029761.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ferris CF. Serotonin diminishes aggression by suppressing the activity of the vasopressin system. Ann N Y Acad Sci. 1996;794:98–103. https://doi.org/10.1111/j.1749-6632.1996.tb32513.x.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Fuller RW. Fluoxetine effects on serotonin function and aggressive behavior. Ann N Y Acad Sci. 1996;794:90–7. https://doi.org/10.1111/j.1749-6632.1996.tb32512.x.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Huhman KL, Solomon MB, Janicki M, Harmon AC, Lin SM, Israel JE, et al. Conditioned defeat in male and female Syrian hamsters. Horm Behav. 2003;44(3):293–9.

    Article 
    PubMed 

    Google Scholar
     

  • Voisin DA, Wakeford A, Nye J, Mun J, Jones SR, Locke J, et al. Sex and social status modify the effects of fluoxetine on socioemotional behaviors in Syrian hamsters and rhesus macaques. Pharmacol Biochem Behav. 2022;215: 173362. https://doi.org/10.1016/j.pbb.2022.173362.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sade DS. Determinants of dominance in a group of freeranging rhesus monkeys. In: Altmann SA, editor. Social communication among primates. Chicago: University of Chicago Press; 1967. p. 99–111.


    Google Scholar
     

  • Snyder-Mackler N, Sanz J, Kohn JN, Brinkworth JF, Morrow S, Shaver AO, et al. Social status alters immune regulation and response to infection in macaques. Science (New York, NY). 2016;354(6315):1041–5. https://doi.org/10.1126/science.aah3580.

    Article 
    CAS 

    Google Scholar
     

  • Michopoulos V, Perez Diaz M, Embree M, Reding K, Votaw JR, Mun J, et al. Oestradiol alters central 5-HT1A receptor binding potential differences related to psychosocial stress but not differences related to 5-HTTLPR genotype in female rhesus monkeys. J Neuroendocrinol. 2014;26(2):80–8. https://doi.org/10.1111/jne.12129.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Shively CA, Register TC, Friedman DP, Morgan TM, Thompson J, Lanier T. Social stress-associated depression in adult female cynomolgus monkeys (Macaca fascicularis). Biol Psychol. 2005;69(1):67–84.

    Article 
    PubMed 

    Google Scholar
     

  • Embree M, Michopoulos V, Votaw JR, Voll RJ, Mun J, Goodman MM, et al. Delayed puberty affects developmental changes in serotonin receptor 1A (5Ht1A) binding potential in female rhesus macaque brain. Biol Psychiat. 2013;73(9):39S.


    Google Scholar
     

  • McKittrick CR, Blanchard DC, Blanchard RJ, McEwen BS, Sakai RR. Serotonin receptor binding in a colony model of chronic social stress. Biol Psychiat. 1995;37(6):383–93. https://doi.org/10.1016/0006-3223(94)00152-s.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Michopoulos V, Powers A, Gillespie CF, Ressler KJ, Jovanovic T. Inflammation in fear- and anxiety-based disorders: PTSD, GAD, and beyond. Neuropsychopharmacology. 2017;42(1):254–70. https://doi.org/10.1038/npp.2016.146.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Jarrell H, Hoffman JB, Kaplan JR, Berga S, Kinkead B, Wilson ME. Polymorphisms in the serotonin reuptake transporter gene modify the consequences of social status on metabolic health in female rhesus monkeys. Physiol Behav. 2008;93(4–5):807–19.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Walker ML, Wilson ME, Gordon TP. Endocrine control of the seasonal occurrence of ovulation in rhesus monkeys housed outdoors. Endocrinology. 1984;114(4):1074–81.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Bernstein IS, Gordon TP, Rose RM. Aggression and social controls in rhesus monkey (Macaca mulatta) groups revealed in group formation studies. Folia Primatol (Basel). 1974;21(2):81–107.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Gammell MP, de Vries H, Jennings DJ, Carlin CM, Hayden TJ. David’s score: a more appropriate dominance ranking method than Clutton-Brock et al.’s index. Animal Behav. 2003;66(3):601–5. https://doi.org/10.1006/anbe.2003.2226.

    Article 

    Google Scholar
     

  • de Vries H, Stevens JMG, Vervaecke H. Measuring and testing the steepness of dominance hierarchies. Anim Behav. 2006;71(3):585–92. https://doi.org/10.1016/j.anbehav.2005.05.015.

    Article 

    Google Scholar
     

  • Shively CA. Social subordination stress, behavior, and central monoaminergic function in female cynomolgus monkeys. Biol Psychiat. 1998;44(9):882–91.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Troisi A. Displacement activities as a behavioral measure of stress in nonhuman primates and human subjects. Stress (Amsterdam, Netherlands). 2002;5(1):47–54.

    Article 
    PubMed 

    Google Scholar
     

  • Graves FC, Wallen K. Androgen-induced yawning in rhesus monkey females is reversed with a nonsteroidal anti-androgen. Horm Behav. 2006;49(2):233–6.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Embree M, Michopoulos V, Votaw JR, Voll RJ, Mun J, Stehouwer JS, et al. The relation of developmental changes in brain serotonin transporter (5HTT) and 5HT1A receptor binding to emotional behavior in female rhesus monkeys: effects of social status and 5HTT genotype. Neuroscience. 2013;228:83–100. https://doi.org/10.1016/j.neuroscience.2012.10.016.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Krajnak K, Rosewell KL, Duncan MJ, Wise PM. Aging, estradiol and time of day differentially affect serotonin transporter binding in the central nervous system of female rats. Brain Res. 2003;990(1–2):87–94.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Parr LA, Boudreau M, Hecht E, Winslow JT, Nemeroff CB, Sanchez MM. Early life stress affects cerebral glucose metabolism in adult rhesus monkeys (Macaca mulatta). Dev Cogn Neurosci. 2012;2(1):181–93. https://doi.org/10.1016/j.dcn.2011.09.003.

    Article 
    PubMed 

    Google Scholar
     

  • Saleem KS, Logothetis N. A combined MRI and histology atlas of the rhesus monkey brain in stereotaxic coordinates. London, Burlington, MA: Academic Press; 2007.


    Google Scholar
     

  • Paxinos G, Huang X-F, Toga AW. The rhesus monkey brain in sterotaxic coordinates. San Diego: Academic Press; 2000.


    Google Scholar
     

  • Rohlfing T, Kroenke CD, Sullivan EV, Dubach MF, Bowden DM, Grant KA, et al. The INIA19 template and NeuroMaps Atlas for primate brain image parcellation and spatial normalization. Front Neuroinform. 2012;6:27. https://doi.org/10.3389/fninf.2012.00027.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Shi Y, Budin F, Yapuncich E, Rumple A, Young JT, Payne C, et al. UNC-emory infant atlases for macaque brain image analysis: postnatal brain development through 12 months. Front Neurosci. 2016;10:617. https://doi.org/10.3389/fnins.2016.00617.

    Article 
    PubMed 

    Google Scholar
     

  • Lammertsma AA, Hume SP. Simplified reference tissue model for PET receptor studies. Neuroimage. 1996;4(3 Pt 1):153–8. https://doi.org/10.1006/nimg.1996.0066.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Mehlman PT, Higley JD, Fernald BJ, Sallee FR, Suomi SJ, Linnoila M. CSF 5-HIAA, testosterone, and sociosexual behaviors in free-ranging male rhesus macaques in the mating season. Psychiatry Res. 1997;72(2):89–102. https://doi.org/10.1016/s0165-1781(97)00084-x.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Michopoulos V, Checchi M, Sharpe D, Wilson ME. Estradiol effects on behavior and serum oxytocin are modified by social status and polymorphisms in the serotonin transporter gene in female rhesus monkeys. Horm Behav. 2011;59(4):528–35. https://doi.org/10.1016/j.yhbeh.2011.02.002.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Thierry B, Iwaniuk AN, Pellis SM. The influence of phylogeny on the social behaviour of macaques (Primates: Cercopithecidae, genus Macaca). Ethology. 2000;106(8):713–28.

    Article 

    Google Scholar
     

  • Balasubramaniam KN, Beisner BA, McCowan B, Bloomsmith MA. Female social structure influences, and is influenced by, male introduction and integration success among captive rhesus macaques (Macaca mulatta). Behaviour. 2021;158(11):1007–42. https://doi.org/10.1163/1568539x-bja10109.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Balasubramaniam KN, Dittmar K, Berman CM, Butovskaya M, Cooper MA, Majolo B, et al. Hierarchical steepness and phylogenetic models: phylogenetic signals in Macaca. Anim Behav. 2012;83(5):1207–18. https://doi.org/10.1016/j.anbehav.2012.02.012.

    Article 

    Google Scholar
     

  • Balasubramaniam KN, Dittmar K, Berman CM, Butovskaya M, Cooper MA, Majolo B, et al. Hierarchical steepness, counter-aggression, and macaque social style scale. Am J Primatol. 2012;74(10):915–25. https://doi.org/10.1002/ajp.22044.

    Article 
    PubMed 

    Google Scholar
     

  • Sueur C, Petit O, De Marco A, Jacobs AT, Watanabe K, Thierry B. A comparative network analysis of social style in macaques. Anim Behav. 2011;82(4):845–52. https://doi.org/10.1016/j.anbehav.2011.07.020.

    Article 

    Google Scholar
     

  • Gartland KN, Brand CM, Ulibarri LR, White FJ. Variation in adult male-juvenile affiliative behavior in Japanese Macaques (Macaca fuscata). Folia Primatol (Basel). 2020;91(6):610–21. https://doi.org/10.1159/000508761.

    Article 
    PubMed 

    Google Scholar
     

  • Reding K, Michopoulos V, Wallen K, Sanchez M, Wilson ME, Toufexis D. Social status modifies estradiol activation of sociosexual behavior in female rhesus monkeys. Horm Behav. 2012;62(5):612–20. https://doi.org/10.1016/j.yhbeh.2012.09.010.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Balasubramaniam KN, Dunayer ES, Gilhooly LJ, Rosenfield KA, Berman CM. Group size, contest competition, and social structure in Cayo Santiago rhesus macaques. Behaviour. 2014;151(12–13):1759–98. https://doi.org/10.1163/1568539X-00003216.

    Article 

    Google Scholar
     

  • Bercovitch FB. Dominance rank and reproductive maturation in male rhesus macaques (Macaca mulatta). J Reprod Fertil. 1993;99(1):113–20. https://doi.org/10.1530/jrf.0.0990113.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Arce M, Michopoulos V, Shepard KN, Ha Q-C, Wilson ME. Diet choice, cortisol reactivity, and emotional feeding in socially housed rhesus monkeys. Physiol Behav. 2010;101(4):446–55. https://doi.org/10.1016/j.physbeh.2010.07.010.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wilson ME, Fisher J, Fischer A, Lee V, Harris RB, Bartness TJ. Quantifying food intake in socially housed monkeys: social status effects on caloric consumption. Physiol Behav. 2008;94(4):586–94.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Meishvili NV, Chalyan VG. Body weight and anxiety in cynomolgus macaques (Macaca fascicularis) males. Bull Exp Biol Med. 2021;170(6):802–4. https://doi.org/10.1007/s10517-021-05159-7.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ravi M, Stevens JS, Michopoulos V. Neuroendocrine pathways underlying risk and resilience to PTSD in women. Front Neuroendocrinol. 2019;55: 100790. https://doi.org/10.1016/j.yfrne.2019.100790.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Suarez-Jimenez B, Gore HE, Hachey J, King HM, Lacreuse A. Testosterone modulation of anxiety in gonadally-suppressed male rhesus monkeys: a role for gonadotropins? Pharmacol Biochem Behav. 2013;104:97–104. https://doi.org/10.1016/j.pbb.2013.01.004.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Murphy DL, Fox MA, Timpano KR, Moya PR, Ren-Patterson R, Andrews AM, et al. How the serotonin story is being rewritten by new gene-based discoveries principally related to SLC6A4, the serotonin transporter gene, which functions to influence all cellular serotonin systems. Neuropharmacology. 2008;55(6):932–60. https://doi.org/10.1016/j.neuropharm.2008.08.034.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Akimova E, Lanzenberger R, Kasper S. The serotonin-1A receptor in anxiety disorders. Biol Psychiat. 2009;66(7):627–35. https://doi.org/10.1016/j.biopsych.2009.03.012.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Tauscher J, Bagby RM, Javanmard M, Christensen BK, Kasper S, Kapur S. Inverse relationship between serotonin 5-HT(1A) receptor binding and anxiety: a [(11)C]WAY-100635 PET investigation in healthy volunteers. Am J Psychiatry. 2001;158(8):1326–8. https://doi.org/10.1176/appi.ajp.158.8.1326.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Moses-Kolko EL, Price JC, Shah N, Berga S, Sereika SM, Fisher PM, et al. Age, sex, and reproductive hormone effects on brain serotonin-1A and serotonin-2A receptor binding in a healthy population. Neuropsychopharmacology. 2011;36(13):2729–40. https://doi.org/10.1038/npp.2011.163.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Stein P, Savli M, Wadsak W, Mitterhauser M, Fink M, Spindelegger C, et al. The serotonin-1A receptor distribution in healthy men and women measured by PET and [carbonyl-11C]WAY-100635. Eur J Nucl Med Mol Imaging. 2008;35(12):2159–68. https://doi.org/10.1007/s00259-008-0850-x.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Jovanovic H, Lundberg J, Karlsson P, Cerin A, Saijo T, Varrone A, et al. Sex differences in the serotonin 1A receptor and serotonin transporter binding in the human brain measured by PET. Neuroimage. 2008;39(3):1408–19. https://doi.org/10.1016/j.neuroimage.2007.10.016.

    Article 
    PubMed 

    Google Scholar
     

  • Pecins-Thompson M, Bethea CL. Ovarian steroid regulation of serotonin-1A autoreceptor messenger RNA expression in the dorsal raphe of rhesus macaques. Neuroscience. 1999;89(1):267–77.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Lu NZ, Bethea CL. Ovarian steroid regulation of 5-HT1A receptor binding and G protein activation in female monkeys. Neuropsychopharmacology. 2002;27(1):12–24. https://doi.org/10.1016/S0893-133X(01)00423-7.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Birzniece V, Johansson IM, Wang MD, Seckl JR, Backstrom T, Olsson T. Serotonin 5-HT(1A) receptor mRNA expression in dorsal hippocampus and raphe nuclei after gonadal hormone manipulation in female rats. Neuroendocrinology. 2001;74(2):135–42.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Jovanovic H, Perski A, Berglund H, Savic I. Chronic stress is linked to 5-HT(1A) receptor changes and functional disintegration of the limbic networks. Neuroimage. 2011;55(3):1178–88. https://doi.org/10.1016/j.neuroimage.2010.12.060.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Savitz J, Lucki I, Drevets WC. 5-HT(1A) receptor function in major depressive disorder. Prog Neurobiol. 2009;88(1):17–31.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Asher J, Michopoulos V, Reding KM, Wilson ME, Toufexis D. Social stress and the polymorphic region of the serotonin reuptake transporter gene modify oestradiol-induced changes on central monoamine concentrations in female rhesus monkeys. J Neuroendocrinol. 2013;25(4):321–8. https://doi.org/10.1111/jne.12009.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Siracusa ER, Negron-Del Valle JE, Phillips D, Platt ML, Higham JP, Snyder-Mackler N, et al. Within-individual changes reveal increasing social selectivity with age in rhesus macaques. Proc Natl Acad Sci USA. 2022;119(49): e2209180119. https://doi.org/10.1073/pnas.2209180119.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Liao Z, Sosa S, Wu C, Zhang P. The influence of age on wild rhesus macaques’ affiliative social interactions. Am J Primatol. 2018;80:2. https://doi.org/10.1002/ajp.22733.

    Article 

    Google Scholar
     

  • Higley JD, King ST Jr, Hasert MF, Champoux M, Suomi SJ, Linnoila M. Stability of interindividual differences in serotonin function and its relationship to severe aggression and competent social behavior in rhesus macaque females. Neuropsychopharmacology. 1996;14(1):67–76.

    Article 
    CAS 
    PubMed 

    Google Scholar
     



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