The reciprocal interaction between serotonin and social behaviour

Neuroscience and Biobehavioral Reviews

Volumn 36, Issue 2, 2012, Pages 786-798

  Kiser, Dominik ^a   SteemerS, Ben ^a   Branchi, Igor ^b   Homberg, Judith R ^a  

^a RADBOUD UNIVERSITY   (Netherlands)

^b ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

Aggression; Attachment; Cooperation; Corticolimbic; Environment; Polymorphism; Serotonin; Social behaviour; Social play

Indexed keywords

5 HYDROXYINDOLEACETIC ACID; SEROTONIN; SEROTONIN 1A RECEPTOR;

AGGRESSIVENESS; ANIMAL BEHAVIOR; CHILD REARING; COOPERATION; EMOTIONAL ATTACHMENT; EMOTIONALITY; GENE; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; GENETIC POLYMORPHISM; GENETIC VARIABILITY; HUMAN; HUMAN VERSUS ANIMAL COMPARISON; MONOAMINE OXIDASE A GENE; NEUROANATOMY; NONHUMAN; PARENTAL BEHAVIOR; PERCEPTIVE DISCRIMINATION; PRIORITY JOURNAL; PSYCHOSOCIAL ENVIRONMENT; REVIEW; SEROTONIN TRANSPORTER GENE; SEROTONINERGIC SYSTEM; SEXUAL BEHAVIOR; SOCIAL BEHAVIOR; SOCIAL DOMINANCE; SOCIAL INTERACTION;

ANIMALS; HUMANS; INTERPERSONAL RELATIONS; SEROTONIN; SEROTONIN AGENTS; SEXUAL BEHAVIOR; SIGNAL TRANSDUCTION; SOCIAL BEHAVIOR; SOCIAL PERCEPTION;

EID: 84855780805     PISSN: 01497634     EISSN: 18737528     Source Type: Journal    
DOI: 10.1016/j.neubiorev.2011.12.009     Document Type: Review

References (172)

1. aan het Rot M., Moskowitz D.S., Pinard G., Young S.N. Social behaviour and mood in everyday life: the effects of tryptophan in quarrelsome individuals. J. Psychiatry Neurosci. 2006, 31:253-262.
2. Abbar M., Courtet P., Bellivier F., Leboyer M., Boulenger J.P., Castelhau D., Ferreira M., Lambercy C., Mouthon D., Paoloni-Giacobino A., Vessaz M., Malafosse A., Buresi C. Suicide attempts and the tryptophan hydroxylase gene. Mol. Psychiatry 2001, 6:268-273.
3. Amodio D.M., Frith C.D. Meeting of minds: the medial frontal cortex and social cognition. Nat. Rev. Neurosci. 2006, 7:268-277.
4. Arborelius L., Eklund M.B. Both long and brief maternal separation produces persistent changes in tissue levels of brain monoamines in middle-aged female rats. Neuroscience 2007, 145:738-750.
5. Arborelius L., Hawks B.W., Owens M.J., Plotsky P.M., Nemeroff C.B. Increased responsiveness of presumed 5-HT cells to citalopram in adult rats subjected to prolonged maternal separation relative to brief separation. Psychopharmacology (Berl.) 2004, 176:248-255.
6. Bachner-Melman R., Dina C., Zohar A.H., Constantini N., Lerer E., Hoch S., Sella S., Nemanov L., Gritsenko I., Lichtenberg P., Granot R., Ebstein R.P. AVPR1a and SLC6A4 gene polymorphisms are associated with creative dance performance. PLoS Genet. 2005, 1:e42.
7. Beacher F.D., Gray M.A., Minati L., Whale R., Harrison N.A., Critchley H.D. Acute tryptophan depletion attenuates conscious appraisal of social emotional signals in healthy female volunteers. Psychopharmacology (Berl.) 2011, 213:603-613.
8. Belsky J., Jonassaint C., Pluess M., Stanton M., Brummett B., Williams R. Vulnerability genes or plasticity genes?. Mol. Psychiatry 2009, 14:746-754.
9. Bethea C.L., Streicher J.M., Coleman K., Pau F.K., Moessner R., Cameron J.L. Anxious behavior and fenfluramine-induced prolactin secretion in young rhesus macaques with different alleles of the serotonin reuptake transporter polymorphism (5HTTLPR). Behav. Genet. 2004, 34:295-307.
10. Bilderbeck A.C., McCabe C., Wakeley J., McGlone F., Harris T., Cowen P.J., Rogers R.D. Serotonergic activity influences the cognitive appraisal of close intimate relationships in healthy adults. Biol. Psychiatry 2011, 69:720-725.
11. Branchi I. The double edged sword of neural plasticity: increasing serotonin levels leads to both greater vulnerability to depression and improved capacity to recover. Psychoneuroendocrinology 2011, 36:339-351.
12. Branchi I., D'Andrea I., Cirulli F., Lipp H.P., Alleva E. Shaping brain development: mouse communal nesting blunts adult neuroendocrine and behavioral response to social stress and modifies chronic antidepressant treatment outcome. Psychoneuroendocrinology 2010, 35:743-751.
13. Branchi, I., D'Andrea, I., Santarelli, S., Bonsignore, L.T., Alleva, E., 2011. The richness of social stimuli shapes developmental trajectories: Are laboratory mouse pups impoverished? Prog. Neuropsychopharmacol. Biol. Psychiatry. January 13 [Epub ahead of print].
14. Brenes J.C., Padilla M., Fornaguera J. A detailed analysis of open-field habituation and behavioral and neurochemical antidepressant-like effects in postweaning enriched rats. Behav. Brain Res. 2009, 197:125-137.
15. Brummett B.H., Boyle S.H., Siegler I.C., Kuhn C.M., Shley-Koch A., Jonassaint C.R., Zuchner S., Collins A., Williams R.B. Effects of environmental stress and gender on associations among symptoms of depression and the serotonin transporter gene linked polymorphic region (5-HTTLPR). Behav. Genet. 2008, 38:34-43.
16. Buckholtz J.W., Meyer-Lindenberg A. MAOA and the neurogenetic architecture of human aggression. Trends Neurosci. 2008, 31:120-129.
17. Buckholtz J.W., Asplund C.L., Dux P.E., Zald D.H., Gore J.C., Jones O.D., Marois R. The neural correlates of third-party punishment. Neuron 2008, 60:930-940.
18. Canli T., Lesch K.P. Long story short: the serotonin transporter in emotion regulation and social cognition. Nat. Neurosci. 2007, 10:1103-1109.
19. Canli T., Qiu M., Omura K., Congdon E., Haas B.W., Amin Z., Herrmann M.J., Constable R.T., Lesch K.P. Neural correlates of epigenesis. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:16033-16038.
20. Caramaschi D., de Boer S.F., Koolhaas J.M. Differential role of the 5-HT1A receptor in aggressive and non-aggressive mice: an across-strain comparison. Physiol. Behav. 2007, 90:590-601.
21. Carola V., Frazzetto G., Pascucci T., Audero E., Puglisi-Allegra S., Cabib S., Lesch K.P., Gross C. Identifying molecular substrates in a mouse model of the serotonin transporter×environment risk factor for anxiety and depression. Biol. Psychiatry 2008, 63:840-846.
22. Carr L., Lacoboni M., Dubeau M.C., Mazziotta J.C., Lenzi G.L. Neural mechanisms of empathy in humans: a relay from neural systems for imitation to limbic areas. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:5497-5502.
23. Cases O., Seif I., Grimsby J., Gaspar P., Chen K., Pournin S., Muller U., Aguet M., Babinet C., Shih J.C. Aggressive behavior and altered amounts of brain serotonin and norepinephrine in mice lacking MAOA. Science 1995, 268:1763-1766.
24. Caspi A., McClay J., Moffitt T.E., Mill J., Martin J., Craig I.W., Taylor A., Poulton R. Role of genotype in the cycle of violence in maltreated children. Science 2002, 297:851-854.
25. Caspi A., Sugden K., Moffitt T.E., Taylor A., Craig I.W., Harrington H., McClay J., Mill J., Martin J., Braithwaite A., Poulton R. Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science 2003, 301:386-389.
26. Caspi A., Hariri A.R., Holmes A., Uher R., Moffitt T.E. Genetic sensitivity to the environment: the case of the serotonin transporter gene and its implications for studying complex diseases and traits. Am. J. Psychiatry 2010, 167:509-527.
27. Chan J.S., Snoeren E.M., Cuppen E., Waldinger M.D., Olivier B., Oosting R.S. The serotonin transporter plays an important role in male sexual behavior: a study in serotonin transporter knockout rats. J. Sex. Med. 2011, 8:97-108.
28. Chen G.L., Vallender E.J., Miller G.M. Functional characterization of the human TPH2 5' regulatory region: untranslated region and polymorphisms modulate gene expression in vitro. Hum. Genet. 2008, 122:645-657.
29. Chen G.L., Novak M.A., Meyer J.S., Kelly B.J., Vallender E.J., Miller G.M. The effect of rearing experience and TPH2 genotype on HPA axis function and aggression in rhesus monkeys: a retrospective analysis. Horm. Behav. 2010, 57:184-191.
30. Chiao J.Y. Neural basis of social status hierarchy across species. Curr. Opin. Neurobiol. 2010, 20:803-809.
31. Chiavegatto S., Dawson V.L., Mamounas L.A., Koliatsos V.E., Dawson T.M., Nelson R.J. Brain serotonin dysfunction accounts for aggression in male mice lacking neuronal nitric oxide synthase. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:1277-1281.
32. Coccaro E.F., Kavoussi R.J. Fluoxetine and impulsive aggressive behavior in personality-disordered subjects. Arch. Gen. Psychiatry 1997, 54:1081-1088.
33. Coccaro E.F., McCloskey M.S., Fitzgerald D.A., Phan K.L. Amygdala and orbitofrontal reactivity to social threat in individuals with impulsive aggression. Biol. Psychiatry 2007, 62:168-178.
34. Cools R., Roberts A.C., Robbins T.W. Serotoninergic regulation of emotional and behavioural control processes. Trends Cogn. Sci. 2008, 12:31-40.
35. Cools R., Nakamura K., Daw N.D. Serotonin and dopamine: unifying affective, activational, and decision functions. Neuropsychopharmacology 2011, 36:98-113.
36. Cooper M.A., Grober M.S., Nicholas C.R., Huhman K.L. Aggressive encounters alter the activation of serotonergic neurons and the expression of 5-HT1A mRNA in the hamster dorsal raphe nucleus. Neuroscience 2009, 161:680-690.
37. Cote F., Thevenot E., Fligny C., Fromes Y., Darmon M., Ripoche M.A., Bayard E., Hanoun N., Saurini F., Lechat P., Dandolo L., Hamon M., Mallet J., Vodjdani G. Disruption of the nonneuronal tph1 gene demonstrates the importance of peripheral serotonin in cardiac function. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:13525-13530.
38. Craig I.W., Halton K.E. Genetics of human aggressive behaviour. Hum. Genet. 2009, 126:101-113.
39. Crisan L.G., Pana S., Vulturar R., Heilman R.M., Szekely R., Druga B., Dragos N., Miu A.C. Genetic contributions of the serotonin transporter to social learning of fear and economic decision making. Soc. Cogn. Affect. Neurosci. 2009, 4:399-408.
40. Crockett M.J., Clark L., Tabibnia G., Lieberman M.D., Robbins T.W. Serotonin modulates behavioral reactions to unfairness. Science 2008, 320:1739.
41. Crockett M.J., Clark L., Hauser M.D., Robbins T.W. Serotonin selectively influences moral judgment and behavior through effects on harm aversion. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:17433-17438.
42. Curley J.P., Jensen C.L., Mashoodh R., Champagne F.A. Social influences on neurobiology and behavior: epigenetic effects during development. Psychoneuroendocrinology 2011, 36:352-371.
43. Dalley J.W., Theobald D.E., Pereira E.A., Li P.M., Robbins T.W. Specific abnormalities in serotonin release in the prefrontal cortex of isolation-reared rats measured during behavioural performance of a task assessing visuospatial attention and impulsivity. Psychopharmacology (Berl.) 2002, 164:329-340.
44. Davey C.G., Allen N.B., Harrison B.J., Yucel M. Increased amygdala response to positive social feedback in young people with major depressive disorder. Biol. Psychiatry 2011, 69:734-741.
45. Davidsdottir S.D., Sveinsson O.A. Health anxiety-increased knowledge and treatment options. Laeknabladid 2010, 96:755-761.
46. de Almeida R.M., Rosa M.M., Santos D.M., Saft D.M., Benini Q., Miczek K.A. 5-HT(1B) receptors, ventral orbitofrontal cortex, and aggressive behavior in mice. Psychopharmacology (Berl.) 2006, 185:441-450.
47. de Boer S.F., Lesourd M., Mocaer E., Koolhaas J.M. Somatodendritic 5-HT(1A) autoreceptors mediate the anti-aggressive actions of 5-HT(1A) receptor agonists in rats: an ethopharmacological study with S-15535, alnespirone, and WAY-100635. Neuropsychopharmacology 2000, 23:20-33.
48. de Boer S.F., Caramaschi D., Natarajan D., Koolhaas J.M. The vicious cycle towards violence: focus on the negative feedback mechanisms of brain serotonin neurotransmission. Front. Behav. Neurosci. 2009, 3:52.
49. de Jong T.R., Veening J.G., Waldinger M.D., Cools A.R., Olivier B. Serotonin and the neurobiology of the ejaculatory threshold. Neurosci. Biobehav. Rev. 2006, 30:893-907.
50. Dohrenwend B.P. Inventorying stressful life events as risk factors for psychopathology: toward resolution of the problem of intracategory variability. Psychol. Bull. 2006, 132:477-495.
51. dos Santos L., de Andrade T.G., Graeff F.G. Social separation and diazepam withdrawal increase anxiety in the elevated plus-maze and serotonin turnover in the median raphe and hippocampus. J. Psychopharmacol. 2010, 24:725-731.
52. Ellis B.J., Boyce W.T., Belsky J., Bakermans-Kranenburg M.J., van I.Jzendoorn M.H. Differential susceptibility to the environment: an evolutionary-neurodevelopmental theory. Dev. Psychopathol. 2011, 23:7-28.
53. Fadda F., Cocco S., Stancampiano R. A physiological method to selectively decrease brain serotonin release. Brain. Res. Brain Res. Protoc. 2000, 5:219-222.
54. Ferrari P.F., van Erp A.M., Tornatzky W., Miczek K.A. Accumbal dopamine and serotonin in anticipation of the next aggressive episode in rats. Eur. J. Neurosci. 2003, 17:371-378.
55. Frazzetto G., Di Lorenzo G., Carola V., Proietti L., Sokolowska E., Siracusano A., Gross C., Troisi A. Early trauma and increased risk for physical aggression during adulthood: the moderating role of MAOA genotype. PLoS One 2007, 2:e486.
56. Fulford A.J., Marsden C.A. Conditioned release of 5-hydroxytryptamine in vivo in the nucleus accumbens following isolation-rearing in the rat. Neuroscience 1998, 83:481-487.
57. Ganasen K.A., Ipser J.C., Stein D.J. Augmentation of cognitive behavioral therapy with pharmacotherapy. Psychiatr. Clin. North. Am. 2010, 33:687-699.
58. Gardner K.L., Thrivikraman K.V., Lightman S.L., Plotsky P.M., Lowry C.A. Early life experience alters behavior during social defeat: focus on serotonergic systems. Neuroscience 2005, 136:181-191.
59. Gartside S.E., Johnson D.A., Leitch M.M., Troakes C., Ingram C.D. Early life adversity programs changes in central 5-HT neuronal function in adulthood. Eur. J. Neurosci. 2003, 17:2401-2408.
60. Gaspar P., Cases O., Maroteaux L. The developmental role of serotonin: news from mouse molecular genetics. Nat. Rev. Neurosci. 2003, 4:1002-1012.
61. Gilissen R., Bakermans-Kranenburg M.J., van I.Jzendoorn M.H., Linting M. Electrodermal reactivity during the Trier Social Stress Test for children: interaction between the serotonin transporter polymorphism and children's attachment representation. Dev. Psychobiol. 2008, 50:615-625.
62. Gunther L., Liebscher S., Jahkel M., Oehler J. Effects of chronic citalopram treatment on 5-HT1A and 5-HT2A receptors in group- and isolation-housed mice. Eur. J. Pharmacol. 2008, 593:49-61.
63. Han X., Wang W., Shao F., Li N. Isolation rearing alters social behaviors and monoamine neurotransmission in the medial prefrontal cortex and nucleus accumbens of adult rats. Brain Res. 2011, 1385:175-181.
64. Hariri A.R., Mattay V.S., Tessitore A., Kolachana B., Fera F., Goldman D., Egan M.F., Weinberger D.R. Serotonin transporter genetic variation and the response of the human amygdala. Science 2002, 297:400-403.
65. Harrison A.A., Everitt B.J., Robbins T.W. Doubly dissociable effects of median- and dorsal-raphe lesions on the performance of the five-choice serial reaction time test of attention in rats. Behav. Brain Res. 1997, 89:135-149.
66. Heils A., Teufel A., Petri S., Stöber G., Riederer P., Bengel D., Lesch K.P. Allelic variation of human serotonin transporter gene expression. J. Neurochem. 1996, 66:2621-2624.
67. Heinz A., Braus D.F., Smolka M.N., Wrase T.J., Puls I., Hermann D., Klein S., Grusser S.M., Flor H., Schumann G., Mann K., Buchel C. Amygdala-prefrontal coupling depends on a genetic variation of the serotonin transporter. Nat. Neurosci. 2005, 8:20-21.
68. Hennig J., Reuter M., Netter P., Burk C., Landt O. Two types of aggression are differentially related to serotonergic activity and the A779C TPH polymorphism. Behav. Neurosci. 2005, 119:16-25.
69. Hensler J.G. Differential regulation of 5-HT1A receptor-G protein interactions in brain following chronic antidepressant administration. Neuropsychopharmacology 2002, 26:565-573.
70. Higley J.D., Mehlman P.T., Poland R.E., Taub D.M., Vickers J., Suomi S.J., Linnoila M. CSF testosterone and 5-HIAA correlate with different types of aggressive behaviors. Biol. Psychiatry 1996, 40:1067-1082.
71. Homberg J.R., Lesch K.P. Looking on the bright side of serotonin transporter gene variation. Biol. Psychiatry 2010, 69:513-519.
72. Homberg J.R., Schiepers O.J., Schoffelmeer A.N., Cuppen E., Vanderschuren L.J. Acute and constitutive increases in central serotonin levels reduce social play behaviour in peri-adolescent rats. Psychopharmacology (Berl.) 2007, 195:175-182.
73. Homberg J.R., de Boer S.F., Raaso H.S., Olivier J.D., Verheul M., Ronken E., Cools A.R., Ellenbroek B.A., Schoffelmeer A.N., Vanderschuren L.J., De Vries T.J., Cuppen E. Adaptations in pre- and postsynaptic 5-HT1A receptor function and cocaine supersensitivity in serotonin transporter knockout rats. Psychopharmacology (Berl.) 2008, 200:367-380.
74. Hu X.Z., Lipsky R.H., Zhu G., Akhtar L.A., Taubman J., Greenberg B.D., Xu K., Arnold P.D., Richter M.A., Kennedy J.L., Murphy D.L., Goldman D. Serotonin transporter promoter gain-of-function genotypes are linked to obsessive-compulsive disorder. Am. J. Hum. Genet. 2006, 78:815-826.
75. Jacobs R.H., Pine D.S., Schoeny M.E., Henry D.B., Gollan J.K., Moy G., Cook E.H., Wakschlag L.S. Maternal depressive history, teen 5HTTLPR genotype, and the processing of emotional faces: Exploring mechanisms of risk. Behav. Res. Ther. 2011, 49:80-84.
76. Jansen F., Heiming R.S., Kloke V., Kaiser S., Palme R., Lesch K.P., Sachser N. Away game or home match: the influence of venue and serotonin transporter genotype on the display of offensive aggression. Behav. Brain Res. 2011, 219:291-301.
77. Jarrell H., Hoffman J.B., Kaplan J.R., Berga S., Kinkead B., Wilson M.E. Polymorphisms in the serotonin reuptake transporter gene modify the consequences of social status on metabolic health in female rhesus monkeys. Physiol. Behav. 2008, 93:807-819.
78. Jequier E., Lovenberg W., Sjoerdsma A. Tryptophan hydroxylase inhibition: the mechanism by which p-chlorophenylalanine depletes rat brain serotonin. Mol. Pharmacol. 1967, 3:274-278.
79. Kalin N.H., Shelton S.E., Fox A.S., Rogers J., Oakes T.R., Davidson R.J. The serotonin transporter genotype is associated with intermediate brain phenotypes that depend on the context of eliciting stressor. Mol. Psychiatry 2008, 13:1021-1027.
80. Kalueff A.V., Fox M.A., Gallagher P.S., Murphy D.L. Hypolocomotion, anxiety and serotonin syndrome-like behavior contribute to the complex phenotype of serotonin transporter knockout mice. Genes Brain Behav. 2007, 6:389-400.
81. Kalueff A.V., Olivier J.D., Nonkes L., Homberg J.R. Conserved role for the serotonin transporter gene in rat and mouse neurobehavioral endophenotypes. Neurosci. Biobehav. Rev. 2009, 34:373-386.
82. Karg K., Burmeister M., Shedden K., Sen S. The serotonin transporter promoter variant (5-HTTLPR), stress, and depression meta-analysis revisited. Evidence of genetic moderation. Arch. Gen. Psychiatry 2011, 68:444-454.
83. Kim-Cohen J., Caspi A., Taylor A., Williams B., Newcombe R., Craig I.W., Moffitt T.E. MAOA, maltreatment, and gene-environment interaction predicting children's mental health: new evidence and a meta-analysis. Mol. Psychiatry 2006, 11:903-913.
84. Kinnally E.L., Capitanio J.P., Leibel R., Deng L., LeDuc C., Haghighi F., Mann J.J. Epigenetic regulation of serotonin transporter expression and behavior in infant rhesus macaques. Genes Brain Behav. 2010, 9:575-582.
85. Knutson B., Panksepp J. Effects of serotonin depletion on the play of juvenile rats. Ann. N. Y. Acad. Sci. 1997, 807:475-477.
86. Knutson B., Wolkowitz O.M., Cole S.W., Chan T., Moore E.A., Johnson R.C., Terpstra J., Turner R.A., Reus V.I. Selective alteration of personality and social behavior by serotonergic intervention. Am. J. Psychiatry 1998, 155:373-379.
87. Koolhaas J.M., de Boer S.F., Buwalda B., van Reenen K. Individual variation in coping with stress: a multidimensional approach of ultimate and proximate mechanisms. Brain Behav. Evol. 2007, 70:218-226.
88. Krawczak M., Trefilov A., Berard J., Bercovitch F., Kessler M., Sauermann U., Croucher P., Nürnberg P., Widdig A., Schmidtke J. Male reproductive timing in Rhesus macaques is influenced by the 5HTTLPR promoter polymorphism of the serotonin transporter gene. Biol. Reprod. 2005, 72:1109-1113.
89. Kriegebaum C., Gutknecht L., Schmitt A., Lesch K.P., Reif A. Serotonin now: Part 1. Neurobiology and developmental genetics. Fortschr. Neurol. Psychiatr. 2010, 78:319-331.
90. Kubala K.H., McGinnis M.Y., Anderson G.M., Lumia A.R. The effects of an anabolic androgenic steroid and low serotonin on social and non-social behaviors in male rats. Brain Res. 2008, 1232:21-29.
91. Kulikov A.V., Osipova D.V., Naumenko V.S., Popova N.K. Association between Tph2 gene polymorphism, brain tryptophan hydroxylase activity and aggressiveness in mouse strains. Genes Brain Behav. 2005, 4:482-485.
92. Lee L.J. Neonatal fluoxetine exposure affects the neuronal structure in the somatosensory cortex and somatosensory-related behaviors in adolescent rats. Neurotox. Res. 2009, 15:212-223.
93. Lesch K.P., Bengel D., Heils A., Sabol S.Z., Greenberg B.D., Petri S., Benjamin J., Muller C.R., Hamer D.H., Murphy D.L. Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science 1996, 274:1527-1531.
94. Lewejohann L., Kloke V., Heiming R.S., Jansen F., Kaiser S., Schmitt A., Lesch K.P., Sachser N. Social status and day-to-day behaviour of male serotonin transporter knockout mice. Behav. Brain Res. 2010, 211:220-228.
95. Lieben C.K., van Oorshouw K., Deutz N.E., Blokland A. Acute tryptophan depletion induced by a gelatin-based mixture impairs object memory but not affective behavior and spatial learning in the rat. Behav. Brain Res. 2004, 151:53-64.
96. Linnoila V.M., Virkkunen M. Aggression, suicidality, and serotonin. J. Clin. Psychiatry 1992, 53(Suppl):46-51.
97. Linnoila M., Virkkunen M., Scheinin M., Nuutila A., Rimon R., Goodwin F.K. Low cerebrospinal fluid 5-hydroxyindoleacetic acid concentration differentiates impulsive from nonimpulsive violent behavior. Life Sci. 1983, 33:2609-2614.
98. Liu Y., Jiang Y., Si Y., Kim J.Y., Chen Z.F., Rao Y. Molecular regulation of sexual preference revealed by genetic studies of 5-HT in the brains of male mice. Nature 2011, 472:95-99.
99. Lukkes J., Vuong S., Scholl J., Oliver H., Forster G. Corticotropin-releasing factor receptor antagonism within the dorsal raphe nucleus reduces social anxiety-like behavior after early-life social isolation. J. Neurosci. 2009, 29:9955-9960.
100. Maestripieri D., Hoffman C.L., Anderson G.M., Carter C.S., Higley J.D. Mother-infant interactions in free-ranging rhesus macaques: relationships between physiological and behavioral variables. Physiol. Behav. 2009, 96:613-619.
101. Maher M.J., Huppert J.D., Chen H., Duan N., Foa E.B., Liebowitz M.R., Simpson H.B. Moderators and predictors of response to cognitive-behavioral therapy augmentation of pharmacotherapy in obsessive-compulsive disorder. Psychol. Med. 2010, 40:2013-2023.
102. Manuck S.B., Flory J.D., Ferrell R.E., Dent K.M., Mann J.J., Muldoon M.F. Aggression and anger-related traits associated with a polymorphism of the tryptophan hydroxylase gene. Biol. Psychiatry 1999, 45:603-614.
103. 6 receptors. Neuropharmacology 2011, 61:400-407.
104. Meyer J.H., Wilson A.A., Rusjan P., Clark M., Houle S., Woodside S., Arrowood J., Martin K., Colleton M. Serotonin2A receptor binding potential in people with aggressive and violent behaviour. J. Psychiatry Neurosci. 2008, 33:499-508.
105. Meyer-Lindenberg A., Buckholtz J.W., Kolachana B., Hariri R., Pezawas L., Blasi G., Wabnitz A., Honea R., Verchinski B., Callicott J.H., Egan M., Mattay V., Weinberger D.R. Neural mechanisms of genetic risk for impulsivity and violence in humans. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:6269-6274.
106. Mileva-Seitz V., Kennedy J., Atkinson L., Steiner M., Levitan R., Matthews S.G., Meaney M.J., Sokolowski M.B., Fleming A.S. Serotonin transporter allelic variation in mothers predicts maternal sensitivity, behavior and attitudes toward 6-month-old infants. Genes Brain Behav. 2011, 10:325-333.
107. Miller J.M., Kinnally E.L., Ogden R.T., Oquendo M.A., Mann J.J., Parsey R.V. Reported childhood abuse is associated with low serotonin transporter binding in vivo in major depressive disorder. Synapse 2009, 63:565-573.
108. Miura H., Qiao H., Ohta T. Attenuating effects of the isolated rearing condition on increased brain serotonin and dopamine turnover elicited by novelty stress. Brain Res. 2002, 926:10-17.
109. Miura H., Qiao H., Ohta T. Influence of aging and social isolation on changes in brain monoamine turnover and biosynthesis of rats elicited by novelty stress. Synapse 2002, 46:116-124.
110. Miura H., Qiao H., Kitagami T., Ohta T., Ozaki N. Effects of fluvoxamine on levels of dopamine, serotonin, and their metabolites in the hippocampus elicited by isolation housing and novelty stress in adult rats. Int. J. Neurosci. 2005, 115:367-378.
111. Moberg T., Nordstrom P., Forslund K., Kristiansson M., Asberg M., Jokinen J. CSF 5-HIAA and exposure to and expression of interpersonal violence in suicide attempters. J. Affect. Disord. 2011, 132:173-178.
112. Morrison K.E., Swallows C.L., Cooper M.A. Effects of dominance status on conditioned defeat and expression of 5-HT1A and 5-HT2A receptors. Physiol. Behav. 2011, 104:283-290.
113. Muchimapura S., Fulford A.J., Mason R., Marsden C.A. Isolation rearing in the rat disrupts the hippocampal response to stress. Neuroscience 2002, 112:697-705.
114. Muchimapura S., Mason R., Marsden C.A. Effect of isolation rearing on pre- and post-synaptic serotonergic function in the rat dorsal hippocampus. Synapse 2003, 47:209-217.
115. Natarajan D., de Boer S.F., Koolhaas J.M. Lack of differential serotonin biosynthesis capacity in genetically selected low and high aggressive mice. Physiol. Behav. 2009, 98:411-415.
116. Newman T.K., Syagailo Y.V., Barr C.S., Wendland J.R., Champoux M., Graessle M., Suomi S.J., Higley J.D., Lesch K.P. Monoamine oxidase A gene promoter variation and rearing experience influences aggressive behavior in rhesus monkeys. Biol. Psychiatry 2005, 57:167-172.
117. Nietzer S.L., Bonn M., Jansen F., Heiming R.S., Lewejohann L., Sachser N., Asan E.S., Lesch K.P., Schmitt A.G. Serotonin transporter knockout and repeated social defeat stress: impact on neuronal morphology and plasticity in limbic brain areas. Behav. Brain Res. 2011, 220:42-54.
118. Olivier J.D., Van Der Hart M.G., Van Swelm R.P., Dederen P.J., Homberg J.R., Cremers T., Deen P.M., Cuppen E., Cools A.R., Ellenbroek B.A. A study in male and female 5-HT transporter knockout rats: an animal model for anxiety and depression disorders. Neuroscience 2008, 152:573-584.
119. Olivier, B., Chan, J.S., Snoeren, E.M., Olivier, J.D., Veening, J.G., Vinkers, C.H., Waldinger, M.D., Oosting, R.S., 2011. Differences in Sexual Behaviour in Male and Female Rodents: Role of Serotonin. Curr. Top Behav. Neurosci. March 4 [Epub ahead of print].
120. Olsson A., Phelps E.A. Social learning of fear. Nat. Neurosci. 2007, 10:1095-1102.
121. Qvarnstrom A., Forsgren E. Should females prefer dominant males. Trends Ecol. Evol. 1998, 13:498-501.
122. Pacheco J., Beevers C.G., Benavides C., McGeary J., Stice E., Schnyer D.M. Frontal-limbic white matter pathway associations with the serotonin transporter gene promoter region (5-HTTLPR) polymorphism. J. Neurosci. 2009, 29:6229-6233.
123. Panksepp J. Neuroevolutionary sources of laughter and social joy: modeling primal human laughter in laboratory rats. Behav. Brain Res. 2007, 182:231-244.
124. Persico A.M., Mengual E., Moessner R., Hall F.S., Revay R.S., Sora I., Arellano J., DeFelipe J., Gimenez-Amaya J.M., Conciatori M., Marino R., Baldi A., Cabib S., Pascucci T., Uhl G.R., Murphy D.L., Lesch K.P., Keller F. Barrel pattern formation requires serotonin uptake by thalamocortical afferents, and not vesicular monoamine release. J. Neurosci. 2001, 21:6862-6873.
125. Pezawas L., Meyer-Lindenberg A., Drabant E.M., Verchinski B.A., Munoz K.E., Kolachana B.S., Egan M.F., Mattay V.S., Hariri A.R., Weinberger D.R. 5-HTTLPR polymorphism impacts human cingulate-amygdala interactions: a genetic susceptibility mechanism for depression. Nat. Neurosci. 2005, 8:828-834.
126. Pluess M., Velders F.P., Belsky J., van I.Jzendoorn M.H., Bakermans-Kranenburg M.J., Jaddoe V.W., Hofman A., Arp P.P., Verhulst F.C., Tiemeier H. Serotonin transporter polymorphism moderates effects of prenatal maternal anxiety on infant negative emotionality. Biol. Psychiatry 2011, 69:520-525.
127. Quirk G.J., Beer J.S. Prefrontal involvement in the regulation of emotion: convergence of rat and human studies. Curr. Opin. Neurobiol. 2006, 16:723-727.
128. Raleigh M.J., McGuire M.T., Brammer G.L., Pollack D.B., Yuwiler A. Serotonergic mechanisms promote dominance acquisition in adult male vervet monkeys. Brain Res. 1991, 559:181-190.
129. Reiner I., Spangler G. Adult attachment and gene polymorphisms of the dopamine D4 receptor and serotonin transporter (5-HTT). Attach. Hum. Dev. 2010, 12:209-229.
130. Rilke O., Freier D., Jahkel M., Oehler J. Dynamic alterations of serotonergic metabolism and receptors during social isolation of low- and high-active mice. Pharmacol. Biochem. Behav. 1998, 59:891-896.
131. Rilke O., Will K., Jahkel M., Oehler J. Behavioral and neurochemical effects of anpirtoline and citalopram in isolated and group housed mice. Prog. Neuropsychopharmacol. Biol. Psychiatry 2001, 25:1125-1144.
132. Risch N., Herrell R., Lehner T., Liang K.Y., Eaves L., Hoh J., Griem A., Kovacs M., Ott J., Merikangas K.R. Interaction between the serotonin transporter gene (5-HTTLPR), stressful life events, and risk of depression: a meta-analysis. JAMA 2009, 301:2462-2471.
133. Robert G., Drapier D., Tue-Ferrer D., Renault A., Reymann J.M. Acute and chronic anxiogenic-like response to fluoxetine in rats in the elevated plus-maze: modulation by stressful handling. Behav. Brain Res. 2011, 220:344-348.
134. Sabol S.Z., Hu S., Hamer D. A functional polymorphism in the monoamine oxidase A gene promoter. Hum. Genet. 1998, 103:273-279.
135. Schiller L., Donix M., Jahkel M., Oehler J. Serotonin 1A and 2A receptor densities, neurochemical and behavioural characteristics in two closely related mice strains after long-term isolation. Prog. Neuropsychopharmacol. Biol. Psychiatry 2006, 30:492-503.
136. Schwandt M.L., Lindell S.G., Chen S., Higley J.D., Suomi S.J., Heilig M., Barr C.S. Alcohol response and consumption in adolescent rhesus macaques: life history and genetic influences. Alcohol 2010, 44:67-80.
137. Scott A.L., Bortolato M., Chen K., Shih J.C. Novel monoamine oxidase A knock out mice with human-like spontaneous mutation. Neuroreport 2008, 19:739-743.
138. Shannon C., Schwandt M.L., Champoux M., Shoaf S.E., Suomi S.J., Linnoila M., Higley J.D. Maternal absence and stability of individual differences in CSF 5-HIAA concentrations in rhesus monkey infants. Am. J. Psychiatry 2005, 162:1658-1664.
139. Snoeren E.M., Chan J.S., de Jong T.R., Waldinger M.D., Olivier B., Oosting R.S. A new female rat animal model for hypoactive sexual desire disorder; behavioral and pharmacological evidence. J. Sex Med. 2011, 8:44-56.
140. Spangler G., Maier U., Geserick B., von Wahlert A. The influence of attachment representation on parental perception and interpretation of infant emotions: a multilevel approach. Dev. Psychobiol. 2010, 52:411-423.
141. Spigset O. Adverse reactions of selective serotonin reuptake inhibitors: reports from a spontaneous reporting system. Drug. Saf. 1999, 20:277-287.
142. Spinelli S., Chefer S., Carson R.E., Jagoda E., Lang L., Heilig M., Barr C.S., Suomi S.J., Higley J.D., Stein E.A. Effects of early-life stress on serotonin(1A) receptors in juvenile Rhesus monkeys measured by positron emission tomography. Biol. Psychiatry 2010, 67:1146-1153.
143. Suomi S.J. Aggression and social behaviour in rhesus monkeys. Novartis Found Symp. 2005, 268:216-222.
144. Suomi S.J. Risk, resilience, and gene×environment interactions in rhesus monkeys. Ann. N. Y. Acad. Sci. 2006, 1094:52-62.
145. Suzuki H., Han S.D., Lucas L.R. Increased 5-HT1B receptor density in the basolateral amygdala of passive observer rats exposed to aggression. Brain Res. Bull. 2010, 83:38-43.
146. Takahashi A., Quadros I.M., de Almeida R.M., Miczek K.A. Brain serotonin receptors and transporters: initiation vs. termination of escalated aggression. Psychopharmacology (Berl.) 2011, 213:183-212.
147. Tavoulari S., Forrest L.R., Rudnick G. Fluoxetine (Prozac) binding to serotonin transporter is modulated by chloride and conformational changes. J. Neurosci. 2009, 29:9635-9643.
148. Trezza V., Baarendse P.J., Vanderschuren L.J. The pleasures of play: pharmacological insights into social reward mechanisms. Trends Pharmacol. Sci. 2010, 31:463-469.
149. Troisi A., Vicario E., Nuccetelli F., Ciani N., Pasini A. Effects of fluoxetine on aggressive behavior of adult inpatients with mental retardation and epilepsy. Pharmacopsychiatry 1995, 28:73-76.
150. Tse W.S., Bond A.J. Serotonergic intervention affects both social dominance and affiliative behaviour. Psychopharmacology (Berl.) 2002, 161:324-330.
151. Uher R. The role of genetic variation in the causation of mental illness: an evolution-informed framework. Mol Psychiatyry 2009, 14:1072-1082.
152. Uher, R., Caspi, A., Houts, R., Sugden, K., Williams, B., Poulton, R., Moffitt, T.E., 2011. Serotonin transporter gene moderates childhood maltreatment's effects on persistent but not single-episode depression: Replications and implications for resolving inconsistent results. J. Affect. Disord. March 23 [Epub ahead of print].
153. van Erp A.M., Miczek K.A. Aggressive behavior, increased accumbal dopamine, and decreased cortical serotonin in rats. J. Neurosci. 2000, 20:9320-9325.
154. van I.Jzendoorn M.H., Caspers K., Bakermans-Kranenburg M.J., Beach S.R., Philibert R. Methylation matters: interaction between methylation density and serotonin transporter genotype predicts unresolved loss or trauma. Biol. Psychiatry 2010, 68:405-407.
155. van der Vegt B., de Boer S.F., Buwalda B., de Ruiter A.J., de Jong J.G., Koolhaas J.M. Enhanced sensitivity of postsynaptic serotonin-1A receptors in rats and mice with high trait aggression. Physiol. Behav. 2001, 74:205-211.
156. Virkkunen M., Narvanen S. Plasma insulin, tryptophan and serotonin levels during the glucose tolerance test among habitually violent and impulsive offenders. Neuropsychobiology 1987, 17:19-23.
157. Virkkunen M., Rawlings R., Tokola R., Poland R.E., Guidotti A., Nemeroff C., Bissette G., Kalogeras K., Karonen S.L., Linnoila M. CSF biochemistries, glucose metabolism, and diurnal activity rhythms in alcoholic, violent offenders, fire setters, and healthy volunteers. Arch. Gen. Psychiatry 1994, 51:20-27.
158. Virkkunen M., Goldman D., Nielsen D.A., Linnoila M. Low brain serotonin turnover rate (low CSF 5-HIAA) and impulsive violence. J. Psychiatry Neurosci. 1995, 20:271-275.
159. Vitiello B., Behar D., Hunt J., Stoff D., Ricciuti A. Subtyping aggression in children and adolescents. J. Neuropsychiatry Clin. Neurosci. 1990, 2:189-192.
160. Walther D.J., Bader M. A unique central tryptophan hydroxylase isoform. Biochem. Pharmacol. 2003, 66:1673-1680.
161. Walther D.J., Peter J.U., Bashammakh S., Hortnagl H., Voits M., Fink H., Bader M. Synthesis of serotonin by a second tryptophan hydroxylase isoform. Science 2003, 299:76.
162. Watson K.K., Ghodasra J.H., Platt M.L. Serotonin transporter genotype modulates social reward and punishment in rhesus macaques. PLoS One 2009, 4:e4156.
163. Way B.M., Taylor S.E. Social influences on health: is serotonin a critical mediator?. Psychosom. Med. 2010, 72:107-112.
164. Way B.M., Taylor S.E. A polymorphism in the serotonin transporter gene moderates cardiovascular reactivity to psychosocial stress. Psychosom. Med. 2011, 73:310-317.
165. Widom C.S., Brzustowicz L.M. MAOA and the cycle of violence: childhood abuse and neglect, MAOA genotype, and risk for violent and antisocial behavior. Biol. Psychiatry 2006, 60:684-689.
166. Williams L.M., Gatt J.M., Kuan S.A., Dobson-Stone C., Palmer D.M., Paul R.H., Song L., Costa P.T., Schofield P.R., Gordon E. A polymorphism of the MAOA gene is associated with emotional brain markers and personality traits on an antisocial index. Neuropsychopharmacology 2009, 34:1797-1809.
167. Witte A.V., Floel A., Stein P., Savli M., Mien L.K., Wadsak W., Spindelegger C., Moser U., Fink M., Hahn A., Mitterhauser M., Kletter K., Kasper S., Lanzenberger R. Aggression is related to frontal serotonin-1A receptor distribution as revealed by PET in healthy subjects. Hum. Brain Mapp. 2009, 30:2558-2570.
168. Wright I.K., Ismail H., Upton N., Marsden C.A. Effect of isolation rearing on 5-HT agonist-induced responses in the rat. Psychopharmacology (Berl.) 1991, 105:259-263.
169. Young S.N., Smith S.E., Pihl R.O., Ervin F.R. Tryptophan depletion causes a rapid lowering of mood in normal males. Psychopharmacology (Berl.) 1985, 87:173-177.
170. Zhang X., Beaulieu J.M., Sotnikova T.D., Gainetdinov R.R., Caron M.G. Tryptophan hydroxylase-2 controls brain serotonin synthesis. Science 2004, 305:217.
171. Zill P., Buttner A., Eisenmenger W., Bondy B., Ackenheil M. Regional mRNA expression of a second tryptophan hydroxylase isoform in postmortem tissue samples of two human brains. Eur. Neuropsychopharmacol. 2004, 14:282-284.
172. Zimmermann P., Mohr C., Spangler G. Genetic and attachment influences on adolescents' regulation of autonomy and aggressiveness. J. Child. Psychol. Psychiatry 2009, 50:1339-1347.