Association between salivary serotonin and the social sharing of happiness

Masahiro Matsunaga, Keiko Ishii, Yohsuke Ohtsubo, Yasuki Noguchi, Misaki Ochi, Hidenori Yamasue, Masahiro Matsunaga, Keiko Ishii, Yohsuke Ohtsubo, Yasuki Noguchi, Misaki Ochi, Hidenori Yamasue

Abstract

Although human saliva contains the monoamine serotonin, which plays a key role in the modulation of emotional states, the association between salivary serotonin and empathic ability remains unclear. In order to elucidate the associations between salivary serotonin levels, trait empathy, and the sharing effect of emotions (i.e., sharing emotional experiences with others), we performed a vignette-based study. Participants were asked to evaluate their happiness when they experience several hypothetical life events, whereby we manipulated the valence of the imagined event (positive, neutral, or negative), as well as the presence of a friend (absent, positive, or negative). Results indicated that the presence of a happy friend significantly enhanced participants' happiness. Correlation analysis demonstrated that salivary serotonin levels were negatively correlated with happiness when both the self and friend conditions were positive. Correlation analysis also indicated a negative relationship between salivary serotonin levels and trait empathy (particularly in perspective taking), which was measured by the Interpersonal Reactivity Index. Furthermore, an exploratory multiple regression analysis suggested that mothers' attention during childhood predicted salivary serotonin levels. Our findings indicate that empathic abilities and the social sharing of happiness decreases as a function of salivary serotonin levels.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Fig 1. Results of the questionnaire.
Fig 1. Results of the questionnaire.
The bar graph shows happiness rating scores as a function of the participants’ emotional valence (positive, neutral, or negative) and the situation of a friend (absent, positive, or negative). Each column and the error bars represent means ± standard errors (n = 212).
Fig 2. Associations between salivary serotonin levels…
Fig 2. Associations between salivary serotonin levels and psychological measures.
(A) The scatterplot demonstrates the negative correlation between salivary serotonin levels and perspective taking (n = 182). (B) The scatterplot demonstrates the negative correlation between salivary serotonin levels and happiness rating scores in the self-positive/friend-positive condition (n = 183).

References

    1. Mascaro JS, Darcher A, Negi LT, Raison CL. The neural mediators of kindness-based meditation: A theoretical model. Front Psychol. 2015; 6: 109 doi:
    1. Morelli SA, Rameson LT, Lieberman MD. The neural components of empathy: predicting daily prosocial behavior. Soc Cogn Affect Neurosci. 2014; 9(1): 39–47. doi:
    1. Morelli SA, Lieberman MD, Zaki J. The emerging study of positive empathy. Soc Personal Psychol Compass. 2015; 9(2): 57–68.
    1. Doherty RW, Orimoto L, Singelis TM, Hatfield E, Hebb J. Emotional contagion: Gender and occupational differences. Psychol Women Q. 1995; 19(3): 355–371.
    1. Hatfield E, Cacioppo JT, Rapson RL. Emotional contagion. Curr Dir Psychol Sci. 1993; 2(3): 96–99.
    1. Wagner U, Galli L, Schott BH, Wold A, van der Schalk J, Manstead AS, Scherer K, Walter H. Beautiful friendship: Social sharing of emotions improves subjective feelings and activates the neural reward circuitry. Soc Cogn Affect Neurosci. 2015; 10(6): 801–808. doi:
    1. Fowler JH, Christakis NA. Dynamic spread of happiness in a large social network: Longitudinal analysis over 20 years in the Framingham Heart Study. BMJ. 2008; 337: a2338 doi:
    1. Kramer AD, Guillory JE, Hancock JT. Experimental evidence of massive-scale emotional contagion through social networks. Proc Natl Acad Sci U S A. 2014; 111(24), 8788–8790. doi:
    1. Kawamichi H, Kitada R, Yoshihara K, Takahashi HK, Sadato N. Interpersonal touch suppresses visual processing of aversive stimuli. Front Hum Neurosci. 2015; 9: 164 doi:
    1. Rimé B, Mesquita B, Philippot P, Boca S. Beyond the emotional event: Six studies on the social sharing of emotion. Cogn Emot. 1991; 5(5/6): 435–465
    1. Kimura M, Yogo M, Daibo I. Development of Japanese version of the emotional contagion scale. Jpn J Interpers Soc Psychol. 2007; 7: 31–38.
    1. Lamm C, Porges EC, Cacioppo JT, Decety J. Perspective taking is associated with specific facial responses during empathy for pain. Brain Res. 2008; 1227: 153–161. doi:
    1. Vuoskoski JK, Eerola T. Can sad music really make you sad? Indirect measures of affective states induced by music and autobiographical memories. Psychol Aesthet Creat Arts. 2012; 6: 204–213.
    1. Lin HC, McFatter R. Empathy and distress: Two distinct but related emotions in response to infant crying. Infant Behav Dev. 2012; 35(4): 887–897. doi:
    1. Dolder PC, Schmid Y, Müller F, Borgwardt S, Liechti ME. LSD acutely impairs fear recognition and enhances emotional empathy and sociality. Neuropsychopharmacology. 2016; 41(11): 2638–2646. doi:
    1. Preller KH, Pokorny T, Hock A, Kraehenmann R, Stämpfli P, Seifritz E, et al. Effects of serotonin 2A/1A receptor stimulation on social exclusion processing. Proc Natl Acad Sci U S A. 2016; 113(18): 5119–5124. doi:
    1. Gröschl M. Current status of salivary hormone analysis. Clin Chem. 2008; 54(11): 1759–1769. doi:
    1. Steptoe A, Wardle J, Marmot M. Positive affect and health-related neuroendocrine, cardiovascular, and inflammatory processes. Proc Natl Acad Sci U S A. 2005; 102(18): 6508–6512. doi:
    1. Izawa S, Sugaya N, Kimura K, Ogawa N, Yamada KC, Shirotsuki K, et al. An increase in salivary interleukin-6 level following acute psychosocial stress and its biological correlates in healthy young adults. Biol Psychol. 2013; 94(2): 249–254. doi:
    1. Izawa S, Saito K, Shirotsuki K, Sugaya N, Nomura S. Effects of prolonged stress on salivary cortisol and dehydroepiandrosterone: A study of a two-week teaching practice. Psychoneuroendocrinology. 2012; 37(6): 852–858. doi:
    1. Tan ZL, Bao AM, Tao M, Liu YJ, Zhou JN. Circadian rhythm of salivary serotonin in patients with major depressive disorder. Neuro Endocrinol Lett. 2007; 28(4): 395–400.
    1. Ferreira JN, Hoffman MP. Interactions between developing nerves and salivary glands. Organogenesis. 2013; 9(3): 199–205. doi:
    1. Roy A. Self-rated childhood emotional neglect and CSF monoamine indices in abstinent cocaine-abusing adults: possible implications for suicidal behavior. Psychiatry Res. 2002; 112(1): 69–75.
    1. Ren TH, Wu J, Yew D, Ziea E, Lao L, Leung WK, et al. Effects of neonatal maternal separation on neurochemical and sensory response to colonic distension in a rat model of irritable bowel syndrome. Am J Physiol Gastrointest Liver Physiol. 2007; 292(3): G849–856. doi:
    1. Berglund KJ, Balldin J, Berggren U, Gerdner A, Fahlke C. Childhood maltreatment affects the serotonergic system in male alcohol-dependent individuals. Alcohol Clin Exp Res. 2013; 37(5): 757–762. doi:
    1. Bravo JA, Dinan TG, Cryan JF. Early-life stress induces persistent alterations in 5-HT1A receptor and serotonin transporter mRNA expression in the adult rat brain. Front Mol Neurosci. 2014; 7: 24 doi:
    1. Germine L, Dunn EC, McLaughlin KA, Smoller JW. Childhood adversity is associated with adult theory of mind and social affiliation, but not face processing. PLoS ONE. 2015; 10(6): e0129612 doi:
    1. Taillieu TL, Brownridge DA, Sareen J, Afifi TO. Childhood emotional maltreatment and mental disorders: Results from a nationally representative adult sample from the United States. Child Abuse Negl. 2016; 59: 1–12 doi:
    1. Beadle JN, Paradiso S, Kovach C, Polgreen L, Denburg NL, Tranel D. Effects of age-related differences in empathy on social economic decision-making. Int Psychogeriatr. 2012; 24(5): 822–833. doi:
    1. Doherty RW, Orimoto L, Singelis TM, Hatfield E, Hebb J. Emotional contagion. Gender and occupational differences. Psychol Women Q. 1995; 19: 355–371.
    1. Faul F, Erdfelder E, Lang AG, Buchner A. G*Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods. 2007; 39(2): 175–191.
    1. Ito Y, Iida T, Yamamura Y, Teramura M, Nakagami Y, Kawai K, et al. Relationships between salivary melatonin levels, quality of sleep, and stress in young Japanese females. Int J Tryptophan Res. 2013; 6(Suppl 1): 75–85. doi:
    1. Ul-Haq Z, Mackay DF, Fenwick E, Pell JP. Association between body mass index and mental health among Scottish adult population: A cross-sectional study of 37,272 participants. Psychol Med. 2014; 44, 2231–2240. doi:
    1. Aketa Y. On a framework for and measures of empathy: An organizational model of empathy by Davis, and a preliminary study of a multidimensional empathy scale (IRI-J). Psychol Report Sophia Uni. 1999; 23: 19–31.
    1. Himichi T, Osanai H, Goto T, Fujita H, Kawamura Y, Davis MH, et al. Development of a Japanese version of the Interpersonal Reactivity Index. Jpn J Psychol. 2017; 88(1), 61–71.
    1. Matsunaga M, Kawamichi H, Koike T, Yoshihara K, Yoshida Y, Takahashi HK, et al. Structural and functional associations of the rostral anterior cingulate cortex with subjective happiness. NeuroImage. 2016; 134: 132–141. doi:
    1. Stafford M, Kuh DL, Gale CR, Mishra G, Richards M. Parent—child relationships and offspring’s positive mental wellbeing from adolescence to early older age. J Posit Psychol. 2016; 11(3): 326–337. doi:
    1. Taylor SE, Way BM, Welch WT, Hilmert CJ, Lehman BJ, Eisenberger NI. Early family environment, current adversity, the serotonin transporter polymorphism, and depressive symptomatology. Biol Psychiatry. 2006; 60: 671–676. doi:
    1. Choi D, Minote N, Sekiya T, Watanuki S. Relationships between trait empathy and psychological well-being in Japanese university students. Psychology. 2016; 7: 1240–1247.
    1. Kranz GS, Kasper S, Lanzenberger R. Reward and the serotonergic system. Neuroscience. 2010; 166(4): 1023–1035. doi:
    1. Price J, Cole V, Goodwin GM. Emotional side-effects of selective serotonin reuptake inhibitors: Qualitative study. Br J Psychiatry. 2009; 195: 211–217. doi:
    1. Kawamichi H, Tanabe HC, Takahashi HK, Sadato N. Activation of the reward system during sympathetic concern is mediated by two types of empathy in a familiarity-dependent manner. Soc Neurosci. 2013; 8(1): 90–100. doi:
    1. Chopik WJ, O’Brien E, Konrath SH. Differences in empathic concern and perspective taking across 63 countries J Cross Cult Psychol. 2017; 48(1): 23–38.

Source: PubMed

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