Choir versus Solo Singing: Effects on Mood, and Salivary Oxytocin and Cortisol Concentrations

T Moritz Schladt, Gregory C Nordmann, Roman Emilius, Brigitte M Kudielka, Trynke R de Jong, Inga D Neumann, T Moritz Schladt, Gregory C Nordmann, Roman Emilius, Brigitte M Kudielka, Trynke R de Jong, Inga D Neumann

Abstract

The quantification of salivary oxytocin (OXT) concentrations emerges as a helpful tool to assess peripheral OXT secretion at baseline and after various challenges in healthy and clinical populations. Both positive social interactions and stress are known to induce OXT secretion, but the relative influence of either of these triggers is not well delineated. Choir singing is an activity known to improve mood and to induce feelings of social closeness, and may therefore be used to investigate the effects of positive social experiences on OXT system activity. We quantified mood and salivary OXT and cortisol (CORT) concentrations before, during, and after both choir and solo singing performed in a randomized order in the same participants (repeated measures). Happiness was increased, and worry and sadness as well as salivary CORT concentrations were reduced, after both choir and solo singing. Surprisingly, salivary OXT concentrations were significantly reduced after choir singing, but did not change in response to solo singing. Salivary OXT concentrations showed high intra-individual stability, whereas salivary CORT concentrations fluctuated between days within participants. The present data indicate that the social experience of choir singing does not induce peripheral OXT secretion, as indicated by unchanged salivary OXT levels. Rather, the reduction of stress/arousal experienced during choir singing may lead to an inhibition of peripheral OXT secretion. These data are important for the interpretation of future reports on salivary OXT concentrations, and emphasize the need to strictly control for stress/arousal when designing similar experiments.

Keywords: choir singing; cortisol; mood; oxytocin; saliva.

Figures

Figure 1
Figure 1
Experimental timeline for the collection of saliva samples. Basal samples (B1 and B2) were collected after 10 and 30 min of resting. Singing samples (S1 and S2) were collected after 10 and 20 min of singing. One post-singing sample (P) was collected 20 min after cessation of singing. The timeline was identical for the solo and choir conditions.
Figure 2
Figure 2
Mood states measured with the State and Trait Anxiety and Depression Inventory (STADI)-state before (“pre”) and after (“post”) 20 min of choir or solo singing, respectively. *p < 0.05 between corresponding choir and solo values. #p < 0.05 between corresponding pre and post values.
Figure 3
Figure 3
Relative change in (A) salivary oxytocin (OXT) concentrations (n = 38) and (B) salivary cortisol (CORT) concentrations (n = 17) in two basal samples (B1, B2), two singing samples (S1, S2) and one post-singing sample (P) collected before, during and after 20 min of choir or solo singing, calculated as percentage of baseline (= mean of B1 + B2 values). Inserts depict absolute concentrations of OXT and CORT in B1 samples of female (F) and male (M) participants. *p < 0.05 between corresponding choir and solo values. a/b/cp < 0.05 versus corresponding aB1, bB2, or cS1 values.
Figure 4
Figure 4
Correlations between (A) basal OXT concentrations and (B) basal CORT concentrations measured in saliva sampled from the same subjects at two different days, with 2–5 days separating the two samples. Black markers represent female subjects; gray markers represent male subjects.

References

    1. Anshel A., Kipper D. A. (1988). The influence of group singing on trust and cooperation. J. Music Ther. 25, 145–155. 10.1093/jmt/25.3.145
    1. Beck R. J., Cesario T. C., Yousefi A., Enamoto H. (2000). Choral singing, performance perception and immune system changes in salivary immunoglobulin A and cortisol. Music Percept. Interdiscip. J. 18, 87–106. 10.2307/40285902
    1. Beetz A., Uvnäs-Moberg K., Julius H., Kotrschal K. (2013). Psychosocial and psychophysiological effects of human-animal interactions: the possible role of oxytocin. Front. Psychol. 3:234. 10.3389/fpsyg.2012.00234
    1. Bendix M., Uvnäs-Moberg K., Petersson M., Gustavsson P., Svanborg P., Åsberg M., et al. . (2015). Plasma oxytocin and personality traits in psychiatric outpatients. Psychoneuroendocrinology 57, 102–110. 10.1016/j.psyneuen.2015.04.003
    1. Brondino N., Fusar-Poli L., Politi P. (2017). Something to talk about: gossip increases oxytocin levels in a near real-life situation. Psychoneuroendocrinology 77, 218–224. 10.1016/j.psyneuen.2016.12.014
    1. Brown C. A., Cardoso C., Ellenbogen M. A. (2016). A meta-analytic review of the correlation between peripheral oxytocin and cortisol concentrations. Front. Neuroendocrinol. 43, 19–27. 10.1016/j.yfrne.2016.11.001
    1. Carson D. S., Berquist S. W., Trujillo T. H., Garner J. P., Hannah S. L., Hyde S. A., et al. . (2015). Cerebrospinal fluid and plasma oxytocin concentrations are positively correlated and negatively predict anxiety in children. Mol. Psychiatry 20, 1085–1090. 10.1038/mp.2014.132
    1. Carter C. S., Pournajafi-Nazarloo H., Kramer K. M., Ziegler T. E., White-Traut R., Bello D., et al. . (2007). Oxytocin: behavioral associations and potential as a salivary biomarker. Ann. N Y Acad. Sci. 1098, 312–322. 10.1196/annals.1384.006
    1. Chanda M. L., Levitin D. J. (2013). The neurochemistry of music. Trends Cogn. Sci. 17, 179–193. 10.1016/j.tics.2013.02.007
    1. Clift S., Hancox G., Morrison I., Hess B., Kreutz G., Stewart D. (2010). Choral singing and psychological wellbeing: quantitative and qualitative findings from english choirs in a cross-national survey. J. Appl. Arts Health 1, 19–34. 10.1386/jaah.1.1.19/1
    1. Cochran D. M., Fallon D., Hill M., Frazier J. A. (2013). The role of oxytocin in psychiatric disorders: a review of biological and therapeutic research findings. Harv. Rev. Psychiatry 21, 219–247. 10.1097/hrp.0b013e3182a75b7d
    1. Coulton S., Clift S., Skingley A., Rodriguez J. (2015). Effectiveness and cost-effectiveness of community singing on mental health-related quality of life of older people: randomised controlled trial. Br. J. Psychiatry 207, 250–255. 10.1192/bjp.bp.113.129908
    1. Crockford C., Deschner T., Ziegler T. E., Wittig R. M. (2014). Endogenous peripheral oxytocin measures can give insight into the dynamics of social relationships: a review. Front. Behav. Neurosci. 8:68. 10.3389/fnbeh.2014.00068
    1. de Jong T. R., Menon R., Bludau A., Grund T., Biermeier V., Klampfl S. M., et al. . (2015). Salivary oxytocin concentrations in response to running, sexual self-stimulation, breastfeeding and the TSST: the regensburg oxytocin challenge (ROC) study. Psychoneuroendocrinology 62, 381–388. 10.1016/j.psyneuen.2015.08.027
    1. Donaldson Z. R., Young L. J. (2008). Oxytocin, vasopressin, and the neurogenetics of sociality. Science 322, 900–904. 10.1126/science.1158668
    1. Fancourt D., Williamon A., Carvalho L. A., Steptoe A., Dow R., Lewis I. (2016). Singing modulates mood, stress, cortisol, cytokine and neuropeptide activity in cancer patients and carers. Ecancermedicalscience 10:631. 10.3332/ecancer.2016.631
    1. Feldman R., Gordon I., Schneiderman I., Weisman O., Zagoory-Sharon O. (2010). Natural variations in maternal and paternal care are associated with systematic changes in oxytocin following parent-infant contact. Psychoneuroendocrinology 35, 1133–1141. 10.1016/j.psyneuen.2010.01.013
    1. Gonzaga G. C., Turner R. A., Keltner D., Campos B., Altemus M. (2006). Romantic love and sexual desire in close relationships. Emotion 6, 163–179. 10.1037/1528-3542.6.2.163
    1. Grape C., Sandgren M., Hansson L.-O., Ericson M., Theorell T. (2002). Does singing promote well-being? An empirical study of professional and amateur singers during a singing lesson. Integr. Physiol. Behav. Sci. 38, 65–74. 10.1007/bf02734261
    1. Grewen K. M., Girdler S. S., Amico J., Light K. C. (2005). Effects of partner support on resting oxytocin, cortisol, norepinephrine and blood pressure before and after warm partner contact. Psychosom. Med. 67, 531–538. 10.1097/01.psy.0000170341.88395.47
    1. Gröschl M. (2008). Current status of salivary hormone analysis. Clin. Chem. 54, 1759–1769. 10.1373/clinchem.2008.108910
    1. Jokinen J., Chatzittofis A., Hellström C., Nordström P., Uvnäs-Moberg K., Asberg M. (2012). Low CSF oxytocin reflects high intent in suicide attempters. Psychoneuroendocrinology 37, 482–490. 10.1016/j.psyneuen.2011.07.016
    1. Kagerbauer S. M., Martin J., Schuster T., Blobner M., Kochs E. F., Landgraf R. (2013). Plasma oxytocin and vasopressin do not predict neuropeptide concentrations in human cerebrospinal fluid. J. Neuroendocrinol. 25, 668–673. 10.1111/jne.12038
    1. Keeler J. R., Roth E. A., Neuser B. L., Spitsbergen J. M., Waters D. J. M., Vianney J.-M. (2015). The neurochemistry and social flow of singing: bonding and oxytocin. Front. Hum. Neurosci. 9:518. 10.3389/fnhum.2015.00518
    1. Kim S., Fonagy P., Koos O., Dorsett K., Strathearn L. (2014). Maternal oxytocin response predicts mother-to-infant gaze. Brain Res. 1580, 133–142. 10.1016/j.brainres.2013.10.050
    1. Kirschbaum C., Hellhammer D. H. (1994). Salivary cortisol in psychoneuroendocrine research: recent developments and applications. Psychoneuroendocrinology 19, 313–333. 10.1016/0306-4530(94)90013-2
    1. Kirschbaum C., Kudielka B. M., Gaab J., Schommer N. C., Hellhammer D. H. (1999). Impact of gender, menstrual cycle phase and oral contraceptives on the activity of the hypothalamus-pituitary-adrenal axis. Psychosom. Med. 61, 154–162. 10.1097/00006842-199903000-00006
    1. Krause S., Pokorny D., Schury K., Doyen-Waldecker C., Hulbert A. L., Karabatsiakis A., et al. . (2016). Effects of the adult attachment projective picture system on oxytocin and cortisol blood levels in mothers. Front. Hum. Neurosci. 10:627. 10.3389/fnhum.2016.00627
    1. Kreutz G. (2014). Does singing facilitate social bonding? Music Med 6, 51–60.
    1. Kreutz G., Bongard S., Rohrmann S., Hodapp V., Grebe D. (2004). Effects of choir singing or listening on secretory immunoglobulin A, cortisol, and emotional state. J. Behav. Med. 27, 623–635. 10.1007/s10865-004-0006-9
    1. Landgraf R., Neumann I. D. (2004). Vasopressin and oxytocin release within the brain: a dynamic concept of multiple and variable modes of neuropeptide communication. Front. Neuroendocrinol. 25, 150–176. 10.1016/j.yfrne.2004.05.001
    1. Laux L., Hock M., Bergner-Köther R., Hodapp V., Renner K.-H. (2013). Das State-Trait-Angst-Depressions-Inventar. Göttingen, DE: Hogrefe.
    1. Lebowitz E. R., Leckman J. F., Feldman R., Zagoory-Sharon O., McDonald N., Silverman W. K. (2016). Salivary oxytocin in clinically anxious youth: associations with separation anxiety and family accomodation. Psychoneuroendocrinology 65, 35–43. 10.1016/j.psyneuen.2015.12.007
    1. Lee H.-J., Macbeth A. H., Pagani J. H., Young W. S., III. (2009). Oxytocin: the great facilitator of life. Prog. Neurobiol. 88, 127–151. 10.1016/j.pneurobio.2009.04.001
    1. McCullough M. E., Churchland P. S., Mendez A. J. (2013). Problems with measuring peripheral oxytocin: can the data on oxytocin and human behavior be trusted? Neurosci. Biobehav. Rev. 37, 1485–1492. 10.1016/j.neubiorev.2013.04.018
    1. Meyer-Lindenberg A., Domes G., Kirsch P., Heinrichs M. (2011). Oxytocin and vasopressin in the human brain: social neuropeptides for translational medicine. Nat. Rev. Neurosci. 12, 524–538. 10.1038/nrn3044
    1. Miller R., Stalder T., Jarczok M., Almeida D. M., Badrick E., Bartels M., et al. . (2016). The CIRCORT database: reference ranges and seasonal changes in diurnal salivary cortisol derived from a meta-dataset comprised of 15 field studies. Psychoneuroendocrinology 73, 16–23. 10.1016/j.psyneuen.2016.07.201
    1. Neumann I. D., Landgraf R. (2012). Balance of brain oxytocin and vasopressin: implications for anxiety, depression, and social behaviors. Trends Neurosci. 35, 649–659. 10.1016/j.tins.2012.08.004
    1. Neumann I. D., Slattery D. A. (2016). Oxytocin in general anxiety and social fear: a translational approach. Biol. Psychiatry 79, 213–221. 10.1016/j.biopsych.2015.06.004
    1. Pierrehumbert B., Torrisi R., Laufer D., Halfon O., Ansermet F., Beck Popovic M. (2010). Oxytocin response to an experimental psychosocial challenge in adults exposed to traumatic experiences during childhood or adolescence. Neuroscience 166, 168–177. 10.1016/j.neuroscience.2009.12.016
    1. Renner K.-H., Hock M., Bergner-Köther R., Laux L. (2016). Differentiating anxiety and depression: the state-trait anxiety-depression inventory. Cogn. Emot. 8, 1–15. 10.1080/02699931.2016.1266306
    1. Rutigliano G., Rocchetti M., Paloyelis Y., Gilleen J., Sardella A., Cappucciati M., et al. . (2016). Peripheral oxytocin and vasopressin: biomarkers of psychiatric disorders? A comprehensive systematic review and preliminary meta-analysis. Psychiatry Res. 241, 207–220. 10.1016/j.psychres.2016.04.117
    1. Schlotz W., Kumsta R., Layes I., Entringer S., Jones A., Wüst S. (2008). Covariance between psychological and endocrine responses to pharmacological challenge and psychosocial stress: a question of timing. Psychosom. Med. 70, 787–796. 10.1097/PSY.0b013e3181810658
    1. Smith A. S., Wang Z. (2014). Hypothalamic oxytocin mediates social buffering of the stress response. Biol. Psychiatry 76, 281–288. 10.1016/j.biopsych.2013.09.017
    1. Torner L., Plotsky P. M., Neumann I. D., de Jong T. R. (2017). Central and peripheral oxytocin response after forced swim in adrenalectomized male wistar rats. Psychoneuroendocrinology 77, 165–174. 10.1016/j.psyneuen.2016.12.006
    1. Tsuji S., Yuhi T., Furuhara K., Ohta S., Shimizu Y., Higashida H. (2015). Salivary oxytocin concentrations in seven boys with autism spectrum disorder received massage from their mothers: a pilot study. Front. Psychiatry 6:58. 10.3389/fpsyt.2015.00058
    1. Valstad M., Alvares G. A., Egknud M., Matziorinis A. M., Andreassen O. A., Westlye L. T., et al. . (2017). The correlation between central and peripheral oxytocin concentrations: a systematic review and meta-analysis. Neurosci. Biobehav. Rev. 78, 117–124. 10.1016/j.neubiorev.2017.04.017
    1. Waldherr M., Neumann I. D. (2007). Centrally released oxytocin mediates mating-induced anxiolysis in male rats. Proc. Natl. Acad. Sci. U S A 104, 16681–16684. 10.1073/pnas.0705860104
    1. Weinstein D., Launay J., Pearce E., Dunbar R. I. M., Stewart L. (2016). Singing and social bonding: changes in connectivity and pain threshold as a function of group size. Evol. Hum. Behav. 37, 152–158. 10.1016/j.evolhumbehav.2015.10.002
    1. Young L. J. (2015). Oxytocin, social cognition and psychiatry. Neuropsychopharmacology 40, 243–244. 10.1038/npp.2014.186

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