Oxytocin enhances neural approach towards social and non-social stimuli of high personal relevance
Kaat Alaerts, Aymara Taillieu, Nicky Daniels, Javier R Soriano, Jellina Prinsen, Kaat Alaerts, Aymara Taillieu, Nicky Daniels, Javier R Soriano, Jellina Prinsen
Abstract
Oxytocin (OT) plays a pivotal role in a variety of complex social behaviors by modulating approach-avoidance motivational tendencies, but recently, its social specificity has been challenged. Here, a randomized, double-blind, placebo-controlled study was conducted with forty young adult men, investigating the effect of a single-dose of OT (24 IU) on behavioral and neural approach-avoidance. Frontal alpha asymmetry, indexing neurophysiological approach-avoidance, was obtained from electroencephalographic recordings while participants were presented with a series of pictures, individually rated in terms of personal relevance (i.e., high versus low positive/negative emotional evocativeness) and categorized as social or non-social. Additionally, participants could prolong (approach) or shorten (avoid) the viewing-time of each picture, providing a measure of behavioral approach-avoidance. Intranasal OT enhanced both behavioral and neural approach (increased viewing-time), particularly towards negatively valenced pictures of both social and non-social nature, thus challenging the notion that OT's effects are specific to social stimuli. Neurally, OT specifically amplified approach-related motivational salience of stimuli that were self-rated to have high personal relevance, but irrespective of their social nature or rated affective valence (positive/negative). Together, these findings provide support to the General Approach-Avoidance Hypothesis of OT, suggesting a role of OT in amplifying the motivational salience of environmental stimuli with high (personal) relevance, but irrespective of their social/non-social nature.Clinical Trial Number: The study design was registered at ClinicalTrials.gov (NCT04443647; 23/06/2020; https://ichgcp.net/clinical-trials-registry/NCT04443647 ).
Conflict of interest statement
The authors declare no competing interests.
© 2021. The Author(s).
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References
- Bartz JA, Zaki J, Bolger N, Ochsner KN. Social effects of oxytocin in humans: Context and person matter. Trends Cogn. Sci. 2011;15:301–309.
- Shamay-Tsoory SG, Fischer M, Dvash J, Harari H, Perach-Bloom N, Levkovitz Y. Intranasal administration of oxytocin increases envy and schadenfreude (gloating) Biol. Psychiatry. 2009;66:864–870. doi: 10.1016/j.biopsych.2009.06.009.
- De Dreu CK, et al. The neuropeptide oxytocin regulates parochial altruism in intergroup conflict among humans. Science. 2010;328:1408–1411. doi: 10.1126/science.1189047.
- Shamay-Tsoory SG, Abu-Akel A. The social salience hypothesis of oxytocin. Biol. Psychiatry. 2016;79:194–202. doi: 10.1016/j.biopsych.2015.07.020.
- Kemp AG, Guastella AJ. The role of oxytocin in human affect: A novel hypothesis. Curr. Dir. Psychol. Sci. 2011;20:222–231. doi: 10.1177/0963721411417547.
- Neumann ID, Wigger A, Torner L, Holsboer F, Landgraf R. Brain oxytocin inhibits basal and stress-induced activity of the hypothalamo-pituitary-adrenal axis in male and female rats: Partial action within the paraventricular nucleus. J. Neuroendocrinol. 2000;12:235–243. doi: 10.1046/j.1365-2826.2000.00442.x.
- Eckstein M, et al. Oxytocin increases eye-gaze towards novel social and non-social stimuli. Soc. Neurosci. 2019;14:594–607. doi: 10.1080/17470919.2018.1542341.
- Harari-Dahan O, Bernstein A. A general approach-avoidance hypothesis of oxytocin: Accounting for social and non-social effects of oxytocin. Neurosci. Biobehav. Rev. 2014;47:506–519. doi: 10.1016/j.neubiorev.2014.10.007.
- Izuma K, Saito DN, Sadato N. Processing of social and monetary rewards in the human striatum. Neuron. 2008;58:284–294. doi: 10.1016/j.neuron.2008.03.020.
- Lin A, Adolphs R, Rangel A. Social and monetary reward learning engage overlapping neural substrates. Soc. Cogn. Affect. Neurosci. 2012;7:274–281. doi: 10.1093/scan/nsr006.
- Norman GJ, et al. Selective influences of oxytocin on the evaluative processing of social stimuli. J. Psychopharmacol. 2011;25:1313–1319. doi: 10.1177/0269881110367452.
- Quintana DS, Guastella AJ. An allostatic theory of oxytocin. Trends Cogn. Sci. 2020;24:515–528. doi: 10.1016/j.tics.2020.03.008.
- Harari-Dahan O, Bernstein A. Oxytocin attenuates social and non-social avoidance: Re-thinking the social specificity of Oxytocin. Psychoneuroendocrinology. 2017;81:105–112. doi: 10.1016/j.psyneuen.2017.04.005.
- Harmon-Jones E, Gable PA, Peterson CK. The role of asymmetric frontal cortical activity in emotion-related phenomena: A review and update. Biol. Psychol. 2010;84:451–462. doi: 10.1016/j.biopsycho.2009.08.010.
- Harmon-Jones E, Gable PA. On the role of asymmetric frontal cortical activity in approach and withdrawal motivation: An updated review of the evidence. Psychophysiology. 2018 doi: 10.1111/psyp.12879.
- Gable P, Harmon-Jones E. Relative left frontal activation to appetitive stimuli: Considering the role of individual differences. Psychophysiology. 2008;45:275–278. doi: 10.1111/j.1469-8986.2007.00627.x.
- Schöne B, Schomberg J, Gruber T, Quirin M. Event-related frontal alpha asymmetries: Electrophysiological correlates of approach motivation. Exp. Brain Res. 2016;234:559–567. doi: 10.1007/s00221-015-4483-6.
- Hietanen JK, Leppanen JM, Peltola MJ, Linna-Aho K, Ruuhiala HJ. Seeing direct and averted gaze activates the approach-avoidance motivational brain systems. Neuropsychologia. 2008;46:2423–2430. doi: 10.1016/j.neuropsychologia.2008.02.029.
- Davidson RJ, Ekman P, Saron CD, Senulis JA, Friesen WV. Approach-withdrawal and cerebral asymmetry: Emotional expression and brain physiology I. J. Pers. Soc. Psychol. 1990;58:330–341. doi: 10.1037/0022-3514.58.2.330.
- Soriano, J.R.R.L., J.; & Alaerts, K. Cross-frequency dynamics of neural, cardiac and respiratory rhythms in the context of effortful cognition and breath focus meditation. In: Virtual Event: Society for Neuroscience (January 2021) (2021).
- Marchewka A, Zurawski Ł, Jednoróg K, Grabowska A. The Nencki Affective Picture System (NAPS): Introduction to a novel, standardized, wide-range, high-quality, realistic picture database. Behav. Res. Methods. 2014;46:596–610. doi: 10.3758/s13428-013-0379-1.
- Leppanen J, Ng KW, Tchanturia K, Treasure J. Meta-analysis of the effects of intranasal oxytocin on interpretation and expression of emotions. Neurosci. Biobehav. Rev. 2017;78:125–144. doi: 10.1016/j.neubiorev.2017.04.010.
- Shahrestani S, Kemp AH, Guastella AJ. The impact of a single administration of intranasal oxytocin on the recognition of basic emotions in humans: A meta-analysis. Neuropsychopharmacology. 2013;38:1929–1936. doi: 10.1038/npp.2013.86.
- Olff M, et al. The role of oxytocin in social bonding, stress regulation and mental health: An update on the moderating effects of context and interindividual differences. Psychoneuroendocrinology. 2013;38:1883–1894. doi: 10.1016/j.psyneuen.2013.06.019.
- Adolph D, von Glischinski M, Wannemüller A, Margraf J. The influence of frontal alpha-asymmetry on the processing of approach- and withdrawal-related stimuli—A multichannel psychophysiology study. Psychophysiology. 2017;54:1295–1310. doi: 10.1111/psyp.12878.
- Harmon-Jones E, Lueck L, Fearn M, Harmon-Jones C. The effect of personal relevance and approach-related action expectation on relative left frontal cortical activity. Psychol. Sci. 2006;17:434–440. doi: 10.1111/j.1467-9280.2006.01724.x.
- Oettl LL, et al. Oxytocin enhances social recognition by modulating cortical control of early olfactory processing. Neuron. 2016;90:609–621. doi: 10.1016/j.neuron.2016.03.033.
- Owen SF, Tuncdemir SN, Bader PL, Tirko NN, Fishell G, Tsien RW. Oxytocin enhances hippocampal spike transmission by modulating fast-spiking interneurons. Nature. 2013;500:458–462. doi: 10.1038/nature12330.
- Ooi YP, Weng SJ, Kossowsky J, Gerger H, Sung M. Oxytocin and autism spectrum disorders: A systematic review and meta-analysis of randomized controlled trials. Pharmacopsychiatry. 2017;50:5–13.
- APA . Diagnostic and Statistical Manual of Mental Disorders. 5. American Psychiatric Association; 2013.
- Mazurek MO, et al. Anxiety, sensory over-responsivity, and gastrointestinal problems in children with autism spectrum disorders. J. Abnorm. Child Psychol. 2013;41:165–176. doi: 10.1007/s10802-012-9668-x.
- Bernaerts S, Boets B, Bosmans G, Steyaert J, Alaerts K. Behavioral effects of multiple-dose oxytocin treatment in autism: A randomized, placebo-controlled trial with long-term follow-up. Mol. Autism. 2020;11:6. doi: 10.1186/s13229-020-0313-1.
- Zink CF, Meyer-Lindenberg A. Human neuroimaging of oxytocin and vasopressin in social cognition. Horm. Behav. 2012;61:400–409. doi: 10.1016/j.yhbeh.2012.01.016.
- World Medical Association Declaration of Helsinki ethical principles for medical research involving human subjects. JAMA. 2013;310:2191–2194. doi: 10.1001/jama.2013.281053.
- Aharon I, Etcoff N, Ariely D, Chabris CF, O'Connor E, Breiter HC. Beautiful faces have variable reward value: fMRI and behavioral evidence. Neuron. 2001;32:537–551. doi: 10.1016/S0896-6273(01)00491-3.
- Jung TP, Makeig S, Westerfield M, Townsend J, Courchesne E, Sejnowski TJ. Removal of eye activity artifacts from visual event-related potentials in normal and clinical subjects. Clin. Neurophysiol. 2000;111:1745–1758. doi: 10.1016/S1388-2457(00)00386-2.
- Allen JJ, Coan JA, Nazarian M. Issues and assumptions on the road from raw signals to metrics of frontal EEG asymmetry in emotion. Biol. Psychol. 2004;67:183–218. doi: 10.1016/j.biopsycho.2004.03.007.
- Jensen O, Mazaheri A. Shaping functional architecture by oscillatory alpha activity: Gating by inhibition. Front. Hum. Neurosci. 2010;4:186. doi: 10.3389/fnhum.2010.00186.
- Guastella AJ, MacLeod C. A critical review of the influence of oxytocin nasal spray on social cognition in humans: Evidence and future directions. Horm. Behav. 2012;61:410–418. doi: 10.1016/j.yhbeh.2012.01.002.
- Guastella AJ, et al. Recommendations for the standardisation of oxytocin nasal administration and guidelines for its reporting in human research. Psychoneuroendocrinology. 2013;38:612–625. doi: 10.1016/j.psyneuen.2012.11.019.
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