Femke T. A. Buisman-Pijlman

Mattie Tops

Stephan C. J. Huijbregts

Frontiers in Psychology

Tops, M

Huijbregts, SCJ

Buisman-Pijlman, FTA

University of Melbourne Institutional Repository

Commentary: Intranasal Oxytocin Treatment Increases Eye-Gaze Behavior toward the Owner in Ancient Japanese Dog Breeds

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GENERAL COMMENTARYpublished: 17 August 2018doi: 10.3389/fpsyg.2018.01473Frontiers in Psychology | www.frontiersin.org 1 August 2018 | Volume 9 | Article 1473Edited by:Debbie M. Kelly,University of Manitoba, CanadaReviewed by:Kurt Kotrschal,Universität Wien, AustriaSylvain Fiset,Université de Moncton, Canada*Correspondence:Mattie Topsm.tops@vu.nlSpecialty section:This article was submitted toComparative Psychology,a section of the journalFrontiers in PsychologyReceived: 19 October 2017Accepted: 26 July 2018Published: 17 August 2018Citation:Tops M, Huijbregts SCJ andBuisman-Pijlman FTA (2018)Commentary: Intranasal OxytocinTreatment Increases Eye-GazeBehavior toward the Owner in AncientJapanese Dog Breeds.Front. Psychol. 9:1473.doi: 10.3389/fpsyg.2018.01473Commentary: Intranasal OxytocinTreatment Increases Eye-GazeBehavior toward the Owner inAncient Japanese Dog BreedsMattie Tops 1*, Stephan C. J. Huijbregts 2 and Femke T. A. Buisman-Pijlman 31Department of Clinical, Neuro & Developmental Psychology, VU University Amsterdam, Amsterdam, Netherlands,2Department of Clinical Child and Adolescent Studies-Neurodevelopmental Disorders, Faculty of Social Sciences, LeidenUniversity, Leiden, Netherlands, 3Discipline of Pharmacology, Faculty of Health and Medical Sciences, University of Adelaide,Adelaide, SA, AustraliaKeywords: oxytocin, habituation, familiarization, human-dog bond, stress coping, threat response, protection,social attachmentA Commentary onIntranasal Oxytocin Treatment Increases Eye-Gaze Behavior toward the Owner in AncientJapanese Dog Breedsby Nagasawa, M., Ogawa, M., Mogi, K., and Kikusui, T. (2017). Front. Psychol. 8:1624.doi: 10.3389/fpsyg.2017.01624Oxytocin in mutually-gazing humans and dogs: Rewarding or stress bonding?Nagasawa et al. (2017) build on their previous research demonstrating a positive loop betweenmutual eye-gazing of European dog breeds and owners and increased oxytocin during interaction(Nagasawa et al., 2015). They now investigated whether this positive loop is present duringinteractions between humans and ancient Japanese dog breeds. These dogs are considered to begenetically closer to wolves and more aggressive. Nagasawa’s team set to increase the stressfulnessof the situation for the dogs by placing two strangers in the experimentation roomwith the dog andits owner. Additionally, owners and strangers were instructed not to talk to each other or to talkto and touch the dog on their initiative. Oxytocin treatment of the dogs enhanced the dogs’ gazingbehavior and increased their owners’ urinary oxytocin levels; the longer the duration of touch, thelower the increase of oxytocin in owners. Surprisingly, psychophysiological measures suggestedthat interaction with oxytocin-treated dogs enhanced owner’s tension/arousal. Based on theseand previous results, Nagasawa et al. (2015, 2017) propose the existence of an oxytocin-mediatedpositive loop in human-dog relationships.Nagasawa et al. (2017) proposed that this positive loop was due to social rewarding effects ofoxytocin release as seen in mother-infant relations. We feel there are other valid explanationsand interpretation of these findings and want to stress the importance of considering andtesting alternative explanations. As highlighted by Rault et al. (2017), it is common place inoxytocin research to assume positive valence without controlling for negative valence and arousal.Additionally, it is surprising that there is a distinction between effect of increased dog gazing andincreased touch on oxytocin levels in the owner. We want to draw attention to an alternativeexplanation for the Nagasawa and other findings, which centers on the role of oxytocin inhabituation of threat responses.Tops et al. Oxytocin and Eye-Gaze Behavior DogsWe want to draw attention to findings that demonstratedthat oxytocin may alter social attention by suppressing vigilancetoward threatening social stimuli, which explains many of itsobserved prosocial effects. Moreover, altered social attention maybe implicated in a role of oxytocin in social habituation processes,particularly in mammals, whereby an individual decreasestheir response to an unfamiliar, dominant, or emotional socialstimulus after repeated exposure (Ebitz et al., 2013; Weitekampet al., 2017). Habituation of threat responses may be a primalfunction of oxytocin in mother-infant and human-dog relations(Buttner, 2016). Dogs can pose a physical threat to peopleand are perceived as threatening by many, for example whenthey are unfamiliar or angry (ÖHman, 1986). Threat appraisalsin dogs are likely to be activated during gazing, becausedogs tend to use eye contact as a threat among conspecifics(Bradshaw and Nott, 1995). Similarly, socially anxious humansavoid direct gaze in their social interaction, which they mayperceive as threatening (Roelofs et al., 2010). Moreover, dogslook referentially to the owner after looking at an unfamiliarobject and show behavioral conditioning that mirrors the owner’sfacial and vocal emotional message (Merola et al., 2012).This data suggests the hypothesis that dogs and humans maystill show context-dependent conditioned and unconditionedresponses to each-other’s gaze. Such threat appraisals may triggeroxytocin responses in an attempt to habituate stress responses tounfamiliar faces and eyes (Ebitz et al., 2013). Consistent with thisfunction, administered oxytocin decreases unconscious vigilanceto threat signals from the eye region (Ebitz et al., 2013; Kanatet al., 2015). Importantly, dogs given oxytocin specifically fixatedless on angry faces (Kis et al., 2017) and on the eye regionof angry faces while physiological arousal was lower (Somppiet al., 2017). This highlights that oxytocin both decreased arousaland reduced eye gazing toward the eyes of angry humans,which can suggest that eye gazing was used during perceivedthreat.Research from animals and human studies suggest a primalfunction of oxytocin in threat perception, with oxytocin reducingaversive avoidance responses to newborns or potential partners(Insel and Young, 2001; Cong et al., 2015). Similarly, oxytocinfacilitates relaxed physiological states during reproduction-related interactions/situations that may otherwise be perceivedas physically threatening, such as birth, breast feeding, andconsensual sexual behavior (Porges, 2003). Interestingly, mothersdisplayed higher oxytocin levels after close, physical interactionswith previously unknown children than with their own children(Bick and Dozier, 2010). Such findings are consistent with anassociation of oxytocin with coping that requires formation oftrust, which in turn facilitates social stress habituation (Kériand Kiss, 2011; Kiss et al., 2011; Tops et al., 2013a,b cf. vonDawans et al., 2012). Effective coping supported by oxytocinrelease, which increases social support seeking, may subsequentlycounter-regulate the oxytocin response itself (Tops et al., 2013b).Voluntary touch may be an important aspect of effective copingof pet dogs and their owners during perceived threat, which canthan result in a counter-regulation of oxytocin (Uvnäs-Moberget al., 2015).Oxytocin may facilitate attachment formation betweenhumans and dogs through its function in threat-coping responseswhich increase trust (Tops et al., 2013a, 2014). A primalfunction of oxytocin in processes of social stress habituationmay also facilitate attachment between humans and dogs thatare seen as guards against threats from others. In line with arole of oxytocin in protective behavior and proximity seekingto protect others, humans show increased support seekingfrom high-threat allies (De Dreu et al., 2012). Additionally,intranasal oxytocin induces protective aggression and in-group vs. out-group favoritism (De Dreu, 2012). Importantly,Bakermans-Kranenburg and van IJzendoorn (2017) highlightthat human oxytocin studies often neglect to identify protectionas an important dimension of parenting and mother-infantrelations.Studies which focus on identifying the role of oxytocinin social reward often neglect the potential role of stresshabituation and do not collect measures to support or refutethese distinct theories. Taking the results of Nagasawa et al.(2017) for example, it seems unlikely that the Japanese dogsafter oxytocin treatment engaged in a threatening type of gazingsuch as staring at their owners. Still, the effects of oxytocinare believed to be context-dependent: the unfamiliar testingconditions involving two strangers and instructed inhibition ofinteractions were potentially stressful to both dogs and owners.The ambiguity of unnaturally suppressed interaction may haveincreased reassurance and protection seeking, and activation ofunconditioned threat appraisals of gazing between dogs andhumans.Importantly, both threat response and positive valence maydirect gazing behavior, but the current study does not let usdistinguish the two. Moreover, oxytocin responses triggered bylow-level threat and by social reward and protection in othercontexts may still be implicated in beneficial effects of livingin good relationships with dogs impacting on human well-being, coping and health (Julius et al., 2012; Kotrschal, 2016,2018). Furthermore, oxytocin’s role in stress coping responsesand habituation may help explain seemingly inconsistent andcontext-dependent results in oxytocin research in general.For instance, several studies in humans found that intranasaloxytocin application produced different or even opposite effectsdepending on whether it was applied in novel or familiarized,habituated conditions (Tops, 2017). To fully understand the roleof oxytocin in eye-gaze between humans and dogs, it is essentialto more fully take into account valence, arousal, familiarity, andhabituation (Tops et al., 2014; Rault et al., 2017).AUTHOR CONTRIBUTIONSAs the first author, MT was involved in all steps of the process,and was the primary writer of the text. SH and FB-P contributedto the write-up.Frontiers in Psychology | www.frontiersin.org 2 August 2018 | Volume 9 | Article 1473Tops et al. Oxytocin and Eye-Gaze Behavior DogsREFERENCESBakermans-Kranenburg, M. J., and van IJzendoorn, M. H. (2017). Oxytocin andhuman sensitive and protective parenting. Curr. Top. Behav. Neurosci. 35,421–448. doi: 10.1007/7854_2017_23Bick, J., and Dozier, M. (2010). Mothers’ and children’s concentrations of oxytocinfollowing close, physical interactions with biological and non-biologicalchildren. Dev. Psychobiol. 52, 100–107.doi: 10.1002/dev.20411Bradshaw, J. W. S., and Nott, H. M. R. 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The use, distribution or reproduction in other forums is permitted, providedthe original author(s) and the copyright owner(s) are credited and that the originalpublication in this journal is cited, in accordance with accepted academic practice.No use, distribution or reproduction is permitted which does not comply with theseterms.Frontiers in Psychology | www.frontiersin.org 3 August 2018 | Volume 9 | Article 1473

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Huijbregts, Stephan C.J.

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Commentary: Intranasal Oxytocin treatment increases Eye-Gaze behavior toward the owner in ancient Japanese dog breeds

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Commentary: Intranasal Oxytocin Treatment Increases Eye-Gaze Behavior toward the Owner in Ancient Japanese Dog Breeds

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