Advertisement

Animal Cognition

, Volume 19, Issue 3, pp 513–522 | Cite as

The effect of oxytocin on biological motion perception in dogs (Canis familiaris)

  • Krisztina KovácsEmail author
  • Anna KisEmail author
  • Orsolya Kanizsár
  • Anna Hernádi
  • Márta Gácsi
  • József Topál
Original Paper

Abstract

Recent studies have shown that the neuropeptide oxytocin is involved in the regulation of several complex human social behaviours. There is, however, little research on the effect of oxytocin on basic mechanisms underlying human sociality, such as the perception of biological motion. In the present study, we investigated the effect of oxytocin on biological motion perception in dogs (Canis familiaris), a species adapted to the human social environment and thus widely used to model many aspects of human social behaviour. In a within-subjects design, dogs (N = 39), after having received either oxytocin or placebo treatment, were presented with 2D projection of a moving point-light human figure and the inverted and scrambled version of the same movie. Heart rate (HR) and heart rate variability (HRV) were measured as physiological responses, and behavioural response was evaluated by observing dogs’ looking time. Subjects were also rated on the personality traits of Neuroticism and Agreeableness by their owners. As expected, placebo-pretreated (control) dogs showed a spontaneous preference for the biological motion pattern; however, there was no such preference after oxytocin pretreatment. Furthermore, following the oxytocin pretreatment female subjects looked more at the moving point-light figure than males. The individual variations along the dimensions of Agreeableness and Neuroticism also modulated dogs’ behaviour. Furthermore, HR and HRV measures were affected by oxytocin treatment and in turn played a role in subjectsʼ looking behaviour. We discuss how these findings contribute to our understanding of the neurohormonal regulatory mechanisms of human (and non-human) social skills.

Keywords

Oxytocin Biological motion Dog (Canis familiarisHeart rate Individual traits 

Notes

Acknowledgments

Financial support was provided by the Hungarian Scientific Research Fund (OTKA K100695, K112138) and the Hungarian Academy of Sciences (MTA-ELTE 01 031). We thank Katinka Tóth for assistance in data collection and Ádám Miklósi for his support.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

Supplementary material 1 (AVI 4493 kb)

References

  1. Andari E, Duhamel J-R, Zalla T, Herbrecht E, Leboyer M, Sirigu A (2010) Promoting social behavior with oxytocin in high-functioning autism spectrum disorders. Proc Natl Acad Sci USA 107:4389–4394. doi: 10.1073/pnas.0910249107 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Andics A, Gácsi M, Faragó T, Kis A, Miklósi Á (2014) Voice-sensitive regions in the dog and human brain are revealed by comparative fMRI. Curr Biol 24:574–578. doi: 10.1016/j.cub.2014.01.058 CrossRefPubMedGoogle Scholar
  3. Beintema JA, Lappe M (2002) Perception of biological motion without local image motion. Proc Natl Acad Sci USA 99:5661–5663. doi: 10.1073/pnas.082483699 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bensky MK, Gosling SD, Sinn DL (2013) The world from a dog’s point of view: a review and synthesis of dog cognition research. Adv Study Behav 45:209–406. doi: 10.1016/B978-0-12-407186-5.00005-7 CrossRefGoogle Scholar
  5. Blake R (1993) Cats perceive biological motion Psychol Sci. doi: 10.1111/j.1467-9280.1993.tb00557.x Google Scholar
  6. Brown J, Kaplan G, Rogers LJ, Vallortigara G (2010) Perception of biological motion in common marmosets (Callithrix jacchus): by females only. Anim Cogn 13(3):555–564CrossRefPubMedGoogle Scholar
  7. Campbell A (2010) Oxytocin and human social behavior. Pers Soc Psychol Rev 14:281–295. doi: 10.1177/1088868310363594 CrossRefPubMedGoogle Scholar
  8. Chang WH, Lee IH, Chen KC, Chi MH, Chiu NT, Yao WJ, Lu RB, Yang YK, Chen PS (2014) Oxytocin receptor gene rs53576 polymorphism modulates oxytocin–dopamine interaction and neuroticism traits—a SPECT study. Psychoneuroendocrinology 47:212–220. doi: 10.1016/j.psyneuen.2014.05.020 CrossRefPubMedGoogle Scholar
  9. Choleris E, Devidze N, Kavaliers M, Pfaff DW (2008) Steroidal/neuropeptide interactions in hypothalamus and amygdala related to social anxiety. Brain Res, Prog. doi: 10.1016/S0079-6123(08)00424-X CrossRefGoogle Scholar
  10. Christov-Moore L, Simpson EA, Coudé G, Grigaityte K, Iacoboni M, Ferrari PF (2014) Empathy: gender effects in brain and behavior. Neurosci Biobehav Rev 46:604–627. doi: 10.1016/j.neubiorev.2014.09.001 CrossRefPubMedGoogle Scholar
  11. Cutting JE, Moore C, Morrison R (1988) Masking the motions of human gait. Percept Psychophys 44:339–347. doi: 10.3758/BF03210415 CrossRefPubMedGoogle Scholar
  12. De Vries GJ (2008) Sex differences in vasopressin and oxytocin innervation of the brain. Prog Brain Res. doi: 10.1016/S0079-6123(08)00402-0 PubMedGoogle Scholar
  13. Dittrich WH, Troscianko T, Lea SEG, Morgan D (1996) Perception of emotion from dynamic point-light displays represented in dance. Perception 25:727–738. doi: 10.1068/p250727 CrossRefPubMedGoogle Scholar
  14. Domes G, Heinrichs M, Gläscher J, Büchel C, Braus DF, Herpertz SC (2007) Oxytocin attenuates amygdala responses to emotional faces regardless of valence. Biol Psychiatry 62:1187–1190. doi: 10.1016/j.biopsych.2007.03.025 CrossRefPubMedGoogle Scholar
  15. Domes G, Lischke A, Berger C, Grossmann A, Hauenstein K, Heinrichs M, Herpertz SC (2010) Effects of intranasal oxytocin on emotional face processing in women. Psychoneuroendocrinology 35:83–93. doi: 10.1016/j.psyneuen.2009.06.016 CrossRefPubMedGoogle Scholar
  16. Donaldson ZR, Young LJ (2008) Oxytocin, vasopressin, and the neurogenetics of sociality. Science 322:900–904. doi: 10.1126/science.1158668 CrossRefPubMedGoogle Scholar
  17. Faragó T, Pongrácz P, Miklósi À, Huber L, Virányi Z, Range F (2010) Dogs’ expectation about signalers’ body size by virtue of their growls. PLoS One. doi: 10.1371/journal.pone.0015175 PubMedPubMedCentralGoogle Scholar
  18. Gácsi M, Gyori B, Miklósi Á, Virányi Z, Kubinyi E, Topál J, Csányi V (2005) Species-specific differences and similarities in the behavior of hand-raised dog and wolf pups in social situations with humans. Dev Psychobiol 47:111–122. doi: 10.1002/dev.20082 CrossRefPubMedGoogle Scholar
  19. Gácsi M, Maros K, Sernkvist S, Faragó T, Miklósi Á (2013) human analogue safe haven effect of the owner: behavioural and heart rate response to stressful social stimuli in dogs. PLoS One. doi: 10.1371/journal.pone.0058475 PubMedPubMedCentralGoogle Scholar
  20. Garcia-Coll C, Kagan J, Reznick JS (1984) Behavioral inhibition in young children. Child Dev 55:1005–1019. doi: 10.2307/1130152 CrossRefGoogle Scholar
  21. Giese MA, Poggio T (2003) Neural mechanisms for the recognition of biological movements. Nat Rev Neurosci 4:179–192. doi: 10.1038/nrn1057 CrossRefPubMedGoogle Scholar
  22. Gimpl G, Wiegand V, Burger K, Fahrenholz F (2002) Cholesterol and steroid hormones: modulators of oxytocin receptor function. Prog Brain Res. doi: 10.1016/S0079-6123(02)39006-X PubMedGoogle Scholar
  23. Gosling SD, Kwan VSY, John OP (2003) A dog’s got personality: a cross-species comparative approach to personality judgments in dogs and humans. J Pers Soc Psychol 85:1161–1169. doi: 10.1037/0022-3514.85.6.1161 CrossRefPubMedGoogle Scholar
  24. Guastella AJ, Mitchell PB, Dadds MR (2008) Oxytocin increases gaze to the eye region of human faces. Biol Psychiatry 63:3–5CrossRefPubMedGoogle Scholar
  25. Hernádi A, Kis A, Kanizsár O, Tóth K, Miklósi B, Topál J (2015) Intranasally administered oxytocin affects how dogs (Canis familiaris) react to the threatening approach of their owner and an unfamiliar experimenter. Behav Processes 119:1–5. doi: 10.1016/j.beproc.2015.07.001 CrossRefPubMedGoogle Scholar
  26. Herzmann G, Bird CW, Freeman M, Curran T (2013) Effects of oxytocin on behavioral and ERP measures of recognition memory for own-race and other-race faces in women and men. Psychoneuroendocrinology 38:2140–2151. doi: 10.1016/j.psyneuen.2013.04.002 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Johansson G (1973) Visual perception of biological motion and a model for its analysis. Percept Psychophys. doi: 10.3758/BF03212378 Google Scholar
  28. Kéri S, Benedek G (2009) Oxytocin enhances the perception of biological motion in humans. Cogn Affect Behav Neurosci 9:237–241. doi: 10.3758/CABN.9.3.237 CrossRefPubMedGoogle Scholar
  29. Kis A, Bence M, Lakatos G, Pergel E, Turcsán B, Pluijmakers J, Vas J, Elek Z, Brúder I, Földi L, Sasvári-Székely M, Miklósi A, Rónai Z, Kubinyi E (2014a) Oxytocin receptor gene polymorphisms are associated with human directed social behavior in dogs (Canis familiaris). PLoS One 9:e83993. doi: 10.1371/journal.pone.0083993 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Kis A, Kanizsár O, Gácsi M, Topál J (2014b) Intranasally administered oxytocin decreases heart rate and increases heart rate variability in dogs. J Vet Behav Clin Appl Res 9:e15. doi: 10.1016/j.jveb.2014.09.050 CrossRefGoogle Scholar
  31. Kis A, Hernádi A, Kanizsár O, Gácsi M, Topál J (2015) Oxytocin induces positive expectations about ambivalent stimuli (cognitive bias) in dogs. Horm Behav 69:1–7. doi: 10.1016/j.yhbeh.2014.12.004 CrossRefPubMedGoogle Scholar
  32. Klin A, Lin DJ, Gorrindo P, Ramsay G, Jones W (2009) Two-year-olds with autism orient to non-social contingencies rather than biological motion. Nature 459:257–261. doi: 10.1038/nature07868 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Krueger C, Tian L (2004) A comparison of the general linear mixed model and repeated measures ANOVA using a dataset with multiple missing data points. Biol Res Nurs 6:151–157. doi: 10.1177/1099800404267682 CrossRefPubMedGoogle Scholar
  34. Lakatos G, Soproni K, Dóka A, Miklósi Á (2009) A comparative approach to dogs’ (Canis familiaris) and human infants’ comprehension of various forms of pointing gestures. Anim Cogn 12:621–631. doi: 10.1007/s10071-009-0221-4 CrossRefPubMedGoogle Scholar
  35. MacKinnon LM, Troje NF, Dringenberg HC (2010) Do rats (Rattus norvegicus) perceive biological motion? Exp Brain Res 205:571–576. doi: 10.1007/s00221-010-2378-0 CrossRefPubMedGoogle Scholar
  36. Manera V, Schouten B, Becchio C, Bara BG, Verfaillie K (2010) Inferring intentions from biological motion: a stimulus set of point-light communicative interactions. Behav Res Methods 42:168–178. doi: 10.3758/BRM.42.1.168 CrossRefPubMedGoogle Scholar
  37. Maros K, Doka A, Miklósi Á (2008) Behavioural correlation of heart rate changes in family dogs. Appl Anim Behav Sci 109:329–341. doi: 10.1016/j.applanim.2007.03.005 CrossRefGoogle Scholar
  38. Miklósi Á, Topál J (2013) What does it take to become “best friends”? Evolutionary changes in canine social competence. Trends Cogn Sci. doi: 10.1016/j.tics.2013.04.005 PubMedGoogle Scholar
  39. Nagasawa M, Mitsui S, En S, Ohatani N, Ohta M, Sakuma Y, Onaka T, Mogi K, Kikusui T (2015) Oxytocin-gaze positive loop and the coevolution of human-dog bonds. Science 80(348):333–336CrossRefGoogle Scholar
  40. Nakayasu T, Watanabe E (2013) Biological motion stimuli are attractive to medaka fish. Anim Cogn. doi: 10.1007/s10071-013-0687-y PubMedPubMedCentralGoogle Scholar
  41. Nishida S (2011) Advancement of motion psychophysics: review 2001–2010. J Vis. doi: 10.1167/11.5.11 Google Scholar
  42. Nitzschner M, Melis AP, Kaminski J, Tomasello M (2012) Dogs (Canis familiaris) evaluate humans on the basis of direct experiences only. PLoS One. doi: 10.1371/journal.pone.0046880 PubMedPubMedCentralGoogle Scholar
  43. Oliva JL, Rault JL, Appleton B, Lill A (2015) Oxytocin enhances the appropriate use of human social cues by the domestic dog (Canis familiaris) in an object choice task. Anim Cogn. doi: 10.1007/s10071-015-0843-7 Google Scholar
  44. Pavlova M, Krägeloh-Mann I, Sokolov A, Birbaumer N (2000) Simultaneous masking of a point-light walker in children. In: Bonnet C (ed) Fechner Day 2000 (strasbg. ISP), pp 279–284Google Scholar
  45. Perry A, Bentin S, Shalev I, Israel S, Uzefovsky F, Bar-On D, Ebstein RP (2010) Intranasal oxytocin modulates EEG mu/alpha and beta rhythms during perception of biological motion. Psychoneuroendocrinology 35:1446–1453. doi: 10.1016/j.psyneuen.2010.04.011 CrossRefPubMedGoogle Scholar
  46. Petrovic P, Kalisch R, Singer T, Dolan RJ (2008) Oxytocin attenuates affective evaluations of conditioned faces and amygdala activity. J Neurosci 28:6607–6615. doi: 10.1523/JNEUROSCI.4572-07.2008 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Range F, Aust U, Steurer M, Huber L (2008) Visual categorization of natural stimuli by domestic dogs. Anim Cogn 11:339–347. doi: 10.1007/s10071-007-0123-2 CrossRefPubMedGoogle Scholar
  48. Rodrigues SM, Saslow LR, Garcia N, John OP, Keltner D (2009) Oxytocin receptor genetic variation relates to empathy and stress reactivity in humans. Proc Natl Acad Sci USA 106:21437–21441. doi: 10.1073/pnas.0909579106 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Romero T, Nagasawa M, Mogi K, Hasegawa T, Kikusui T (2014) Oxytocin promotes social bonding in dogs. Proc Natl Acad Sci USA 111:9085–9090. doi: 10.1073/pnas.1322868111 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Schöberl I, Kortekaas K, Schöberl FF, Kotrschal K (2014) Algorithm-supported visual error correction (AVEC) of heart rate measurements in dogs, Canis lupus familiaris. Behav Res Methods. doi: 10.3758/s13428-014-0546-z PubMedCentralGoogle Scholar
  51. Schouten B, Troje NF, Brooks A, van der Zwan R, Verfaillie K (2010) The facing bias in biological motion perception: effects of stimulus gender and observer sex. Atten Percept Psychophys 72:1256–1260. doi: 10.3758/APP.72.5.1256 CrossRefPubMedGoogle Scholar
  52. Simion F, Regolin L, Bulf H (2008) A predisposition for biological motion in the newborn baby. Proc Natl Acad Sci USA 105:809–813. doi: 10.1073/pnas.0707021105 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Skuse DH, Gallagher L (2009) Dopaminergic–neuropeptide interactions in the social brain. Trends Cogn Sci. doi: 10.1016/j.tics.2008.09.007 PubMedGoogle Scholar
  54. Smeltzer MD, Curtis JT, Aragona BJ, Wang Z (2006) Dopamine, oxytocin, and vasopressin receptor binding in the medial prefrontal cortex of monogamous and promiscuous voles. Neurosci Lett 394:146–151. doi: 10.1016/j.neulet.2005.10.019 CrossRefPubMedGoogle Scholar
  55. Suomi SJ (1983) Social development in rhesus monkeys: consideration of individual differences. In: Oliverio A, Zappella M (eds) The behavior of human infants. Plenum Press, New York, pp 71–92. doi: 10.1007/978-1-4613-3784-3_5 CrossRefGoogle Scholar
  56. Suomi SJ (1985) Response styles in monkeys: experiential effects. In: Klar H, Siever L (eds) Biologic response styles: clinical implications. American Psychiatric Press, Washington, pp 1–18Google Scholar
  57. Suomi SJ (1986) Anxiety-like disorders in young primates. In: Gittelman R (ed) Anxiety disorders of childhood. Guilford Press, New York, pp 1–23Google Scholar
  58. Takaoka A, Morisaki A, Fujita K (2013) Cross-modal concept of human gender in dogs (Canis familiaris). Jpn J Anim Psychol 130:123–130CrossRefGoogle Scholar
  59. Thielke LE, Udell MAR (2015) The role of oxytocin in relationships between dogs and humans and potential applications for the treatment of separation anxiety in dogs. Biol Rev. doi: 10.1111/brv.12235 PubMedGoogle Scholar
  60. Tomonaga M (2001) Visual search for biological motion patterns in chimpanzees (Pan troglodytes). Psychol Int J Psychol Orient 44:46–59Google Scholar
  61. Troje NF, Westhoff C (2006) The inversion effect in biological motion perception: evidence for a “Life Detector”? Curr Biol 16:821–824. doi: 10.1016/j.cub.2006.03.022 CrossRefPubMedGoogle Scholar
  62. Vallortigara G, Regolin L, Marconato F (2005) Visually inexperienced chicks exhibit spontaneous preference for biological motion patterns. PLoS Biol 3:1312–1316. doi: 10.1371/journal.pbio.0030208 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Krisztina Kovács
    • 1
    • 2
    Email author
  • Anna Kis
    • 1
    • 2
    Email author
  • Orsolya Kanizsár
    • 1
  • Anna Hernádi
    • 1
    • 2
  • Márta Gácsi
    • 3
  • József Topál
    • 1
  1. 1.Institute of Cognitive Neuroscience and Psychology, Research Centre for Natural SciencesHungarian Academy of SciencesBudapestHungary
  2. 2.Department of EthologyEötvös Loránd UniversityBudapestHungary
  3. 3.MTA-ELTE Comparative Ethology Research GroupBudapestHungary

Personalised recommendations