Animal Cognition

, Volume 21, Issue 4, pp 447–456 | Cite as

Sex, skull length, breed, and age predict how dogs look at faces of humans and conspecifics

  • Zsófia Bognár
  • Ivaylo B. IotchevEmail author
  • Enikő Kubinyi
Original Paper


The gaze of other dogs and humans is informative for dogs, but it has not been explored which factors predict face-directed attention. We used image presentations of unfamiliar human and dog heads, facing the observer (portrait) or facing away (profile), and measured looking time responses. We expected dog portraits to be aversive, human portraits to attract interest, and tested dogs of different sex, skull length and breed function, which in previous work had predicted human-directed attention. Dog portraits attracted longer looking times than human profiles. Mesocephalic dogs looked at portraits longer than at profiles, independent of the species in the image. Overall, brachycephalic dogs and dogs of unspecified breed function (such as mixed breeds) displayed the longest looking times. Among the latter, females observed the images for longer than males, which is in line with human findings on sex differences in processing faces. In a subsequent experiment, we tested whether dog portraits functioned as threatening stimuli. We hypothesized that dogs will avoid food rewards or approach them more slowly in the presence of a dog portrait, but found no effect of image type. In general, older dogs took longer to approach food placed in front of the images and mesocephalic dogs were faster than dogs of other skull length types. The results suggest that short-headed dogs are more attentive to faces, while sex and breed function predict looking times through complex interactions.


Gaze following Perception Breed differences Dog cognition 



The authors would like to thank Flóra Szánthó, Tamás Faragó, Fanni Tompai and Antal Dóka for assistance in the laboratory, Borbála Turcsán, Lisa Wallis and Patrizia Piotti for statistical consultancy, Kauê Machado Costa for useful comments on the manuscript and editing, József Topál, Dóra Szabó, Fanni Lehoczki for general consultancy, Ákos Árokszállási for the randomization script and the owners of the dogs for their time and assistance.

Author contribution’s

ZB contributed to experimental design, data collection, explorative analysis; IBI helped in writing, final analysis; EK was involved in experimental design, explorative analysis, writing.


This project has received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (Grant Agreement No. 680040) and from the Bolyai Foundation of the Hungarian Academy of Sciences.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This study on dogs complies with the current laws of Hungary. According to the corresponding definition by law (‘1998. évi XXVIII. Törvény’ 3. §/9.—the Animal Protection Act), non-invasive studies on dogs are currently allowed to be done without any special permission in Hungary. We confirm that the procedures comply with national and EU legislation. Owners provided written consent to their participation. Our Consent Form was based on the Ethical Codex of the Hungarian Psychologists (2004).

Supplementary material

10071_2018_1180_MOESM1_ESM.docx (175 kb)
Supplementary material 1.Data: (DOCX 175 kb) 
Video 1

Dogs respond with social behaviours towards dog portraits. Shown in this sequence, examples of barking, growling, averted gaze, yawning, explorative sniffing. Video abstract: (MP4 17858 kb)


  1. Adams B, Chan A, Callahan H, Milgram NW (2000) The canine as a model of human cognitive aging: recent developments. Prog Neuropsychopharmacol Biol Psychiatry 24:675–692. CrossRefPubMedGoogle Scholar
  2. Armony JL, Dolan RJ (2002) Modulation of spatial attention by fear-conditioned stimuli: an event-related fMRI study. Neuropsychologia 40:817–826. CrossRefPubMedGoogle Scholar
  3. Bálint A, Faragó T, Miklósi Á, Pongrácz P (2016) Threat-level-dependent manipulation of signaled body size: dog growls’ indexical cues depend on the different levels of potential danger. Anim Cogn. PubMedCrossRefGoogle Scholar
  4. Bartal IB-a, Decety J, Mason P et al (2011) Empathy and pro-social behavior in rats. Science 334:1427–1430. CrossRefPubMedCentralGoogle Scholar
  5. Bayliss AP, di Pellegrino G, Tipper SP (2005) Sex differences in eye gaze and symbolic cueing of attention. Q J Exp Psychol 58:631–650. CrossRefGoogle Scholar
  6. Chan YM, Pianta MJ, McKendrick AM (2014) Older age results in difficulties separating auditory and visual signals in time. J Vis 14:1–11. CrossRefGoogle Scholar
  7. Chapagain D, Range F, Huber L, Virányi Z (2018) Cognitive aging in dogs. Gerontology 64(2):165–171CrossRefPubMedGoogle Scholar
  8. Choleris E, Kavaliers M (1999) Social learning in animals: sex differences and neurobiological analysis. Pharmacol Biochem Behav 64:767–776. CrossRefPubMedGoogle Scholar
  9. Connellan J, Baron-Cohen S, Wheelwright S et al (2000) Sex differences in human neonatal social perception. Infant Behav Dev 23:113–118. CrossRefGoogle Scholar
  10. Csibra G, Hernik M, Mascaro O et al (2016) Statistical treatment of looking-time data. Dev Psychol 52:521–536. CrossRefPubMedPubMedCentralGoogle Scholar
  11. Cummings BJ, Head E, Ruehl W et al (1996) The canine as an animal model of human aging and dementia. Neurobiol Aging 17:259–268. CrossRefPubMedGoogle Scholar
  12. Darwin C (1872) The expression of emotion in animals and man. London, England, MurrayCrossRefGoogle Scholar
  13. de Waal FB (1996) Macaque social culture: development and perpetuation of affiliative networks. J Comp Psychol 110:147–154. CrossRefPubMedGoogle Scholar
  14. Decety J (2011) The neuroevolution of empathy. Ann N Y Acad Sci 1231:35–45. CrossRefPubMedGoogle Scholar
  15. Doherty TJ (2003) Invited review: aging and sarcopenia. J Appl Physiol 95:1717–1727. CrossRefPubMedGoogle Scholar
  16. Evans HE, De Lahunta A (2013) Miller's anatomy of the dog-E-Book. Elsevier Health SciencesGoogle Scholar
  17. Gácsi M, Györi B, Virányi Z et al (2009a) Explaining dog wolf differences in utilizing human pointing gestures: selection for synergistic shifts in the development of some social skills. PLoS ONE 4:4–9. CrossRefGoogle Scholar
  18. Gácsi M, McGreevy PD, Kara E, Miklósi Á (2009b) Effects of selection for cooperation and attention in dogs. Behav Brain Funct 5:31. CrossRefPubMedPubMedCentralGoogle Scholar
  19. Georgevsky D, Carrasco JJ, Valenzuela M, McGreevy PD (2013) Domestic dog skull diversity across breeds, breed groupings, and genetic clusters. J Vet Behav Clin Appl Res 9:228–234. CrossRefGoogle Scholar
  20. Hare B, Tomasello M (2005) Human-like social skills in dogs? Trends Cogn Sci 9:439–444. CrossRefPubMedGoogle Scholar
  21. Head E, Cotman CW, Milgram NW (2000) Canine cognition, aging and neuropathology. Prog Neuro Psychopharmacol Biol Psychiatry 24:671–673CrossRefGoogle Scholar
  22. Helton WS (2009) Cephalic index and perceived dog trainability. Behav Processes 82:355–358. CrossRefPubMedGoogle Scholar
  23. Henry JD, von Hippel W, Baynes K (2009) Social inappropriateness, executive control, and aging. Psychol Aging 24:239–244. CrossRefPubMedGoogle Scholar
  24. Kaminski J, Nitzschner M (2013) Do dogs get the point? A review of dog-human communication ability. Learn Motiv 44:294–302. CrossRefGoogle Scholar
  25. Kaminski J, Hynds J, Morris P, Waller BM (2017) Human attention affects facial expressions in domestic dogs. Sci Rep 7:12914. CrossRefPubMedPubMedCentralGoogle Scholar
  26. Kubinyi E, Turcsán B, Miklósi Á (2009) Dog and owner demographic characteristics and dog personality trait associations. Behav Processes 81:392–401. CrossRefPubMedGoogle Scholar
  27. Lutchmaya S, Baron-Cohen S, Raggatt P (2002) Foetal testosterone and eye contact in 12-month-old human infants. Infant Behav Dev 25:327–335. CrossRefGoogle Scholar
  28. McGreevy P, Grassi TD, Harman AM (2004) A strong correlation exists between the distribution of retinal ganglion cells and nose length in the dog. Brain Behav Evol 63:13–22. CrossRefPubMedGoogle Scholar
  29. McKinley J, Sambrook TD (2000) Use of human-given cues by domestic dogs (Canis familiaris) and horses (Equus caballus). Anim Cogn 3:13–22. CrossRefGoogle Scholar
  30. Miklosi A (2014) Dog behaviour, evolution, and cognition. OUP OxfordGoogle Scholar
  31. Miklósi Á, Soproni K (2006) A comparative analysis of animals’ understanding of the human pointing gesture. Anim Cogn 9:81–93. CrossRefPubMedGoogle Scholar
  32. Miklósi Á, Polgárdi R, Topál J, Csányi V (2000) Intentional behaviour in dog-human communication: an experimental analysis of “showing” behaviour in the dog. Anim Cogn 3:159–166. CrossRefGoogle Scholar
  33. Miklósi Á, Kubinyi E, Zsófia V et al (2003) A simple reason for a big difference: wolves do not look back at humans, but dogs do. Curr Biol 13:763–766. CrossRefPubMedGoogle Scholar
  34. Müller CA, Mayer C, Dorrenberg S et al (2011) Female but not male dogs respond to a size constancy violation. Biol Lett 7:689–691. CrossRefPubMedPubMedCentralGoogle Scholar
  35. Müller CA, Schmitt K, Barber ALA, Huber L (2015) Dogs can discriminate emotional expressions of human faces. Curr Biol 25:601–605. CrossRefPubMedGoogle Scholar
  36. Nagasawa M, Murai K, Mogi K, Kikusui T (2011) Dogs can discriminate human smiling faces from blank expressions. Anim Cogn 14:525–533. CrossRefPubMedGoogle Scholar
  37. Öhman A (1986) Face the beast and fear the face: animal and social fears as prototypes for evolutionary analyses of emotion. Psychophysiology 23:123–145CrossRefPubMedGoogle Scholar
  38. Owsley C, Sekuler R, Boldt C (1981) Aging and low-contrast vision: face perception. Invest Ophthalmol Visual Sci 21(2):362–365Google Scholar
  39. Range F, Virányi Z (2011) Development of gaze following abilities in wolves (Canis lupus). PLoS ONE. CrossRefPubMedPubMedCentralGoogle Scholar
  40. Ruffman T, Morris-Trainor Z (2011) Do dogs understand human facial expressions? J Vet Behav Clin Appl Res 6:78–79. CrossRefGoogle Scholar
  41. Schenkel R (1967) Submission: its features and function in the wolf and dog. Integr Comp Biol 7:319–329. CrossRefGoogle Scholar
  42. Schmidt MJ, Neumann AC, Amort KH et al (2011) Cephalometric measurements and determination of general skull type of cavalier king charles spaniels. Vet Radiol Ultrasound 52:436–440. CrossRefPubMedGoogle Scholar
  43. Slessor G, Laird G, Phillips LH et al (2010) Age-related differences in gaze following: does the age of the face matter? J Gerontol Ser B Psychol Sci Soc Sci 65B:536–541. CrossRefGoogle Scholar
  44. Somppi S, Törnqvist H, Hänninen L et al (2012) Dogs do look at images: eye tracking in canine cognition research. Anim Cogn 15:163–174. CrossRefPubMedGoogle Scholar
  45. Soproni K, Miklósi A, Topál J, Csányi V (2002) Dogs’ (Canis familiaris) responsiveness to human pointing gestures. J Comp Psychol 116:27–34. CrossRefPubMedGoogle Scholar
  46. Spencer SJ, Steele CM, Quinn DM (1999) Stereotype threat and women’s math performance. J Exp Soc Psychol 35:4–28. CrossRefGoogle Scholar
  47. Steele CM, Aronson J (1995) Stereotype threat and the intellectual test performance of African Americans. J Pers Soc Psychol 69:797–811. CrossRefPubMedGoogle Scholar
  48. Stone HR, McGreevy PD, Starling MJ, Forkman B (2016) Associations between domestic-dog morphology and behaviour scores in the dog mentality assessment. PLoS ONE. CrossRefPubMedPubMedCentralGoogle Scholar
  49. Szabó D, Gee NR, Miklósi Á (2016) Natural or pathologic? Discrepancies in the study of behavioral and cognitive signs in aging family dogs. J Vet Behav Clin Appl Res 11:86–98CrossRefGoogle Scholar
  50. Téglás E, Gergely A, Kupán K et al (2012) Dogs’ gaze following is tuned to human communicative signals. Curr Biol 22:209–212. CrossRefPubMedGoogle Scholar
  51. Thomas C, Moya L, Avidan G et al (2007) Reduction in white matter connectivity, revealed by diffusion tensor imaging, may account for age-related changes in face perception. J Cogn Neurosci 20:268–284. CrossRefGoogle Scholar
  52. Törnqvist H, Somppi S, Koskela A et al (2015) Comparison of dogs and humans in visual scanning of social interaction. R Soc Open Sci 2:150341. CrossRefPubMedPubMedCentralGoogle Scholar
  53. Turcsán B, Szánthó F, Miklósi Á, Kubinyi E (2014) Fetching what the owner prefers? Dogs recognize disgust and happiness in human behaviour. Anim Cogn. PubMedCrossRefGoogle Scholar
  54. Udell MAR, Dorey NR, Wynne CDL (2008) Wolves outperform dogs in following human social cues. Anim Behav 76:1767–1773. CrossRefGoogle Scholar
  55. Udell MAR, Dorey NR, Wynne CDL (2010) What did domestication do to dogs? A new account of dogs’ sensitivity to human actions. Biol Rev 85:327–345. CrossRefPubMedGoogle Scholar
  56. Udell MAR, Ewald M, Dorey NR, Wynne CDL (2014) Exploring breed differences in dogs (Canis familiaris): does exaggeration or inhibition of predatory response predict performance on human-guided tasks? Anim Behav 89:99–105. CrossRefGoogle Scholar
  57. Ueda S, Kumagai G, Otaki Y et al (2014) A comparison of facial color pattern and gazing behavior in canid species suggests gaze communication in gray wolves (Canis lupus). PLoS ONE 9:e98217. CrossRefPubMedPubMedCentralGoogle Scholar
  58. Wallis LJ, Range F, Müller CA et al (2014) Lifespan development of attentiveness in domestic dogs: drawing parallels with humans. Front Psychol 5:1–13. CrossRefGoogle Scholar
  59. Wobber C, Hare B, Koler-Matznick J et al (2009) Breed differences in domestic dogs’ (Canis familiaris) comprehension of human communicative signals. Interact Stud 10:206–224. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of EthologyEötvös Loránd UniversityBudapestHungary

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