How dogs scan familiar and inverted faces: an eye movement study

Abstract

Faces play an important role in communication and identity recognition in social animals. Domestic dogs often respond to human facial cues, but their face processing is weakly understood. In this study, facial inversion effect (deficits in face processing when the image is turned upside down) and responses to personal familiarity were tested using eye movement tracking. A total of 23 pet dogs and eight kennel dogs were compared to establish the effects of life experiences on their scanning behavior. All dogs preferred conspecific faces and showed great interest in the eye area, suggesting that they perceived images representing faces. Dogs fixated at the upright faces as long as the inverted faces, but the eye area of upright faces gathered longer total duration and greater relative fixation duration than the eye area of inverted stimuli, regardless of the species (dog or human) shown in the image. Personally, familiar faces and eyes attracted more fixations than the strange ones, suggesting that dogs are likely to recognize conspecific and human faces in photographs. The results imply that face scanning in dogs is guided not only by the physical properties of images, but also by semantic factors. In conclusion, in a free-viewing task, dogs seem to target their fixations at naturally salient and familiar items. Facial images were generally more attractive for pet dogs than kennel dogs, but living environment did not affect conspecific preference or inversion and familiarity responses, suggesting that the basic mechanisms of face processing in dogs could be hardwired or might develop under limited exposure.

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References

  1. Adachi I, Kuwahata H, Fujita K (2007) Dogs recall their owner’s face upon hearing the owner’s voice. Anim Cogn 10:17–21

    PubMed  Article  Google Scholar 

  2. Althoff RR, Cohen NJ (1999) Eye-movement-based memory effect: a reprocessing effect in face perception. J Exp Psychol Learn Mem Cogn 25:997–1010

    PubMed  Article  CAS  Google Scholar 

  3. Autier-Dérian D, Deputte BL, Chalvet-Monfray K, Coulon M, Mounier L (2013) Visual discrimination of species in dogs (Canis familiaris). Anim Cogn 16:637–651

    PubMed  Article  Google Scholar 

  4. Barrera G, Mustaca A, Bentosela M (2011) Communication between domestic dogs and humans: effects of shelter housing upon the gaze to the human. Anim Cogn 14:727–734

    PubMed  Article  Google Scholar 

  5. Barton J, Radcliffe N, Cherkasova MV, Edelman J, Intriligator JM (2006) Information processing during face recognition: the effects of familiarity, inversion, and morphing on scanning fixations. Perception 35:1089–1105

    PubMed  Article  Google Scholar 

  6. Bethell EJ, Holmes A, Maclarnon A, Semple S (2012) Evidence that emotion mediates social attention in rhesus macaques. PLoS ONE 7(8):e44387. doi:10.1371/journal.pone.0044387

    PubMed Central  PubMed  Article  CAS  Google Scholar 

  7. Bovet D, Vauclair J (2000) Picture recognition in animals and humans. Behav Brain Res 109:143–165

    PubMed  Article  CAS  Google Scholar 

  8. Bruce C (1982) Face recognition by monkeys: absence of an inversion effect. Neuropsychologia 20:515–521

    PubMed  Article  CAS  Google Scholar 

  9. Bruce V, Young A (1986) Understanding face recognition. Br J Psychol 77:305–327

    PubMed  Article  Google Scholar 

  10. Brunet PM, Heisz JJ, Mondloch CJ, Shore DI, Schmidt LA (2009) Shyness and face scanning in children. J Anxiety Disord 23:909–914

    PubMed  Article  Google Scholar 

  11. Cotman CW, Head E (2008) The Canine (Dog) Model of human aging and disease: dietary, environmental and immunotherapy approaches. J Alzheimers Dis 15:685–707

    PubMed  CAS  Google Scholar 

  12. Coulon M, Deputte BL, Heyman Y, Baudoin C (2009) Individual recognition in domestic cattle (Bos taurus): evidence from 2D-images of heads from different breeds. PLoS ONE 4(2):e4441. doi:10.1371/journal.pone.0004441

    PubMed Central  PubMed  Article  CAS  Google Scholar 

  13. Coulon M, Baudoin C, Heyman Y, Deputte BL (2011) Cattle discriminate between familiar and unfamiliar conspecifics by using only head visual cues. Anim Cogn 14:279–290

    PubMed  Article  Google Scholar 

  14. Dahl CD, Wallraven C, Bülthoff HH, Logothetis NK (2009) Humans and macaques employ similar face-processing strategies. Curr Biol 19:509–513

    PubMed  Article  CAS  Google Scholar 

  15. Diamond R, Carey S (1986) Why faces are and are not special: an effect of expertise. J Exp Psychol 115:107–117

    Article  CAS  Google Scholar 

  16. Fagot J, Martin-Malivel J, De′py D (1999) What is the evidence for an equivalence between objects and pictures in birds and nonhuman primates? Curr Psychol Cogn 18:923–949

    Google Scholar 

  17. Gamble AL, Rapee RM (2010) The time-course of attention to emotional faces in social phobia. J Behav Ther Exp Psychiatry 41(1):39–44

    PubMed  Article  Google Scholar 

  18. Gibboni RR, Zimmerman PE, Gothard KM (2009) Individual differences in scan paths correspond with serotonin transporter genotype and behavioral phenotype in rhesus monkeys (Macaca mulatta). Front Behav Neurosci 3(50):1–11. doi:10.3389/neuro.08.050.2009

    Google Scholar 

  19. Gothard KM, Brooks KN, Peterson MA (2009) Multiple perceptual strategies used by macaque monkeys for face recognition. Anim Cogn 12:155–167

    PubMed  Article  Google Scholar 

  20. Guo K, Robertson RG, Mahmoodi S, Tadmor Y, Young MP (2003) How do monkeys view faces?: a study of eye movements. Exp Brain Res 150:363–374

    PubMed  Google Scholar 

  21. Guo K, Meints K, Hall C, Hall S, Mills D (2009) Left gaze bias in humans, rhesus monkeys and domestic dogs. Anim Cogn 12:409–418

    PubMed  Article  Google Scholar 

  22. Hattori Y, Kano F, Tomonaga M (2010) Differential sensitivity to conspecific and allospecific cues in chimpanzees and humans: a comparative eye-tracking study. Biol Lett 6:610–613

    PubMed Central  PubMed  Article  Google Scholar 

  23. Heisz JJ, Shore DI (2008) More efficient scanning for familiar faces. J Vis 8(1):1–10. doi:10.1167/8.1.9

    PubMed  Article  Google Scholar 

  24. Henderson JM, Hollingworth A (1999) High-level scene perception. Annu Rev Psychol 50:243–271

    PubMed  Article  CAS  Google Scholar 

  25. Hirata S, Fuwa K, Sugama K, Kusunoki K, Fujita S (2010) Facial perception of conspecifics: chimpanzees (Pan troglodytes) preferentially attend to proper orientation and open eyes. Anim Cogn 13:679–688

    PubMed  Article  Google Scholar 

  26. Horn L, Range F, Huber L (2013) Dogs’ attention towards humans depends on their relationship, not only on social familiarity. Anim Cogn 16:435–443

    PubMed  Article  Google Scholar 

  27. Jakovcevic A, Elgier AM, Mustaca A, Bentosela M (2012) Do more sociable dogs gaze longer to the human face than less sociable ones? Behav Process 90:217–222

    Article  Google Scholar 

  28. Johnston RA, Edmonds AJ (2009) Familiar and unfamiliar face recognition: a review. Memory 17:577–596

    PubMed  Article  Google Scholar 

  29. Kano F, Tomonaga M (2011) Perceptual mechanism underlying gaze guidance in chimpanzees and humans. Anim Cogn 14:377–386

    PubMed  Article  Google Scholar 

  30. Kaspar K, König P (2012) Emotions and personality traits as high-level factors in visual attention: a review. Front Hum Neurosci 6:321. doi:10.3389/fnhum.2012.00321

    PubMed Central  PubMed  Article  Google Scholar 

  31. Keating CF, Keating EG (1993) Monkeys and mug shots: cues used by rhesus monkeys (Macaca mulatta) to recognize a human face. J Comp Psychol 107:131–139

    PubMed  Article  CAS  Google Scholar 

  32. Kendrick KM, Atkins K, Hinton MR, Broad KD, Fabre-Nys C, Keverne EB (1995) Facial and vocal discrimination in sheep. Anim Behav 49:1665–1676

    Article  Google Scholar 

  33. Kendrick KM, Atkins K, Hinton MR, Heavens P, Keverne B (1996) Are faces special for sheep? Evidence from facial and object discrimination learning tests showing effects of inversion and social familiarity. Behav Process 38:19–35

    Article  Google Scholar 

  34. Kujala MV, Törnqvist H, Somppi S, Hänninen L, Krause CM, Kujala J, Vainio O (2013) Reactivity of dogs’ brain oscillations to visual stimuli measured with non-invasive electroencephalography. PLoS ONE 8(5):e61818. doi:10.1371/journal.pone.0061818

    PubMed Central  PubMed  Article  CAS  Google Scholar 

  35. Lakatos G (2011) Evolutionary approach to communication between humans and dogs. Ann Ist Super Sanità 47:373–377

    PubMed  Google Scholar 

  36. Leonard TK, Blumenthal G, Gothard KM, Hoffman KL (2012) How macaques view familiarity and gaze in conspecific faces. Behav Neurosci. doi:10.1037/a0030348

    PubMed  Google Scholar 

  37. Leopold DA, Rhodes G (2010) A Comparative view of face perception. J Comp Psychol 124:233–251

    PubMed Central  PubMed  Article  Google Scholar 

  38. Marechal L, Roeder JJ (2010) Recognition of faces of known individuals in two lemur species (Eulemur fulvus and E. macaco). Anim Behav 79:1157–1163

    Article  Google Scholar 

  39. Maurer D, Le Grand R, Mondloch CJ (2002) The many faces of configural processing. Trends Cogn Sci 6:255–260

    PubMed  Article  Google Scholar 

  40. Neiworth JJ, Hassett JM, Sylvester CJ (2007) Face processing in humans and new world monkeys: the influence of experiential and ecological factors. Anim Cogn 10:125–134

    PubMed  Article  Google Scholar 

  41. Niu Y, Todd RM, Anderson AK (2012) Affective salience can reverse the effects of stimulus-driven salience on eye movements in complex scenes. Front Psychol 3:336. doi:10.3389/fpsyg.2012.00336

    PubMed Central  PubMed  Google Scholar 

  42. Parr LA (2011a) The evolution of face processing in primates. Philos Trans R Soc B 366:1764–1777

    Article  Google Scholar 

  43. Parr LA (2011b) The inversion effect reveals species differences in face processing. Acta Psychol (Amst) 138:204–210

    Article  Google Scholar 

  44. Parr LA, Dove T, Hopkins WD (1998) Why faces may be special: evidence of the inversion effect in chimpanzees. J Cogn Neurosci 10:615–622

    PubMed  Article  CAS  Google Scholar 

  45. Parr LA, Winslow JT, Hopkins WD, de Waal FBM (2000) Recognizing facial cues: individual discrimination by chimpanzees (Pan troglodytes) and rhesus monkeys (Macaca mulatta). J Comp Psychol 114:47–60

    PubMed Central  PubMed  Article  CAS  Google Scholar 

  46. Parr LA, Siebert E, Taubert J (2011) Effect of familiarity and viewpoint on face recognition in chimpanzees. Perception 40:863–872

    PubMed Central  PubMed  Article  Google Scholar 

  47. Passalacqua C, Marshall-Pescini S, Barnard S, Lakatos G, Valsecchi P, Previde EP (2011) Human-directed gazing behaviour in puppies and adult dogs, Canis lupus familiaris. Anim Behav 82:1043–1050

    Article  Google Scholar 

  48. Phelps MT, Roberts WA (1994) Memory for pictures of upright and inverted primate faces in humans (Homo sapiens), squirrel monkeys (Saimiri sciureus), and pigeons (Columba livia). J Comp Psychol 108:114–125

    PubMed  Article  CAS  Google Scholar 

  49. Pokorny JJ, de Waal FBM (2009) Monkeys recognize the faces of group mates in photographs. Proc Natl Acad Sci USA 106:21539–21543

    PubMed Central  PubMed  Article  Google Scholar 

  50. Pokorny JJ, Webb CE, de Waal FB (2011) An inversion effect modified by expertise in capuchin monkeys. Anim Cogn 14:839–846

    PubMed  Article  Google Scholar 

  51. Racca A, Amadei E, Ligout S, Guo K, Meints K, Mills D (2010) Discrimination of human and dog faces and inversion responses in domestic dogs (Canis familiaris). Anim Cogn 13:525–533

    PubMed  Article  Google Scholar 

  52. Rossion B (2008) Picture-plane inversion leads to qualitative changes of face perception. Acta Psychol (Amst) 128:274–289

    Article  Google Scholar 

  53. Schell A, Rieck K, Schell K, Hammerschmidt K, Fischer J (2011) Adult but not juvenile Barbary macaques spontaneously recognize group members from pictures. Anim Cogn 14:503–509

    PubMed Central  PubMed  Article  Google Scholar 

  54. Somppi S, Törnqvist H, Hanninen L, Krause C, Vainio O (2012) Dogs do look at images: eye tracking in canine cognition research. Anim Cogn 15:163–174

    PubMed  Article  Google Scholar 

  55. Stone SM (2010) Human facial discrimination in horses: can they tell us apart? Anim Cogn 13:51–61

    PubMed  Article  Google Scholar 

  56. Tanaka JW, Farah MJ (1993) Parts and wholes in face recognition. Q J Exp Psychol A 46:225–245

    PubMed  Article  CAS  Google Scholar 

  57. Tate AJ, Fischer H, Leigh AE, Kendrick KM (2006) Behavioural and neurophysiological evidence for face identity and face emotion processing in animals. Philos Trans R Soc Lond B Biol Sci 361:2155–2172

    PubMed Central  PubMed  Article  Google Scholar 

  58. Téglás E, Gergely A, Kupán K, Miklósi Á, Topál J (2012) Dogs’ Gaze following is tuned to human communicative signals. Curr Biol 22:209–212

    PubMed  Article  CAS  Google Scholar 

  59. Topál J, Miklósi Á, Gácsi M, Dóka A, Pongrácz P, Kubinyi E, Virányi Z, Csányi V (2009) The dog as a model for understanding human social behavior. In: Brockmann HJ, Roper TJ, Naguib M, Wynne-Edwards KE, Mitani JC, Simmons LW (eds) Advances in the study of behavior, vol 39. Academic Press, Burlington, pp 71–116

    Google Scholar 

  60. Törnqvist H, Kujala MV, Somppi S, Hänninen L, Pastell M, Krause CM, Kujala J, Vainio O (2013) Visual event-related potentials of dogs: a non-invasive electroencephalography study. Anim Cogn. doi:10.1007/s10071-013-0630-2

    Google Scholar 

  61. Udell MAR, Dorey NR, Wynne CDL (2010a) The performance of stray dogs (Canis familiaris) living in a shelter on human-guided object-choice tasks. Anim Behav 79:717–725

    Article  Google Scholar 

  62. Udell MA, Dorey NR, Wynne CD (2010b) What did domestication do to dogs? A new account of dogs’ sensitivity to human actions. Biol Rev 85:327–345

    PubMed  Article  Google Scholar 

  63. van Belle G, Ramon M, Lefèvre P, Rossion B (2010) Fixation patterns during recognition of personally familiar and unfamiliar faces. Front Psychology 1:20. doi:10.3389/fpsyg.2010.00020

    Google Scholar 

  64. Vas J, Topál J, Gácsi M, Miklósi A, Csányi V (2005) A friend or an enemy? Dogs’ reaction to an unfamiliar person showing behavioural cues of threat and friendliness at different times. Appl Anim Behav Sci 94:99–115

    Article  Google Scholar 

  65. Wobber V, Hare B, Koler-Matznick J, Wrangham R, Tomasello M (2009) Breed differences in domestic dogs’ (Canis familiaris) comprehension of human communicative signals. Interact Stud 10:206–224

    Article  Google Scholar 

  66. Yarbus AL (1967) Eye movements and vision. Plenum Press, New York

    Book  Google Scholar 

  67. Yin RK (1969) Looking at upside-down faces. J Exp Psychol 81:141–145

    Article  Google Scholar 

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Acknowledgments

This study was financially supported by the Academy of Finland (project #137931 to O.Vainio and projects #129346 and #137511 to C.M. Krause) and Foundation of Emil Aaltonen. Special thanks to all pet dog owners for dedication to the training of dogs and providing photographs. We thank also Reeta Törne for assisting in the experiments and data preparation; Timo Murtonen for the custom-built calibration system and chin rests; Katja Irvankoski, Matti Pastell, Antti Flyck and Kristian Törnqvist for the technical support; and Mari Palviainen for the help in kennel dog training. The authors declare that they have no conflict of interest.

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Correspondence to Sanni Somppi.

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Somppi, S., Törnqvist, H., Hänninen, L. et al. How dogs scan familiar and inverted faces: an eye movement study. Anim Cogn 17, 793–803 (2014). https://doi.org/10.1007/s10071-013-0713-0

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Keywords

  • Domestic dog
  • Eye movement tracking
  • Face processing
  • Face inversion effect
  • Face familiarity