Visual Attention in Dogs and the Evolution of Non-Verbal Communication

  • Alejandra RossiEmail author
  • Daniel Smedema
  • Francisco J. Parada
  • Colin Allen


The common history of Homo sapiens and Canis lupus familiaris dates back to between 11,000 and 32,000 years ago, when some wolves (Canis lupus) started living closely with humans. Although we cannot reach back into the past to measure the relative roles of wolves and humans in the ensuing domestication process, it was perhaps the first involving humans and another animal species. Yet its consequences for both species’ history are not completely understood. One of the puzzling aspects yet to be understood about the human–dog dyad is how dogs so readily engage in communication in the context of a social interactions with humans. To be sensitive to the meaning of human speech and gestures, dogs need to attend to various visual and vocal cues, in order to reconstruct the messages from patterns of human behavior that remain stable over time, while also generalizing to unfamiliar, novel contexts. This chapter will discuss this topic in light of some of the recent findings about dogs’ perceptual capacities for social cues. We describe some of the new technologies that are being used to better describe these perceptual processes, and present the results of a preliminary experiment using a portable eye-tracking system to gather data about dogs’ visual attention in a social interaction with humans, ending with a discussion of the possible cognitive mechanisms underlying dogs’ use of human social cues.


Static Distal Gray Wolf Visual Behavior Human Gesture Canis Lupus Familiaris 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This research and the first author were supported by the Office of Vice Provost for Research of Indiana University. We wish to thank our participants and their owners for participating in this study. The authors would also like to thank to Mr. Jeff Sturgeon for technical advice, Dr. Bennett Bertenthal for helpful comments and discussion, Dr. Nicholas Port and the IU School of Optometry for their generous help and last but not least to the Indiana Statistical Consulting Center, particularly to Stephanie Dickinson for her guidance.


  1. Axelsson, E., Ratnakumar, A., Arendt, M. L., Maqbool, K., Webster, M. T., Perloski, M., et al. (2013). The genomic signature of dog domestication reveals adaptation to a starch-rich diet. Nature, 495(7441), 360–364.Google Scholar
  2. Bailey, I., Myatt, J. P., Wilson, A. M. (2013). Group hunting within the Carnivora: Physiological, cognitive and environmental influences on strategy and cooperation. Behavioral Ecology and Sociobiology, 67(1), 1–17.Google Scholar
  3. Bar-Yosef, O. (1998). On the nature of transitions: The middle to upper Palaeolithic and the Neolithic revolution. Cambridge Archaeological Journal, 8(2), 141–163.Google Scholar
  4. Barton, R. A. (1996). Neocortex size and behavioural ecology in primates. Proceedings of the Royal Society B, 263(1367), 173–177.Google Scholar
  5. Bernstein, I. S. (1970). Primate status hierarchies. Primate Behavior, 1, 71–109.Google Scholar
  6. Bertenthal, B., & Boyer, T. (2012). Developmental changes in Infants' visual attention to pointing. Journal of Vision, 12(9), 480.Google Scholar
  7. Brugman, H., & Russel, A. (2004). Annotating multimedia/multi-modal resources with ELAN. Proceedings of the Fourth International Conference on Language Resources and Evaluation (pp. 2065–2068). Citeseer.Google Scholar
  8. Buttelmann, D., & Tomasello, M. (2013). Can domestic dogs (Canis familiaris) use referential emotional expressions to locate hidden food? Animal Cognition, 16(1), 137–145.Google Scholar
  9. Cappuccio, M. L., & Shepherd, S. V. (2013). 13 Pointing Hand: Joint Attention and Embodied Symbols. The Hand, an Organ of the Mind: What the Manual Tells the Mental, 303.Google Scholar
  10. Clutton-Brock, J. (1995). Origins of the dog: Domestication and early history. In: J. Serpell (Ed.), The domestic dog: Its evolution, behaviour, and interactions with people (pp. 7–20). Cambridge: Cambridge University Press.Google Scholar
  11. Clutton-Brock, J. (1999). A natural history of domesticated mammals (2nd ed.). New York, USA: Natural History Museum.Google Scholar
  12. Clutton-Brock, J., & Wilson, D. E. (2002). Mammals. Smithsonian handbooks (1st US ed.). London: DK.Google Scholar
  13. Cordoni, G., & Palagi, E. (2008). Reconciliation in wolves (Canis lupus): New evidence for a comparative perspective. Ethology, 114(3), 298–308.Google Scholar
  14. Coren, S. (2005). How dogs think: Understanding the canine mind. New York: Simon and Schuste.Google Scholar
  15. Crockford, S. J., & Iaccovoni, A. (2000). Dogs through time: An archaeological perspective. Proceedings of the 1st ICAZ Symposium on the History of the Domestic Dog. BAR international series, Vol. 889. Oxford, England: Archaeopress.Google Scholar
  16. Dalton, K. M., Nacewicz, B. M., Johnstone, T., Schaefer, H. S., Gernsbacher, M. A., Goldsmith, H. H., Alexander, A. L., et al. (2005). Gaze fixation and the neural circuitry of face processing in autism. Nature Neuroscience, 8(4), 519–526.Google Scholar
  17. Davis, S. J. M., & Valla, F. R. (1978). Evidence for domestication of dog 12,000 years ago in Natufian of Israel. Nature, 276(5688), 608–610.Google Scholar
  18. Diamond, J. (2002). Evolution, consequences and future of plant and animal domestication. Nature, 418(6898), 700–707.Google Scholar
  19. Driscoll, C. A., Macdonald, D. W., & O’Brien, S. J. (2009). From wild animals to domestic pets, an evolutionary view of domestication. Proceedings of the National Academy of Sciences USA, 106, 19971–9978.Google Scholar
  20. Duchowski, A. T. (2007). Eye tracking methodology: Theory and practice. New York: Springer.Google Scholar
  21. Elgier, A. M., Jakovcevic, A., Mustaca, A. E., & Bentosela, M. (2009). Learning and owner-stranger effects on interspecific communication in domestic dogs (Canis familiaris). Behavioural Processes, 81(1), 44–49.Google Scholar
  22. Felmingham, K. L., Rennie, C., Manor, B., & Bryant, R. A. (2011). Eye tracking and physiological reactivity to threatening stimuli in posttraumatic stress disorder. Journal of Anxiety Disorders, 25(5), 668–673.Google Scholar
  23. Fukuzawa, M., Mills, D. S., & Cooper, J. J. (2005). More than just a word: Non-semantic command variables affect obedience in the domestic dog (Canis familiaris). Applied Animal Behaviour Science, 91(1), 129–141.Google Scholar
  24. Gomez, J. C. (2005). Species comparative studies and cognitive development. Trends in Cognitive Sciences, 9(3), 118–125.Google Scholar
  25. Gredebäck, G., Johnson, S., & Von Hofsten, C. (2009). Eye tracking in infancy research. Developmental Neuropsychology, 35(1), 1–19.Google Scholar
  26. Hare, B., Brown, M., Williamson, C., & Tomasello, M. (2002). The domestication of social cognition in dogs. Science, 298(5598), 1634–1636.Google Scholar
  27. Hare, B., & Tomasello, M. (2005). Human-like social skills in dogs? Trends in Cognitive Sciences, 9(9), 439–444.Google Scholar
  28. Hattori, Y., Kano, F., & Tomonaga, M. (2010). Differential sensitivity to conspecific and allospecific cues in chimpanzees and humans: Acomparative eye-tracking study. Biology Letters, 6(5), 610–613.Google Scholar
  29. Hemmer, H. (1990). Domestication: The decline of environmental appreciation (2nd ed.). Cambridge, England: Cambridge University Press.Google Scholar
  30. 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. Animal Cognition, 13(5), 679–688.Google Scholar
  31. Holzman, P. S., Proctor, L. R., Levy, D. L., Yasillo, N. J., Meltzer, H. Y., & Hurt, S. W. (1974). Eye-tracking dysfunctions in schizophrenic patients and their relatives. Archives of General Psychiatry, 31(2), 143.Google Scholar
  32. Ittyerah, M., & Gaunet, F. (2009). The response of guide dogs and pet dogs (Canis Familiaris) to cues of human referential communication (pointing and gaze). Animal Cognition, 12(2), 257–265.Google Scholar
  33. Kaminski, J., Call, J., & Fischer, J. (2004). Word learning in a domestic dog: Evidence for “fast mapping”. Science, 304(5677), 1682–1683.Google Scholar
  34. Kaminski, J., Neumann, M., Brauer, J., Call, J., & Tomasello, M. (2011). Dogs, Canis familiaris, communicate with humans to request but not to inform. Animal Behaviour, 82(4), 651–658Google Scholar
  35. Kano, F., Hirata, S., Call, J., & Tomonaga, M. (2011). The visual strategy specific to humans among hominids: A study using the gap-overlap paradigm. Vision research, 51(23–24), 2348–2355.Google Scholar
  36. Kano, F., & Tomonaga, M. (2009). How chimpanzees look at pictures: A comparative eye-tracking study. Proceedings of the Royal Society of London. Series B: Biological, 276(1664), 1949–1955.Google Scholar
  37. Kano, F., & Tomonaga, M. (2010). Attention to Emotional Scenes Including Whole-Body Expressions in Chimpanzees (Pan troglodytes). Journal of Comparative Psychology, 124(3), 287–294.Google Scholar
  38. Kano, F., & Tomonaga, M. (2013). Head-mounted eye tracking of a chimpanzee under naturalistic conditions. PLoS ONE, 8(3), e59785.Google Scholar
  39. Kjaersgaard, A., Pertoldi, C., Loeschcke, V., & Hansen, D. W. (2008). Tracking the gaze of birds. Journal of Avian Biology, 39(4), 466–469.Google Scholar
  40. Koler-Matznick, J. (2002). The origin of the dog revisited. Anthrozoos, 15(2), 98–118.Google Scholar
  41. Lakatos, G., Soproni, K., Doka, A., & Miklósi, A. (2009). A comparative approach to dogs’ (Canis familiaris) and human infants’ comprehension of various forms of pointing gestures. Animal Cognition, 12(4), 621–631.Google Scholar
  42. Larson, G., Karlsson, E. K., Perri, A., Webster, M. T., Ho, S. Y., Peters, J., et al. (2012). Rethinking dog domestication by integrating genetics, archeology, and biogeography. Proceedings of the National Academy of Sciences USA, 109(23), 8878–8883.Google Scholar
  43. Lupo, K. (2011). A dog is for hunting.Ethnozooarchaeology: The present and past of human–animal relationships, 4–12.Google Scholar
  44. Machado, C. J., & Nelson, E. E. (2011). Eye-tracking with Nonhuman primates is now more accessible than ever before. American Journal of Primatology, 73(6), 562–569.Google Scholar
  45. Mech, L. D. (1970). The wolf: The ecology and behavior of an endangered species. (1st ed.). Published for the American Museum of Natural History. Garden City, New York: Natural History Press.Google Scholar
  46. Mech, L. D. (2012). Wolf. New York: Random House Digital.Google Scholar
  47. Merola, I., Prato-Previde, E., & Marshall-Pescini, S. (2012). Dogs’ social referencing towards owners and strangers. PLoS ONE, 7(10), e47653.Google Scholar
  48. Miklósi, A., Pongracz, P., Lakatos, G., Topal, J., & Csanyi, V. (2005). A comparative study of the use of visual communicative signals in interactions between dogs (Canis familiaris) and humans and cats (Felis catus) and humans. Journal of Comparative Psychology, 119(2), 179–186.Google Scholar
  49. Moore, C. E., & Dunham, P. J. (1995). Joint attention: Its origins and role in development. New York: Lawrence Erlbaum Associates, Inc.Google Scholar
  50. Muro, C., Escobedo, R., Spector, L., & Coppinger, R. P. (2011). Wolf-pack (Canis lupus) hunting strategies emerge from simple rules in computational simulations. Behavioural Processes, 88(3), 192–197.Google Scholar
  51. Olsen, S. J. (1985).Origins of the domestic dog: The fossil record. Tucson, Arizona: University of Arizona Press.Google Scholar
  52. Packer, C., & Ruttan, L. (1988). The evolution of cooperative hunting. The American Naturalist, 132(2), 159–198.Google Scholar
  53. Palagi, E., & Cordoni, G. (2009). Postconflict third-party affiliation in Canis lupus: Do wolves share similarities with the great apes? Animal Behaviour, 78(4), 979–986.Google Scholar
  54. Pilley, J. W., & Reid, A. K. (2011). Border collie comprehends object names as verbal referents. Behavioural Processes, 86(2), 184–195.Google Scholar
  55. Ramos, D., & Ades, C. (2012). Two-item sentence comprehension by a dog (Canis familiaris). PLoS ONE, 7(2), e29689.Google Scholar
  56. Reader, S. M., Laland, K. N. (2002). Social intelligence, innovation, and enhanced brain size in primates. Proceedings of the National Academy of Sciences USA, 99(7), 4436–4441.Google Scholar
  57. Ruusila, V., Pesonen, M. (2004). Interspecific cooperation in human (Homo sapiens) hunting: The benefits of a barking dog (Canis familiaris). Annales Zoologici Fennici, 41(4), 545–549.Google Scholar
  58. Serpell, J. (1995). The domestic dog: Its evolution, behaviour, and interactions with people. Cambridge: Cambridge University Press.Google Scholar
  59. Shepherd, S. V. (2010). Following gaze: Gaze-following behavior as a window into social cognition. Frontiers in Integrative Neuroscience, 4(5), 1–13.Google Scholar
  60. Shultz, S., & Dunbar, R. I. (2007). The evolution of the social brain: Anthropoid primates contrast with other vertebrates. Proceedings of the Royal Society B: Biological Sciences, 274(1624), 2429–2436.Google Scholar
  61. Smith, L. B., Yu, C., & Pereira, A. F. (2011). Not your mother’s view: The dynamics of toddler visual experience. Developmental Science, 14(1), 9–17.Google Scholar
  62. Somppi, S., Tornqvist, H., Hanninen, L., Krause, C., & Vainio, O. (2011). Dogs do look at images: Eye tracking in canine cognition research. Animal Cognition, 11(1), 167–174.Google Scholar
  63. Soproni, K., Miklósi, A., Topal, J., & Csanyi, V. (2001). Comprehension of human communicative signs in pet dogs (Canis familiaris). Journal of Comparative Psychology, 115(2), 122–126.Google Scholar
  64. Soproni, K., Miklósi, A., Topal, J., & Csanyi, V. (2002). Dogs’ (Canis familiaris) responsiveness to human pointing gestures. Journal of Comparative Psychology, 116(1), 27–34.Google Scholar
  65. Spencer, J. P., Smith, L. B., & Thelen, E. (2001). Tests of a dynamic systems account of the A-not-B error: The influence of prior experience on the spatial memory abilities of two-year-olds. Child development, 72(5), 1327–1346.Google Scholar
  66. Sullivan, J. O. (1978). Variability in the wolf, a group hunter. In R. L. Hall & H. S. Sharp (Eds.) Wolf and man: Evolution in parallel ( pp. 31–40). New York: Academic Press.Google Scholar
  67. Teglas, E., Gergely, A., Kupan, K., Miklósi, A., & Topal, J. (2012). Dogs’ gaze following is tuned to human communicative signals. Current Biology, 22(3), 209–212.Google Scholar
  68. Tinbergen, N. (1963). On aims and methods of ethology. Zeitschrift für Tierpsychologie, 20(4), 410–433.Google Scholar
  69. Vila, C., Savolainen, P., Maldonado, J. E., Amorim, I. R., Rice, J. E., Honeycutt, R. L., et al. (1997). Multiple and ancient origins of the domestic dog. Science, 276(5319), 1687–1689.Google Scholar
  70. Weisdorf, J. L. (2005). From foraging to farming: Explaining the Neolithic Revolution. Journal of Economic Surveys, 19(4), 561–586.Google Scholar
  71. Williams, F. J., Mills, D. S., & Guo, K. (2011). Development of a head-mounted, eye-tracking system for dogs. Journal of neuroscience methods, 194(2), 259–265.Google Scholar
  72. Yarbus, A. L., Haigh, B., & Rigss, L. A. (1967).Eye movements and vision (vol 2. vol 5.10). New York: Plenum press.Google Scholar
  73. Zola, S., & Manzanares, C. (2011). A Simple behavioral task combined with Noninvasive infrared eye-tracking for examining the potential impact of viruses and vaccines on memory and other cognitive functions in humans and Nonhuman primates. Journal of Medical Primatology, 40(4), 282–283.Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Alejandra Rossi
    • 1
    • 2
    Email author
  • Daniel Smedema
    • 1
  • Francisco J. Parada
    • 2
    • 3
  • Colin Allen
    • 1
  1. 1.Cognitive Science ProgramIndiana UniversityBloomingtonUSA
  2. 2.Program in NeuroscienceIndiana UniversityBloomingtonUSA
  3. 3.Psychological and Brain SciencesIndiana UniversityBloomingtonUSA

Personalised recommendations