Animal Cognition

, Volume 16, Issue 6, pp 973–982 | Cite as

Visual event-related potentials of dogs: a non-invasive electroencephalography study

  • Heini Törnqvist
  • Miiamaaria V. Kujala
  • Sanni Somppi
  • Laura Hänninen
  • Matti Pastell
  • Christina M. Krause
  • Jan Kujala
  • Outi Vainio
Original Paper

Abstract

Previously, social and cognitive abilities of dogs have been studied within behavioral experiments, but the neural processing underlying the cognitive events remains to be clarified. Here, we employed completely non-invasive scalp-electroencephalography in studying the neural correlates of the visual cognition of dogs. We measured visual event-related potentials (ERPs) of eight dogs while they observed images of dog and human faces presented on a computer screen. The dogs were trained to lie still with positive operant conditioning, and they were neither mechanically restrained nor sedated during the measurements. The ERPs corresponding to early visual processing of dogs were detectable at 75–100 ms from the stimulus onset in individual dogs, and the group-level data of the 8 dogs differed significantly from zero bilaterally at around 75 ms at the most posterior sensors. Additionally, we detected differences between the responses to human and dog faces in the posterior sensors at 75–100 ms and in the anterior sensors at 350–400 ms. To our knowledge, this is the first illustration of completely non-invasively measured visual brain responses both in individual dogs and within a group-level study, using ecologically valid visual stimuli. The results of the present study validate the feasibility of non-invasive ERP measurements in studies with dogs, and the study is expected to pave the way for further neurocognitive studies in dogs.

Keywords

Electroencephalography Event-related potential Dog Canis familiaris Visual cognition 

References

  1. Adachi I, Kuwahata H, Fujita K (2007) Dogs recall their owner’s face upon hearing the owner’s voice. Anim Cogn 10:17–21PubMedCrossRefGoogle Scholar
  2. Allison T, Ginter H, McCarthy G, Nobre AC, Puce A, Luby M, Spencer DD (1994) Face recognition in human extrastriate cortex. J Neurophysiol 71:821–825PubMedGoogle Scholar
  3. Allison T, Puce A, Spencer DD, McCarthy G (1999) Electrophysiological studies of human face perception. I: potentials generated in occipitotemporal cortex by face and non-face stimuli. Cereb Cortex 9:415–430PubMedCrossRefGoogle Scholar
  4. Autier-Dérian D, Deputte BL, Chalvet-Monfray K, Coulon M, Mounier L (2013) Visual discrimination of species in dogs (Canis familiaris). Anim Cogn. doi:10.1007/s10071-013-0600-8 PubMedGoogle Scholar
  5. Avidan G, Harel M, Hendler T, Ben-Bashat D, Zohary E, Malach R (2002) Contrast sensitivity in human visual areas and its relationship to object recognition. J Neurophysiol 87:3102–3116PubMedGoogle Scholar
  6. Berendt M, Hogenhaven H, Flagstad A, Dam M (1999) Electroencephalography in dogs with epilepsy: similarities between human and canine findings. Acta Neurol Scand 99:276–283PubMedCrossRefGoogle Scholar
  7. Berns GS, Brooks AM, Spivak M (2012) Functional MRI in awake unrestrained dogs. PLoS ONE. doi:10.1371/journal.pone.0038027 PubMedGoogle Scholar
  8. Bichsel P, Oliver JE, Coulter DB, Brown J (1988) Recording of visual-evoked potentials in dogs with scalp electrodes. J Vet Intern Med 2:145–149PubMedCrossRefGoogle Scholar
  9. Bruce V, Young AW (1998) In the eye of the beholder: the science of face perception. University Press, OxfordGoogle Scholar
  10. Bruce CJ, Desimone R, Gross CG (1981) Visual properties of neurones in a polysensory area in the superior temporal sulcus of the macaque. J Neurophysiol 46:369–384PubMedGoogle Scholar
  11. Carmel D, Bentin S (2002) Domain specificity versus expertise: factors influencing distinct processing of faces. Cognition 83:1–29PubMedCrossRefGoogle Scholar
  12. Caton R (1875) The electric currents of the brain. Br Med J 2:278Google Scholar
  13. Coles MGH, Rugg MD (1995) Event-related brain potentials: an introduction. In: Rugg MD, Coles MGH (eds) Electrophysiology of mind: event-related brain potentials and cognition, 1st edn. Oxford University Press, New York, pp 1–26Google Scholar
  14. Fukushima H, Hirata S, Ueno A, Matsuda G, Fuwa K, Sugama K, Kusunoki K, Hirai M, Hiraki K, Tomonaga M, Hasegawa T (2010) Neural correlates of face and object perception in an awake chimpanzee (Pan troglodytes) examined by scalp-surface event-related potentials. PLoS ONE. doi:10.1371/journal.pone.0013366 Google Scholar
  15. Gardner JL, Sun P, Waggoner RA, Ueno K, Tanaka K, Cheng K (2005) Contrast adaptation and representation in human early visual cortex. Neuron 47:607–620PubMedCrossRefGoogle Scholar
  16. Gross CG, Rocha-Miranda CE, Bender DB (1972) Visual properties of neurons in inferotemporal cortex of the Macaque. J Neurophysiol 35:96–111PubMedGoogle Scholar
  17. Guo K, Meints K, Hall C, Hall S, Mills D (2009) Left gaze bias in humans, rhesus monkeys and domestic dogs. Anim Cogn 12:409–418PubMedCrossRefGoogle Scholar
  18. Haider M, Spong P, Lindsley DB (1964) Attention, vigilance, and cortical evoked-potentials in humans. Science 145:180–182PubMedCrossRefGoogle Scholar
  19. Hänninen L, Mäkelä JP, Rushen J, de Passillé AM, Saloniemi H (2008) Assessing sleep state in calves through electrophysiological and behavioural recordings: a preliminary study. Appl Anim Behav Sci 111:235–250CrossRefGoogle Scholar
  20. Hare B, Brown M, Williamson C, Tomasello M (2002) The domestication of social cognition in dogs. Science 298:1634–1636PubMedCrossRefGoogle Scholar
  21. Haxby JV, Horwitz B, Ungerleider LG, Maisog JM, Pietrini P, Grady CL (1994) The functional organization of human extrastriate cortex: a PET-rCBF study of selective attention to faces and locations. J Neurosci 14:6336–6353PubMedGoogle Scholar
  22. Howell TJ, Conduit R, Toukhsati S, Bennett P (2012) Auditory stimulus discrimination recorded in dogs, as indicated by mismatch negativity (MMN). Behav Process 89:8–13CrossRefGoogle Scholar
  23. James FMK, Allen DG, Bersenas AME, Grovum WL, Kerr CL, Monteith G, Parent JM, Poma R (2011) Investigation of the use of three electroencephalographic electrodes for long-term electroencephalographic recording in awake and sedated dogs. Am J Vet Res 72:384–390PubMedCrossRefGoogle Scholar
  24. Jeserevics J, Viitmaa R, Cizinauskas S, Sainio K, Jokinen TS, Snellman M, Bellino C, Bergamasco L (2007) Electroencephalography findings in healthy and finnish spitz dogs with epilepsy: visual and background quantitative analysis. J Vet Intern Med 21:1299–1306PubMedCrossRefGoogle Scholar
  25. Kanwisher N, McDermott J, Chun MM (1997) The fusiform face area: a module in human extrastriate cortex specialized for face perception. J Neurosci 17:4302–4311PubMedGoogle Scholar
  26. Kendrick KM (1991) How the sheep’s brain controls the visual recognition of animals and humans. J Anim Sci 69:5008–5016PubMedGoogle Scholar
  27. Kendrick KM (1994) Neurobiological correlates of visual and olfactory recognition in sheep. Behav Process 33:89–112CrossRefGoogle Scholar
  28. Kendrick KM, Baldwin BA (1987) Cells in temporal cortex of conscious sheep can respond preferentially to the sight of faces. Science 236:448–450PubMedCrossRefGoogle Scholar
  29. King AS (1999) Physiological and clinical anatomy of the domestic mammals. Volume 1. Central nervous system. Oxford University Press, OxfordGoogle Scholar
  30. Koelsch S, Heinke W, Sammler D, Olthoff D (2006) Auditory processing during deep propofol sedation and recovery from unconsciousness. Clin Neurophysiol 117:1746–1759PubMedCrossRefGoogle Scholar
  31. Kujala MV, Tanskanen T, Parkkonen L, Hari R (2009) Facial expressions of pain modulate observer’s long-latency responses in superior temporal sulcus. Hum Brain Mapp 30:3910–3923PubMedCrossRefGoogle Scholar
  32. Leopold DA, Rhodes G (2010) A comparative view of face perception. J Comp Psychol 124:233–251PubMedCrossRefGoogle Scholar
  33. Lopes da Silva FH, van Rotterdam A, Storm van Leeuwen W, Tielen AM (1970a) Dynamic characteristics of visual evoked potentials in the dog. I. Cortical and subcortical potentials evoked by sine wave modulated light. Electroencephalogr Clin Neurophysiol 29:246–259PubMedCrossRefGoogle Scholar
  34. Lopes da Silva FH, van Rotterdam A, Storm van Leeuwen W, Tielen AM (1970b) Dynamic characteristics of visual evoked potentials in the dog. II. Beta frequency selectivity in evoked potentials and background activity. Electroencephalogr Clin Neurophysiol 29:260–268PubMedCrossRefGoogle Scholar
  35. Luck SJ (2005) An introduction to the event-related potential technique. The MIT Press, LondonGoogle Scholar
  36. Mangun GR (1995) Neural mechanisms of visual selective attention. Psychophysiology 32:4–18PubMedCrossRefGoogle Scholar
  37. McCarthy G, Puce A, Gore JC, Allison T (1997) Face-specific processing in the human fusiform gyrus. J Cogn Neurosci 9:605–610PubMedCrossRefGoogle Scholar
  38. McKone E, Kanwisher N, Duchaine BC (2006) Can generic expertise explain special processing for faces? Trends Cogn Sci 11:8–15PubMedCrossRefGoogle Scholar
  39. Nagasawa M, Murai K, Mogi K, Kikusui T (2011) Dogs can discriminate human smiling faces from blank expressions. Anim Cogn 14:525–533PubMedCrossRefGoogle Scholar
  40. O’Donnell B, Swearer J, Smith L, Hokama H, McCarley R (1997) A topographic study of ERPs elicited by visual feature discrimination. Brain Topogr 10:133–143PubMedCrossRefGoogle Scholar
  41. Otten LJ, Rugg MD (2005) Interpreting event-related brain potentials. In: Handy TC (ed) Event-related potentials. A methods handbook. The MIT Press, Cambridge, pp 3–16Google Scholar
  42. Pellegrino FC, Sica REP (2004) Canine electroencephalographic recording technique: findings in normal and epileptic dogs. Clin Neurophysiol 115:477–487PubMedCrossRefGoogle Scholar
  43. Perrett DI, Rolls ET, Caan W (1982) Visual neurones responsive to faces in the monkey temporal cortex. Exp Brain Res 47:329–342PubMedCrossRefGoogle Scholar
  44. Perrett DI, Smith PA, Potter DD, Mistlin AJ, Head AS, Milner AD, Jeeves MA (1985) Visual cells in the temporal cortex sensitive to face view and gaze direction. Proc R Soc Lond B 223:293–317PubMedCrossRefGoogle Scholar
  45. Perrett DI, Mistlin AJ, Chitty AJ, Smith PA, Potter DD, Broennimann R, Harries M (1988) Specialized face processing and hemispheric asymmetry in man and monkey: evidence from single unit and reaction time studies. Behav Brain Res 29:245–258PubMedCrossRefGoogle Scholar
  46. Pineda JA, Sebestyen G, Nava C (1994) Face recognition as a function of social attention in non-human primates: an ERP study. Cogn Brain Res 2:1–12CrossRefGoogle Scholar
  47. Puce A, Allison T, Gore JC, McCarthy G (1995) Face-sensitive regions in human extrastriate cortex studied by functional MRI. J Neurophysiol 74:1192–1199PubMedGoogle Scholar
  48. 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 13:525–533PubMedCrossRefGoogle Scholar
  49. Range F, Aust U, Steurer M, Huber L (2008) Visual categorization of natural stimuli by domestic dogs. Anim Cogn 11:339–347PubMedCrossRefGoogle Scholar
  50. Rolls ET (1994) Brain mechanisms for invariant visual recognition and learning. Behav Process 33:113–138CrossRefGoogle Scholar
  51. Rolls ET, Baylis GC (1986) Size and contrast have only small effects on the responses to faces of neurons in the cortex of the superior temporal sulcus of the monkey. Exp Brain Res 65:38–48PubMedCrossRefGoogle Scholar
  52. Somppi S, Törnqvist H, Hänninen L, Krause C, Vainio O (2012) Dogs do look at images: eye tracking in canine cognition research. Anim Cogn 15:163–174PubMedCrossRefGoogle Scholar
  53. Tarr MJ, Cheng YD (2003) Learning to see faces and objects. Trends Cogn Sci 7:23–30PubMedCrossRefGoogle Scholar
  54. 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 B 361:2155–2172CrossRefGoogle Scholar
  55. Ternman E, Hänninen L, Pastell M, Agenäs S, Nielsen P (2012) Sleep in dairy cows recorded with a non-invasive EEG technique. Appl Anim Behav Sci 140:25–32CrossRefGoogle Scholar
  56. Tsao DY, Freiwald WA, Knutsen TA, Mandeville JB, Tootell RBH (2003) Faces and objects in macaque cerebral cortex. Nat Neurosci 6:989–995PubMedCrossRefGoogle Scholar
  57. Tsao DY, Freiwald WA, Tootell RBH, Livingstone MS (2006) A cortical region consisting entirely of face-selective cells. Science 311:670–674PubMedCrossRefGoogle Scholar
  58. Ueno A, Hirata S, Fuwa K, Sugama K, Kusunoki K, Matsuda G, Fukushima H, Hiraki K, Tomonaga M, Hasegawa T (2008) Auditory ERPs to stimulus deviance in an awake chimpanzee (Pan troglodytes): towards hominid cognitive neurosciences. PLoS ONE. doi:10.1371/journal.pone.0001442 Google Scholar
  59. Ueno A, Hirata S, Fuwa K, Sugama K, Kusunoki K, Matsuda G, Fukushima H, Hiraki K, Tomonaga M, Hasegawa T (2010) Brain activity in an awake chimpanzee in response to the sound of her own name. Biol Lett 6:311–313PubMedCrossRefGoogle Scholar
  60. Van der Marel E, Dagnelie G, Spekreijse H (1984) Subdurally recorded pattern and luminance EPs in the alert rhesus monkey. Electroencephalogr Clin Neurophysiol 57:354–368PubMedCrossRefGoogle Scholar
  61. Vogel EK, Luck SJ (2000) The visual N1 component as an index of a discrimination process. Psychophysiology 37:190–203PubMedCrossRefGoogle Scholar
  62. Woodman GF (2012) Homologues of human ERP components in nonhuman primates. In: Luck SJ, Kappenman ES (eds) Oxford handbook of event-related potential components, 1st edn. Oxford University Press, New York, pp 611–626Google Scholar
  63. Woodman GF, Kang M-S, Rossi AF, Schall JD (2007) Nonhuman primate event-related potentials indexing covert shifts of attention. Proc Natl Acad Sci USA 104:15111–15116PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Heini Törnqvist
    • 1
    • 2
  • Miiamaaria V. Kujala
    • 1
    • 3
    • 4
  • Sanni Somppi
    • 1
  • Laura Hänninen
    • 5
  • Matti Pastell
    • 6
  • Christina M. Krause
    • 2
  • Jan Kujala
    • 3
    • 7
  • Outi Vainio
    • 1
  1. 1.Department of Equine and Small Animal Medicine, Faculty of Veterinary MedicineUniversity of Helsinki HelsinkiFinland
  2. 2.Cognitive Science, Institute of Behavioural Sciences, Faculty of Behavioural SciencesUniversity of HelsinkiHelsinkiFinland
  3. 3. Brain Dynamics and Cognition Team, Lyon Neuroscience Research CenterINSERM U1028, CNRS UMR5292BronFrance
  4. 4.Department of Biomedical Engineering and Computational ScienceAalto UniversityEspooFinland
  5. 5.Department of Production Animal Medicine, Faculty of Veterinary MedicineUniversity of HelsinkiHelsinkiFinland
  6. 6.Department of Agricultural Sciences, Faculty of Agriculture and ForestryUniversity of HelsinkiHelsinkiFinland
  7. 7.Brain Research Unit, O. V. Lounasmaa LaboratoryAalto UniversityEspooFinland

Personalised recommendations