Skip to main content
Log in

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

  • Original Paper
  • Published:
Animal Cognition Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

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

    Article  PubMed  Google Scholar 

  • Allison T, Ginter H, McCarthy G, Nobre AC, Puce A, Luby M, Spencer DD (1994) Face recognition in human extrastriate cortex. J Neurophysiol 71:821–825

    PubMed  CAS  Google Scholar 

  • 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 9:415–430

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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 87:3102–3116

    PubMed  Google Scholar 

  • Berendt M, Hogenhaven H, Flagstad A, Dam M (1999) Electroencephalography in dogs with epilepsy: similarities between human and canine findings. Acta Neurol Scand 99:276–283

    Article  PubMed  CAS  Google Scholar 

  • Berns GS, Brooks AM, Spivak M (2012) Functional MRI in awake unrestrained dogs. PLoS ONE. doi:10.1371/journal.pone.0038027

    PubMed  Google Scholar 

  • Bichsel P, Oliver JE, Coulter DB, Brown J (1988) Recording of visual-evoked potentials in dogs with scalp electrodes. J Vet Intern Med 2:145–149

    Article  PubMed  CAS  Google Scholar 

  • Bruce V, Young AW (1998) In the eye of the beholder: the science of face perception. University Press, Oxford

    Google Scholar 

  • 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 46:369–384

    PubMed  CAS  Google Scholar 

  • Carmel D, Bentin S (2002) Domain specificity versus expertise: factors influencing distinct processing of faces. Cognition 83:1–29

    Article  PubMed  Google Scholar 

  • Caton R (1875) The electric currents of the brain. Br Med J 2:278

    Google Scholar 

  • 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 1–26

    Google Scholar 

  • 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 

  • Gardner JL, Sun P, Waggoner RA, Ueno K, Tanaka K, Cheng K (2005) Contrast adaptation and representation in human early visual cortex. Neuron 47:607–620

    Article  PubMed  CAS  Google Scholar 

  • Gross CG, Rocha-Miranda CE, Bender DB (1972) Visual properties of neurons in inferotemporal cortex of the Macaque. J Neurophysiol 35:96–111

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Haider M, Spong P, Lindsley DB (1964) Attention, vigilance, and cortical evoked-potentials in humans. Science 145:180–182

    Article  PubMed  CAS  Google Scholar 

  • 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 111:235–250

    Article  Google Scholar 

  • Hare B, Brown M, Williamson C, Tomasello M (2002) The domestication of social cognition in dogs. Science 298:1634–1636

    Article  PubMed  CAS  Google Scholar 

  • 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 14:6336–6353

    PubMed  CAS  Google Scholar 

  • Howell TJ, Conduit R, Toukhsati S, Bennett P (2012) Auditory stimulus discrimination recorded in dogs, as indicated by mismatch negativity (MMN). Behav Process 89:8–13

    Article  Google Scholar 

  • 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 72:384–390

    Article  PubMed  Google Scholar 

  • 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 21:1299–1306

    Article  PubMed  Google Scholar 

  • Kanwisher N, McDermott J, Chun MM (1997) The fusiform face area: a module in human extrastriate cortex specialized for face perception. J Neurosci 17:4302–4311

    PubMed  CAS  Google Scholar 

  • Kendrick KM (1991) How the sheep’s brain controls the visual recognition of animals and humans. J Anim Sci 69:5008–5016

    PubMed  CAS  Google Scholar 

  • Kendrick KM (1994) Neurobiological correlates of visual and olfactory recognition in sheep. Behav Process 33:89–112

    Article  Google Scholar 

  • Kendrick KM, Baldwin BA (1987) Cells in temporal cortex of conscious sheep can respond preferentially to the sight of faces. Science 236:448–450

    Article  PubMed  CAS  Google Scholar 

  • King AS (1999) Physiological and clinical anatomy of the domestic mammals. Volume 1. Central nervous system. Oxford University Press, Oxford

    Google Scholar 

  • Koelsch S, Heinke W, Sammler D, Olthoff D (2006) Auditory processing during deep propofol sedation and recovery from unconsciousness. Clin Neurophysiol 117:1746–1759

    Article  PubMed  CAS  Google Scholar 

  • 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 30:3910–3923

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • 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 29:246–259

    Article  PubMed  CAS  Google Scholar 

  • 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 29:260–268

    Article  PubMed  CAS  Google Scholar 

  • Luck SJ (2005) An introduction to the event-related potential technique. The MIT Press, London

    Google Scholar 

  • Mangun GR (1995) Neural mechanisms of visual selective attention. Psychophysiology 32:4–18

    Article  PubMed  CAS  Google Scholar 

  • McCarthy G, Puce A, Gore JC, Allison T (1997) Face-specific processing in the human fusiform gyrus. J Cogn Neurosci 9:605–610

    Article  PubMed  CAS  Google Scholar 

  • McKone E, Kanwisher N, Duchaine BC (2006) Can generic expertise explain special processing for faces? Trends Cogn Sci 11:8–15

    Article  PubMed  Google Scholar 

  • Nagasawa M, Murai K, Mogi K, Kikusui T (2011) Dogs can discriminate human smiling faces from blank expressions. Anim Cogn 14:525–533

    Article  PubMed  Google Scholar 

  • O’Donnell B, Swearer J, Smith L, Hokama H, McCarley R (1997) A topographic study of ERPs elicited by visual feature discrimination. Brain Topogr 10:133–143

    Article  PubMed  Google Scholar 

  • 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 3–16

    Google Scholar 

  • Pellegrino FC, Sica REP (2004) Canine electroencephalographic recording technique: findings in normal and epileptic dogs. Clin Neurophysiol 115:477–487

    Article  PubMed  Google Scholar 

  • Perrett DI, Rolls ET, Caan W (1982) Visual neurones responsive to faces in the monkey temporal cortex. Exp Brain Res 47:329–342

    Article  PubMed  CAS  Google Scholar 

  • 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 223:293–317

    Article  PubMed  CAS  Google Scholar 

  • 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 29:245–258

    Article  PubMed  CAS  Google Scholar 

  • 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 2:1–12

    Article  CAS  Google Scholar 

  • Puce A, Allison T, Gore JC, McCarthy G (1995) Face-sensitive regions in human extrastriate cortex studied by functional MRI. J Neurophysiol 74:1192–1199

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Range F, Aust U, Steurer M, Huber L (2008) Visual categorization of natural stimuli by domestic dogs. Anim Cogn 11:339–347

    Article  PubMed  Google Scholar 

  • Rolls ET (1994) Brain mechanisms for invariant visual recognition and learning. Behav Process 33:113–138

    Article  Google Scholar 

  • 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 65:38–48

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Tarr MJ, Cheng YD (2003) Learning to see faces and objects. Trends Cogn Sci 7:23–30

    Article  PubMed  Google Scholar 

  • 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 361:2155–2172

    Article  Google Scholar 

  • 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 140:25–32

    Article  Google Scholar 

  • Tsao DY, Freiwald WA, Knutsen TA, Mandeville JB, Tootell RBH (2003) Faces and objects in macaque cerebral cortex. Nat Neurosci 6:989–995

    Article  PubMed  CAS  Google Scholar 

  • Tsao DY, Freiwald WA, Tootell RBH, Livingstone MS (2006) A cortical region consisting entirely of face-selective cells. Science 311:670–674

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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 6:311–313

    Article  PubMed  Google Scholar 

  • Van der Marel E, Dagnelie G, Spekreijse H (1984) Subdurally recorded pattern and luminance EPs in the alert rhesus monkey. Electroencephalogr Clin Neurophysiol 57:354–368

    Article  PubMed  Google Scholar 

  • Vogel EK, Luck SJ (2000) The visual N1 component as an index of a discrimination process. Psychophysiology 37:190–203

    Article  PubMed  CAS  Google Scholar 

  • 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 611–626

    Google Scholar 

  • 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 104:15111–15116

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by the Academy of Finland (project #137931 to OV, and #115215 and #137511 to CMK), Foundations’ Post-Doc Pool (Kone Foundation), Finnish Cultural Foundation, Advancement of Technology Foundation, Emil Aaltonen Foundation and the BRAHE network (Brain Research collaboration between Aalto University and the University of Helsinki). We thank Timo Murtonen for the custom-made dog chin rest and EEG trigger system; Aino Pikkusaari, Pirkko Nokkala and Martti Siimekselä for the stimulus photos; Mari Palviainen for the help in training of the dogs and conducting the EEG pilot measurements; Tarja Pääkkönen for the advice in the EEG recordings; Mari Vainionpää for the help in the computed tomography acquisition; Antti Flyck and Kristian Törnqvist for the technical support and Katja Irvankoski for the help with Presentation® software.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Heini Törnqvist.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Törnqvist, H., Kujala, M.V., Somppi, S. et al. Visual event-related potentials of dogs: a non-invasive electroencephalography study. Anim Cogn 16, 973–982 (2013). https://doi.org/10.1007/s10071-013-0630-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10071-013-0630-2

Keywords

Navigation