Time-resolved classification of dog brain signals reveals early processing of faces, species and emotion

Dogs process faces and emotional expressions much like humans, but the time windows important for face processing in dogs are largely unknown. By combining our non-invasive electroencephalography (EEG) protocol on dogs with machine-learning algorithms, we show category-specific dog brain responses to pictures of human and dog facial expressions, objects, and phase-scrambled faces. We trained a support vector machine classifier with spatiotemporal EEG data to discriminate between responses to pairs of images. The classification accuracy was highest for humans or dogs vs. scrambled images, with most informative time intervals of 100–140 ms and 240–280 ms. We also detected a response sensitive to threatening dog faces at 30–40 ms; generally, responses differentiating emotional expressions were found at 130–170 ms, and differentiation of faces from objects occurred at 120–130 ms. The cortical sources underlying the highest-amplitude EEG signals were localized to the dog visual cortex.

[1]  G. Rhodes,et al.  A comparative view of face perception. , 2010, Journal of comparative psychology.

[2]  M. Nagasawa,et al.  Dogs can discriminate human smiling faces from blank expressions , 2011, Animal Cognition.

[3]  O. Lind,et al.  High visual acuity revealed in dogs , 2017, PloS one.

[4]  Juliane Kaminski,et al.  Paedomorphic Facial Expressions Give Dogs a Selective Advantage , 2013, PloS one.

[5]  M. Eimer,et al.  Event-related brain potential correlates of emotional face processing , 2007, Neuropsychologia.

[6]  H. Hughes,et al.  Effects of flash luminance and positional expectancies on visual response latency , 1984, Perception & psychophysics.

[7]  Corinna Cortes,et al.  Support-Vector Networks , 1995, Machine Learning.

[8]  R. Dolan,et al.  Effects of Attention and Emotion on Face Processing in the Human Brain An Event-Related fMRI Study , 2001, Neuron.

[9]  Decoding Human Emotional Faces in the Dog's Brain , 2018 .

[10]  Aapo Hyvärinen,et al.  Fast and robust fixed-point algorithms for independent component analysis , 1999, IEEE Trans. Neural Networks.

[11]  D. Coulter,et al.  Recording of visual-evoked potentials in dogs with scalp electrodes. , 1988, Journal of veterinary internal medicine.

[12]  Miiamaaria V. Kujala,et al.  Human Empathy, Personality and Experience Affect the Emotion Ratings of Dog and Human Facial Expressions , 2017, PloS one.

[13]  Heini Törnqvist,et al.  Dogs Evaluate Threatening Facial Expressions by Their Biological Validity – Evidence from Gazing Patterns , 2016, PloS one.

[14]  M. Eimer,et al.  An ERP study on the time course of emotional face processing , 2002, Neuroreport.

[15]  K. Kendrick,et al.  Behavioural and neurophysiological evidence for face identity and face emotion processing in animals , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[16]  Heini Törnqvist,et al.  Dogs do look at images: eye tracking in canine cognition research , 2012, Animal Cognition.

[17]  Sai Sheshan Roy Gotoor,et al.  Separate brain areas for processing human and dog faces as revealed by awake fMRI in dogs (Canis familiaris) , 2018, Learning & Behavior.

[18]  D. Mills,et al.  Dogs recognize dog and human emotions , 2016, Biology Letters.

[19]  Ludwig Huber,et al.  The Processing of Human Emotional Faces by Pet and Lab Dogs: Evidence for Lateralization and Experience Effects , 2016, PloS one.

[20]  T. Holroyd,et al.  Emotional Automaticity Is a Matter of Timing , 2010, The Journal of Neuroscience.

[21]  Antonio Schettino,et al.  Shedding light on emotional perception: Interaction of brightness and semantic content in extrastriate visual cortex , 2016, NeuroImage.

[22]  S. Mineka,et al.  Fears, phobias, and preparedness: toward an evolved module of fear and fear learning. , 2001, Psychological review.

[23]  Heini Törnqvist,et al.  Reactivity of Dogs' Brain Oscillations to Visual Stimuli Measured with Non-Invasive Electroencephalography , 2013, PloS one.

[24]  Daniel Mills,et al.  Discrimination of human and dog faces and inversion responses in domestic dogs (Canis familiaris) , 2010, Animal Cognition.

[25]  L. Mounier,et al.  Visual discrimination of species in dogs (Canis familiaris) , 2013, Animal Cognition.

[26]  Nikos K. Logothetis,et al.  Facial-Expression and Gaze-Selective Responses in the Monkey Amygdala , 2007, Current Biology.

[27]  Ludwig Huber,et al.  Dogs Can Discriminate Emotional Expressions of Human Faces , 2015, Current Biology.

[28]  Daniel G. Bradley,et al.  How Much Is That in Dog Years? The Advent of Canine Population Genomics , 2014, PLoS genetics.

[29]  G. Berns,et al.  Awake fMRI Reveals Brain Regions for Novel Word Detection in Dogs , 2018, Front. Neurosci..

[30]  Joseph E LeDoux Emotion circuits in the brain. , 2009, Annual review of neuroscience.

[31]  J. Theeuwes,et al.  Angry faces hold the eyes , 2011 .

[32]  Andreas Schulze-Bonhage,et al.  Anatomical specificity of functional amygdala imaging of responses to stimuli with positive and negative emotional valence , 2009, Journal of Neuroscience Methods.

[33]  G. Yovel Neural and cognitive face-selective markers: An integrative review , 2016, Neuropsychologia.

[34]  Ludwig Huber,et al.  Discrimination of familiar human faces in dogs (Canis familiaris) , 2013, Learning and motivation.

[35]  Francesca M. M. Citron Neural correlates of written emotion word processing: A review of recent electrophysiological and hemodynamic neuroimaging studies , 2012, Brain and Language.

[36]  A. Jedynak,et al.  Rapid extraction of emotional expression: evidence from evoked potential fields during brief presentation of face stimuli , 2003, Neuropsychologia.

[37]  J. J. Lange,et al.  An ERP study of visual spatial attention and letter target detection for isoluminant and nonisoluminant stimuli. , 1997, Psychophysiology.

[38]  Luis Concha,et al.  Our Faces in the Dog's Brain: Functional Imaging Reveals Temporal Cortex Activation during Perception of Human Faces , 2016, PloS one.

[39]  M. Malinowska,et al.  Diversity of connections of the temporal neocortex with amygdaloid nuclei in the dog (Canis familiaris). , 1997, Acta neurobiologiae experimentalis.

[40]  F. Reinoso-suárez,et al.  Amygdaloid projections to prefrontal and motor cortex. , 1977, Science.

[41]  Wenfeng Feng,et al.  Three stages of facial expression processing: ERP study with rapid serial visual presentation , 2010, NeuroImage.

[42]  Daniel D. Dilks,et al.  Awake fMRI reveals a specialized region in dog temporal cortex for face processing , 2015, PeerJ.

[43]  Jian-Zhi Wang,et al.  From Structure to Behavior in Basolateral Amygdala-Hippocampus Circuits , 2017, Front. Neural Circuits.

[44]  A. Ohman,et al.  "Unconscious anxiety": phobic responses to masked stimuli. , 1994, Journal of abnormal psychology.

[45]  Karim Jerbi,et al.  Exceeding chance level by chance: The caveat of theoretical chance levels in brain signal classification and statistical assessment of decoding accuracy , 2015, Journal of Neuroscience Methods.

[46]  D. Amaral,et al.  Amygdalo‐cortical projections in the monkey (Macaca fascicularis) , 1984, The Journal of comparative neurology.

[47]  S J Luck,et al.  Visual event-related potentials index focused attention within bilateral stimulus arrays. II. Functional dissociation of P1 and N1 components. , 1990, Electroencephalography and clinical neurophysiology.

[48]  W. Freiwald,et al.  Face Processing Systems: From Neurons to Real-World Social Perception. , 2016, Annual review of neuroscience.

[49]  Robert Oostenveld,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2010, Comput. Intell. Neurosci..

[50]  C. Krause,et al.  How dogs scan familiar and inverted faces: an eye movement study , 2013, Animal Cognition.

[51]  Thomas E. Nichols,et al.  Nonparametric permutation tests for functional neuroimaging: A primer with examples , 2002, Human brain mapping.

[52]  Werner Sommer,et al.  Does processing of emotional facial expressions depend on intention? Time-resolved evidence from event-related brain potentials , 2012, Biological Psychology.

[53]  W. Dunn,et al.  Significant Neuroanatomical Variation Among Domestic Dog Breeds , 2019, The Journal of Neuroscience.

[54]  L. Kaufman,et al.  On the relation between somatic evoked potentials and fields. , 1981, The International journal of neuroscience.

[55]  Daniel Mills,et al.  Left gaze bias in humans, rhesus monkeys and domestic dogs , 2009, Animal Cognition.

[56]  J. Kujala,et al.  Visual event-related potentials of dogs: a non-invasive electroencephalography study , 2013, Animal Cognition.

[57]  Martin Luessi,et al.  MEG and EEG data analysis with MNE-Python , 2013, Front. Neuroinform..

[58]  Mark W. Becker,et al.  Please Scroll down for Article the Quarterly Journal of Experimental Psychology Early Detection and Avoidance of Threatening Faces during Passive Viewing , 2022 .

[59]  M. Siniscalchi,et al.  Orienting asymmetries and physiological reactivity in dogs’ response to human emotional faces , 2018, Learning & behavior.