Brain imaging reveals neuronal circuitry underlying the crow’s perception of human faces

Crows pay close attention to people and can remember specific faces for several years after a single encounter. In mammals, including humans, faces are evaluated by an integrated neural system involving the sensory cortex, limbic system, and striatum. Here we test the hypothesis that birds use a similar system by providing an imaging analysis of an awake, wild animal’s brain as it performs an adaptive, complex cognitive task. We show that in vivo imaging of crow brain activity during exposure to familiar human faces previously associated with either capture (threatening) or caretaking (caring) activated several brain regions that allow birds to discriminate, associate, and remember visual stimuli, including the rostral hyperpallium, nidopallium, mesopallium, and lateral striatum. Perception of threatening faces activated circuitry including amygdalar, thalamic, and brainstem regions, known in humans and other vertebrates to be related to emotion, motivation, and conditioned fear learning. In contrast, perception of caring faces activated motivation and striatal regions. In our experiments and in nature, when perceiving a threatening face, crows froze and fixed their gaze (decreased blink rate), which was associated with activation of brain regions known in birds to regulate perception, attention, fear, and escape behavior. These findings indicate that, similar to humans, crows use sophisticated visual sensory systems to recognize faces and modulate behavioral responses by integrating visual information with expectation and emotion. Our approach has wide applicability and potential to improve our understanding of the neural basis for animal behavior.

[1]  H. Davis Prediction and preparation: Pavlovian implications of research animals discriminating among humans. , 2002, ILAR journal.

[2]  L. F. Barrett,et al.  Handbook of Emotions , 1993 .

[3]  Yoshimi Anzai,et al.  Statistical mapping of functional olfactory connections of the rat brain in vivo , 2004, NeuroImage.

[4]  N. Logothetis,et al.  Cholinergic Control of Visual Categorization in Macaques , 2011, Front. Behav. Neurosci..

[5]  上村 和夫,et al.  Quantification of brain function : tracer kinetics and image analysis in brain PET : proceedings of Brain PET '93 Akita : Quantification of Brain Function, Akita, Japan, 29-31 May, 1993 , 1993 .

[6]  G. Hunt,et al.  Tool-Making New Caledonian Crows Have Large Associative Brain Areas , 2010, Brain, Behavior and Evolution.

[7]  J. D. McGaugh The amygdala modulates the consolidation of memories of emotionally arousing experiences. , 2004, Annual review of neuroscience.

[8]  Shigeru Watanabe Effect of lesions in the ectostriatum and Wulst on species and individual discrimination in pigeons , 1992, Behavioural Brain Research.

[9]  J. Marzluff,et al.  Social learning spreads knowledge about dangerous humans among American crows , 2012, Proceedings of the Royal Society B: Biological Sciences.

[10]  M. Mintun,et al.  Integrated and automated data analysis method for neuronal activation studies using O-15 water PET , 1993 .

[11]  Edward E. Smith,et al.  Spatial working memory in humans as revealed by PET , 1993, Nature.

[12]  Ralph Adolphs,et al.  Fear, faces, and the human amygdala , 2008, Current Opinion in Neurobiology.

[13]  H. P. Zeigier,et al.  Vision, brain, and behavior in birds. , 1994 .

[14]  Patrick O. McGowan,et al.  The Neurological Ecology of Fear: Insights Neuroscientists and Ecologists Have to Offer one Another , 2011, Front. Behav. Neurosci..

[15]  L. Regolin,et al.  Cerebral and behavioural assymetries in animal social recognition , 2012 .

[16]  Michael E Phelps,et al.  Impact of animal handling on the results of 18F-FDG PET studies in mice. , 2006, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[17]  I. Schwab Vision, Brain, and Behavior in Birds , 1994 .

[18]  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.

[19]  J. Fell,et al.  The specific contribution of neuroimaging versus neurophysiological data to understanding cognition , 2009, Behavioural Brain Research.

[20]  J. Withey,et al.  Lasting recognition of threatening people by wild American crows , 2010, Animal Behaviour.

[21]  J. Haxby,et al.  Neural systems for recognition of familiar faces , 2007, Neuropsychologia.

[22]  Jonas Rose,et al.  Neural Correlates of Executive Control in the Avian Brain , 2005, PLoS biology.

[23]  G. Ball,et al.  Topography in the preoptic region: Differential regulation of appetitive and consummatory male sexual behaviors , 2007, Frontiers in Neuroendocrinology.

[24]  T. Powell,et al.  The functional organization of the isthmo‐optic nucleus in the pigeon , 1972, The Journal of physiology.

[25]  Colline Poirier,et al.  MRI in small brains displaying extensive plasticity , 2009, Trends in Neurosciences.

[26]  G. Rhodes,et al.  Are you always on my mind? A review of how face perception and attention interact , 2007, Neuropsychologia.

[27]  Shigeru Watanabe,et al.  Visual Wulst analyses “where” and entopallium analyses “what” in the zebra finch visual system , 2011, Behavioural Brain Research.

[28]  J. Wattel Handbook of Birds of the world. , 1993 .

[29]  D. Davies,et al.  Subdivisions of the arcopallium/posterior pallial amygdala complex are differentially involved in the control of fear behaviour in the Japanese quail , 2009, Brain Research Bulletin.

[30]  J. Goodson The vertebrate social behavior network: Evolutionary themes and variations , 2005, Hormones and Behavior.

[31]  N. Daw,et al.  Differential roles of human striatum and amygdala in associative learning , 2011, Nature Neuroscience.

[32]  J. D. Hoyo,et al.  Handbook of the Birds of the World , 2010 .

[33]  A. Reiner,et al.  Thalamostriatal projection neurons in birds utilize LANT6 and neurotensin: a light and electron microscopic double-labeling study , 1995, Journal of Chemical Neuroanatomy.

[34]  J. Wild,et al.  Afferent and efferent projections of the central caudal nidopallium in the pigeon (Columba livia) , 2009, The Journal of comparative neurology.

[35]  R. Myers Quantification of brain function using PET , 1996 .

[36]  Karl J. Friston,et al.  Localisation in PET Images: Direct Fitting of the Intercommissural (AC—PC) Line , 1989, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[37]  A. N. Bowers,et al.  Visual circuits of the avian telencephalon: evolutionary implications , 1999, Behavioural Brain Research.

[38]  G. Schellenberg,et al.  Preclinical evidence of Alzheimer changes: convergent cerebrospinal fluid biomarker and fluorodeoxyglucose positron emission tomography findings. , 2009, Archives of neurology.

[39]  E. Izawa,et al.  Neural-activity mapping of memory-based dominance in the crow: neural networks integrating individual discrimination and social behaviour control , 2011, Neuroscience.

[40]  R. Cotterill,et al.  Mammalian and Avian Neuroanatomy and the Question of Consciousness in Birds , 2006, The Biological Bulletin.