Abstract
While viewing faces, human adults often demonstrate a natural gaze bias towards the left visual field, that is, the right side of the viewee’s face is often inspected first and for longer periods. Using a preferential looking paradigm, we demonstrate that this bias is neither uniquely human nor limited to primates, and provide evidence to help elucidate its biological function within a broader social cognitive framework. We observed that 6-month-old infants showed a wider tendency for left gaze preference towards objects and faces of different species and orientation, while in adults the bias appears only towards upright human faces. Rhesus monkeys showed a left gaze bias towards upright human and monkey faces, but not towards inverted faces. Domestic dogs, however, only demonstrated a left gaze bias towards human faces, but not towards monkey or dog faces, nor to inanimate object images. Our findings suggest that face- and species-sensitive gaze asymmetry is more widespread in the animal kingdom than previously recognised, is not constrained by attentional or scanning bias, and could be shaped by experience to develop adaptive behavioural significance.
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References
Asthana HS, Mandal MK (2001) Visual field bias in the judgment of facial expression of emotion. J Gen Psychol 128:21–29
Branson NJ, Rogers LJ (2006) Relationship between paw preference strength and noise phobia in Canis familiaris. J Comp Psychol 120:176–183
Bukach CM, Gauthier I, Tarr M (2006) Beyond faces and modularity: the power of an expertise framework. Trends Cogn Sci 10:159–166
Burt DM, Perrett DI (1997) Perceptual asymmetries in judgements of facial attractiveness, age, gender, speech and expression. Neuropsychologia 35:685–693
Butler S, Gilchrist ID, Burt DM, Perrett DI, Jones E, Harvey M (2005) Are the perceptual biases found in chimeric face processing reflected in eye-movement patterns? Neuropsychologia 43:52–59
Bulter SH, Harvey M (2006) Perceptual biases in chimeric face processing: eye-movement patterns cannot explain it all. Brain Res 1124:96–99
Chiang CH, Ballantyne AO, Trauner DA (2000) Development of perceptual asymmetry for free viewing of chimeric stimuli. Brain Cognit 44:415–425
de Haan M, Pascalis O, Johnson MH (2002) Specialization of neural mechanisms underlying face recognition in human infants. J Cognit Neurosci 14:199–209
Diamond R, Carey S (1986) Why faces are and are not special: an effect of expertise. J Exp Psychol Gen 115:107–117
Emery NJ (2000) The eyes have it: the neuroethology, function and evolution of social gaze. Neurosci Biobehav Rev 24:581–604
Failla CV, Sheppard DM, Bradshaw JL (2003) Age and responding-hand related changes in performance of neurologically normal subjects on the line-bisection and chimeric-faces tasks. Brain Cognit 52:353–363
Farah MJ, Aguirre GK (1999) Imaging visual recognition: PET and fMRI studies of the functional anatomy of human visual recognition. Trends Cogn Sci 3:179–186
Ferrari PF, Gallese V, Rizzolatti G, Fogassi L (2003) Mirror neurons responding to the observation of ingestive and communicative mouth actions in the monkey ventral premotor cortex. Eur J Neurosci 17:1703–1714
Gilbert C, Bakan P (1973) Visual asymmetry in perception of faces. Neuropsychologia 11:355–362
Grega DM, Sackeim HA, Sanchez E, Cohen BH, Hough S (1988) Perceiver bias in the processing of human faces: neuropsychological mechanisms. Cortex 24:91–117
Grossmann T, Johnson MH (2007) The development of the social brain in infancy. Eur J Neurosci 25:909–919
Guo K, Benson PJ (1998) Involuntary eye movements in response to first- and second-order motion. Neuroreport 9:3543–3548
Guo K, Robertson RG, Mahmoodi S, Tadmor Y, Young MP (2003) How do monkeys view faces? A study of eye movements. Exp Brain Res 150:363–374
Guo K, Mahmoodi S, Robertson RG, Young MP (2006) Longer fixation duration while viewing face images. Exp Brain Res 171:91–98
Guo K (2007) Initial fixation placement in face images is driven by top–down guidance. Exp Brain Res 181:673–677
Hamilton CR, Vermeire BA (1988) Complementary hemispheric-specialization in monkeys. Science 242:1691–1694
Hare B, Brown M, Williamson C, Tomasello M (2002) The domestication of social cognition in dogs. Science 298:1634–1636
Hare B, Tomasello M (2005) Human-like social skills in dogs. Trends Cogn Sci 9:439–444
Hauser MD (1993) Right hemisphere dominance for the production for the production of facial expression in monkeys. Science 261:475–477
Heath RL, Rouhana A, Ghanem DA (2005) Asymmetric bias in perception of facial affect among Roman and Arabic script readers. Laterality 10:51–64
Indersmitten T, Gur RC (2003) Emotion processing in chimeric faces: hemispheric asymmetries in expression and recognition of emotions. J Neurosci 23:3820–3825
Kendrick KM (2006) Brain asymmetries for face recognition and emotion control in sheep. Cortex 42:96–98
Killeen PR (2005) An alternative to null-hypothesis significance tests. Psychol Sci 16:345–353
Leonards U, Scott-Samuel NE (2005) Idiosyncratic initiation of saccadic face exploration in humans. Vision Res 45:2677–2684
Leslie KR, Johnson-Frey SH, Grafton ST (2004) Functional imaging of the face and hand imitation: towards a motor theory of empathy. Neuroimage 21:601–607
McKone E, Kanwisher N, Duchaine BC (2006) Can generic expertise explain special processing for faces? Trends Cogn Sci 11:8–15
Mendelson MJ, Haith MM, Goldman-Rakic PS (1982) Face scanning and responsiveness to social cues in infant rhesus monkeys. Dev Psychol 18:222–228
Meints K, Plunkett K, Harris PL (1999) When does an ostrich become a bird? The role of typicality in early word comprehension. Dev Psychol 35:1072–1078
Mertens I, Siegmund H, Grusser OJ (1993) Gaze motor asymmetries in the perception of faces during a memory task. Neuropsychologia 31:989–998
Miklósi A, Kubinyi E, Topál J, Gácsi M, Virányi Z, Csányi V (2003) A simple reason for a big difference: Wolves do not look back at humans, but dogs do. Curr Biol 13:763–766
Mondloch CJ, Maurer D, Ahola S (2006) Becoming a face expert. Psychol Sci 17:930–934
Morris RD, Hopkins WD (1993) Perception of human chimeric faces by chimpanzees: evidence for a right hemisphere advantage. Brain Cognit 21:111–122
Nicholls MER, Roberts GR (2002) Can free-viewing perceptual asymmetries be explained by scanning, pre-motor or attentional biases? Cortex 38:113–136
Niemeier M, Stojanoski B, Greco A (2007) Influence of time and spatial frequency on the perceptual bias: evidence for competition between hemispheres. Neuropsychologia 45:1029–1040
Parr LA, Winslow JT, Hopkins WD (2000) Recognizing facial cues: individual discrimination by chimpanzees (Pan troglodytes and rhesus monkeys (Macaca mulatta). J Comp Psychol 114:1–14
Pascalis O, Demont E, de Haan M, Campbell R (2001) Recognition of faces of different species: a developmental study between 5 and 8 years of age. Infant Child Dev 10:39–45
Pascalis O, de Haan M, Nelson CA (2002) Is face processing species-specific during the first year of life? Science 14:199–209
Philips ML, David AS (1997) Viewing strategies for simple and chimeric faces: an investigation of perceptual bias in normal and schizophrenic patients using visual scan paths. Brain Cognit 32:225–238
Poyser F, Caldwell C, Cobb M (2006) Dog paw preference shows liability and sex differences. Behav Processes 73:216–221
Quaranta A, Siniscalchi M, Frate A, Vallortigara G (2004) Paw preference in dogs: relations between lateralised behaviour and immunity. Behav Brain Res 153:521–525
Quaranta A, Siniscalchi M, Frate A, Iacoviello R, Buonavoglia C, Vallortigara G (2006) Lateralised behaviour and immune response in dogs: relations between paw preference and interferon-γ, interleukin-10 and IgG antibodies production. Behav Brain Res 166:236–240
Quaranta A, Siniscalchi M, Vallortigara G (2007) Asymmetric tail-wagging responses by dogs to different emotive stimuli. Curr Bio 17:R199–R201
Quaranta A, Siniscalchi M, Albrizio M, Volpe S, Buonavoglia C, Vallortigara G (2008) Influence of behavioural lateralization on interleukin-2 and interleukin-6 gene expression in dogs before and after immunization with rabies vaccine. Behav Brain Res 186:256–260
Rhodes G (1986) Perceptual asymmetries in face recognition. Brain Cognit 4:197–218
Rosenfeld SA, Van Hoesen GW (1979) Face recognition in the rhesus monkey. Neuropsychologia 17:503–509
Rossion B, Gauthier I (2002) How does the brain process upright and inverted faces? Behav Cognit Neurosci Rev 1:63–75
Rossion B, Joyce CA, Cottrell GW, Tarr MJ (2003) Early lateralization and orientation tuning for face, word, and object processing in the visual cortex. NeuroImage 20:1609–1624
Sovrano VA, Rainoldi C, Bisazza A, Vallortigara G (1999) Roots of brain specializations: preferential left-eye use during mirror-image inspection in six species of teleost fish. Behav Brain Res 106:175–180
Tan U (1987) Paw preferences in dogs. Int J Neurosci 32:825–829
Tan U, Calsikan S (1987) Allometry and asymmetry in the dog brain: the right hemisphere is heavier regardless of paw preference. Int J Neurosci 35:189–194
Tanaka J, Kiefer M, Bukach CM (2004) A holistic account of the own-race effect in face recognition: evidence from a cross-cultural study. Cognition 93:1–9
Tarr MJ, Cheng YD (2003) Learning to see faces and objects. Trends Cogn Sci 7:23–30
Topál J, Gácsi M, Miklósi Á, Virányi Z, Kubinyi E, Csányi V (2005) Attachment to humans: a comparative study on hand-reared wolves and differently socialized dog puppies. Anim Behav 70:1367–1375
Vaid J, Singh M (1989) Asymmetries in the perception of facial affect: Is there an influence of reading habits? Neuropsychologia 27:1277–1287
Valentine T (1988) Upside-down faces: a review of the effects of inversion upon face recognition. Br J Psychol 79:471–491
Vallortigara G (1992) Right hemisphere advantage for social recognition in the chick. Neuropsychologia 30:761–768
Vallortigara G, Andrew RJ (1991) Lateralization of response by chicks to change in a model partner. Anim Behav 41:187–194
Vallortigara G, Andrew RJ (1994) Differential involvement of right and left hemisphere in individual recognition in the domestic chick. Behav Processes 33:41–58
Vallortigara G, Rogers LJ (2005) Survival with an asymmetrical brain: Advantages and disadvantages of cerebral lateralization. Behav Brain Sci 28:575–589
Vermeire BA, Hamilton CR (1998) Inversion effect for faces in split-brain monkeys. Neuropsychologia 36:1003–1014
Vilà C, Savolainen P, Maldonado JE, Amorim IR, Rice JE, Honeycutt RL, Crandall KA, Lundeberg J, Wayne RK (1997) Multiple and ancient origins of the domestic dog. Science 276:1687–1689
Virányi Z, Gácsi M, Kubinyi E, Topál J, Belényi B, Ujfalussy D, Miklósi A (2008) Comprehension of human pointing gestures in young human-reared wolves (Canis lupus) and dogs (Canis familiaris). Anim Cogn 11:373–387
Wells DL (2003) Lateralised behaviour in the domestic dog, Canis familiaris. Behav Processes 61:27–35
Yovel G, Kanwisher N (2005) The neural basis of the behavioral face-inversion effect. Curr Biol 15:2256–2262
Zucca P, Sovrano VA (2008) Animal lateralization and social recognition: Quails use their left visual hemifield when approaching a companion and their right visual hemifield when approaching a stranger. Cortex 44:13–20
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Guo, K., Meints, K., Hall, C. et al. Left gaze bias in humans, rhesus monkeys and domestic dogs. Anim Cogn 12, 409–418 (2009). https://doi.org/10.1007/s10071-008-0199-3
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DOI: https://doi.org/10.1007/s10071-008-0199-3