Spontaneous voice–face identity matching by rhesus monkeys for familiar conspecifics and humans

Recognition of a particular individual occurs when we reactivate links between current perceptual inputs and the previously formed representation of that person. This recognition can be achieved by identifying, separately or simultaneously, distinct elements such as the face, silhouette, or voice as belonging to one individual. In humans, those different cues are linked into one complex conceptual representation of individual identity. Here we tested whether rhesus macaques (Macaca mulatta) also have a cognitive representation of identity by evaluating whether they exhibit cross-modal individual recognition. Further, we assessed individual recognition of familiar conspecifics and familiar humans. In a free preferential looking time paradigm, we found that, for both species, monkeys spontaneously matched the faces of known individuals to their voices. This finding demonstrates that rhesus macaques possess a cross-modal cognitive representation of individuals that extends from conspecifics to humans, revealing the adaptive potential of identity recognition for individuals of socioecological relevance.

[1]  J. Cutting,et al.  Recognizing friends by their walk: Gait perception without familiarity cues , 1977 .

[2]  J. Kaplan Fight interference and altruism in rhesus monkeys , 1978 .

[3]  Lance M. Optican,et al.  Unix-based multiple-process system, for real-time data acquisition and control , 1982 .

[4]  M. Philip,et al.  Facial and Vocal Individual Recognition in the Common Chimpanzee , 1983 .

[5]  F. Waal,et al.  Reconciliation and Redirected Affection in Rhesus Monkeys , 1983 .

[6]  F. D. de Waal,et al.  The formal hierarchy of rhesus macaques: An investigation of the bared‐teeth display , 1985, American journal of primatology.

[7]  Richard H. Porter,et al.  Recognition of kin through characteristic body odors , 1986 .

[8]  L. Luttrell,et al.  Mechanisms of social reciprocity in three primate species: Symmetrical relationship characteristics or cognition? , 1988 .

[9]  Marsha Kaitz Recognition of familiar individuals by touch , 1992, Physiology & Behavior.

[10]  D. Rendall,et al.  Vocal recognition of individuals and kin in free-ranging rhesus monkeys , 1996, Animal Behaviour.

[11]  H. Gouzoules,et al.  Agonistic screams and the classification of dominance relationships: are monkeys fuzzy logicians? , 1998, Animal Behaviour.

[12]  M J Owren,et al.  The role of vocal tract filtering in identity cueing in rhesus monkey (Macaca mulatta) vocalizations. , 1998, The Journal of the Acoustical Society of America.

[13]  James R. Anderson,et al.  Social stimuli and social rewards in primate learning and cognition , 1998, Behavioural Processes.

[14]  O. Pascalis,et al.  Face recognition in primates: a cross-species study , 1998, Behavioural Processes.

[15]  R. Lickliter,et al.  Intersensory redundancy guides attentional selectivity and perceptual learning in infancy. , 2000, Developmental psychology.

[16]  W. Fitch The evolution of speech: a comparative review , 2000, Trends in Cognitive Sciences.

[17]  J. Winslow,et al.  Recognizing facial cues: individual discrimination by chimpanzees (Pan troglodytes) and rhesus monkeys (Macaca mulatta). , 2000, Journal of comparative psychology.

[18]  J. Vauclair,et al.  Picture recognition in animals and humans , 2000, Behavioural Brain Research.

[19]  R. Johnston,et al.  Individual recognition by use of odours in golden hamsters: the nature of individual representations , 2001, Animal Behaviour.

[20]  O. Pascalis,et al.  Is Face Processing Species-Specific During the First Year of Life? , 2002, Science.

[21]  S. Kojima,et al.  Identification of vocalizers by pant hoots, pant grunts and screams in a chimpanzee , 2003, Primates.

[22]  D. Perrett,et al.  Evidence from rhesus macaques suggests that male coloration plays a role in female primate mate choice , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[23]  N. Logothetis,et al.  Neuroperception: Facial expressions linked to monkey calls , 2003, Nature.

[24]  E. Vatikiotis-Bateson,et al.  `Putting the Face to the Voice' Matching Identity across Modality , 2003, Current Biology.

[25]  Katalin M. Gothard,et al.  How do rhesus monkeys (Macaca mulatta) scan faces in a visual paired comparison task? , 2004, Animal Cognition.

[26]  Laurie R Santos,et al.  Primate brains in the wild: the sensory bases for social interactions , 2004, Nature Reviews Neuroscience.

[27]  D. Pisoni,et al.  Crossmodal Source Identification in Speech Perception , 2004, Ecological psychology : a publication of the International Society for Ecological Psychology.

[28]  M. Delgado,et al.  Perceptions of moral character modulate the neural systems of reward during the trust game , 2005, Nature Neuroscience.

[29]  L. Bahrick,et al.  The development of infant learning about specific face-voice relations. , 2005, Developmental psychology.

[30]  Elizabeth M. Brannon,et al.  Monkeys Match the Number of Voices They Hear to the Number of Faces They See , 2005, Current Biology.

[31]  Keiji Tanaka,et al.  Prior experience of rotation is not required for recognizing objects seen from different angles , 2005, Nature Neuroscience.

[32]  Michael L. Platt,et al.  Monkeys Pay Per View: Adaptive Valuation of Social Images by Rhesus Macaques , 2005, Current Biology.

[33]  O. Pascalis,et al.  Plasticity of face processing in infancy. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[34]  C. Waitt,et al.  Perceptual considerations in the use of colored photographic and video stimuli to study nonhuman primate behavior , 2006, American journal of primatology.

[35]  D. Lewkowicz,et al.  The decline of cross-species intersensory perception in human infants. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[36]  I. Adachi,et al.  Dogs recall their owner's face upon hearing the owner's voice , 2006, Animal Cognition.

[37]  T. Matsuzawa,et al.  Japanese macaques form a cross-modal representation of their own species in their first year of life , 2006, Primates.

[38]  Stephen V. Shepherd,et al.  Social status gates social attention in monkeys , 2006, Current Biology.

[39]  A. Little,et al.  Selective attention toward female secondary sexual color in male rhesus macaques , 2006, American journal of primatology.

[40]  Roy D. Patterson,et al.  Vocal-Tract Resonances as Indexical Cues in Rhesus Monkeys , 2007, Current Biology.

[41]  Christoph D. Dahl,et al.  Individuation and holistic processing of faces in rhesus monkeys , 2007, Proceedings of the Royal Society B: Biological Sciences.

[42]  I. Adachi,et al.  Cross-modal representation of human caretakers in squirrel monkeys , 2007, Behavioural Processes.

[43]  J. Silk Social Components of Fitness in Primate Groups , 2007, Science.

[44]  A. Iriki,et al.  The neuroscience of primate intellectual evolution: natural selection and passive and intentional niche construction , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[45]  Y. Sugita Face perception in monkeys reared with no exposure to faces , 2008, Proceedings of the National Academy of Sciences.

[46]  Mary A. Peterson,et al.  Multiple perceptual strategies used by macaque monkeys for face recognition , 2008, Animal Cognition.

[47]  David Reby,et al.  Cross-modal individual recognition in domestic horses (Equus caballus) , 2009, Proceedings of the National Academy of Sciences.

[48]  B. Deputte,et al.  Matching Vocalizations to Faces of Familiar Conspecifics in Grey-Cheeked Mangabeys (Lophocebus albigena) , 2009, Folia Primatologica.

[49]  Jennifer J. Pokorny,et al.  Monkeys recognize the faces of group mates in photographs , 2009, Proceedings of the National Academy of Sciences.

[50]  D. Lewkowicz,et al.  The emergence of multisensory systems through perceptual narrowing , 2009, Trends in Cognitive Sciences.

[51]  O. Pascalis,et al.  Development of the other-race effect during infancy: evidence toward universality? , 2009, Journal of experimental child psychology.

[52]  R. Seyfarth,et al.  Seeing who we hear and hearing who we see , 2009, Proceedings of the National Academy of Sciences.

[53]  D. Lewkowicz,et al.  Heterochrony and Cross-Species Intersensory Matching by Infant Vervet Monkeys , 2009, PloS one.

[54]  T. Matsuzawa,et al.  Plasticity of ability to form cross-modal representations in infant Japanese macaques. , 2009, Developmental science.

[55]  Roger K. R. Thompson,et al.  How to read a picture: Lessons from nonhuman primates , 2010, Proceedings of the National Academy of Sciences.

[56]  Pier Francesco Ferrari,et al.  Towards a bottom-up perspective on animal and human cognition , 2010, Trends in Cognitive Sciences.

[57]  S. Campanella,et al.  Integrating face and voice in person perception , 2007, Trends in Cognitive Sciences.