Developmental shifts in social cognition: socio-emotional biases across the lifespan in rhesus monkeys

  • Alexandra G. RosatiEmail author
  • Alyssa M. Arre
  • Michael L. Platt
  • Laurie R. Santos
Original Article
Part of the following topical collections:
  1. An evolutionary perspective on the development of primate sociality


Humans exhibit a suite of developmental changes in social cognition across the lifespan. To what extent are these developmental patterns unique? We first review several social domains in which humans undergo critical ontogenetic changes in socio-cognitive processing, including social attention and theory of mind. We then examine whether one human developmental transition—a shift in socio-emotional preferences—also occurs in non-human primates. Specifically, we experimentally measured socio-emotional processing in a large population of rhesus macaques (Macaca mulatta) ranging from infancy to old age. We tested whether macaques, like humans, also exhibited developmental shifts from a negativity bias at younger ages, indicating preferential attention to negative socio-emotional stimuli, to a positivity bias at older ages. We first assessed monkeys’ (n = 337) responses to negative socio-emotional stimuli by comparing their duration of looking towards photos of negative conspecific signals (threat displays) versus matched neutral expressions. In contrast to the pattern observed in humans, we found that older monkeys were more attentive to negative emotional stimuli than were younger monkeys. In a second study, we used the same method to examine monkeys’ (n = 132) attention to positive (affiliative displays) versus matched neutral expressions. Monkeys did not exhibit an overall preference for positive stimuli, nor major age-related changes in their attention. These results indicate that while monkeys show robust ontogenetic shifts in social preferences, they differ from humans by exhibiting an increasing negativity bias with age. Studies of comparative cognitive development can therefore provide insight into the evolutionary origins of human socio-cognitive development.

Significance statement

Humans are characterized by complex and flexible social behavior. Understanding the proximate psychological mechanisms and developmental processes that underpin these social behaviors can shed light on the evolutionary history of our species. We used a comparative developmental approach to identify whether a key component of human social cognition, responses to emotionally-charged social stimuli, are shared with other primates. Humans exhibit important shifts in this aspect of our social cognition: younger individuals attend more to negative stimuli, whereas older adults tend to focus on positive information. These shifts are thought to appropriately tailor our age-dependent social goals. We found that, unlike humans, rhesus monkeys show an increasing negativity bias with age. By examining primate cognition across the lifespan, this work can help disentangle how complex forms of social behavior emerge across species.


Social cognition Comparative development Primates Socio-emotional biases Emotional signals 



We thank the editors of the special issue; two anonymous reviewers for comments on the manuscript; Lindsey Jones, Samantha Monier, and Alondra Arguello for assistance with data collection and coding; and Kerby Shedden at the University of Michigan’s Consulting for Statistics, Computing and Analytics Research (CSCAR) for statistical advice. The authors are grateful to the Cayo Santiago Santiago Field Station and staff including Angelina Ruiz Lambides, Nahiri Rivera Barreto, Giselle Caraballo Cruz, and Bianca Giura for their research support.


This work was supported by NIMH (R01MH096875), a National Center for Research Resources CM-5-P40RR003640-13 award to the Caribbean Primate Research Center and the University of Puerto Rico, and an Office of Research Infrastructure Programs (ORIP) of the National Institutes of Health (NIH) through Grant Number 5P40OD012217 to the Caribbean Primate Research Center and the University of Puerto Rico. LRS was supported by the James S. McDonnell Foundation (no. 220020242).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethics approval

All non-invasive behavioral tests were approved by the Institutional Animal Care and Use Committee (IACUC) for Yale University (no. 2014-11624), as well as the Cayo Santiago IACUC (#8310106) administered through the University of Puerto Rico Medical Sciences Campus. All tests adhered to site guidelines for animal research.

Supplementary material

Video S1

(MP4 73383 kb)

265_2018_2573_MOESM1_ESM.pdf (132 kb)
ESM 1 (PDF 131 kb)


  1. Adams RB, Kleck RE (2005) Effects of direct and averted gaze on the perception of facially communicated emotion. Emotion 5:3–11PubMedGoogle Scholar
  2. Adams RB, Gordon HL, Baird AA, Ambady N, Kleck RE (2003) Effects of gaze on amygdala sensitivity to anger and fear faces. Science 300:1536PubMedGoogle Scholar
  3. Alberts SC, Altmann J, Brockman DK, Cords M, Fedigan LM, Pusey A, Stoinski TS, Strier KB, Morris WF, Bronikowski AM (2013) Reproductive aging patterns in primates reveal that humans are distinct. Proc Natl Acad Sci U S A 110:13440–13445PubMedPubMedCentralGoogle Scholar
  4. Almeling L, Hammerschmidt K, Senn-Reulen H, Freund AM, Fischer J (2016) Motivational shifts in aging monkeys and the origins of social selectivity. Curr Biol 26:1744–1749PubMedGoogle Scholar
  5. Almeling L, Senn-Reulen H, Hammerschmidt K, Freund AM, Fischer J (2017) Social interactions and activity patterns of old Barbary macaques: further insights into the foundations of social selectivity. Am J Primatol 79:e22711Google Scholar
  6. Baayen RH (2008) Analyzing linguistic data. A practical introduction to statistics. Cambridge University Press, CambridgeGoogle Scholar
  7. Bates D (2010) The LME4 package: linear mixed-effects models using S4 classes,
  8. Bateson P, Laland KN (2013) Tinbergen’s four questions: an appreciation and an update. Trends Ecol Evol 28:712–718PubMedGoogle Scholar
  9. Bercovitch FB (1997) Reproductive strategies of rhesus macaques. Primates 38:247–263Google Scholar
  10. Bernstein IS, Ehardt CL (1985) Age-sex differences in the expression of agonistic behavior in rhesus monkey (Macaca mulatta) groups. J Comp Psychol 99:115–132PubMedGoogle Scholar
  11. Bernstein IS, Ehardt CL (1986) Modification of aggression through socialization and the special case of adult and adolescent male rhesus monkeys (Macaca mulatta). Am J Primatol 10:213–227Google Scholar
  12. Bethell EJ, Holmes A, MacLarnon A, Semple S (2012) Evidence that emotion mediates social attention in rhesus macaques. PLoS One 7:e44387PubMedPubMedCentralGoogle Scholar
  13. Bjorklund DF (2018) A metatheory for cognitive development (or “Piaget is dead” revisited). Child Dev (published online,
  14. Bjorklund DF, Bering JM (2003) Big brains, slow development and social complexity: the developmental and evolutionary origins of social cognition. In: Brüne M, Ribbert H, Schiefenhövel W (eds) The social brain: evolution and pathology. Wiley, Chichester, pp 113–151Google Scholar
  15. Bjorklund DF, Green BL (1992) The adaptive nature of cognitive immaturity. Am Psychol 47:46–54Google Scholar
  16. Bogin B (1999) Evolutionary perspective on human growth. Annu Rev Anthropol 28:109–153PubMedGoogle Scholar
  17. Bogin B (2010) Evolution of human growth. In: Muehlenbein M (ed) Human evolutionary biology. Cambridge University Press, Cambridge, pp 379–395Google Scholar
  18. Bogin B, Smith BH (1996) Evolution of the human life cycle. Am J Hum Biol 8:703–716PubMedGoogle Scholar
  19. Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White JSS (2008) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135Google Scholar
  20. Bornstein MH, Sigman MD (1986) Continuity in mental development from infancy. Child Dev 57:251–274PubMedGoogle Scholar
  21. Braeuer J, Call J, Tomasello M (2005) All great ape species follow gaze to distant locations and around barriers. J Comp Psychol 119:145–154Google Scholar
  22. Braeuer J, Call J, Tomasello M (2007) Chimpanzees really know what others can see in a competitive situation. Anim Cogn 10:439–448Google Scholar
  23. Brooks R, Meltzoff AN (2005) The development of gaze following and its relation to language. Dev Sci 8:535–543PubMedPubMedCentralGoogle Scholar
  24. Brooks R, Meltzoff AN (2008) Infant gaze following and pointing predict accelerated vocabulary growth through two years of age: a longitudinal, growth curve modeling study. J Child Lang 35:207–220PubMedGoogle Scholar
  25. Buttelman D, Schuette S, Carpenter M, Call J, Tomasello M (2012) Great apes infer others’ goals based on context. Anim Cogn 15:1037–1053Google Scholar
  26. Buttelman D, Buttelman F, Carpenter M, Call J, Tomasello M (2017) Great apes distinguish true from false beliefs in an interactive helping task. PLoS One 12:e0173793Google Scholar
  27. Call J, Tomasello M (2008) Does the chimpanzee have a theory of mind? 30 years later. Trends Cogn Sci 12:187–192PubMedGoogle Scholar
  28. Call J, Hare B, Carpenter M, Tomasello M (2004) Unwilling’ versus ‘unable’: chimpanzees’ understanding of human intentional action. Dev Sci 7:488–498PubMedGoogle Scholar
  29. Canteloup C, Piraux E, Poulin N, Meunier H (2016) Do Tonkean macaques (Macaca tonkeana) perceive what conspecifics do and do not see? PeerJ 4:e1693PubMedPubMedCentralGoogle Scholar
  30. Carstensen LL (2006) The influence of a sense of time on human development. Science 312:1913–1915PubMedPubMedCentralGoogle Scholar
  31. Carstensen LL, Fredrickson BL (1998) Influence of HIV status and age on cognitive representations of others. Health Psychol 17:494–503PubMedPubMedCentralGoogle Scholar
  32. Carstensen LL, Loeckenhoff CE (2003) Aging, emotion, and evolution: the bigger picture. Ann N Y Acad Sci 1000:152–179PubMedGoogle Scholar
  33. Carstensen LL, Mikels JA (2005) At the intersection of emotion and cognition: aging and the positivity effect. Curr Dir Psychol Sci 14:117–121Google Scholar
  34. Carstensen LL, Isaacowitz DM, Charles ST (1999) Taking time seriously: a theory of socioemotional selectivity. Am Psychol 54:165–181PubMedGoogle Scholar
  35. Carstensen LL, Fung HH, Charles ST (2003) Socioemotional selectivity theory and the regulation of emotion in the second half of life. Motiv Emot 27:103–123Google Scholar
  36. Carstensen LL, Turan B, Scheibe S, Ram N, Ersner-Hershfield H, Samanez-Larkin GR, Brooks KP, Nesselroade JR (2011) Emotional experience improves with age: evidence based on over 10 years of experience sampling. Psychol Aging 26:21–33PubMedPubMedCentralGoogle Scholar
  37. Change A, Potential E, Kisley M, Wood S, Burrows CL (2007) Looking at the sunny side of life: age-related change in an event-related potential measure of the negativity bias. Psychol Sci 18:838–844Google Scholar
  38. Charles ST, Mather M, Carstensen LL (2003) Aging and emotional memory: the forgettable nature of negative images for older adults. J Exp Psychol Gen 132:310–324PubMedGoogle Scholar
  39. Csibra G (2010) Recognizing communicative intentions in infancy. Mind Lang 25:141–168Google Scholar
  40. Csibra G, Gergely G (2009) Natural pedagogy. Trends Cogn Sci 13:148–153PubMedGoogle Scholar
  41. Dawson G, Toth K, Abbott R, Osterling J, Munson J, Estes A, Liaw J (2004) Early social attention impairments in autism: social orienting, joint attention, and attention to distress. Dev Psychol 40:271–283PubMedGoogle Scholar
  42. D'Entremont B, Hains SMJ, Muir DW (1997) A demonstration of gaze following in 3-to 6- month-olds. Infant Behav Dev 20:569–572Google Scholar
  43. Drayton LA, Santos LR (2015) A decade of theory of mind research on Cayo Santiago: insights into rhesus macaque social cognition. Am J Primatol 78:106–116Google Scholar
  44. Dubuc C, Allen WL, Cascio J, Lee DS, Maestripieri D, Petersdorf M, Winters S, Higham JP (2016) Who cares? Experimental attention biases provide new insights into a mammalian sexual signal. Behav Ecol 27:68–74PubMedGoogle Scholar
  45. Ferrari PF, Kohler E, Fogassi L, Gallese V (2000) The ability to follow eye gaze and its emergence during development in macaque monkeys. Proc Natl Acad Sci U S A 97:3997–14002Google Scholar
  46. Ferrari PF, Coude G, Gallese V, Fogassi L (2008) Having access to others’ mind through gaze: the role of ontogenetic and learning processes in gaze-following behavior of macaques. Soc Neurosci 3:239–249PubMedGoogle Scholar
  47. Ferrari PF, Pauker A, Ionica C, Suomi SJ (2009) Reciprocal face-to-face communication between rhesus macaque mothers and their newborn infants. Curr Biol 19:1768–1772PubMedPubMedCentralGoogle Scholar
  48. Fischer J (2017) On the social life and motivation changes of aging monkeys. Gerontology 63:572–579PubMedGoogle Scholar
  49. Flom R, Lee K, Muir D (eds) (2007) Gaze-following: its development and significance. Erlbaum, MahwahGoogle Scholar
  50. Flombaum JI, Santos S (2005) Rhesus monkeys attribute perceptions to others. Curr Biol 15:447–452PubMedGoogle Scholar
  51. Fox J, Weisberg S, Friendly M, Hong J, Andersen R, Firth D, Taylor S (2016) Package ‘effects’: effect displays for linear, generalized linear, and other models,
  52. Fredrickson BL (1995) Socioemotional behavior at the end of college life. J Soc Pers Relat 12:261–276Google Scholar
  53. Fredrickson BL, Carstensen LL (1990) Choosing social partners: how old age and anticipated endings make people more selective. Psychol Aging 5:335–347PubMedPubMedCentralGoogle Scholar
  54. Fung HH, Isaacowitz DM (2016) The role of time and time perspective in age-related processes: introduction to the special issue. Psychol Aging 31:553–557PubMedGoogle Scholar
  55. Gergely G, Nadasdy Z, Csibra G, Biro S (1995) Taking the intentional stance at 12 months of age. Cognition 56:165–193Google Scholar
  56. Gomez JC (2005) Species comparative studies and cognitive development. Trends Cogn Sci 9:118–125PubMedGoogle Scholar
  57. Gothard KM, Battaglia FP, Erickson CA, Spitler KM, Amaral DG (2007) Neural responses to facial expression and face identity in the monkey amygdala. J Neurophysiol 97:1671–1683PubMedGoogle Scholar
  58. Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162Google Scholar
  59. Hare B, Call J, Agnetta B, Tomasello M (2000) Chimpanzees know what conspecifics do and do not see. Anim Behav 59:771–785PubMedGoogle Scholar
  60. Hare B, Call J, Tomasello M (2001) Do chimpanzees know what conspecifics know? Anim Behav 61:139–151PubMedGoogle Scholar
  61. Hare B, Call J, Tomasello M (2006) Chimpanzees deceive a human competitor by hiding. Cognition 101:495–514PubMedGoogle Scholar
  62. Hawkes K (2004) Human longevity: the grandmother effect. Nature 428:128–129Google Scholar
  63. Hawkes K, O’Connell JF, Blurton Jones G, Alvarez H, Charnov EL (1998) Grandmothering, menopause, and the evolution of human life histories. Proc Natl Acad Sci U S A 95:1336–1339PubMedPubMedCentralGoogle Scholar
  64. Higham JP, Hughes KD, Brent LJN, Dubuc C, Engelhardt A, Heistermann M, Maestripieri D, Santos LR, Stevens M (2011) Familiarity affects the assessment of female facial signals of fertility by free-ranging male rhesus macaques. Proc R Soc Lond B 278:3452–3458Google Scholar
  65. Hoffman KL, Gothard KM, Schmid MC, Logothetis NK (2007) Facial-expression and gaze-selective responses in the monkeys amygdala. Curr Biol 17:766–772PubMedGoogle Scholar
  66. Hoffman CL, Higham JP, Mas-Rivera A, Ayala JE, Maestripieri D (2010) Terminal investment and senescence in rhesus macaques (Macaca mulatta) on Cayo Santiago. Behav Ecol 21:972–978PubMedPubMedCentralGoogle Scholar
  67. Hughes KD, Santos LR (2012) Rotational displacement skills in the rhesus macaques (Macaca mulatta). J Comp Psychol 126:421–432PubMedPubMedCentralGoogle Scholar
  68. Isaacowitz DM, Wadlinger HA, Goren D, Wilson HR (2006a) Is there an age-related positivity effect in visual attention? A comparison of two methodologies. Emotion 6:511–516PubMedGoogle Scholar
  69. Isaacowitz DM, Wadlinger HA, Goren D, Wilson HR (2006b) Selective preference in visual fixation away from negative images in old age? An eye-tracking study. Psychol Aging 21:40–48PubMedGoogle Scholar
  70. Isaacowitz DM, Toner K, Goren D, Wilson HR (2008) Looking while unhappy: mood-congruent gaze in young adults, positive gaze in older adults. Psychol Sci 19:848–853PubMedPubMedCentralGoogle Scholar
  71. Ito TA, Cacioppo JT, Lang PJ (1998) Eliciting affect using the international affective picture system: bivariate evaluation and ambivalence. Personal Soc Psychol Bull 24:855–879Google Scholar
  72. Janson CH, van Schaik CP (1993) Ecological risk aversion in juvenile primates: slow and steady wins the race. In: Pereira ME, Fairbanks LA (eds) Juvenile primates: life history, development, and behavior. The University of Chicago Press, Chicago, pp 57–76Google Scholar
  73. Kaminski J, Call J, Tomasello M (2008) Chimpanzees know what others know, but not what they believe. Cognition 109:224–234PubMedGoogle Scholar
  74. Kano F, Call J (2014) Cross-species variation in gaze following and conspecific preference among great apes, human infants and adults. Anim Behav 91:137–150Google Scholar
  75. Kano F, Hirata S, Call J (2015) Social attention in the two species of Pan: bonobos make more eye contact than chimpanzees. PLoS One 10:e0129684PubMedPubMedCentralGoogle Scholar
  76. Kaplan H, Hill K, Lancaster J, Hurtado AM (2000) A theory of human life history evolution: diet, intelligence, and longevity. Evol Anthropol 9:156–185Google Scholar
  77. Klin A, Lin DJ, Gorrindo P, Ramsay G, Jones W (2009) Two-year-olds with autism orient to non-social contingencies rather than biological motion. Nature 459:257–263PubMedPubMedCentralGoogle Scholar
  78. Krachun C, Carpenter M, Call J, Tomasello M (2007) A competitive nonverbal false belief task for children and apes. Dev Sci 12:521–535Google Scholar
  79. Krupenye C, K F, Hirata S, Call J, Tomasello M (2016) Great apes anticipate that other individuals will act according to false beliefs. Science 354:110–114PubMedGoogle Scholar
  80. Kuhn G, Pagano A, Maani S, Bunce D (2015) Age-related decline in the reflexive component of overt gaze following. Q J Exp Psychol 68:1073–1081Google Scholar
  81. Kulik L, Amici F, Langos D, Widdig A (2015) Sex differences in the development of aggressive behavior in rhesus macaques (Macaca mulatta). Int J Primatol 36:764–789Google Scholar
  82. Kuznetsova A, Brockhoff PB, Christensen RHB (2015) lmerTest: tests in linear mixed effects models. Package ‘lmerTest’. R package version 2.0–33,
  83. Lacreuse A, Russell JL, Hopkins W, Herndon JG (2014) Cognitive and motor aging in female chimpanzees. Neurobiol Aging 35:623–632PubMedGoogle Scholar
  84. Leigh SR (2004) Brain growth, life history, and cognition in primate and human evolution. Am J Primatol 62:139–164PubMedGoogle Scholar
  85. Leigh SR (2012) Brain size growth and life history in human evolution. Evol Biol 39:587–599Google Scholar
  86. Luo Y, Johnson SC (2009) Recognizing the role of perception in action at 6 months. Dev Sci 12:142–149PubMedGoogle Scholar
  87. MacLean EL, Hare B (2012) Bonobos and chimpanzees infer the target of another’s attention. Anim Behav 83:345–353Google Scholar
  88. Maestripieri D, Wallen K (1997) Affiliative and submissive communication in rhesus macaques. Primates 38:127–138Google Scholar
  89. Marticorena D, Ruiz AM, Mukerji C, Goddu A, Santos LR (2011) Monkeys represent others’ knowledge but not their beliefs. Dev Sci 14:1406–1416PubMedPubMedCentralGoogle Scholar
  90. Martin A, Santos LR (2014) The origins of belief representation: monkeys fail to automatically represent others’ beliefs. Cognition 130:300–308PubMedGoogle Scholar
  91. Martin A, Santos LR (2016) What cognitive representations support primate theory of mind? Trends Cogn Sci 20:375–382PubMedGoogle Scholar
  92. Mather M, Carstensen LL (2003) Aging and attentional biases for emotional faces. Psychol Aging 14:409–415Google Scholar
  93. Mather M, Carstensen LL (2005) Aging and motivated cognition: the positivity effect in attention and memory. Trends Cogn Sci 9:469–502Google Scholar
  94. Matsuzawa T (2007) Comparative cognitive development. Dev Sci 10:97–103PubMedGoogle Scholar
  95. Matsuzawa T, Tomonaga M, Tanaka M (eds) (2006) Cognitive development in chimpanzees. Springer-Verlag, TokyoGoogle Scholar
  96. Melis AP, Call J, Tomasello M (2006) Chimpanzees conceal visual and auditory information from others. J Comp Psychol 120:154–162PubMedGoogle Scholar
  97. Moll H, Tomasello M (2004) 12- and 18-month-old infants follow gaze to spaces behind barriers. Dev Sci 7:F1–F9PubMedGoogle Scholar
  98. Moll H, Tomasello M (2006) Level 1 perspective-taking at 24 months of age. Br J Dev Psychol 24:603–613Google Scholar
  99. Morril RJ, Paukner A, Ferrari PF, Ghazanfar AA (2012) Monkey lipsmacking develops like the human speech rhythm. Dev Sci 15:557–568Google Scholar
  100. Mosher CP, Zimmerman PE, Gothard KM (2011) Videos of conspecifics elicit interactive looking patterns and facial expressions in monkeys. Behav Neurosci 125:639–652PubMedPubMedCentralGoogle Scholar
  101. Myowa-Yamakoshi M, Tomonaga M, Tanaka M, Matsuzawa T (2003) Preference for human direct gaze in infant chimpanzees (Pan troglodytes). Cognition 89:B53–B64PubMedGoogle Scholar
  102. Myowa-Yamakoshi M, Yamaguchi MK, Tomanaga M, Tanaka M, Matsuzawa T (2005) Development of face recognition in infant chimpanzees (Pan troglodytes). Cogn Dev 20:49–63Google Scholar
  103. N’Diaye K, Sander K, Vuilleumier P (2009) Self-relevance processing in the human amygdala: gaze direction, facial expression, and emotion intensity. Emotion 9:798–806PubMedGoogle Scholar
  104. Okamoto S, Tomonaga M, Ishii K, Kawai N, Tanaka M, Matsuzawa T (2002) An infant chimpanzee (Pan troglodytes) follows human gaze. Anim Cogn 5:107–114PubMedGoogle Scholar
  105. Okamoto-Barth S, Call J, Tomasello M (2007) Great apes’ understanding of other individuals’ line of sight. Psychol Sci 18:462–468PubMedGoogle Scholar
  106. Okamoto-Barth S, Tomonaga M, Tanaka M, Matsuzawa T (2008) Development of using experimenter-given cues in infant chimpanzees: longitudinal changes in behavior and cognitive development. Dev Sci 11:98–108PubMedGoogle Scholar
  107. Onishi KH, Baillargeon R (2005) Do 15-month-old infants understand false beliefs? Science 308:255–258PubMedPubMedCentralGoogle Scholar
  108. Ono T, Nishijo H (2000) Neurophysiological basis of emotion in primates: neuronal responses in the monkey amygdala and anterior cingulate cortex. In: Gazzaniga MS (ed) The new cognitive neurosciences. MIT Press, Cambridge, pp 1099–1114Google Scholar
  109. Parr LA, Heintz M (2009) Facial expression recognition in rhesus monkeys, Macaca mulatta. Anim Behav 77:1507–1513PubMedPubMedCentralGoogle Scholar
  110. Parr LA, Waller BM, Fugate J (2005) Emotional communication in primates: implications for neurobiology. Curr Opin Neurobiol 15:1–5Google Scholar
  111. Parr LA, Waller BM, Burrows AM, Gothard KM, Vick SJ (2010) MaqFACS: a muscle-based facial movement coding system for the rhesus macaque. Am J Phys Anthropol 143:625–630PubMedPubMedCentralGoogle Scholar
  112. Partan SR (2002) Single and multichannel signal composition: facial expressions and vocalizations of rhesus macaques (Macaca mulatta). Behaviour 139:993–1027Google Scholar
  113. Paukner A, Slonecker EM, Murphy AM, Wooddell LJ, Dettmer AM (2018) Sex and rank affect how infant rhesus macaques look at faces. Dev Psychobiol 60:187–193PubMedGoogle Scholar
  114. Pereira M, Fairbanks LA (2002) Juvenile primates: life history, development and behavior. University of Chicago Press, ChicagoGoogle Scholar
  115. Phelps EA, LeDoux JE (2005) Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 28:175–187Google Scholar
  116. Phillips W, Barnes JL, Mahajan N, Yamuguchi M, Santos LR (2009) Unwilling’ versus ‘unable’: capuchin monkeys’ (Cebus apella) understanding of human intentional action. Dev Sci 12:938–945PubMedGoogle Scholar
  117. R Development Core Team (2018) A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna Google Scholar
  118. Robson SL, Wood B (2008) Hominin life history: reconstruction and evolution. J Anat 212:394–425PubMedPubMedCentralGoogle Scholar
  119. Rosati AG, Hare B (2009) Looking past the model species: diversity in gaze-following skills across primates. Curr Opin Neurobiol 19:45–51PubMedGoogle Scholar
  120. Rosati AG, Santos LR (2017) Tolerant Barbary macaques maintain juvenile levels of social attention in old age, but despotic rhesus macaques do not. Anim Behav 130:199–207PubMedPubMedCentralGoogle Scholar
  121. Rosati AG, Santos LR, Hare B (2010) Primate social cognition: thirty years after Premack and woodruff. In: Platt ML, Ghazanfar AA (eds) Primate Neuroethology. Oxford University Press, Oxford, pp 117–143Google Scholar
  122. Rosati AG, Wobber V, Hughes K, Santos LR (2014) Comparative developmental psychology: how is human cognitive development unique? Evol Psychol 12:448–473PubMedGoogle Scholar
  123. Rosati AG, Arre AM, Platt ML, Santos LR (2016) Rhesus monkeys show human-like changes in gaze following across the lifespan. Proc R Soc B 283:20160376PubMedGoogle Scholar
  124. Sandel AA, MacLean EL, Hare B (2011) Evidence from four lemur species that ringtailed lemur social cognition converges with that of haplorhine primates. Anim Behav 81:925–931Google Scholar
  125. Santos LR, Nissen AG, Ferrugia JA (2006) Rhesus monkeys, Macaca mulatta, know what others can and cannot hear. Anim Behav 71:1175–1181Google Scholar
  126. Schuppli C, Isler K, van Schaik CP (2012) How to explain the unusually late age at skill competence among humans. J Hum Evol 63:843–850PubMedGoogle Scholar
  127. Schwartz G (2012) Growth, development, and life history throughout the evolution of Homo. Curr Anthropol 53:S395–S408Google Scholar
  128. Senju A, Csibra G (2008) Gaze following in human infants depends on communicative signals. Curr Biol 18:668–671PubMedGoogle Scholar
  129. Shepherd SV (2010) Following gaze: gaze-following behaviors as a window into social cognition. Front Integr Neurosci 4:5PubMedPubMedCentralGoogle Scholar
  130. Simpson EA, Miller GM, Ferrari PF, Suomi SJ, Pauker A (2015) Neonatal imitation and early social experience predict gaze following abilities in infant monkeys. Sci Rep 6:20233Google Scholar
  131. Simpson EA, Nicolini Y, Shetler M, Suomi SJ, Ferrari PF, Pauker A (2016a) Experience-independent sex differences in newborn macaques: females are more social than males. Sci Rep 6:19669PubMedPubMedCentralGoogle Scholar
  132. Simpson EA, Paukner A, Sclafani V, Kaburu SSK, Suomi SJ, Ferrari PF (2016b) Acute oxytocin improves memory and gaze following in male but not female nursery-reared infant macaques. Psychopharmacology 234:497–506PubMedPubMedCentralGoogle Scholar
  133. Slessor G, Phillips LH, Bull R (2008) Age-related declines in basic social perception: evidence from tasks assessing eye-gaze processing. Psychol Aging 23:812–822PubMedGoogle Scholar
  134. Slessor G, Venturini C, Bonny EJ, Insch PM, Rokaszewicz A, Finnerty AN (2016) Specificity of age-related differences in eye-gaze following: evidence from social and nonsocial stimuli. J Gerontol B Psychol Sci Soc Sci 71:11–22PubMedGoogle Scholar
  135. Spaniol J, Voss A, Grady CL (2008) Aging and emotional memory: cognitive mechanisms underlying the positivity effect. Psychol Aging 23:859–872PubMedGoogle Scholar
  136. Spelke ES (1985) Preferential-looking methods as tools for the study of cognition in infancy. In: Krasnegor GGNA (ed) Measurement of audition and vision in the first year of postnatal life: a methodological overview. Ablex Publishing, Westport, pp 323–363Google Scholar
  137. Spelke ES, Breinlinger K, Macomber J, Jacobson K (1992) Origins of knowledge. Psychol Rev 99:605–632PubMedGoogle Scholar
  138. Teufel C, Gutmann A, Pirow R, Fischer J (2010) Facial expressions modulate the ontogenetic trajectory of gaze-following among monkeys. Dev Sci 13:913–922PubMedGoogle Scholar
  139. Thierry B (2007) Unity in diversity: lessons from macaque societies. Evol Anthropol 16:224–238Google Scholar
  140. Tinbergen N (1963) On aims and methods of ethology. Z Tierpsychol 20:410–433Google Scholar
  141. Tomasello M, Carpenter M (2005) The emergence of social cognition in three young chimpanzees. Monogr Soc Res Child Dev 70:vii-132PubMedGoogle Scholar
  142. Tomasello M, Carpenter M (2007) Shared intentionality. Dev Sci 10:121–125PubMedGoogle Scholar
  143. Tomasello M, Hare B, Fogleman T (2001) The ontogeny of gaze following in chimpanzee, Pan troglodytes, and rhesus macaques, Macaca mulatta. Anim Behav 61:335–343Google Scholar
  144. Tomasello M, Carpenter M, Call J, Behne T, Moll H (2005) Understanding and sharing intentions: the origins of cultural cognition. Behav Brain Sci 28:675–735PubMedGoogle Scholar
  145. Tomonaga M (2006) Development of chimpanzee social cognition in the first 2 years of life. In: Matsuzawa T, Tomonaga M, Tanaka M (eds) Cognitive development in chimpanzees. Springer-Verlag, Tokyo, pp 182–197Google Scholar
  146. Tomonaga M, Tanaka M, Matsuzawa T, Myowa-Yamakoshi M, Kosugi D, Mizuno Y, Okamoto S, Yamaguchi M, Bard K (2004) Development of social cognition in infant chimpanzees (Pan trogiodytes): face recognition, smiling, gaze, and the lack of triadic interactions. Jpn Psychol Res 46:227–235Google Scholar
  147. Toth K, Munson J, Meltzoff AN, Dawson G (2006) Early predictors of communication development in young children with autism spectrum disorder: joint attention, imitation, and toy play. J Austism Dev Disord 36:993–1005Google Scholar
  148. Vaish A, Grossman T, Woodward A (2008) Not all emotions are created equal: the negativity bias in social-emotional development. Psychol Bull 134:383–403PubMedPubMedCentralGoogle Scholar
  149. Volkmar F, Chawarska K, Klin A (2005) Autism in infancy and early childhood. Annu Rev Psychol 56:315–336PubMedGoogle Scholar
  150. Vouloumanos A, Martin A, Onishi KH (2014) Do 6-month-olds understand that speech can communicate? Dev Sci 17:872–879PubMedGoogle Scholar
  151. Wellman HM (2011) Developing a theory of mind. In: Goswami U (ed) The Blackwell handbook of childhood cognitive development. Wiley-Blackwell, Malden, pp 258–284Google Scholar
  152. Wellman HM, Liu D (2004) Scaling of theory of mind tasks. Child Dev 75:523–541PubMedGoogle Scholar
  153. Wellman HM, Cross D, Watson J (2001) Meta-analysis of theory of mind development: the truth about false belief. Child Dev 72:655–684PubMedGoogle Scholar
  154. Wobber V, Herrmann E, Hare B, Wrangham R, Tomasello M (2014) Differences in the early cognitive development of children and great apes. Dev Psychobiol 56:547–573PubMedGoogle Scholar
  155. Woodward AL (1998) Infants selectively encode the goal object of an actors reach. Cognition 69:1–34PubMedGoogle Scholar
  156. Woodward AL, Sommerville JA, Guajardo JJ (2001) How infants make sense of intentional action. In: Malle BF, Moses LJ, Baldwin DA (eds) Intentions and intentionality: foundations of social cognition. The MIT Press, Cambridge, pp 149–169Google Scholar
  157. Zuur A, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effect models and extensions in ecology. Springer, New YorkGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Departments of Psychology and AnthropologyUniversity of MichiganAnn ArborUSA
  2. 2.Department of PsychologyYale UniversityNew HavenUSA
  3. 3.Departments of Neuroscience, Psychology, and MarketingUniversity of PennsylvaniaPhiladelphiaUSA

Personalised recommendations