Neonatal imitation in Rhesus Macaques
Open accessAbstract
The emergence of social behaviors early in life is likely crucial for the development of mother-infant relationships. Some of these behaviors, such as the capacity of neonates to imitate adult facial movements, were previously thought to be limited to humans and perhaps the ape lineage. Here we report the behavioral responses of infant rhesus macaques (Macaca mulatta) to the following human facial and hand gestures: lip smacking, tongue protrusion, mouth opening, hand opening, and opening and closing of eyes (control condition). In the third day of life, infant macaques imitate lip smacking and tongue protrusion. On the first day of life, the model's mouth openings elicited a similar matched behavior (lip smacking) in the infants. These imitative responses are present at an early stage of development, but they are apparently confined to a narrow temporal window. Because lip smacking is a core gesture in face-to-face interactions in macaques, neonatal imitation may serve to tune infants' affiliative responses to the social world. Our findings provide a quantitative description of neonatal imitation in a nonhuman primate species and suggest that these imitative capacities, contrary to what was previously thought, are not unique to the ape and human lineage. We suggest that their evolutionary origins may be traced to affiliative gestures with communicative functions.
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Rhesus macaques display basic aspects of complex social behaviors typically considered uniquely human, including social imitation, prosocial behaviors, and understanding others' perceptions.
“Critically, rhesus macaques display basic aspects of complex social behaviors that are typically considered ‘uniquely human’ (Frith and Frith, 2007; Saxe, 2006). These include social imitation (Ferrari et al., 2006; Subiaul, 2004), prosocial behaviors (Chang et al., 2011; Masserman et al., 1964), as well as understanding others’ perceptions (Flombaum and Santos, 2005; Santos et al., 2006).”
From Oxytocin and social cognition in rhesus macaques: Implications for understanding and treating human psychopathology (2014) · cites this paper as Ferrari et al., 2006
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Action recognition in the premotor cortex
Gallese, V., Fadiga, L., Fogassi, L., & Rizzolatti, G. (1996) · Brain · doi:10.1093/brain/119.2.593 · Cited by 4,968 · see citing works
Self-citationNeurophysiological mechanisms underlying the understanding and imitation of action
Rizzolatti, G., Fogassi, L., & Gallese, V. (2001) · Nature Reviews Neuroscience · doi:10.1038/35090060 · Cited by 3,302 · see citing works
Self-citationImitation of Facial and Manual Gestures by Human Neonates
Meltzoff, A. N., & Moore, M. (1977) · Science · doi:10.1126/science.198.4312.75 · Cited by 3,277 · see citing works
Parietal Lobe: From Action Organization to Intention Understanding
Fogassi, L., Ferrari, P. F., Gesierich, B., Rozzi, S., Chersi, F., & Rizzolatti, G. (2005) · Science · doi:10.1126/science.1106138 · Cited by 1,990 · see citing works
Self-citationNewborn Infants Imitate Adult Facial Gestures
Meltzoff, A. N., & Moore, M. (1983) · Child Development · doi:10.1111/j.1467-8624.1983.tb00496.x · Cited by 956 · see citing works
Learning by imitation: A hierarchical approach
Byrne, R. W., & Russon, A. E. (1998) · Behavioral and Brain Sciences · doi:10.1017/s0140525x98001745 · Cited by 885 · see citing works
Discrimination and imitation of facial expression by neonates
Field, T. M., Woodson, R., Greenberg, R., & Cohen, D. (1982) · Science · doi:10.1126/science.7123230 · Cited by 864 · see citing works
Conformity to cultural norms of tool use in chimpanzees
Whiten, A., Horner, V., & de Waal, F. Β. Μ. (2005) · Nature · doi:10.1038/nature04047 · Cited by 786 · see citing works
Meltzoff, A. N., & Moore, M. (1989) · Developmental Psychology · doi:10.1037/0012-1649.25.6.954 · Cited by 745 · see citing works
Ferrari, P. F., Gallese, V., Rizzolatti, G., & Fogassi, L. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02601.x · Cited by 728 · see citing works
Self-citationMeltzoff, A. N., & Jean Decety, A. (2003) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2002.1261 · Cited by 713 · see citing works
Causes and consequences of imitation
Heyes, C. M. (2001) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(00)01661-2 · Cited by 620 · see citing works
Whiten, A., Custance, D. M., Gomez, J.-C., Teixidor, P., & Bard, K. A. (1996) · Journal of comparative psychology · doi:10.1037/0735-7036.110.1.3 · Cited by 464 · see citing works
The Facial Displays of the Catarrhine Monkeys and Apes
Hooff, V. (2017) · Routledge eBooks · doi:10.4324/9781315127392-2 · Cited by 416 · see citing works
Resonance behaviors and mirror neurons.
Rizzolatti, G., Fadiga, L., Fogassi, L., & D, V. G. M. (1999) · PubMed · Cited by 329 · see citing works
Self-citationPrimate life history and evolution
DeRousseau, C. J. (1990) · Wiley-Liss eBooks · Cited by 290 · see citing works
Meltzoff, A. N., & Moore, M. (1992) · Infant Behavior and Development · doi:10.1016/0163-6383(92)80015-m · Cited by 282 · see citing works
From mirror neurons to imitation: Facts and speculations
Rizzolatti, G., Fadiga, L., Fogassi, L., & D, V. G. M. (2002) · Cambridge University Press eBooks · doi:10.1017/cbo9780511489969.015 · Cited by 279 · see citing works
Self-citationImitation of the sequential structure of actions by chimpanzees (Pan troglodytes).
Whiten, A. (1998) · Journal of comparative psychology · doi:10.1037/0735-7036.112.3.270 · Cited by 267 · see citing works
Voelkl, B., & Huber, L. (2000) · Animal Behaviour · doi:10.1006/anbe.2000.1457 · Cited by 260 · see citing works
Visalberghi, E. M., & Fragaszy, D. M. (1990) · Cambridge University Press eBooks · doi:10.1017/cbo9780511665486.011 · Cited by 241 · see citing works
Self-citationThe role of person and object in eliciting early imitation
Legerstee, M. (1991) · Journal of Experimental Child Psychology · doi:10.1016/0022-0965(91)90086-8 · Cited by 241 · see citing works
A 10-year perspective of motherless-mother monkey behavior.
Ruppenthal, G. C., & Al, E. (1976) · Journal of Abnormal Psychology · doi:10.1037//0021-843x.85.4.341 · Cited by 218 · see citing works
Nadel, J. (2002) · Cambridge University Press eBooks · doi:10.1017/cbo9780511489969.003 · Cited by 194 · see citing works
Only tongue protrusion modeling is matched by neonates
Anisfeld, M. (1996) · Developmental Review · doi:10.1006/drev.1996.0006 · Cited by 188 · see citing works
Imitation in neonatal chimpanzees (Pan troglodytes)
Myowa‐Yamakoshi, M., Tomonaga, M., Tanaka, M., & Matsuzawa, T. (2004) · Developmental Science · doi:10.1111/j.1467-7687.2004.00364.x · Cited by 178 · see citing works
Anisfeld, M. (1991) · Developmental Review · doi:10.1016/0273-2297(91)90003-7 · Cited by 176 · see citing works
Visalberghi, E. M., & Addessi, E. (2000) · Animal Behaviour · doi:10.1006/anbe.2000.1425 · Cited by 168 · see citing works
Self-citationPovinelli, D. J., & Povinelli, T. J. (1996) · International Journal of Primatology · doi:10.1007/bf02735269 · Cited by 152 · see citing works
"Do Monkeys Ape?"—Ten Years After
Visalberghi, E. M., & Fragaszy, D. M. (2002) · The MIT Press eBooks · doi:10.7551/mitpress/3676.003.0019 · Cited by 134 · see citing works
Self-citationExploring the Presence of Imitation during Early Infancy
Abravanel, E., & Sigafoos, A. D. (1984) · Child Development · doi:10.2307/1129950 · Cited by 125 · see citing works
Heimann, M., Nelson, K. E., & SCHALLER, J. (1989) · Scandinavian Journal of Psychology · doi:10.1111/j.1467-9450.1989.tb01072.x · Cited by 123 · see citing works
Releaser-induced recognition learning.
Suboski, M. D. (1990) · Psychological Review · doi:10.1037/0033-295x.97.2.271 · Cited by 112 · see citing works
Imitative skills between birth and six months
Fontaine, R. (1984) · Infant Behavior and Development · doi:10.1016/s0163-6383(84)80047-8 · Cited by 112 · see citing works
Moving primate genomics beyond the chimpanzee genome
Goodman, M., Grossman, L. I., & Wildman, D. E. (2005) · Trends in Genetics · doi:10.1016/j.tig.2005.06.012 · Cited by 97 · see citing works
Cognitive structure and development in nonhuman primates
Williams (1990) · Choice Reviews Online · doi:10.5860/choice.27-6340 · Cited by 93 · see citing works
Imitation of facial gestures by an infant chimpanzee
Myowa, M. (1996) · Primates · doi:10.1007/bf02381408 · Cited by 81 · see citing works
Principles Of Developmental Psychology
Butterworth, G. E. (2014) · Psychology Press eBooks · doi:10.4324/9781315804675 · Cited by 77 · see citing works
Macaques (Macaca nemestrina) recognize when they are being imitated
Paukner, A., Anderson, J. R., Borelli, E., Visalberghi, E. M., & Ferrari, P. F. (2005) · Biology Letters · doi:10.1098/rsbl.2004.0291 · Cited by 77 · see citing works
Self-citationThe ontogeny of communication in the stumptail macaque (Macaca arctiodes)
Chevalier‐Skolnikoff, S. (1974) · Medical Entomology and Zoology · Cited by 72 · see citing works
Ferrari, P. F., Maiolini, C., Addessi, E., Fogassi, L., & Visalberghi, E. M. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.01.009 · Cited by 68 · see citing works
Self-citationComparison of Development and Life History in Pan and Cebus
Fragaszy, D. M., & Bard, K. A. (1997) · International Journal of Primatology · doi:10.1023/a:1026339712071 · Cited by 66 · see citing works
Natural imitation induced by joint attention in Japanese monkeys
Kumashiro, M., Ishibashi, H., Uchiyama, Y., Itakura, S., Murata, A., & Iriki, A. (2003) · International Journal of Psychophysiology · doi:10.1016/s0167-8760(03)00126-0 · Cited by 58 · see citing works
Gestural Communication and Its Cognitive Implications in Pigtail Macaques (Macaca Nemestrina)
Dario Maestripieri, A. (1996) · Behaviour · doi:10.1163/156853996x00576 · Cited by 57 · see citing works
Changes in imitative behavior during early infancy
Field, T. M., Goldstein, S., Vega‐Lahr, N., & Porter, K. (1986) · Infant Behavior and Development · doi:10.1016/0163-6383(86)90015-9 · Cited by 52 · see citing works
Galloway, A. T., Addessi, E., Fragaszy, D. M., & Visalberghi, E. M. (2005) · International Journal of Primatology · doi:10.1007/s10764-005-0729-7 · Cited by 44 · see citing works
Self-citationBard, K. A., & Russell, C. L. (1999) · Cited by 38 · see citing works
Bush's policy stopped US gaining stem-cell lead
Lanza, R., & Green, R. M. (2005) · Nature · doi:10.1038/438422a · Cited by 7 · see citing works
Flagged first, then by citations
Research works printed but not linked: 2
- Anisfeld M 1991 Neonatal imitation: Review Developmental Rev 11 60 97
- Kugiumutzakis G 1999 Genesis and development of early infant mimesis to facial and vodal models Nadel J Butterworth G Imitation in infancy Cambridge Cambridge University Press 36 59
Cited by
Sorted by citations
Putting the Altruism Back into Altruism: The Evolution of Empathy
de Waal, F. B. M. (2008) · Annual Review of Psychology · doi:10.1146/annurev.psych.59.103006.093625 · Cited by 2,483 · see citing works
Imitation, empathy, and mirror neurons
Iacoboni, M. (2009) · Annual Review of Psychology · doi:10.1146/annurev.psych.60.110707.163604 · Cited by 1,606 · see citing works
Mammalian empathy: behavioural manifestations and neural basis
de Waal, F. B. M., & Preston, S. D. (2017) · Nature Reviews Neuroscience · doi:10.1038/nrn.2017.72 · Cited by 957 · see citing works
Eight problems for the mirror neuron theory of action understanding in monkeys and humans
Hickok, G. (2009) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2009.21189 · Cited by 887 · see citing works
Brain basis of human social interaction: from concepts to brain imaging
Hari, R., & Kujala, M. V. (2009) · Physiological Reviews · doi:10.1152/physrev.00041.2007 · Cited by 638 · see citing works
Haidt, J., & Joseph, C. (2008) · The Innate Mind, Volume 3 · doi:10.1093/acprof:oso/9780195332834.003.0019 · Cited by 650 · see citing works
Mirror neurons: from origin to function
Cook, R., Bird, G., Catmur, C., Press, C., & Heyes, C. (2014) · Behavioral and Brain Sciences · doi:10.1017/s0140525x13000903 · Cited by 632 · see citing works
Hurley, S. (2008) · Behavioral and Brain Sciences · doi:10.1017/s0140525x07003123 · Cited by 512 · see citing works
Expanding the mirror: vicarious activity for actions, emotions, and sensations
Keysers, C., & Gazzola, V. (2009) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2009.10.006 · Cited by 472 · see citing works
Kraskov, A., Dancause, N., Quallo, M. M., Shepherd, S., & Lemon, R. N. (2009) · Neuron · doi:10.1016/j.neuron.2009.12.010 · Cited by 298 · see citing works
Social cognition and the evolution of language: constructing cognitive phylogenies
Fitch, W. T., Huber, L., & Bugnyar, T. (2010) · Neuron · doi:10.1016/j.neuron.2010.03.011 · Cited by 264 · see citing works
“Monkeys show cognitive imitation by copying an expert’s use of a rule (Subiaul et al., 2004), recognize when they are being imitated (Paukner et al., 2005; Paukner et al., 2009), and imitate adult facial movements as neonates (Ferrari et al., 2006, 2009).”
Comprehensive longitudinal study challenges the existence of neonatal imitation in humans
Oostenbroek, J., Suddendorf, T., Nielsen, M., Redshaw, J., Kennedy-Costantini, S., Davis, J., Clark, S., & Slaughter, V. (2016) · Current Biology · doi:10.1016/j.cub.2016.03.047 · Cited by 262 · see citing works
Simpson, E. A., Murray, L., Paukner, A., & Ferrari, P. F. (2014) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2013.0289 · Cited by 150 · see citing works
Self-citationFrom monkey mirror neurons to primate behaviours: possible ‘direct’ and ‘indirect’ pathways
Ferrari, P. F., Bonini, L., & Fogassi, L. (2009) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2009.0062 · Cited by 120 · see citing works
Self-citationEvolution of mirror systems: a simple mechanism for complex cognitive functions
Bonini, L., & Ferrari, P. F. (2011) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2011.06002.x · Cited by 89 · see citing works
Self-citationInhaled oxytocin increases positive social behaviors in newborn macaques
Simpson, E. A., Sclafani, V., Paukner, A., Hamel, A. F., Novak, M. A., Meyer, J. S., Suomi, S. J., & Ferrari, P. F. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1402471111 · Cited by 82 · see citing works
Self-citationChang, S. W. C., & Platt, M. L. (2014) · Brain Research · doi:10.1016/j.brainres.2013.11.006 · Cited by 71 · see citing works
Field, T. (2012) · Psychology · doi:10.4236/psych.2012.36066 · Cited by 50 · see citing works
- Authors
- Ferrari, P. F., Visalberghi, E., Paukner, A., Fogassi, L., Ruggiero, A., & Suomi, S. J.
- Affiliations
- University of Parma (IT)
- National Research Council (IT)
- National Institutes of Health (US)
- Corresponding author
- Ferrari, Pier F
- Venue
- PLoS Biology
- Publisher
- Public Library of Science (PLoS)
- Published
- 2006-09-05
- Volume
- 4
- Issue
- 9
- Pages
- e302
- ISSN
- 1544-9173 (ISSN-L)
- 1545-7885
- PMC
- PMC1560174
- OpenAlex
- W2132307087
- Cited by
- 354
- References
- 49
- Citations by year
- 2026: 15 · 2025: 8 · 2024: 12 · 2023: 6 · 2022: 8 · 2021: 12 · 2020: 7 · 2019: 13 · 2018: 12 · 2017: 19 · 2016: 25 · 2015: 22 · 2014: 24 · 2013: 30 · 2012: 20
- FWCI
- 35.81
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS Biology (publishedVersion, public-domain)
- Europe PMC (PubMed Central) (publishedVersion, public-domain)
- PubMed (publishedVersion)
- Nottingham Trent University's Institutional Repository (Nottingham Trent Repository) (acceptedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- National Institutes of Health
- National Institute of Child Health and Human Development
- NHLBI Division of Intramural Research
- Topics
- Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
- Social Sciences › Psychology › Developmental and Educational Psychology › Child and Animal Learning Development
- Life Sciences › Neuroscience › Cognitive Neuroscience › Face Recognition and Perception
- Keywords
- neonatal imitation, rhesus monkeys, facial gestures, tongue protrusion, mother-infant relationship, affiliative behavior, social behavior development
- MeSH terms
- Animals, Animals, Newborn, Behavior, Animal, Facial Expression, Female, Imitative Behavior, Macaca mulatta, Male, Maternal Behavior, Mouth, Nonverbal Communication, Social Behavior, Time Factors, Tongue
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