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Research Article

Spontaneous expression of mirror self-recognition in monkeys after learning precise visual-proprioceptive association for mirror images

Liangtang Chang, Shikun Zhang, Mu-ming Poo, and Neng Gong
  1. aInstitute of Neuroscience, State Key Laboratory of Neuroscience, Chinese Academy of Sciences (CAS) Key Laboratory of Primate Neurobiology, CAS Center for Excellence in Brain Science and Intelligence Technology, Shanghai Institutes for Biological Sciences, CAS, Shanghai 200031, China

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PNAS March 21, 2017 114 (12) 3258-3263; first published February 13, 2017; https://doi.org/10.1073/pnas.1620764114
Liangtang Chang
aInstitute of Neuroscience, State Key Laboratory of Neuroscience, Chinese Academy of Sciences (CAS) Key Laboratory of Primate Neurobiology, CAS Center for Excellence in Brain Science and Intelligence Technology, Shanghai Institutes for Biological Sciences, CAS, Shanghai 200031, China
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Shikun Zhang
aInstitute of Neuroscience, State Key Laboratory of Neuroscience, Chinese Academy of Sciences (CAS) Key Laboratory of Primate Neurobiology, CAS Center for Excellence in Brain Science and Intelligence Technology, Shanghai Institutes for Biological Sciences, CAS, Shanghai 200031, China
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Mu-ming Poo
aInstitute of Neuroscience, State Key Laboratory of Neuroscience, Chinese Academy of Sciences (CAS) Key Laboratory of Primate Neurobiology, CAS Center for Excellence in Brain Science and Intelligence Technology, Shanghai Institutes for Biological Sciences, CAS, Shanghai 200031, China
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  • For correspondence: mpoo@ion.ac.cn ngong@ion.ac.cn
Neng Gong
aInstitute of Neuroscience, State Key Laboratory of Neuroscience, Chinese Academy of Sciences (CAS) Key Laboratory of Primate Neurobiology, CAS Center for Excellence in Brain Science and Intelligence Technology, Shanghai Institutes for Biological Sciences, CAS, Shanghai 200031, China
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  • For correspondence: mpoo@ion.ac.cn ngong@ion.ac.cn
  1. Contributed by Mu-ming Poo, January 10, 2017 (sent for review June 10, 2016; reviewed by Olaf Blanke and Sid Kouider)

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Significance

Self-awareness is a higher intelligence that can be revealed by mirror self-recognition (MSR) in humans. Testing MSR has become the main approach to examining the existence of self-recognition in animals, and only a few species have passed the test. However, it remains controversial whether failing the MSR test is a result of the lack of an animal’s self-recognition ability or the inadequacy of the mirror test. We found that MSR spontaneously appeared in rhesus monkeys after training for precise visual-proprioceptive association for mirror images. Thus, bodily self-consciousness may be a cognitive ability present in many more species than previously thought, and could be revealed by MSR when the animal acquired visual-proprioceptive association for the images in the mirror.

Abstract

Mirror self-recognition (MSR) is generally considered to be an intrinsic cognitive ability found only in humans and a few species of great apes. Rhesus monkeys do not spontaneously show MSR, but they have the ability to use a mirror as an instrument to find hidden objects. The mechanism underlying the transition from simple mirror use to MSR remains unclear. Here we show that rhesus monkeys could show MSR after learning precise visual-proprioceptive association for mirror images. We trained head-fixed monkeys on a chair in front of a mirror to touch with spatiotemporal precision a laser pointer light spot on an adjacent board that could only be seen in the mirror. After several weeks of training, when the same laser pointer light was projected to the monkey's face, a location not used in training, all three trained monkeys successfully touched the face area marked by the light spot in front of a mirror. All trained monkeys passed the standard face mark test for MSR both on the monkey chair and in their home cage. Importantly, distinct from untrained control monkeys, the trained monkeys showed typical mirror-induced self-directed behaviors in their home cage, such as using the mirror to explore normally unseen body parts. Thus, bodily self-consciousness may be a cognitive ability present in many more species than previously thought, and acquisition of precise visual-proprioceptive association for the images in the mirror is critical for revealing the MSR ability of the animal.

  • mirror self-recognition
  • rhesus monkey
  • bodily self-consciousness
  • visual-proprioceptive association
  • instrumental mirror use

Footnotes

  • ↵1To whom correspondence may be addressed. Email: mpoo{at}ion.ac.cn or ngong{at}ion.ac.cn.
  • Author contributions: M.-m.P. and N.G. designed research; L.C. and S.Z. performed research; L.C., S.Z., and N.G. analyzed data; and M.-m.P. and N.G. wrote the paper.

  • Reviewers: O.B., Ecole Polytechnique Fédérale de Lausanne; and S.K., Ecole Normale Supérieure and CNRS.

  • The authors declare no conflict of interest.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1620764114/-/DCSupplemental.

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Visual-proprioceptive training leads to monkey MSR
Liangtang Chang, Shikun Zhang, Mu-ming Poo, Neng Gong
Proceedings of the National Academy of Sciences Mar 2017, 114 (12) 3258-3263; DOI: 10.1073/pnas.1620764114

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Visual-proprioceptive training leads to monkey MSR
Liangtang Chang, Shikun Zhang, Mu-ming Poo, Neng Gong
Proceedings of the National Academy of Sciences Mar 2017, 114 (12) 3258-3263; DOI: 10.1073/pnas.1620764114
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  • Biological Sciences
  • Psychological and Cognitive Sciences

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  • Monkeys pass the mirror test—again
    - Mar 16, 2017
Proceedings of the National Academy of Sciences: 114 (12)
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