Mirror self-recognition in primates: Difference between revisions

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Since the original demonstration of [[mirror self-recognition]] in [[chimpanzee]]s and the failure of macaques to show [[self-awareness]] in reaction to their mirror images<ref name=Gallup1/>, many studies have investigated '''mirror self-recognition in primates'''. While members of most species of [[great apes]] have shown compelling evidence that they recognize themselves, no [[monkey]] has convincingly done so<ref name=Gallup2/>. This apparent and evolutionarily recent [[cognitive divide]] within the order Primates continues to generate resistance and considerable debate, with recurring efforts to obtain data that would bridge the divide.
Since the original demonstration of [[mirror self-recognition]] in [[chimpanzee]]s and the failure of macaques to show [[self-awareness]] in reaction to their mirror images<ref name=Gallup1/>, many studies have investigated '''mirror self-recognition in primates'''. While members of most species of [[great apes]] have shown compelling evidence that they recognize themselves, no [[monkey]] has convincingly done so<ref name=Gallup2/>. This apparent and evolutionarily recent [[cognitive divide]] within the order Primates continues to generate considerable debate, with recurring efforts to obtain data that would provide clarification.


== Great apes ==
== Great apes ==
Line 14: Line 14:
== Monkeys ==
== Monkeys ==


One recent challenge to what's known as the cognitive division hypothesis of self-recognition was a claim of mirror self-recognition in [[rhesus monkey]]s<ref name=Rajala1/>. Individually housed monkeys sometimes manipulated an acrylic block screwed into their skull for neurophysiological experiments, and some of these manipulations occurred while the monkeys looked at their reflection in a mirror. However, the same monkeys failed to show any signs of self-recognition on a conventional mark test. Furthermore, no baseline observations were reported, and no quantitative data were presented on manipulation of the block while looking elsewhere. The mark test requires applying the mark in such a way that the subject will not know the mark is there until it is seen in a mirror. It seems likely that the acrylic blocks on the monkeys' heads<ref name=Rajala1/> provided strong tactile cues that negate their status as a suitable alternative to more conventional marks in [[mark test]]s.
One recent challenge to what's known as the cognitive division hypothesis of self-recognition was a claim of mirror self-recognition in [[rhesus monkey]]s<ref name=Rajala1/><ref name=Zimmer1/>. Individually housed monkeys sometimes manipulated an acrylic block screwed into their skull for neurophysiological experiments, and some of these manipulations occurred while the monkeys looked at their reflection in a mirror. However, the same monkeys failed to show any signs of self-recognition on a conventional mark test. Furthermore, no baseline observations were reported, and no quantitative data were presented on manipulation of the block while looking elsewhere. The mark test requires applying the mark in such a way that the subject will not know the mark is there until it is seen in a mirror. It seems likely that the acrylic blocks on the monkeys' heads<ref name=Rajala1/> provided strong tactile cues that negate their status as a suitable alternative to more conventional marks in [[mark test]]s.


One particularly intriguing aspect of how monkeys respond to mirrors is that even though they show no signs of self-recognition, they can learn to use mirrored cues to locate otherwise hidden objects<ref name=Anderson2/>. In one study, macaques that saw the reflection of an object suspended above them reached for the object<ref name=Itakura1/>. It is therefore unsurprising that objects attached to a monkey's head would elicit investigation. Contrary to the claim that traditional marks are not sufficiently salient, rhesus monkeys readily investigate such marks when applied to body parts that can be seen directly<ref name=Gallup7/>.
One particularly intriguing aspect of how monkeys respond to mirrors is that even though they show no signs of self-recognition, they can learn to use mirrored cues to locate otherwise hidden objects<ref name=Anderson2/>. In one study, macaques that saw the reflection of an object suspended above them reached for the object<ref name=Itakura1/>. It is therefore unsurprising that objects attached to a monkey's head would elicit investigation. Contrary to the claim that traditional marks are not sufficiently salient, rhesus monkeys readily investigate such marks when applied to body parts that can be seen directly<ref name=Gallup7/>.
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<ref name=Roma1>Roma P. G, Silberberg A, Huntsberry M. E, Christensen C. J, Ruggier A. M, et al.  (2007) Mark tests for mirror self-recognition in capuchin monkeys (''Cebus apella'') trained to touch marks. Am J Primatol 69: 989–1000. </ref>
<ref name=Roma1>Roma P. G, Silberberg A, Huntsberry M. E, Christensen C. J, Ruggier A. M, et al.  (2007) Mark tests for mirror self-recognition in capuchin monkeys (''Cebus apella'') trained to touch marks. Am J Primatol 69: 989–1000. </ref>
<ref name=Macellini1>Macellini S, Ferrari P. F, Bonini L, Fogassi L, Paukner A (2010) A modified mark test for own-body recognition in pig-tailed macaques (''Macaca nemestrina''). Anim Cogn 13: 631–639. </ref>
<ref name=Macellini1>Macellini S, Ferrari P. F, Bonini L, Fogassi L, Paukner A (2010) A modified mark test for own-body recognition in pig-tailed macaques (''Macaca nemestrina''). Anim Cogn 13: 631–639. </ref>
 
<ref name=Zimmer1>The debate about this article is highlighted in a blog post by [[Carl Zimmer]]: [http://blogs.discovermagazine.com/loom/2010/09/29/monkeys-in-the-mirror-and-the-nature-of-science/ Monkeys in the mirror and the nature of science].</ref>
}}
}}[[Category:Suggestion Bot Tag]]

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This page is an adaptation of an article by James R. Anderson and Gordon G. Gallup Jr, originally published in PLoS Biology in 2011[1] under a Creative Commons Attribution license.

Since the original demonstration of mirror self-recognition in chimpanzees and the failure of macaques to show self-awareness in reaction to their mirror images[2], many studies have investigated mirror self-recognition in primates. While members of most species of great apes have shown compelling evidence that they recognize themselves, no monkey has convincingly done so[3]. This apparent and evolutionarily recent cognitive divide within the order Primates continues to generate considerable debate, with recurring efforts to obtain data that would provide clarification.

Great apes

Great apes typically display mirror self-recognition by showing diminished social responses toward the reflection and spontaneously using the mirror to investigate parts of their body that cannot be seen without a mirror. Self-recognition is confirmed by appropriate mirror-guided exploration of otherwise unknown and invisible marks usually applied to the individual's head[2][4]. It is important to note the typical focus and concentration of great apes as they use the reflection to pick their teeth, explore their ears, or investigate their genitals. At best, only fleeting or incidental touches near the mark have been reported in a few monkeys during mark tests[5]. No monkey has ever been shown to use its reflection to carefully inspect a directly non-visible body part such as inside its mouth or behind an ear, in spite of repeated attempts to make things easier for monkeys. Such attempts include early and prolonged exposure to mirrors, paired and group exposure, use of angled mirrors (to avoid gaze aversion), contactable and portable mirrors, operant training of mark-directed responses, and efforts to make the mark more salient[5][6].

Positive evidence of self-recognition in great apes and the lack of evidence in monkeys suggest the emergence of a qualitative difference in self-awareness during primate evolution, a possibility supported by other lines of evidence[3][7][8]. Any new claim that monkeys share the same capacity for self-recognition as great apes therefore requires rigorous evidence that must stand up to careful scrutiny.

Monkeys

One recent challenge to what's known as the cognitive division hypothesis of self-recognition was a claim of mirror self-recognition in rhesus monkeys[9][10]. Individually housed monkeys sometimes manipulated an acrylic block screwed into their skull for neurophysiological experiments, and some of these manipulations occurred while the monkeys looked at their reflection in a mirror. However, the same monkeys failed to show any signs of self-recognition on a conventional mark test. Furthermore, no baseline observations were reported, and no quantitative data were presented on manipulation of the block while looking elsewhere. The mark test requires applying the mark in such a way that the subject will not know the mark is there until it is seen in a mirror. It seems likely that the acrylic blocks on the monkeys' heads[9] provided strong tactile cues that negate their status as a suitable alternative to more conventional marks in mark tests.

One particularly intriguing aspect of how monkeys respond to mirrors is that even though they show no signs of self-recognition, they can learn to use mirrored cues to locate otherwise hidden objects[11]. In one study, macaques that saw the reflection of an object suspended above them reached for the object[12]. It is therefore unsurprising that objects attached to a monkey's head would elicit investigation. Contrary to the claim that traditional marks are not sufficiently salient, rhesus monkeys readily investigate such marks when applied to body parts that can be seen directly[13].

When first confronted with a mirror, monkeys typically show a range of social responses that diminish over time. Comparisons of these reactions with those shown in the presence of a live conspecific behind a transparent partition reveal some differences[14][15]. Fish also show different brain activation in response to their mirror image and a live conspecific[16]. But simple discrimination clearly does not equate to self-recognition; although it is indeed "social," the reflection represents atypical behavior, only ever mimicking in real time what the observer does. Therefore it is to be expected that the responses will not be exactly the same as those triggered by a live conspecific.

In contrast to great apes, however, monkeys never fully make the transition from other- to self-directed mirror-mediated responding. In one study of rhesus monkeys with years of mirror experience, the monkeys showed diminished social responses to the reflection, and mostly exhibited only passing interest in the mirror. However, simply moving the mirror to a new location (e.g., from one side of the cage to the other) produced a short-lived, but dramatic reinstatement of vigorous social responding to the reflection[17]. In a follow-up study five years later, the mirror was simply turned away from the home cage of two monkeys. Several days later, when it was turned back to face the cage, both animals reacted as if they were seeing monkeys they had never seen before, showing intensive social and aggressive behavior directed toward the reflection[18].

Over the years, several claims of self-recognition in monkeys have appeared, and comparative self-recognition research remains a "hot topic." In one study, conspicuous marks were applied to the heads of cotton-top tamarins[19]. Some of the monkeys reportedly met the criteria for self-recognition, but a subsequent attempt to replicate these results failed, leading to the following conclusion:

"Overall, results suggest that cotton-top tamarins fail to exhibit any evidence of mirror-guided behavior….Taken together, the results…tilt the scale back in favor of a phylogenetic gap between monkeys and at least some apes"[20].

Research trends

Recent assessments of whether monkeys recognize themselves include modifications of the mark test, and alternatives to mirror-image stimulation. In one variant of the mark test, marmoset monkeys were marked with chocolate paste rather than odorless dye, in a deliberate attempt to increase the monkeys' attention to the mark. However, this did not lead to mirror-guided exploration of the mark[21]. In an exploration of capuchin monkeys' reactions to video images of themselves, capuchins clearly distinguished between real-time images and images delayed by one second[22]. Although they showed no explicit signs of self-recognition, they were sensitive to the visual consequences of their own movements. In another video study, Japanese macaques were extensively trained to use a tool to retrieve food, and then direct view of their hand was replaced by a video image. Bimodal sensory neurons in the parietal cortex were found to fire, similar to mirror neurons, not only when the monkey directly saw an object approaching its hand, but also when the scene was visible only on the video monitor[23].

Two recent studies that involved marking the bodies of monkeys failed to find any evidence of mirror self-recognition. Adopting a procedure originally devised to assess spontaneous interest in visible marks[13], capuchin monkeys were marked on directly visible body areas to give them enhanced experience of the correspondence between their marked body and their reflection. Despite being trained to touch such marks, when marks were confined to their face the monkeys failed to use of their reflection to touch or try to remove them[24]. When pig-tailed macaques were allowed to see marks on their bodies only in a mirror, they did not use the reflection to reach for and investigate the marks. This suggests that common mechanisms underlie body and facial self-recognition[25].

References

  1. ↑ Anderson JR, Gallup GG (2011). "Which primates recognize themselves in mirrors?". PLoS Biol 9 (3): e1001024. DOI:10.1371/journal.pbio.1001024. PMID 21390247. PMC PMC3046971. Research Blogging. [e]
  2. ↑ 2.0 2.1 Gallup G. G Jr (1970) Chimpanzees: self-recognition. Science 167: 86–87.
  3. ↑ 3.0 3.1 Gallup G. G Jr, Anderson J. R, Platek S. M (2011) Self-recognition. In: Gallagher S, editor. Oxford handbook of the self. Oxford: Oxford University Press. In press.
  4. ↑ Gallup G. G Jr (1994) Self-recognition: research strategies and experimental design. In: Parker S. T, Mitchell R. W, Boccia M. L, editors. Self-awareness in animals and humans: developmental perspectives. New York: Cambridge University Press. pp. 35–50.
  5. ↑ 5.0 5.1 Anderson J. R, Gallup G. G Jr (1999) Self-recognition in nonhuman primates: past and future challenges. In: Haug M, Whalen R. E, editors. Animal models of human emotion and cognition. Washington (District of Columbia): American Psychological Association. pp. 175–194.
  6. ↑ Gallup G. G Jr, Anderson J. R, Shillito D. J (2002) The mirror test. In: Bekoff M, Allen C, Burghardt G. M, editors. The cognitive animal: empirical and theoretical perspectives on animal cognition. Cambridge (Massachusetts): MIT Press. pp. 325–333.
  7. ↑ Gallup G. G Jr (1982) Self-awareness and the emergence of mind in primates. Am J Primatol 2: 237–248.
  8. ↑ Gallup G. G Jr (1987) Self-awareness. In: Mitchell G, Erwin J, editors. Comparative primate biology, Volume 2B. Behavior cognition and motivation. , New York: Alan R. Liss. pp. 3–16.
  9. ↑ 9.0 9.1 Rajala A. Z, Reininger K. R, Lancaster K. M, Populin L. C (2010) Rhesus monkeys (Macaca mulatta) do recognize themselves in the mirror: Implications for the evolution of self-recognition. PLoS ONE 9: e12865. doi:10.1371/journal.pone.0012865.
  10. ↑ The debate about this article is highlighted in a blog post by Carl Zimmer: Monkeys in the mirror and the nature of science.
  11. ↑ Anderson J. R (1986) Mirror-mediated finding of hidden food by monkeys (Macaca tonkeana and Macaca fascicularis). J Comp Psychol 100: 237–242.
  12. ↑ Itakura S (1987) Use of a mirror to direct their responses in Japanese monkeys (Macaca fuscata fuscata). Primates 28: 343–352.
  13. ↑ 13.0 13.1 Gallup G. G Jr, Wallnau L. B, Suarez S. D (1980) Failure to find self-recognition in mother-infant and infant-infant rhesus monkey pairs. Folia Primatol 33: 210–219.
  14. ↑ Anderson J. R (1983) Responses to mirror-image stimulation and assessment of self-recognition in mirror- and peer-reared stumptail macaques. Q J Exp Psychol 25: 201–212.
  15. ↑ de Waal FB, Dindo M, Freeman CA, Hall MJ (2005). "The monkey in the mirror: hardly a stranger". Proc Natl Acad Sci U S A 102 (32): 11140-7. DOI:10.1073/pnas.0503935102. PMID 16055557. PMC PMC1183568. Research Blogging. [e]
  16. ↑ Desjardins J. K, Fernald R. D (2010) What do fish make of mirror images? Biol Lett 6: 744–747.
  17. ↑ Suarez S. D, Gallup G. G Jr (1986) Social responding to mirrors in rhesus macaques (Macaca mulatta): effects of changing mirror location. Am J Primatol 11: 239–244.
  18. ↑ Gallup G. G Jr, Suarez S. D (1991) Social responding to mirrors in rhesus monkeys (Macaca mulatta): effects of temporary mirror removal. J Comp Psychol 105: 376–379.
  19. ↑ Hauser M. D, Kralik J, Botto-Mahan C, Garrett M, Oser J (1995) Self- recognition in primates: phylogeny and the salience of species-typical features. Proc Natl Acad Sci U S A 92: 10811–10814.
  20. ↑ Hauser M. D, Miller C. T, Liu K, Gupta R (2001) Cotton-top tamarins (Saguinus oedipus) fail to show mirror-guided self-exploration. Am J Primatol 53: 131–137.
  21. ↑ Heschl A, Burkart J (2006) A new mark test for mirror self-recognition in non-human primates. Primates 47: 187–198.
  22. ↑ Anderson J. R, Kuroshima H, Paukner A, Fujita K (2009) Capuchin monkeys (Cebus apella) respond to video images of themselves. Anim Cogn 12: 55–62.
  23. ↑ Iriki A, Tanaka M, Obayashi S, Iwamura Y (2001) Self-images in the video monitor coded by monkey intraparietal neurons. Neurosci Res 40: 163–173.
  24. ↑ Roma P. G, Silberberg A, Huntsberry M. E, Christensen C. J, Ruggier A. M, et al. (2007) Mark tests for mirror self-recognition in capuchin monkeys (Cebus apella) trained to touch marks. Am J Primatol 69: 989–1000.
  25. ↑ Macellini S, Ferrari P. F, Bonini L, Fogassi L, Paukner A (2010) A modified mark test for own-body recognition in pig-tailed macaques (Macaca nemestrina). Anim Cogn 13: 631–639.
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