Rhesus Monkeys (Macaca mulatta) Do Recognize Themselves in the Mirror: Implications for the Evolution of Self-Recognition

Self-recognition in front of a mirror is used as an indicator of self-awareness. Along with humans, some chimpanzees and orangutans have been shown to be self-aware using the mark test. Monkeys are conspicuously absent from this list because they fail the mark test and show persistent signs of social responses to mirrors despite prolonged exposure, which has been interpreted as evidence of a cognitive divide between hominoids and other species. In stark contrast with those reports, the rhesus monkeys in this study, who had been prepared for electrophysiological recordings with a head implant, showed consistent self-directed behaviors in front of the mirror and showed social responses that subsided quickly during the first experimental session. The self-directed behaviors, which were performed in front of the mirror and did not take place in its absence, included extensive observation of the implant and genital areas that cannot be observed directly without a mirror. We hypothesize that the head implant, a most salient mark, prompted the monkeys to overcome gaze aversion inhibition or lack of interest in order to look and examine themselves in front of the mirror. The results of this study demonstrate that rhesus monkeys do recognize themselves in the mirror and, therefore, have some form of self-awareness. Accordingly, instead of a cognitive divide, they support the notion of an evolutionary continuity of mental functions.     

What mirror self-recognition in nonhumans can tell us about aspects of self

Research on mirror self-recognition where animals are observed for mirror-guided self-directed behaviour has predominated the empirical approach to self-awareness in nonhuman primates. The ability to direct behaviour to previously unseen parts of the body such as the inside of the mouth, or grooming the eye by aid of mirrors has been interpreted as recognition of self and evidence of a self-concept. Three decades of research has revealed that contrary to monkeys, most great apes (humans, common chimpanzees, pygmy chimpanzees and orangutans but not the gorilla) have convincingly displayed the capacity to recognize self by mirrors. The putative discontinuity in phylogeny of the ability suggests the existence of a so-called cognitive gap between great apes and the rest of the animal kingdom. However, methodological and theoretical inconsistencies regarding the empirical approach prevail. For instance, the observation of self-directed behaviour might not be as straightforward as it seems. In addition, the interpretation of mirror self-recognition as an index of self-awareness is challenged by alternative explanations, raising doubt about some assumptions behind mirror self-recognition. To evaluate the significance of the test in discussions of the concept of self this paper presents and analyses some major arguments raised on the mirror task.     

Mirror-Mark Tests Performed on Jackdaws Reveal Potential Methodological Problems in the Use of Stickers in Avian Mark-Test Studies

Some animals are capable of recognizing themselves in a mirror, which is considered to be demonstrated by passing the mark test. Mirror self-recognition capacity has been found in just a few mammals having very large brains and only in one bird, the magpie (Pica pica). The results obtained in magpies have enormous biological and cognitive implications because the fact that magpies were able to pass the mark test meant that this species is at the same cognitive level with great apes, that mirror self-recognition has evolved independently in the magpie and great apes (which diverged 300 million years ago), and that the neocortex (which is not present in the bird''s brains) is not a prerequisite for mirror self-recognition as previously believed. Here, we have replicated the experimental design used on magpies to determine whether jackdaws (Corvus monedula) are also capable of mirror self-recognition by passing the mark test. We found that our nine jackdaws showed a very high interest towards the mirror and exhibited self-contingent behavior as soon as mirrors were introduced. However, jackdaws were not able to pass the mark test: both sticker-directed actions and sticker removal were performed with a similar frequency in both the cardboard (control) and the mirror conditions. We conclude that our jackdaws'' behaviour raises non-trivial questions about the methodology used in the avian mark test. Our study suggests that the use of self-adhesive stickers on sensitive throat feathers may open the way to artefactual results because birds might perceive the stickers tactilely.     

Contingency checking and self-directed behaviors in giant manta rays: Do elasmobranchs have self-awareness?

Elaborate cognitive skills arose independently in different taxonomic groups. Self-recognition is conventionally identified by the understanding that one’s own mirror reflection does not represent another individual but oneself, which has never been proven in any elasmobranch species to date. Manta rays have a high encephalization quotient, similar to those species that have passed the mirror self-recognition test, and possess the largest brain of all fish species. In this study, mirror exposure experiments were conducted on two captive giant manta rays to document their response to their mirror image. The manta rays did not show signs of social interaction with their mirror image. However, frequent unusual and repetitive movements in front of the mirror suggested contingency checking; in addition, unusual self-directed behaviors could be identified when the manta rays were exposed to the mirror. The present study shows evidence for behavioral responses to a mirror that are prerequisite of self-awareness and which has been used to confirm self-recognition in apes.     

Mirror-mediated responses of California scrub jays (Aphelocoma californica) during a caching task and the mark test

Mirror self-recognition, as an index of self-awareness, has been proposed as a precursor for more complex social cognitive abilities, such as prosocial reasoning and cooperative decision-making. Indeed, evidence for mirror self-recognition has been shown for animals possessing complex social cognitive abilities such as great apes, dolphins, elephants and corvids. California scrub jays (Aphelocoma californica) have provided strong evidence that non-human animals are capable of mental state attribution. For instance, scrub jays are reported to use their experience stealing the food of others to infer that other birds may similarly intend to steal from them. If a concept of “self” is required for such complex social cognitive abilities, then scrub jays might be expected to show mirror self-recognition. Thus, we examined whether California scrub jays are capable of mirror self-recognition using two experimental contexts: a caching task and the mark test. During the caching task, we compared the extent to which scrub jays protected their food after caching alone, in the presence of a conspecific and in the presence of a mirror. The birds did not engage in more cache protection behaviours with a mirror present than when caching alone, suggesting scrub jays may have recognized their reflection and so did not expect cache theft. Alternative explanations for this behaviour are also discussed. During the mark test, the scrub jays were surreptitiously marked with a red or plumage-coloured control sticker. The scrub jays showed no evidence of mirror self-recognition during the mark test, as the birds did not preferentially attempt to remove the red mark in the presence of a mirror. Together, the results provide mixed evidence of the mirror self-recognition abilities of California scrub jays. We highlight the need to develop alternative approaches for evaluating mirror self-recognition in non-human animals to better understand its relationship with complex social cognition.     

Human cognitive ecology: an instructive framework for comparative primatology

In this review, research on human cognitive ecology is compared with studies of the cognitive ecologies of apes-especially the common chimpanzee. The objective was to assess the feasibility of extending an activity-theory framework developed in studies of humans to an integrated approach for studying the cognitive accomplishments and skills of other primates living in the wild. Six generalizations were abstracted from studies of humans: 1) Social and material environments are arranged to facilitate production. 2) Human activity is shaped by conceptual and cultural principles that provide underlying logic for working knowledge and practice. 3) Schemata (multimodal, mental representations of procedures, strategies, and techniques) govern performance in a domain. 4) Working knowledge, skills, and social identities are co-constructed in communities of practice. 5) Rehearsal improves skilled performances, from which reputations as well as material products are derived. 6) Planning and emergence are in productive tension in human practices. These generalizations are applied to findings in the literature regarding the behavior of chimpanzees and other apes in the wild to assess the potential utility of a situated-activity approach for comparative studies of primate cognition. It is argued in the Discussion that schemata constitute a common core of higher primate intelligence. Planning, emergence, and alterations of the environment to facilitate production further characterize human and chimpanzee or gorilla behaviors to varying degrees. Less apparent in the nonhuman-primate literature is evidence of governing principles, rehearsal, and skill-based reputations or identities entailing theories of mind. Nonetheless, recent observations in the wild suggest that further research is warranted to explore the rudiments of each of these components to enhance our understanding of the ecology of primate cognition and its evolutionary history.     

Space use selectivity by chimpanzees and gorillas in an indoor-outdoor enclosure

Understanding the relationship between physical environments and nonhuman primate behavior is a key element for effective care and management in a range of settings. The physical features of the captive environment, including not only gross useable space but also environmental complexity, can have a significant influence on primate behavior and ultimately, animal welfare. But despite this connection, there remains relatively little conclusive data on how captive primates, especially great apes, use the spaces provided to them, especially in modern, indoor-outdoor enclosures that have become more prevalent in recent years. In this study, we used four years of detailed data on where 23 great apes (chimpanzees and gorillas) positioned themselves within a modern, indoor-outdoor zoo enclosure to determine not only how the apes utilized their space but also how access to outdoor areas affected their spatial selectivity. We found that both species used relatively little of their available space: chimpanzees and gorillas spent half their time in only 3.2 and 1.5% of their useable three-dimensional space, respectively. Chimpanzees utilized the outdoor space more than gorillas, but access to the outdoors did not affect space selectivity in the indoor area for either species. Although both species of ape were highly selective in their space use, consideration should be given to the importance of providing the choice to locate in a variety of spaces, including outdoor areas. These data represent an extremely detailed account of space selectivity by great apes in an indoor-outdoor environment and have substantial implications for future facility design and captive primate management.     

Mirror-induced behavior in the magpie (Pica pica): evidence of self-recognition

Comparative studies suggest that at least some bird species have evolved mental skills similar to those found in humans and apes. This is indicated by feats such as tool use, episodic-like memory, and the ability to use one's own experience in predicting the behavior of conspecifics. It is, however, not yet clear whether these skills are accompanied by an understanding of the self. In apes, self-directed behavior in response to a mirror has been taken as evidence of self-recognition. We investigated mirror-induced behavior in the magpie, a songbird species from the crow family. As in apes, some individuals behaved in front of the mirror as if they were testing behavioral contingencies. When provided with a mark, magpies showed spontaneous mark-directed behavior. Our findings provide the first evidence of mirror self-recognition in a non-mammalian species. They suggest that essential components of human self-recognition have evolved independently in different vertebrate classes with a separate evolutionary history.     

Monkeys with mirrors: Some questions for primate psychology

Monkeys do not appear to recognize themselves in mirrors but display social responses to the reflection. This article comprehensively reviews the literature concerning monkeys’ reactions to mirrors, describing the interest shown in reflections, the reinforcing effects of mirror-image stimulation, the social responses of the monkeys, their interpretation of objects reflected in a mirror, and their performance in tests of self-recognition. In all cases limitations of the methods employed restrict conclusions about the monkeys’ behavior. Detailed behavioral observations coupled with comparisons of the psychological properties of mirrors with those of other stimuli promise to reveal more useful information about cognitive mechanisms and abilities of monkeys and other primates.     

Monkeys and apes: Are their cognitive skills really so different?

Differences in cognitive skills across taxa, and between monkeys and apes in particular, have been explained by different hypotheses, although these often are not supported by systematic interspecific comparisons. Here, we directly compared the cognitive performance of the four great apes and three monkey species (spider monkeys, capuchin monkeys, and long‐tailed macaques), differing in their phylogenetic‐relatedness and socioecology. We tested subjects on their ability to remember object locations (memory task), track object displacements (transposition task), and obtain out‐of‐reach rewards (support task). Our results showed no support for an overall clear‐cut distinction in cognitive skills between monkeys and apes as species performance varied substantially across tasks. Although we found differences in performance at tracking object displacements between monkeys and apes, interspecific differences in the other two tasks were better explained in terms of differential socioecology, especially differential levels of fission–fusion dynamics. A cluster analysis using mean scores of each condition of the three tasks for each species suggested that the only dichotomy might be between members of the genus Pan and the rest of the tested species. These findings evidence the importance of using multiple tasks across multiple species in a comparative perspective to test different explanations for the enhancement of specific cognitive skills. Am J Phys Anthropol 143:188–197, 2010. © 2010 Wiley‐Liss, Inc.     

Brief communication: Reaction to fire by savanna chimpanzees (Pan troglodytes verus) at Fongoli,Senegal: Conceptualization of “fire behavior” and the case for a chimpanzee model

The use and control of fire are uniquely human traits thought to have come about fairly late in the evolution of our lineage, and they are hypothesized to correlate with an increase in intellectual complexity. Given the relatively sophisticated cognitive abilities yet small brain size of living apes compared to humans and even early hominins, observations of wild chimpanzees' reactions to naturally occurring fire can help inform hypotheses about the likely responses of early hominins to fire. We use data on the behavior of savanna chimpanzees (Pan troglodytes verus) at Fongoli, Senegal during two encounters with wildfires to illuminate the similarities between great apes and humans regarding their reaction to fire. Chimpanzees' close relatedness to our lineage makes them phylogenetically relevant to the study of hominid evolution, and the open, hot and dry environment at Fongoli, similar to the savanna mosaic thought to characterize much of hominid evolution, makes these apes ecologically important as a living primate model as well. Chimpanzees at Fongoli calmly monitor wildfires and change their behavior in anticipation of the fire's movement. The ability to conceptualize the “behavior” of fire may be a synapomorphic trait characterizing the human‐chimpanzee clade. If the cognitive underpinnings of fire conceptualization are a primitive hominid trait, hypotheses concerning the origins of the control and use of fire may need revision. We argue that our findings exemplify the importance of using living chimpanzees as models for better understanding human evolution despite recently published suggestions to the contrary. Am J Phys Anthropol, 2010. © 2009 Wiley‐Liss, Inc.     

Self-awareness in dreaming.

The process by which self-awareness or subjective experience (consciousness) is maintained has been conceptually and phenomenologically associated primarily with the waking state. In the present study the authors investigate, through introspective reports, the existence and variety of self-awareness in dreaming and whether this phenomenon could, under certain conditions, be distinguished into primary and reflective consciousness. For consistency with theory and dreaming research, instead of reflective consciousness we used the term 'reflective awareness.' Findings indicate that self-awareness in dreaming can be found in its both primary and reflective modes. Phenomenologically, primary consciousness exists in four basic modalities: perceptual, experiential, cognitive, and memory-based recognition. Expressions of these primary consciousness modalities are accessible through introspective interviews during waking. Based on participants' statements, reflective consciousness (awareness) in dreaming was initiated by noticing positive and negative feelings and by personally defined oddities. These findings point to a possible oscillation between primary and reflective consciousness in dreaming. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

New data on the brain and cognitive abilities of birds

New evidence of functional analogies and homologies of avian and mammalian brains is presented, as is a revised nomenclature of the most important brain structures. Comparative characteristics of the avian brain and criteria for its progressive development in the phylogeny have been considered. We studied the possibility to use Portmann??s index as one of the indicators of brain development in different avian species. We substantiated the necessity to chose for investigation new sets of avian species with medium (Parus caeruleus and Loxia curvirostra) and low (Larus glaucescens) levels of brain complexity to maintain fully valuable grounds for comparing the cognitive abilities in birds. The main experimentally supported proofs of the existence of elementary thinking and some other cognitive functions in the higher birds have been reviewed. The high levels of cognitive processes that underlie the tool using ability in birds, as well as the similarity to those processes in apes, have been demonstrated from the results obtained in the first decade of the 21st century. Comparative studies on proto-instrumental activity confirmed the ability of hooded crows and ravens to find urgent solution of tool-using tasks. Although birds with a medium level of brain complexity display seemingly rational behavior, it is plausible that they use simpler rules being unable to understand the task logic. It was shown that birds of different orders with a high level of brain complexity demonstrate similar dynamics in the development of abstract concepts. Crossbills, which have a medium level of brain complexity, were able to develop the same concepts at a lower level than the corvids; whereas the seagulls and pigeons, which possess a low level of cognitive abilities, were not able to operate any abstractions and were incapable of solving other cognitive tests. The fact that corvids, parrots, and apes have similar abilities to solve some cognitive tasks supports the hypothesis of the convergent evolution of the brain and cognition in birds and primates.     

Old world monkeys compare to apes in the primate cognition test battery

Understanding the evolution of intelligence rests on comparative analyses of brain sizes as well as the assessment of cognitive skills of different species in relation to potential selective pressures such as environmental conditions and social organization. Because of the strong interest in human cognition, much previous work has focused on the comparison of the cognitive skills of human toddlers to those of our closest living relatives, i.e. apes. Such analyses revealed that apes and children have relatively similar competencies in the physical domain, while human children excel in the socio-cognitive domain; in particular in terms of attention sharing, cooperation, and mental state attribution. To develop a full understanding of the evolutionary dynamics of primate intelligence, however, comparative data for monkeys are needed. We tested 18 Old World monkeys (long-tailed macaques and olive baboons) in the so-called Primate Cognition Test Battery (PCTB) (Herrmann et al. 2007, Science). Surprisingly, our tests revealed largely comparable results between Old World monkeys and the Great apes. Single comparisons showed that chimpanzees performed only better than the macaques in experiments on spatial understanding and tool use, but in none of the socio-cognitive tasks. These results question the clear-cut relationship between cognitive performance and brain size and--prima facie--support the view of an accelerated evolution of social intelligence in humans. One limitation, however, is that the initial experiments were devised to tap into human specific skills in the first place, thus potentially underestimating both true nonhuman primate competencies as well as species differences.     

Involuntary autobiographical memories and their relation to other forms of spontaneous thoughts

Involuntary autobiographical memories are memories of personal events that come to mind spontaneously—that is, with no conscious initiation of the retrieval process. Such spontaneously arising memories were long ignored in cognitive psychology, which generally has focused on controlled and strategic forms of remembering, studied in laboratory settings. Recent evidence shows that involuntary memories of past events are highly frequent in daily life, and that they represent a context-sensitive, and associative way of recollecting past events that involves little executive control. They operate by constraints that favour recent events and events with a distinct feature overlap to the current situation, which optimizes the probability of functional relevance to the ongoing situation. In addition to adults, they are documented in young children and great apes and may be an ontogenetic and evolutionary forerunner of strategic retrieval of past events. Findings suggest that intrusive involuntary memories observed clinically after traumatic events should be viewed as a dysfunctional subclass of otherwise functional involuntary autobiographical memories. Because of their highly constrained, situation-dependent and automatic nature, involuntary autobiographical memories form a distinct category of spontaneous thought that cannot be equated with mind wandering.This article is part of the theme issue ‘Offline perception: voluntary and spontaneous perceptual experiences without matching external stimulation’.     

Evolutionary psychology of spatial representations in the hominidae

Comparatively little is known about the inherited primate background underlying human cognition, the human cognitive "wild-type." Yet it is possible to trace the evolution of human cognitive abilities and tendencies by contrasting the skills of our nearest cousins, not just chimpanzees, but all the extant great apes, thus showing what we are likely to have inherited from the common ancestor. By looking at human infants early in cognitive development, we can also obtain insights into native cognitive biases in our species. Here, we focus on spatial memory, a central cognitive domain. We show, first, that all nonhuman great apes and 1-year-old human infants exhibit a preference for place over feature strategies for spatial memory. This suggests the common ancestor of all great apes had the same preference. We then examine 3-year-old human children and find that this preference reverses. Thus, the continuity between our species and the other great apes is masked early in human ontogeny. These findings, based on both phylogenetic and ontogenetic contrasts, open up the prospect of a systematic evolutionary psychology resting upon the cladistics of cognitive preferences.     

Social Awareness in Monkeys

Tests of self-awareness in nonhuman primates have to date beenconcerned almost entirely with the recognition of an animal'sreflection in a mirror. By contrast, we know much less aboutnon-human primates' perception of their place within a socialnetwork, or of their understanding of themselves as individualswith unique sets of social relationships. Here we review evidencethat monkeys who fail the mirror test may nonetheless behaveas if they recognize themselves as distinct individuals, eachof whom occupies a unique place in society and has a specificset of relations with others. A free-ranging vervet monkey,baboon, or macaque recognizes other members of his group asindividuals. He also recognizes matrilineal kin groups, lineardominance rank orders, and behaves as if he recognizes his ownunique place within them. This sense of "social self" in monkeys,however, is markedly different from self-awareness in humans.Although monkeys may behave in ways that accurately place themselveswithin a social network, they are unaware of the knowledge thatallows them to do so: they do not know what they know, cannotreflect on what they know, and cannot become the object of theirown attention.     

The Anatomical and Evolutionary Relationship between Self-awareness and Theory of Mind

Although theories that examine direct links between behavior and brain remain incomplete, it is known that brain expansion significantly correlates with caloric and oxygen demands. Therefore, one of the principles governing evolutionary cognitive neuroscience is that cognitive abilities that require significant brain function (and/or structural support) must be accompanied by significant fitness benefit to offset the increased metabolic demands. One such capacity is self-awareness (SA), which (1) is found only in the greater apes and (2) remains unclear in terms of both cortical underpinning and possible fitness benefit. In the current experiment, transcranial magnetic stimulation (TMS) was applied to the prefrontal cortex during a spatial perspective-taking task involving self and other viewpoints. It was found that delivery of TMS to the right prefrontal region disrupted self-, but not other-, perspective. These data suggest that self-awareness may have evolved in concert with other right hemisphere cognitive abilities.