Neuroscience and Biobehavioral Reviews 82 (2017) 110–123

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Neuroscience and Biobehavioral Reviews

journal homepage: www.elsevier.com/locate/neubiorev

Review article

Do monkeys have a theory of mind? How to answer the question?

Hélène Meunier a,b,∗
a
Centre de Primatologie de l’Université de Strasbourg, 67207 Niederhausbergen, France
b
Laboratoire de Neurosciences Cognitives et Adaptatives, UMR 7364, CNRS et Université de Strasbourg, France

a r t i c l e i n f o a b s t r a c t

Article history: Since Premack and Woodruf (1978), the study of mindreading abilities in nonhumans, especially primates,
Received 27 May 2016 has been thoroughly investigated. But attempts to understand the evolution of this aspect of human intel-
Received in revised form 22 October 2016 ligence have mainly focused on comparisons between apes and human infants, while relatively little is
Accepted 9 November 2016
known about the abilities of monkeys. This lack of data on monkeys seems mainly due to the hypothesis
Available online 18 November 2016
of a cognitive “gap” between apes and monkeys. However, in recent years monkeys have been featuring
more prominently in the landscape of social cognition research, and some of these systematic studies
Keywords:
appear promising. This paper reviews i) current knowledge about monkeys’ socio-cognitive abilities,
Social cognition
Theory of mind
especially regarding gaze processing, attention and intention reading, and perspective-taking, ii) alter-
Attention reading native hypotheses regarding the underlying mechanisms of such complex behaviors, and iii) potential
Intention reading new perspectives and future directions for studying ToM in monkeys.
Perspective taking © 2016 Elsevier Ltd. All rights reserved.
Minimal theory of mind
Submentalizing
Comparative study
Nonhuman primate
Monkey

Contents

1. General introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 110

2. Early beginnings . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 111
3. What about monkeys? the state of the art . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 112
3.1. Gaze following . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 112
3.2. Perspective-taking . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 117
3.3. Attention reading abilities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 117
3.4. Intention reading abilities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 117
3.5. False beliefs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 118
4. Complex behaviors but simple minds? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 119
4.1. Methodological puzzle . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 119
4.2. Theoretical puzzle . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 119
5. Believers, skeptics, theoretical solutions: where does it all leave us? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 120
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 121

1. General introduction languages, tools and technologies, mathematical symbols, graphic

symbols from maps to art, and creating complex social institutions
Human beings have historically been considered unique in the such as governments and religions (Tomasello and Rakoczy, 2003).
way they comprehend the world by creating and using complex However, what being human means continues to raise major sci-
entific and philosophical questions. This broad topic has given rise
to passionate debate, as criteria of human uniqueness have fallen
∗ Corresponding author at: Centre de Primatologie de l’Université de Strasbourg, one after the other. What made our species so different from other
Fort Foch – 67207 Niederhausbergen, France. species? What drove the evolution of cognition, and what are the
E-mail address: hmeunier@unistra.fr evolutionary dynamics of our intelligence?

http://dx.doi.org/10.1016/j.neubiorev.2016.11.007
0149-7634/© 2016 Elsevier Ltd. All rights reserved.
 H. Meunier / Neuroscience and Biobehavioral Reviews 82 (2017) 110–123
It may be our species’ ability to think about the thoughts of
others that provides the ontogenetic foundation for much of what
is considered unique to human cognition (Herrmann et al., 2007).
Human social cognition is believed to be largely based on our abil-
ity to assess the psychological states of others, on remarkable and
powerful cognitive mechanisms that allow us to understand and
even foresee others’ behavior. Humans are dependent on their
mind reading abilities for navigating through their social world.
For example, while interacting with others, we routinely use sub-
tle cues, such as small eye movements, to assess what others are
thinking (i.e., if a person you are speaking to looks at your name
tag, you can infer from that eye movement that he or she does
not know your name) (Corkum and Moore, 1995). On the basis of
what a person infers from such cues about perceptions, intentions,
and beliefs of others, one can flexibly adjust one’s own behavior to
communicate, teach, or even deceive social partners (e.g., Baron-
Cohen, 1999). Reading others’ minds has thus been considered as
a milestone in human development and has led many researchers
to investigate the origins of the cognitive mechanisms underlying
this ability.
Spoken language is a cornerstone of our social cognition, and
linguistic skills have thus been considered indispensable for our
mind reading abilities (e.g. Astington and Jenkins 1999). But human
infants appear capable of attributing some states of mind to oth-
ers even when their language skills are still poor (e.g. Baillargeon
et al., 2010). Tomasello et al. (2005) have thus proposed that lan-
guage might be a by-product of mind reading abilities rather than
a mandatory component. In this case, mind reading abilities could
potentially exist in nonverbal, nonhuman species.
One valuable approach for unraveling the evolution of mind
reading abilities is to investigate similarities and differences
between humans and other closely related species (Byrne, 1995;
MacLean et al., 2012; Nunn, 2011; Shettleworth, 2010; Suddendorf
and Whiten, 2001). As our closest relatives, nonhuman primates
are a good candidate for such attempts to reconstruct cognitive
evolution (but see also deWaal and Ferrari 2010). Moreover, nonhu-
man primates have brains that are approximately twice as large as
expected compared to other mammals of comparable size (Barton,
2006), and they present a correlation between relative brain size
and phylogenetic proximity to humans, i.e., the brains of apes (cor-
rected for body size) tend to be larger than the brains of monkeys,
which in turn tend to be larger than the brains of prosimians
(Montgomery et al., 2010). As our large brain is energetically very
costly, its origins and evolution are also a source of interest. But
the evolution of unusually large brains in some groups of animals,
notably primates, has long been and still is a puzzle. Although
early explanations tended to emphasize the brain’s role in sensory
or technical competences linked to ecological pressures (foraging
skills, innovations, and way-finding), the balance of evidence now
clearly favors the suggestion that social pressures and more par-
ticularly the computational demands of living in large complex
societies and group dynamics (and notably fission-fusion dynam-
ics, Amici et al., 2008) that selected for large brains (Dunbar and
Shultz, 2007, see also Dunbar, 2009 for a review, but see also Reader
and Laland, 2002; Reader et al., 2011 and Herrmann et al., 2007
for alternative views). But all these hypotheses agree on humans’
remarkable ability to attribute mental states to others, further high-
lighting nonhuman primates as a key model in the study of the
origins and evolution of these capacities that are fundamental to
human social life.
In this review, after a brief summary of the main steps in the
comparative approach to the study of human and nonhuman pri-
mate minds, I will consider what we know and what is still missing
regarding monkeys for answering the title question of this paper.
I will then address current issues and recent alternative hypothe-
ses regarding the cognitive mechanisms underlying behaviors that
111
seem to require mentalizing in monkeys. To conclude, I will report
new perspectives and suggest some future directions for studying
mindreading in monkeys.
2. Early beginnings
Premack and Woodruff (1978) laid an early keystone for a
comparative approach with their provocative question “Does the
chimpanzee have a theory of mind?” (but see also Piaget and
Inhelder 1967; Menzel 1974, and Humphrey, 1976 for pioneer
investigations on the topic). Premack and Woodruff (1978) under-
lined the importance of investigating similarities and differences
between the minds of chimpanzee and humans. Since then,
research on mindreading, or following Premack and Woodruff and
many others: “theory of mind” (hereafter ToM), has grown expo-
nentially.
Although it focused on a nonhuman species, Premack and
Woodruff’s (1978) study was first extremely influential for human
developmental psychology, being the starting point for a huge
amount of research on the ontogeny of ToM in human infants and
their understanding of false beliefs (Wimmer and Perner, 1983).
Many studies have investigated young children’s understanding of
the psychological states of others more generally, including goals
and intentions, perceptions, knowledge, and beliefs. Before they
reach 12 months of age, human infants begin to understand that
others have goals and intentions (e.g., Gergely et al., 2002; Behne
et al., 2005). At around their first birthday they understand that
others see things and know things, according to what they saw a
few moments earlier, (e.g., Moll and Tomasello, 2004, 2007; Onishi
and Baillargeon, 2005), and by at least their second birthday they
understand that others have perspectives that differ from their own
(Moll and Tomasello, 2006). Thus, developmental psychologists
have demonstrated that humans are not born with an adult-like
ToM but that before their second birthday they are competent
at perceiving the intentionality of others’ actions and their per-
ceptions (Behne et al., 2005). Moreover, this research contributed
importantly to the understanding of non-normally developing chil-
dren (see Baron-Cohen et al., 2013).
Research on ToM in nonhuman species has significantly grown
later, resulting notably in the publication of an impressive database
constituted by Byrne and Whiten (Byrne and Whiten 1990, 1991)
on what appeared to be cases of deceptive behavior. These obser-
vations suggested that many monkeys and apes could take into
account what others could and could not see and engage in decep-
tive behaviors mainly by monitoring and manipulating others’
visual attention, but also by recognizing others’ desires and goals
(Whiten, 2013). However, this collection of observations in uncon-
trolled conditions in the wild cannot provide a definitive answer to
Premack and Woodruff’s famous question, or provide unambigu-
ous evidence regarding nonhuman primates’ abilities to attribute
mental states to others. Premack (1988) already suggested experi-
mental approaches comparable to those used with human infants
to investigate ToM in chimpanzees, and even conducted some pilot
studies. Since then, many experimental procedures have been used
with apes, mainly chimpanzees. Povinelli et al. (1990) provided
the first ‘positive’ results on chimpanzees’ inferences regarding
guessing and knowing. However, after critiques and alternative
hypothesis to explain the results (Heyes 1993 and below), in the
decade following Povinelli et al. (1990) refinements to protocols
and interpretations converged to favor negative results regarding
chimpanzees’ ability to take the visual perspective of others (e.g.
Povinelli and Eddy 1996; Call et al., 2000; see Tomasello and Call
1997; for a review).
The new millennium saw a turning point with the now-famous
landmark papers by Hare et al. (2000, 2001). The so-called object-
112 H. Meunier / Neuroscience and Biobehavioral Reviews 82 (2017) 110–123
choice task, in which subjects use a human cue to infer the correct
choice of a reward hidden in one of a number of containers, was
until 2000 s one of the most commonly used paradigms. This
task involved thus apes − or monkeys − and a human experi-
menter interacting in a cooperative context. This paradigm does
not fit the social context of spontaneous visual perspective-taking
in nonhuman primates (see Johnson and Karin-D’Arcy, 2006 for
a review), and it has limited ecological relevance for nonhuman
primates given the role of competition in their daily life (Byrne
and Whiten, 1988). Considering these two points, Hare et al. (2000,
2001) proposed an experimental design in which subjects were
tested with conspecifics (rather than a human experimenter) and
in a competitive context (rather than a cooperative one). They
tested whether subordinate subjects would more likely go for a
food item that a more dominant individual was not able to see
than towards one that was in the dominant’s line of sight. Subor-
dinate chimpanzees did indeed do this, leading the researchers to
conclude that chimpanzees are capable of first-level perspective-
taking, i.e., understanding what others can and cannot see. The
researchers then increased the difficulty level for chimpanzees, by
manipulating the dominant’s knowledge; the question now was
whether subordinate chimpanzees would understand what a com-
petitor had seen earlier and encode it to know what the dominant
now knows. The experimental results showed that chimpanzees
took into account what a competitor might have seen earlier, and
adjusted their behavior based on the knowledge state of the com-
petitor. Although these elegant paradigms gave a new momentum
to research and enhanced our knowledge about ToM in nonhuman
primates, the research also generated many commentaries and cri-
tiques (e.g., Lurz 2009; Penn and Povinelli 2007; Whiten 2013),
with some authors proposing low-level alternative hypotheses to
explain the results (see the section “Complex behaviors but simple
minds?” for more details).
3. What about monkeys? the state of the art
As already mentioned most research on social intelligence in pri-
mates has focused on great apes, particularly chimpanzees; other
primates including monkeys have been relatively neglected. This
so-called “chimpocentrism” (Beck, 1982; Miklósi, 2002) prevents
an adequate understanding of the evolution of cognition (but see
Bolhuis and Wynne 2009; deWaal and Ferrari 2010). One likely
reason for the relative lack of relevant research on monkeys is that
comparative studies often showed superior mental abilities in apes
compared to monkeys (e.g., Byrne, 1995, 2000; Reader and Laland,
2002; Tomasello and Call, 1997). However, many of the reported
differences may be explained by different tests tapping into dif-
ferent cognitive capacities; moreover, even research programs
that tested both apes and monkeys using similar protocols often
compared highly trained apes to naive monkeys, probably overesti-
mating the differences between monkeys and apes (Tomasello and
Call, 1997). Even if between-species comparisons using a variety of
different tasks have been extremely instructive regarding unique
aspects of human development (Hare, 2011), it now appears nec-
essary to compare species more systematically and reliably, using
similar standardized paradigms, for a better understanding of phy-
logenetic patterns. Until recently, however, (e.g., Herrmann et al.,
2007; Schmitt, Pankau, and Fischer, 2012), studies had not sys-
tematically compared a representative range of behavioral abilities
using the same methods in human and nonhuman individuals. Such
studies have flourished only in the last five years, as importance of
comparing different species to understand cognition becomes more
widely acknowledged (MacLean et al., 2012); an increasing num-
ber of species, even some that are phylogenetically distant from
humans, now feature in comparative studies (e.g., Amici et al., 2010;
Sandel et al., 2011). This type of large-scale comparative work is
now considered essential for testing current hypotheses regarding
the evolution of communication and social cognition (see MacLean
et al., 2012 for a review).
Regarding more specifically ToM, it is described as an emer-
gent property rather than a specialized capacity, which appears
to depend on its constituting capacities − hereafter called compo-
nents −: type and level of represented mental states, and contextual
factors (Sterck and Begeer 2010). Most studies on ToM focus on
only one of these components. Baron-Cohen (1995) attempted to
differentiate between components by studying their impairment
in autism. He highlighted abilities to share attention, to detect eye
direction and to detect intention (interpreting self-propelled mov-
ing stimuli in terms of volitional mental states of goal and desire).
Following this reasoning, comparative psychologists switched from
asking about chimpanzees’ understanding of epistemic states to
perceptual states, recognizing also that the human ToM system
might not be evolutionarily hegemonic (e.g. Hare et al., 2000;
Povinelli and Eddy, 1996b). Below, I review what we know and
what appears necessary to better investigate ToM in monkeys −
briefly introduced and compared with the literature on humans
and apes. I organize the material according to the following ToM
components: gaze following, perspective-taking, attention read-
ing, intention comprehension, and the historical hallmark of ToM:
false-belief (see also Table 1).
3.1. Gaze following
Gaze following constitutes a key developmental building block
and regulates social interactions (e.g., Meltzoff and Brooks 2007;
Teufel et al., 2010). Humans and other animals can acquire a great
amount of information by following the gaze of others toward a spe-
cific direction or object. Also known as joint attention or referential
looking, gaze following is observed in human babies starting around
4 months of age (Carpenter et al., 1998). By 12 months of age, infants
can follow others’ gaze referentially (Meltzoff and Brooks, 2007)
and use pointing as an object-directed action (Woodward and
Guajardo, 2002). In nonhuman primates, the clearest evidence for
the ability to follow gaze comes from experimental work on great
apes, notably chimpanzees. Based on a series of studies, Povinelli
and Eddy (1996a,b, 1997) concluded that chimpanzees can follow a
human experimenter’s gaze, but that they can neither use this infor-
mation to learn about objects nor to understand the “mental state”
of the individual providing the gaze cues. Studies testing gaze fol-
lowing in monkeys have shown mixed results. Spider and capuchin
monkeys (Amici et al., 2009) appear able to follow gaze around
barriers, whereas in Itakura’s (1996) study of eleven species of
prosimians, monkeys and apes, only orangutans and chimpanzees
followed a human experimenter’s gaze (eyes, head and pointing
in a corresponding direction); various monkey species did not.
However, replacing a human model by a conspecific, Tomasello
et al. (1998) showed that both apes (chimpanzees) and monkeys
(rhesus, stumptailed and pigtailed macaques, sooty mangabeys)
could follow gaze. Moreover, long-tailed macaques (Goossens et al.,
2012) appear capable of geometrical gaze following, i.e., they follow
gaze to a hidden location, and thus seem to represent space out-
side their own visual field. A recent study (Micheletta and Waller,
2012) has highlighted the importance of relationship quality and
species’ social style, by reporting that friendship improved gaze-
following responses in a tolerant species of macaque. These results
suggest that in some conditions, monkeys resemble apes in fol-
lowing another individual’s gaze, especially if the gaze model is a
conspecific. The varying results obtained in these studies highlight
the importance of the experimental paradigm and its ecological
validity for the subject when studying cognitive abilities. Moreover,
little remains known about how the model’s identity or behavior, or
Table 1
Details of experiments investigating one or several components of ToM in Apes (a) and Monkeys (b). GF = Gaze following, PT = Perspective taking (Level 1), AR = Attention reading, IR = Intention reading, FB = False beliefs, 1 = Positive
result, 0 = Negative result. *Level 2 PT. **Results varied according to the conditions. ***The number of subjects varied from 16 to 22 according to the experiments. ◦ Experimenter is cooperative in motivational trial but becomes
unable or unwilling to give food to the subject in test trials.

Table 1a
Studies Species # Sub- ToM Component investigated Social partner Social context Experimental task details
jects

GF PT AR IR FB

Premack and Woodruff
(1978)
Povinelli et al. (1990)
Povinelli and Eddy (1996a)
Pan troglodytes 1 1 Human Neutral An adult chimpanzee was shown a series of videotaped scenes of a
human actor struggling with a variety of problems and was then asked
to choose between several photographs, including one representing a
solution to the problem.
Pan troglodytes 4 1 Human Cooperative The subjects chose between information about the location of hidden
food provided by 2 experimenters who randomly alternated between
two roles (the guesser and the knower).
Pan troglodytes 7 1 Human Neutral Authors investigated whether subjects were following the gaze of

H. Meunier / Neuroscience and Biobehavioral Reviews 82 (2017) 110–123

Povinelli
and
Eddy
(1996b)
Itakura (1996)
Povinelli and Eddy (1997)
Tomasello et al. (1998)
Peignot and Anderson
(1999)
Call and Tomasello (1999)
Call et al. (2000)
Hare et al. (2000)
Kaminski et al. (2004)
Liebal et al. (2004)
Call et al. (2004)
Melis et al. (2006)
humans in response to movement of the head and/or eyes.
Pan 6 1 Human Cooperative Subjects chose between one of two experimenters, one was facing
troglodytes them and the other one was back turned, to visually communicate
with him.
0 Human Cooperative Subjects chose between one of two experimenters, one whose vision
was occluded and one whose vision was not occluded, to visually
communicate with him.
Pan troglodytes 6 1 Human Neutral Subjects were tested in a gaze-monitoring task to examine whether
Pongo pygmaeus 1 they would look where the experimenter looked and/or pointed.
Pan troglodytes 7 1 Human Neutral Subjects were tested at determining the specific location in space
behind them into which a human looks.
Pan troglodytes 15 1 Conspecific Neutral Experimenter induced one individual to look at food being displayed
and observed the reaction of the subject that was looking at that
individual − follow the gaze of its conspecific or not.
Gorilla gorilla gorilla 10 0 Human Cooperative Subjects were tested for their ability to use experimenter gaze
orientation in an object-choice task.
Pongo pygmaeus 2 0 Human Cooperative Subjects needed to find a reward in a series of finding games in which
Pan troglodytes 5 a human (the hider) hid a reward in one of two identical containers,
and another experimenter (the communicator) observed the hiding
process and attempted to help the participant by placing a marker on
the container that she believed to hold the reward. Depending on
conditions, the communicator had true or false belief.
Pan troglodytes 15 0 Human Cooperative The subjects chose between information about the location of hidden
food provided by 2 experimenters who randomly alternated between
two roles (the guesser and the knower).
Pan troglodytes 7 1 Conspecific Competitive In a competitive paradigm involving two individuals, subordinate
subjects chose between going to the food that both competitors could
see, or the food that only they could see.
Pan paniscus 3 1 Human Cooperative Subjects requested food from a human observer who was in one of
Pan troglodytes 7 various attentional states.
Pongo pygmaeus 6
Gorilla gorilla gorilla 5 1 Human Cooperative Subjects requested food from a human experimenter, whom body
Pan paniscus 4 orientation (front vs back) varied. The location of the food also varied
Pongo pygmaeus 6 (in front or behind the experimenter). Subjects were free to move
Pan troglodytes 9 around the experimenter. Subjects’ visual and auditory signals as well
as their moves were measured.
Pan troglodytes 12 1 Human Cooperative◦ Subjects’ behaviour was recorded according to whether a human was
unwilling or unable to give them food.
Pan troglodytes 7 1 Human Competitive Subjects were competing against a human who would prevent them
from obtaining food if their approaches were detected. Subjects were
given the choice of obtaining food silently or noisily when the
competitor’s back was turned.

113
Table 1 (Continued)

114
Table 1a
Studies Species # Sub- ToM Component investigated Social partner Social context Experimental task details
jects

GF PT AR IR FB

Wood et al. (2007) Pan troglodytes 25 1 Human Cooperative Subjects’ spontaneous foraging behavior was recorded in response to
actions performed by a human experimenter towards one of two
containers, i.e. Intentional (reached directly for a food container),
Accidental (flopped his hand onto a container in an accidental manner),
Hand occupied (touched one of the containers with his elbow while
the associated hand was occupied), and/or Hand empty (performed
the same elbow touch action while the associated hand was free).
Hostetter et al. (2007) Pan troglodytes 116 1 Human Cooperative Subjects requested food from a human experimenter, whom eyes state
varied. Subjects’ visual and auditory signals were measured.
Braüer et al. (2008) Pan troglodytes 11 0 Conspecific Competitive In a competitive paradigm involving two individuals, subordinate
subjects chose between going to the food, for which dominant heard
the placing, or the food placed silently.

H. Meunier / Neuroscience and Biobehavioral Reviews 82 (2017) 110–123

Kaminski et al. (2008) Pan troglodytes 12 0 Conspecific Competitive Subjects’ understanding of false belief were tested in a paradigm
involving competition with a conspecific.
Hattori et al. (2010a) Pan troglodytes 8 1 Conspecific Neutral Eye-tracking technique was used to measure subjects’ eye movements
in response to pictures of a conspecifc looking at or reaching for one of
two identical objects.
Tempelmann et al. (2011) Gorilla gorilla gorilla 4 1 Human Cooperative Subjects requested food from a human experimenter, whom body and
Pan paniscus 5 face orientation varied. Subjects’ visual and auditory signals were
Pongo pygmaeus 6 measured.
Pan troglodytes 18
Bania and Stromberg Gorilla gorilla gorilla 6 1/0** Human Cooperative Subjects chose between one of two experimenters to visually
(2013) communicate with him. Experimenters attentional states varied
according to body’s and/or face’s and/or eyes’ orientation as well as
vision occluded versus not occluded.
Kano and Call (2014) Pan paniscus 8 1 Conspecific Neutral Eye-tracking technique was used to measure subjects’ eye movements
Pan troglodytes 14 in response to a video of a conspecifc repeatedly turning his head to
Pongo abelii 7 one of two identical objects.
Karg et al. (2016) Pan troglodytes 16 0* Conspecific Competitive The subjects were competing with a conspecific over two food sticks.
While the subjects could see that both were the same size, to the
competitor one appeared bigger than the other.
Krupenye et al. (2016) Pan paniscus 8 1 na na Subjects were tested using an anticipatory looking test on videos, in
Pan troglodytes 14 which a human actor interact with an unreal apelike character (KK). In
Pongo pygmaeus 7 a first experiment, the actor attempted to search for KK, who had
hidden himself in one of two large haystacks. In a second experiment,
the actor attempted to retrieve a stone that KK had stolen and hidden
in one of two boxes. According to the experimental conditions, the
actor had a true or a false belief of the situation.

Table 1b
Studies Species # Sub- ToM Component investigated Social partner Social context Experimental task details
jects

GF PT AR IR FB

Anderson et al. (1995) Cebus apella 3 0 Human Cooperative Subjects were tested in a gaze-monitoring task to examine whether
they would look where the experimenter looked and/or pointed.
Itakura (1996) Eulemur fulvus 3 0 Human Neutral Subjects were tested in a gaze-monitoring task to examine whether
Eulemur macaco 4 they would look where the experimenter looked and/or pointed.
Saimiri sciureus 10
Cebus apella 3
Cebus capucinus 3
Macaca arctoides 1
Macaca mulatta 3
Macaca nemestrina 2
Macaca tonkeana 4
Tomasello et al. (1998) Cercocebus atys torquatus Unknown 1 Conspecific Neutral Experimenter induced one individual to look at food being displayed
Macaca mulatta Unknown and observed the reaction of the subject that was looking at that
Macaca arctoides 17 individual − follow the gaze of its conspecific or not.
Macaca nemestrina Unknown
Hare et al. (2003) Cebus apella 11 0 Conspecific Competitive In a competitive paradigm involving two individuals, subordinate
subjects chose between going to the food that both competitors could
see, or the food that only they could see.
Vick and Anderson (2003) Papio anubis 4 1/0** Human Competitive Subjects retrieved one of two pieces of food in front of a human
experimenter/competitor, while competitor’s face and/or eyes were
oriented towards one of the two food items.
Flombaum and Santos Macaca mulatta 20*** 1 1 Human Competitive Subjects could “steal” a contested grape from one of two human

H. Meunier / Neuroscience and Biobehavioral Reviews 82 (2017) 110–123

(2005) competitors, one being incapable of seeing the grape and the other one
being visually aware.
Santos et al. (2006) Macaca mulatta 27 1 Human Competitive Subjects were presented with the opportunity to take grapes from a
human competitor who was looking away. One of two grapes was
placed inside a silent container, and the other was placed inside a
noisy container.
Burkart Callithrix 10 1 Conspecific Competitive In a competitive paradigm involving two individuals, subordinate
and jac- subjects chose between going to the food that both competitors could
Heschl chus see, or the food that only they could see.
(2007) 0 Human Cooperative Subjects were tested for their ability to use experimenter gaze
orientation in an object-choice task.
Hattori et al. (2007) Cebus apella 5 1 Human Cooperative Subjects requested food, out of reach on a table, from a human
experimenter, whom eyes orientation varied. Subjects’ visual and
auditory signals were measured.
Wood et al. (2007) Sanguinus oedipus 10 1 Human Cooperative Subjects’ spontaneous foraging behavior was recorded in response to
Macaca mulatta 104 actions performed by a human experimenter towards one of two
containers, i.e. Intentional (reached directly for a food container),
Accidental (flopped his hand onto a container in an accidental manner),
Hand occupied (touched one of the containers with his elbow while
the associated hand was occupied), and/or Hand empty (performed
the same elbow touch action while the associated hand was free).
Amici et al. (2009) Ateles geoffroyi 13 1 Human Neutral Authors investigated whether subjects were following the gaze of a
Cebus apella 12 human whom looked behind an opaque barrier placed outside the
testing room.
Phillips et al. (2009) Cebus apella 6 1 Human Cooperative◦ Subjects’ behavior was recorded according to whether a human is
unwilling or unable to give them food.
Hattori et al. (2010b) Cebus apella 6 1 Human Cooperative Subjects requested food from a human experimenter, whom body
and/or eyes orientation varied. The food was either in the
experimenter’s hand or on a table in front of him. Subjects’ request
actions were quantified.
Marticorena et al. (2011) Macaca mulatta 48 0 Human Neutral Subjects were tested with a looking-time measure of false belief
understanding.
Goossens et al. (2012) Macaca fascicularis 13 1 Conspecific Neutral Animals were tested in subject-demonstrator pairs of conspecifics,
with the demonstrator’s attention drawn to a hidden area. It was
recorded whether the subject relocated to a position where he was
able to see the area of interest.

115
Table 1 (Continued)
Table 1a
Studies
Maille et al. (2012)
Micheletta and Waller
(2012)
Schmitt et al. (2012)
Meunier et al. (2013)
Bourjade et al. (2014)
Bray
et al.
(2014)
Martin and Santos (2014)
Overduin-de Vries et al.
(2014)
Canteloup et al. (2015a)
Canteloup et al. (2015b)
Costes-Thiré et al. (2015a)
Costes-Thiré et al. (2015b)
Defolie et al. (2015)
Canteloup et al. (2016)
116
Species # Sub- ToM Component investigated Social partner Social context Experimental task details
jects
GF PT AR IR FB
Cercocebus torquatus 9 1/0** Human Cooperative Subjects requested food, out of reach on a table, from a human
torquatus experimenter, whom body, face and eyes orientation varied. Subjects’
visual and auditory signals were measured.
Macaca nigra 7 1 Conspecific Neutral Experimenter induced one individual to look at food being displayed
and observed the reaction of the subject that was looking at that
individual − follow the gaze of its conspecific or not.
Macaca fascicularis 13 1 Human Cooperative An experimenter tried to retrieve a reward out of one of two cups but
Papio anubis 5 failed. In the first test, she tried in vain to remove a lid; in the second
test, a Plexiglas barrier blocked her access to the cup. The subject was
then allowed to choose one of the cups.
Papio anubis 9 1/0** Human Cooperative Subjects requested food, out of reach on a table, from a human
experimenter, whom body and face orientation varied. Subjects’ visual
H. Meunier / Neuroscience and Biobehavioral Reviews 82 (2017) 110–123
and auditory signals were measured.
Papio anubis 16 1 Human Cooperative Subjects requested food from a human experimenter, whom body
and/or eyes orientation varied. The food was in the experimenter’s
hand. Subjects’ visual and auditory signals were measured.
Lemur 10 1 Human Competitive Subjects competed against a human who would prevent them from
catta obtaining food if their approaches were detected. In each session, only
a single cue (noisy or silent) was present and approaches of subjects
were compared between sessions. The competitor’s body was facing
away from the food.
12 0 Human Competitive Subjects competed against a human who would prevent them from
obtaining food if their approaches were detected. Subjects were given
the choice of obtaining food silently or noisily when the competitor’s
back was turned.
Macaca mulatta 121 0 Human Neutral Subjects were tested with a looking time method to investigate if they
are automatically influenced by another agent’s beliefs when tracking
an object’s location.
Macaca fascicularis 11 1 Conspecific Competitive In a competitive paradigm involving two individuals, subordinate
subjects chose between going to the food that both competitors could
see, or the food that only they could see.
Macaca tonkeana 6 1/0** Human Cooperative Subjects requested food, out of reach on a table, from a human
experimenter, whom body, face and eyes orientation varied. Subjects’
visual and auditory signals were measured.
Macaca mulatta 5 1/0** Human Cooperative Subjects requested food, out of reach on a table, from a human
experimenter, whom body, face and eyes orientation varied. Subjects’
visual and auditory signals were measured.
Macaca tonkeana 21 0 Human Competitive Subjects were presented with the opportunity to take grapes from a
human competitor who was looking away. One of two grapes was
placed inside a silent container, and the other was placed inside a
noisy container.
Macaca tonkeana 16 0 Human Cooperative Subjects’ spontaneous foraging behavior was recorded in response to
Cebus apella 12 actions performed by a human experimenter towards one of two
containers, i.e. Intentional (reached directly for a food container),
Accidental (flopped his hand onto a container in an accidental manner),
Hand occupied (touched one of the containers with his elbow while
the associated hand was occupied), and/or Hand empty (performed
the same elbow touch action while the associated hand was free).
Cebus apella 5 1/0** Human Cooperative Subjects requested food, out of reach on a table, from a human
experimenter, whom body, face and eyes orientation varied. Subjects’
visual and auditory signals were measured.
Macaca tonkeana 11 1 Conspecific Competitive In a competitive paradigm involving two individuals, subordinate
subjects chose between going to the food that both competitors could
see, or the food that only they could see.
 H. Meunier / Neuroscience and Biobehavioral Reviews 82 (2017) 110–123
other specific social dynamics (e.g., social style; friendship) affect
individual propensity to follow gaze. Two recent studies (Hattori
et al., 2010a; Kano and Call, 2014) compared gaze following in great
apes species and humans in response to videos or pictures of con-
specific and allospecific models. All species were found to follow
conspecific gaze; results were less impressive with an allospecific
model. The authors concluded that gaze following in great apes and
humans is modulated by both subject species and model species,
but more information is clearly required concerning propensity for
and underlying mechanisms of gaze following in other primates:
monkeys and prosimians.
3.2. Perspective-taking
An important component of ToM, and perhaps the most studied
in nonhuman species, is the ability to take the visual perspective
of another individual (Emery, 2000; Povinelli and Eddy, 1996b).
This can range from the capacity to discern what another individ-
ual can and cannot perceive from her own point of view (Level 1,
Flavell et al., 1981; e.g. Itakura 2004; Braüer et al., 2005; Povinelli
and Eddy, 1996a), to the more advanced capacity to form a mental
representation of the visual knowledge of the other (Level 2, Flavell
et al., 1981, Fig. 1). Level 2 is achieved when an individual under-
stands not only what can and cannot be seen from a certain point
of view but also how a given object is seen or presented. Research
on human infants suggests that level 1 perspective-taking devel-
ops towards the end of the first year of life (Luo and Baillargeon,
2007; Sodian, et al., 2007), with level 2 emerging during the third
year of life. In nonhuman primates, the object-choice task has been
used in the last couple of decades to test Level 1 perspective-
taking, without providing conclusive results either in great apes
(e.g., Call et al., 2000; Peignot and Anderson, 1999) or monkeys
(e.g., Anderson et al., 1995; Burkart and Heschl, 2007). However,
positive results reported by Hare et al. (2000), who used a com-
petitive feeding paradigm in chimpanzees, triggered an increase in
studies on this topic, including a wider range of subject species.
Still, the findings from related studies remain mixed concern-
ing monkeys’ visual perspective-taking abilities. Capuchins (Hare
et al., 2003), marmosets (Burkart and Heschl, 2007) and Tonkean
macaques (Canteloup et al., 2016) behave as if they take the visual
perspective of conspecifics, but their choices might simply be based
on the more dominant conspecific’s behavior (simple cognitive
mechanisms) rather than true perspective-taking. However, using
a more controlled setup (i.e., the dominant is visible to the sub-
ordinate but has no visual access to the food or the subordinate
either before or during the trial), Overduin-de Vries et al., (2014)
showed that long-tailed macaques appeared to understand what
a conspecific competitor could see. In another type of competi-
tive paradigm, ring-tailed lemurs (Bray et al., 2014) and rhesus
macaques (Flombaum and Santos, 2005) have also demonstrated
Level 1 visual perspective-taking, by stealing food preferentially
from a human competitor unable versus able to see the subject.
To our knowledge only one recent study has investigated Level
2 perspective-taking in chimpanzees, by testing whether they are
able to ascribe false perceptions to others in a competitive paradigm
(Karg et al., 2016). Using an elegant procedure, the authors showed
that even though they were able to solve the task, chimpanzees
appeared to attribute their own preference to the other, rather than
truly understood the other’s mistaken perspective. There are no
Level 2 perspective-taking studies in monkeys.
As is clear from the literature reviewed in this section, stud-
ies of perspective-taking have focused on the visual modality. A
few recent studies have approached the issue from an auditory
perspective; this approach is of particular interest because audi-
tory perspective-taking cannot be explained by behavior-reading,
as auditory cues are invisible. Several species have been tested,
117
including chimpanzees (Melis et al., 2006; Braüer et al., 2008), mon-
keys (rhesus macaques, Santos et al., 2006; Tonkean macaques,
Costes-Thiré et al., 2015a) and lemurs (Bray et al., 2014). There are
conflicting results for both chimpanzees and monkeys and nega-
tive for lemurs. More research including larger samples and a wider
diversity of species is necessary for knowing whether monkeys are
able to take the auditory perspective of others, or even to establish
a link between hearing and knowing.
3.3. Attention reading abilities
Sensitivity to others’ eye gaze is also fundamental for identifying
the attentional states of conspecifics. This makes communication
more efficient; by choosing the right time to start communicat-
ing the cost of the communicative act can be optimized. Attention
reading in a communicative context is one of the criteria defin-
ing intentional communication (Leavens et al., 2005). There is
strong evidence that both great apes and monkeys are sensitive
to the attentional state of others when gesturing, but it is not
clear which cues are the most relevant for assessing the attentional
state of a partner. Studies on great apes have revealed sensitivity
to gross cues as body orientation (Kaminski et al., 2004; Krause
and Fouts, 1997; Liebal et al., 2004; Povinelli and Eddy, 1996a)
and face orientation (Kaminski et al., 2004; Tempelmann et al.,
2011), as well as more subtle cues such as the state of the eyes
(Barth et al., 2005; Bethell et al., 2007; Hostetter et al., 2007;
Bania and Stromberg 2013). Studies on monkeys have reported dis-
crimination of gross cues only, i.e. body and face orientation of a
human partner (mangabeys: Maille et al., 2012; baboons: Meunier
et al., 2013; Vick and Anderson, 2003; macaques: Canteloup et al.,
2015a,b, capuchins: Defolie et al., 2015). But the cooperative and
interspecific nature of these studies might explain these results.
Capuchins have been reported to be sensitive to a human part-
ner’s eyes in terms of their visual behavior but not their gestural
behavior (Hattori et al., 2007), and when the food was held in the
human’s hand (dyadic situation) but not in a more complex triadic
situation in which the food was on a table (Hattori et al., 2010b).
Recently, Bourjade et al. (2014) showed that baboons were also sen-
sitive to the state of another individual’s eyes. In this study food was
also held in the experimenter’s hand, and baboons gestured more
and looked more at the experimenter when her eyes were open
compared to when they were closed. Again, we cannot exclude the
possibility that divergent results between studies and species are
due to differences in methods of study. These preliminary studies
have produced interesting results, and have introduced new species
to this field, but standardized experimental paradigms with greater
ecological validity now appear necessary to make further advances.
3.4. Intention reading abilities
Two levels of understanding intentions are described: compre-
hension of intentions towards an object (e.g., understanding of a
“failed attempt” at an action) and comprehension of intentions
towards an agent (e.g., discrimination between prosocial versus
antisocial behaviors). Studies have revealed that human infants
before the age of 1 year already understand the goals of others (e.g.,
Behne et al., 2005; Gergely et al., 1995), and at around their first
birthday they understand others’ intentions (e.g., Gergely et al.,
2002; Schwier et al., 2006) and knowledge of others (e.g., Moll
and Tomasello, 2007; Onishi and Baillargeon, 2005). To investigate
such abilities in nonhuman primates, similar paradigms involv-
ing imitation have been proposed, especially to great apes but
also more recently to monkeys. Capuchins, tamarins, macaques
and chimpanzees have been reported to discern goal-directed,
intentional actions of humans (Call et al., 2004; Phillips et al.,
2009; Wood et al., 2007; Schmitt et al., 2012). Like children, chim-
118 H. Meunier / Neuroscience and Biobehavioral Reviews 82 (2017) 110–123
Fig. 1. Level 1 versus level 2 visual perspective taking.
panzees showed more patience when a human was trying but
failing rather than unwilling to share (Behne et al., 2005; Call et al.,
2004). Moreover, Wood et al. (2007) used an object-choice task to
test whether tamarins, macaques and chimpanzees infer other’s
goal, by measuring subject response to actions performed by a
human experimenter. Experimenter’s action was either intentional
or accidental towards one of two containers in that if subjects
distinguish between intentional and accidental actions, then they
should selectively inspect the container targeted by the exper-
imenter’s intentional action but not that targeted by accidental
action, what they did. However, a recent study on macaques and
capuchins (Costes-Thiré et al., 2015b) failed to replicate these
results using a similar paradigm. Unfortunately, intention reading
abilities have been studied in relatively few species of monkeys, and
protocols are variable across studies; new data are eagerly awaited.
3.5. False beliefs
One of the most important milestones in the development of
ToM is gaining the ability to attribute false beliefs, i.e., recognize
that others can have beliefs about the world that differ. To do
this, it is suggested that one must understand how knowledge is
formed, that people’s beliefs are based on their knowledge, that
mental states can differ from reality, and that people’s behav-
ior can be predicted by their mental states. Numerous versions
of the false-belief task have been developed, based on the initial
task proposed by Wimmer and Perner (1983). One crucial advance
came with the development of nonverbal tasks appropriate for
preverbal human infants and nonhuman species. Human infants
succeed in nonverbal tasks of false belief before their second,
or even first, birthday (Onishi and Baillargeon 2005; Baillargeon
et al., 2010; Kovács et al., 2010), whereas apes, even if they show
knowledge-ignorance understanding, fail in false belief tasks (Call
and Tomasello, 1999; Kaminski et al., 2008; Krachun et al., 2009).
Only two recent studies appear to have focused on monkeys’ belief
representations (Marticorena et al., 2011; Martin and Santos, 2014)
and both concluded that monkeys do not represent others’ false
beliefs.
To sum up, until the 2000s, the overwhelming consensus was
that ToM abilities were unique to our species and that chimpanzees
and other nonhuman primates did not understand the psycholog-
ical states of others (e.g., Heyes, 1998; Povinelli and Vonk, 2003,
see Cheney and Seyfarth, 1990 and Tomasello and Call, 1997 for
reviews on that period). However, starting with the shift to com-
petitive paradigms initiated by Hare et al. (2000, 2001), studies
on great apes, particularly chimpanzees, have revealed that they
act according to the actions and perceptions of others, show-
ing strong evidence that they understand the psychological states
of others in different domains (e.g., Call and Tomasello, 2008;
Tomasello et al., 2003). More recently, studies have addressed
the issue of ToM more deeply in monkeys, revealing impressive
communicative and social capacities in several monkey species.
 H. Meunier / Neuroscience and Biobehavioral Reviews 82 (2017) 110–123
Even though questions remain about monkeys’ mindreading abil-
ities, recent systematic studies show that some species behave
according to other’s attention, intentions and perceptions. More-
over, in some tasks monkeys perform very much like apes (Schmitt
et al., 2012, 2013). These results question the clear-cut relationship
between cognitive performance and relative brain size, and high-
light the interest of expanding research on cognition evolution to
more monkey species, including large-scale comparative studies
and standardization of methods. Such a development will facili-
tate drawing reliable inferences about the evolutionary dynamics
of primate intelligence and bring new information regarding the
universality of socio-cognitive capacities. However, as recently
underlined by Shettleworth (2012), researchers must also remem-
ber to systematically consider low-level explanations of results,
sometimes more difficult due to the physical and developmental
resemblances between nonhuman primates (especially apes) and
humans. The next section is dedicated to this issue, addressing cur-
rent debates and hypotheses regarding underlying mechanisms of
what might first appear to be complex cognitive abilities.
4. Complex behaviors but simple minds?
Shortly after publication of the first quantitative studies report-
ing positive results about nonhuman primates’ mindreading
abilities (e.g., Povinelli et al., 1990), appeared critiques and anal-
yses proposing alternative explanations based on simple cognitive
mechanisms such as associative or referential learning (Heyes,
1993). Over the ensuing 25 years there have been many discus-
sions, reviews and critiques dedicated to what is still today an
open debate that is essentially between two general and oppos-
ing stances: behavior-reading versus mindreading. More recent,
less intuitive but promising alternatives include ‘minimal theory
of mind’ (Butterfill and Apperly, 2013) and submentalizing (Heyes,
2014). In fact the debate appears to have two facets: methodological
and theoretical (see also Heyes, 2015).
4.1. Methodological puzzle
On the one hand is a methodological puzzle: researchers try
to find an experimental procedure that can reveal abilities that
cannot be explained by simpler cognitive mechanisms (the par-
simony principle), thereby favoring more advanced explanatory
cognitive processes. This problem, now known as the logical prob-
lem or Povinelli’s problem (seeHurley and Nudds, 2006; Lurz, 2009;
Lurz et al., 2014; Povinelli and Vonk, 2004), led many researchers
to argue that any positive evidence for mindreading in animals can
be just as plausibly explained by a behavior-reading hypothesis
as by a mindreading hypothesis (Heyes, 1998; Lurz, 2011a; Lurz
and Krachun, 2011; Lurz et al., 2014; Povinelli and Vonk, 2004;
Shettleworth, 2010). The lack of consensus about whether any non-
human species can attribute any mental state to another, continues
despite more than 35 years of research since Premack and Woodruff
(1978) first raised the question.
Commentators appear to be divided into two main camps: ‘skep-
tics’ and ‘believers’ (see Lurz et al., 2014 for more details). Skeptics
are those who think that there is sufficient evidence that ani-
mals are not mindreaders, and that behavioral similarities between
humans and nonhumans need not imply psychological similarities
(Povinelli et al., 2000). The skeptics refer to experiments with neg-
ative outcomes (e.g. Call and Tomasello, 1999; Karin-D’Arcy et al.,
2002; Povinelli and Eddy, 1996). By contrast, ‘believers’ − mainly
comparative psychologists − think that there is sufficient evidence
that some nonhuman species (at least chimpanzees) are mindread-
ers; they refer to experiments yielding positive results (e.g. Call
et al., 2004; Fletcher and Carruthers 2013; Hare et al., 2000, 2001,
119
2006; Melis et al., 2006). But fundamentally this debate appears
fruitless, and it has certainly contributed to changes in the social
structure of research on animal mindreading over the last 30 years
(Heyes, 2015). Skeptics, by proposing behavior-reading explana-
tions for each positive demonstration of mindreading (e.g. Perner,
2012) may in fact have inhibited research on mindreading, as more
researchers have gradually become more doubtful about mindread-
ing abilities in nonhumans (Seyfarth and Cheney 2013; Penn and
Povinelli 2007, 2013; Whiten 2013) or at least about the possibil-
ity clearly demonstrating them. Thus we see a diminishing number
of research groups actually conducting experimental research on
animal mindreading; in the past 15 years or so the field has been
mainly dominated by one group in Leipzig, minimizing exchanges
of theoretical perspectives (Heyes, 2015).
However, none of the arguments, empirical or theoretical,
advanced by either the skeptics or the believers appear irrefutable
(Hare and Tomasello 2004; Lyons and Santos 2006; Lurz and
Krachun 2011; Lurz et al., 2014) to overcome Povinelli’s problem
(e.g. Heyes 1998; Lurz 2011a, 2011b; Lurz and Krachun 2011). Lurz
et al. (2014) have called this position ‘optimistic agnosticism,’ and
suggest suspending judgment on mindreading abilities in nonhu-
mans until more adequate procedures have been designed and
tested.
4.2. Theoretical puzzle
On the other hand is a theoretical problem: there is no clear
definition of what it is to engage in mindreading, and there is
difficulty in conceptualizing alternatives to ‘full-blown’ mindread-
ing (see Heyes, 2015 for more details). The debate outlined above,
which is also found in developmental psychology regarding human
infants’ mindreading abilities (e.g., Baillargeon et al., 2010; Kovács
et al, 2010; Southgate et al., 2007; Carruthers 2013; versus Perner
and Ruffman, 2005; Ruffman, 2014), suggests that at least some
aspects of ToM may be achieved without cognitively demanding
executive resources and thus in a way that is cognitively efficient,
i.e., fast and automatic. This assessment, combined with growing
evidence that adult humans can ascribe mental states to others in a
fast, cognitively efficient, and implicit way (e.g. Samson et al., 2010;
Kovács et al, 2010; Schneider et al., 2012), stimulated a search for
approaches intermediate between the two extreme ones presented
above. Thus, two promising alternative hypotheses have recently
been proposed. An attempt to resolve the theoretical puzzle came
from Apperly and Butterfill (2009), Butterfill and Apperly (2013).
Arguing that explicit ToM is too slow and cognitively demanding
for use in many types of everyday social interaction, they proposed
that at least two distinct systems and forms of representation are
involved in ToM: a first system that employs simple representations
to achieve fast, resource-efficient processing, and a second, slower,
more complex and controlled system that depends on language and
executive resources to achieve powerful and flexible processing.
In their alternative hypothesis, Butterfill and Apperly thus con-
sider, for the first system, a form of cognition called “minimal
theory of mind”, which does not involve mental representations
as such but does involve representation of simple relational men-
tal states allowing to track perceptions, goals or beliefs. One major
aspect of this alternative hypothesis is the recommended distinc-
tion between ToM ability and ToM cognition: whereas ToM ability
involves exploiting or influencing facts about states, ToM cogni-
tion involves representing states, and full-blown ToM cognition
involves the use of these representations to construct explana-
tions of actions (Butterfill and Apperly, 2013). Thus, ToM ability
exploits facts that are not necessarily the same as the facts rep-
resented in ToM cognition (Butterfill and Apperly, 2013). Based
on goal-directedness, encounters between agents and objects, and
registration of these encounters and their causality, Butterfill and
120 H. Meunier / Neuroscience and Biobehavioral Reviews 82 (2017) 110–123
Apperly’s construction can explain success on complex social tasks
including goal ascription and false belief tasks without having a
full-blown ToM (see Butterfill and Apperly, 2013, 2016 for more
details, but also Michael and Christensen, 2016 and Christensen
and Michael, 2016 for alternative hypothesis proposing multi-
systems architecture for mindreading). This approach has become
very influential in developmental psychology and I present it here
because it might explain most of the results obtained in nonhuman
species regarding ToM. Another promising alternative hypothesis
has been proposed by Heyes (2014): the submentalizing hypothe-
sis. Heyes describes it mainly as an alternative to the classical view
of implicit ToM, i.e., ToM involving thinking about mental states in
a fast, automatic way rather than a slow, controlled way, in that
she presented submentalizing as a process that does not involve
thinking about others’ mental states at all. Briefly, submentaliz-
ing involves domain-general cognitive mechanisms for memory
and attention that simulate the effects of full-blown ToM in social
contexts. Interestingly, this alternative also suggests that the same
domain-general processes can provide a fast and efficient alterna-
tive to ToM in everyday life, allowing people (and also nonhumans)
to navigate a wide range of social situations without thinking about
mental states. In this way, submentalizing could be both a sub-
strate and a substitute for ToM (Heyes (2014)). Moreover, unlike
behavioral strategies, submentalizing does not involve reasoning
about actions on objects by agents but instead parses the world in
terms of features such as color, shape and movement (Santiesteban
et al., 2014; Heyes 2015). Heyes (2014) analyzed several key proce-
dures that have been used to seek evidence of implicit mentalizing
in humans (automatic representation of what others see: Samson
et al., 2010; Zwickel, 2009; what they intend: Sebanz et al., 2003;
what they falsely believe about the locations of objects: Kovács
et al., 2010; Senju et al., 2009), and in each case she concluded
that the results do not provide evidence of implicit mentalizing but
instead of submentalizing, including processes that mediate invol-
untary attentional orienting, spatial coding of response locations,
object-centered spatial coding of stimulus locations, retroactive
interference, and distraction (see Heyes (2014) for more details),
but not mental state attribution. Heyes’ alternative conceptualiza-
tion is also of particular interest for investigating ToM in nonhuman
species. Both minimal ToM and submentalizing hypotheses offer
new hypotheses and thus new perspectives for improving our
understanding of cognitive mechanisms underlying complex social
behaviors in monkeys that, at first sight, suggest ToM.
5. Believers, skeptics, theoretical solutions: where does it
all leave us?
As discussed above, it appears that all explanations regarding
underlying cognitive processes − lower or higher − can potentially
explain complex social behaviors of monkeys. Clearly, ‘Povinelli’s
problem’ has not yet been overcome by the experimental proce-
dures used so far, even though many of them are innovative and
elegant. In other words, while research has significantly advanced
the field in many ways, there is no empirical reason to favor any
one explanation; results of any given study can be explained with
reference to full-blown ToM, implicit ToM, or submentalizing (e.g.
Heyes 1994, 1998, 2015; Lurz and Krachun 2011; Penn et al., 2008;
Penn and Povinelli 2007; Shettleworth 1998, 2010). Of course, the
parsimony principle (Morgan’s canon, Morgan, 1894) is often used
to prioritize lower-level explanations, even if the data fail to dis-
tinguish it from competing higher-level explanations. However,
several kinds of parsimony principles can be considered, and it
seems likely that full-blown ToM might be favored when apply-
ing some kinds of parsimony principles whereas behavior-reading
would be preferred when applying other kinds; but constructing a
hierarchy of different parsimony principles appears difficult if not
impossible (Fitzpatrick (2008)). Rather, as Fitzpatrick (2008) sug-
gested and taking into account the current debates, evidentialism
appears more appropriate here. According to Fitzpatrick, (2008, p.
242), “ in no case should we endorse an explanation of animal behavior
in terms of cognitive process X on the basis of the available evidence
if that evidence gives us no reason to prefer it to an alternative expla-
nation in terms of a different cognitive process Y — whether this be
lower or higher on the ‘ psychical scale ”’. From this point of view,
for moving towards solutions to the methodological and theoreti-
cal puzzles that surround research on ToM, the priority is to start
with a clear and precise definition of which type of cognitive mech-
anisms is under study. The challenge could then be formulated as
finding experimental procedures that would allow discrimination
between the possible cognitive mechanisms that might underlie
the complex behaviors being studied (see also Heyes 2015; Lurz
et al., 2014). Without such a rigorous approach, it seems impossi-
ble to truly advance knowledge about the psychological processes
involved in these astounding social behaviors, or to test mentalistic
against nonmentalistic alternatives.
An elegant paradigm that could fulfill the above-cited criteria
for testing implicit versus full-blown ToM, is the experience pro-
jection (Whiten, 1996, but see also Cheney and Seyfarth (1990)
for an elegant pioneering study involving this concept), or in other
words, the use of self-informed belief induction variables (Heyes,
1998). An example of this is the well-known “goggles experiment”,
in which subjects are exposed to opaque and translucent goggles
that differ only by their distinctively colored rims, and they need
to use their own experience of seeing through these goggles to
infer what another sees when he is wearing them (see Heyes, 1998
for more details). This experimental protocol was later refined by
Povinelli and Vonk (2003, 2004), Vonk and Povinelli (2011) and
then by Karg and colleagues from the Leipzig group (2015), by test-
ing whether chimpanzees attribute their previous self-experience
with the object to the experimenter in a competitive context. While
Vonk and Povinelli’s (2011) described negative results based on
three subjects, Karg et al. (2015) tested 19 subjects and reported
positive results showing that chimpanzees attributed their previ-
ous self-experience with an object to the experimenter in such a
competitive context (but not in a non-competitive gaze-following
task). Even though powerful and proposed more than two decades
ago, goggles-like experiments have been reported only in the two
chimpanzee studies mentioned above, and only one similar type of
study has been conducted on monkeys (Cheney and Seyfarth, 1990).
The study on monkeys produced negative results, but the design
was less controlled that in the more recent ape studies, and could
not rule out some behavior-reading explanations. Applying modern
adaptations of goggles experiments to other great apes species as
well as monkeys could greatly improve our understanding of these
species complex social behaviors and of what define the uniqueness
of our own ToM.
Another protocol that could overcome Povinelli’s problem has
been proposed by Lurz and Krachun (2011). They suggested a
competitive paradigm based on the fact that chimpanzees seem
to understand that their own perspective (appearance) can differ
from reality (Krachun et al., 2009; Karg et al., 2014). More pre-
cisely, the idea consists of testing a chimpanzee in a competitive
game involving large and small grapes placed inside containers
that look identical but that differ by their optical properties, i.e.
size-distorting or not. Provided that the subject is aware of the
optical illusion (he can see the baiting procedure and understand
the difference between appearance and reality), the idea is to test
whether chimpanzees also understand that others can hold a mis-
taken perspective, i.e., here that the competitor will choose the
magnified and thus apparently larger grape that is smaller in reality
(see Lurz and Krachun, 2011 for more details, and Lurz et al., 2014
 H. Meunier / Neuroscience and Biobehavioral Reviews 82 (2017) 110–123
for a variant). To our knowledge, this procedure has not yet been
proposed to chimpanzees or any other nonhuman species. How-
ever, Karg et al. (2016) used a similar method with chimpanzees,
replacing the magnifying containers by a visual barrier that pre-
vented the competitor from seeing part of an edible bread stick.
On the subject’s side, two same-sized edible sticks were attached
to the visual barriers, but one extended beyond the edge of the
board more than the other, such that it seemed bigger from the
competitor’s perspective. By this method Karg et al. (2016) investi-
gated whether chimpanzees could predict that a conspecific’s false
perspective differed from their own and from reality. Their results
suggested that chimpanzees successfully predicted which edible
stick the competitor would choose only when they were guided
by their own preference, but they did not demonstrate level 2
perspective-taking. However, unlike in the protocol suggested by
Lurz and Krachun (2011), the subjects had no opportunity to expe-
rience the competitor’s perspective, whereas recent studies have
highlighted the crucial role of self-experience in the understand-
ing others’ differing perspectives (Karg et al., 2015). This procedure,
even though technically demanding could be used with monkeys.
However, we need first to investigate monkeys’ abilities to discrim-
inate appearance from reality. If monkeys can do this, then provided
that they benefit before the tests from self-experience of a com-
petitor’s perspective, the Karg et al. (2016) method could be very
revealing.
To go further, if the full-blown ToM hypothesis can be
clearly eliminated, Heyes (2015) suggested using methods such as
Bugnyar’s (2011) competitive paradigm for testing implicit ToM
versus submentalizing alternatives, but by additionally using inan-
imate control stimuli. In his study, Bugnyar (2011) addressed the
ravens’ ability to apply different behavioral responses to poten-
tial competitors with a varying degree of information about cache
locations and also tested whether they base their pilfering deci-
sions on a learned rule. By replacing a conspecific by an inanimate
object in some conditions, one could compare subjects’ behavior
when tested with a conspecific versus this inanimate object, and if
subjects behave differently, reject domain-general cognitive mech-
anisms for memory and attention that can simulate the effects of
full-blown ToM in social contexts, i.e. submentalizing (see above).
Applying this paradigm to monkeys also appears technically feasi-
ble and thus promising.
Moreover, whatever the proposed protocol, it is of interest to
develop variants based on other sensory modalities, especially
the auditory modality. Behavior-reading via auditory perception
appears more difficult than via visual perception, as ostensive
signals are removed. Thus, even though technically demanding,
protocols using this sensory modality might prove valuable for a
better understanding of ToM abilities in monkeys. Finally, for a
better comparison with humans, and for limiting some technical
constraints, greater use of video stimuli combined with looking-
time measures should be used to greater advantage in studies of
ToM abilities in monkeys.
To conclude, none of the potential protocols proposed here is
perfect; some of them have already been questioned by philoso-
phers (Lurz, 2009; Perner 2012), and all will surely attract critiques
and commentaries. However, these protocols can at least poten-
tially overcome some of the longstanding methodological problems
surrounding research on ToM. Step-by-step progress in the field
appears the most likely way of moving toward being able to answer
to what extent and how do monkeys understand others’ minds.
Moreover, given the diverse methodological possibilities suggested
by philosophers, cognitive psychologists, and comparative psychol-
ogists, exchanges of critiques and commentaries between skeptics
and believers are fertile and valuable. Although the vigorous crit-
ical debates reviewed here might appear fruitless at first sight,
they are actually a driving force for finding innovative ways to
121
advance the scientific study of ToM both in human and nonhu-
man species. So even if monkeys have not yet been tested using
experimental procedures that could allow us to reliably answer the
question of whether they have ToM, some promising approaches
have recently been proposed (and successfully empirically tested
in chimpanzees, Karg et al., 2015). The fact that monkeys display
complex social behaviors such as attention reading, perspective-
taking abilities, and tactical deception, combined with their greater
phylogenetic distance from humans relative to apes, makes them
promising research models for understanding the roots of our spec-
tacular ability to deal with our complex social world.
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