David and colleagues examined VPT and ToM in high functioning adults with Asperger syndrome compared to age and IQ matched TD adults. Participants completed two tasks, one examined VPT and the other examined ToM. In the ToM task participants were presented with a virtual image of a person with one item either side of them. The person could be displaying one of three possible body, face and hand postures (positive, neutral, or negative) toward one of the objects. An example of a positive hand gesture would be pointing, whereas negative would be holding the hand out with the palm facing forwards (similar to a "stop" signal). The participant's task was to identify which object the other person desired (mentalizing for other) or which they would desire themselves (mentalizing for self). In the VPT task the participant was presented with the same image of the person with two objects, one of which was elevated. The participant had to identify which object was elevated from their own point of view, or from that of the other person using a laterality judgment (i.e., the item on *my left* is higher). Measures of speed and accuracy were taken from each participant. In the ToM task results showed that the ASD participants were significantly slower and less accurate at identifying the correct answer when mentalizing for other. They were also trending toward slower mentalizing for self (as accuracy on this task was subjective accuracy could not be measured). There were no differences found between groups for speed or accuracy in the VPT task, for self or other. The authors acknowledged that the VPT task may have been too easy compared to the mentalizing task which may explain differences across tasks. One limitation is that this task does not require participants to take the visual perspective of the other, but only to judge what is on the left or right. Spatial-transformation tasks (Parsons, 1987; Zacks et al., 1999) requires participants to make laterality judgments about an item in relation to another person, but it is not clear if these are the same as VPT tasks. Further research is needed into these paradigms in order to assess where they fall in relation to perspective taking.

Similarly, Zwickel et al. (2011) examined VPT and ToM in adults with autism and age and IQ matched TD adults using a laterality judgment paradigm. In the VPT task participants viewed videos of animated triangles (Castelli et al., 2002), and during the videos a dot appeared to the left or right of the triangle. Participants were asked simply "*was the dot on your left or right*." On incongruent trials a dot on the participant's left fell on the right of the triangle (or vice versa), while on congruent trials a dot on the participant's left was also on the left of the triangle (or both on the right). Critically, this congruency only arises if the triangle is perceived as an animate active creature. Both typical and autistic participants showed a congruency effect in this task, demonstrating that they could spontaneously consider the left/right orientation of an animated shape. However, the autistic participants were less good at judging the mental states of the triangles in the same animations. This is consistent with the findings of David et al. (2010). Similarly, it is not clear if this task truly demands calculation of the *visual perspective* of another agent rather than just their orientation. More research is needed to explore the use of visuo-spatial perspective taking paradigms in autism.

#### **EVALUATING VPT IN AUTISM**

We have reviewed 13 studies of VPT in autism, and suggest that 7 of these assessed VPT1, 3 assessed VPT2 and 3 were unclear or assessed laterality (see **Table 1**). Of the 7 studies examining VPT1, 5 report no differences between typical and autistic participants while the other 2 find that participants with autism perform worse than typical participants. Of the 3 studies examining VPT2, 2 report group differences and the third does not.

There are several interesting issues arising from this review which can guide future research. One important problem is that the boundary between VPT levels one and two is not always clear. A task might be intended to assess VPT1, but participants might choose to use a VPT2 strategy. Or if a study designed to measure VPT2 could also be completed using line of sight, it is possible that people with autism could pass based on this information. This is particularly the case in studies which name the item which can be seen from a particular location [e.g., *place Fred so he can see the red side*, (Hobson, 1984)]. Here the child need only consider Fred's line of sight to the red part of the cube, but some children might prefer to consider the relationship of the whole cube to the rest of the scene including the child's own viewpoint. Thus, this task could be solved by a VPT1 or VPT2 strategy. To minimize this issue, we suggest that line of sight tasks seem to be the clearest way to assess VPT 1 (Leslie and Frith, 1988; Baron-Cohen, 1989; Leekam et al., 1997; Warreyn et al., 2005), whilst item appearance tasks appear to be the best way to assess VPT2 (Hamilton et al., 2009) see **Figures 1A,B**.

A related issue is the use of different strategies by different participants. However well an experimenter designs a task, it is always possible that participants could solve the puzzle in a different way. For example, many VPT tasks could potentially be solved

**Table 1 | Summary of studies included in this review.**

with a purely spatial mental rotation (Zacks and Tversky, 2005). This approach is less efficient, but it is possible that different groups of participants prefer to use different strategies. One way to approach this issue is to consider the use of appropriate control tasks to assess other cognitive skills such as children's memory abilities (especially for complex displays), their language skills (for complex questions) and their abilities to perform spatial transformations. The comparison of an experimental task and a closely matched control task in the method of fine cuts (Frith and Happe, 1994) would allow for close examination of the cognitive components which distinguish the different levels of perspective taking. For example, Surtees et al. (2013) suggests that VPT2 requires an embodied spatial transformation while VPT1 does not. If this is the case, then VPT2 abilities should correlate with performance on other tasks requiring embodiment, but not to mental rotation tasks that do not involve bodies. If different groups of participants use different strategies to perform VPT tasks, this might also emerge in the relationship between their VPT skill and other cognitive skills.

Furthermore, this raises another important question concerning how the social and spatial elements of VPT2 fit together: Does intact VPT require spatial *and* social information, or could it be done using just one of these? If VPT2 can be completed using social *or* spatial information it makes sense that it can be unimpaired even in the face of significant ToM deficits, as participants' could rely on the use of spatial information to complete a task. Langdon and Coltheart (2001) suggested that tasks using questions about item location (i.e., Tan and Harris (1991)) were particularly open to completion via spatial cues making it possible for those with social difficulty to perform. However, if VPT2 requires the integration of both spatial and social information to be effective, then even good spatial ability would not completely compensate for poor social processing. Again, determining the strategies and cognitive mechanisms that different participants use to perform VPT tasks is critical here.

Another issue concerns the participant populations tested. The majority of studies presented in this review were conducted on children, and several on groups of children with impaired cognitive functioning. It is difficult to collect reaction time data from children, meaning that more subtle differences in VPT ability related to an inability to integrate social and spatial information may be missed. The two studies conducted with adults (David et al., 2010; Zwickel et al., 2011) did not find group differences but did not use typical VPT tasks. It is possible that [as found in ToM research (Ozonoff et al., 1991)], high functioning adults may be able to pass VPT. Whether this is due to a better understanding of the questions asked, or the development of an alternative strategy for completion of the tasks is unclear. Both of these suggestions warrant further research and careful consideration of the paradigms used to examine VPT.

There are also issues in the lack of consistency in matching groups. Though some of the studies have used rigorous matching techniques (Yirmiya et al., 1994; Hamilton et al., 2009; David et al., 2010), others took no measure of cognitive ability in their typical participants. Both Reed and Peterson (1990) and Hobson (1984) argue for evidence of unimpaired VPT2 performance in autism. However, they both compared groups of older ASD children to younger typical children. This suggests that at the very least the participants with autism may be displaying a delay in the development of VPT (similar performance to younger children as opposed to an age matched group) and that it may be inappropriate to label their performance as unimpaired. By comparing ASD participants to both age and ability matched control participants, it becomes possible to make stronger claims as to whether performance on a task is normal, impaired or simply delayed. These findings present a strong case for using carefully chosen control groups in studies looking for evidence of impairment in a population such as autism.

## **FUTURE DIRECTIONS**

Understanding the relationship between VPT and ToM is important. Both of these require the consideration that the other person has a different representation of the world to oneself, either a different visual representation or a different belief. Early studies suggested that VPT is intact in autism while ToM is impaired. This motivated the idea that it is easy to distinguish visual representations of self and other because VPT allows concrete feedback by physically moving to a different location (Leslie (1987). In contrast, ToM requires more abstract representations which people with ASD find difficult. More recent data suggest that VPT2 and ToM are linked in typical children (Hamilton et al., 2009), in those with specific language impairment (Farrant et al., 2006) and in the brain (Aichhorn et al., 2006). This implies that VPT2 and ToM may share similar underlying cognitive mechanisms. Certainly, many false belief tasks rely on the ability to distinguish what people have seen (Sally did not see Anne move the marble) which draws upon VPT. VPT has been found to activate the temporo-parietal junction, an area commonly found to be activated by ToM tasks (Aichhorn et al., 2006). It has been suggested that ToM may be driven by different mechanisms or strategies in people with autism compared to TD people (Tan and Harris, 1991). We believe it may also be worth considering that this could also be the case for VPT in people with autism. If both are being driven by different mechanisms it may explain why some studies have shown VPT to be unimpaired alongside impaired ToM (Tan and Harris, 1991) and vice versa (Hamilton et al., 2009). Further studies of the relationship between ToM and VPT would be very useful, as would studies examining the cognitive mechanisms which underlie each.

It is also worth considering how researchers can tease apart the specific contributions of social and spatial mechanism in VPT. Several VPT tasks have been used successfully in TD individuals which have allowed researchers to emphasize the spatial or social aspects. The use of these paradigms may provide us with useful information about perspective taking in autism. As described earlier, Samson et al. (2005) investigated the social components of VPT in an implicit perspective taking task. Results showed that participants could not ignore the perspective of an avatar, and made slower responses when the avatar could not see something which the participant could see. Another VPT task with strong social demands is Keysar et al. (2003) director task. In this task the participants stand behind a shelf holding several items while another person stands in from (the director) and gives instructions of which items to choose. Not all items are visible to the director and so the participant must be able to take the directors perspective into account to avoid choosing items that they cannot see. The authors found that participants were not able to inhibit their own perspective when choosing items and often made incorrect responses. This task has been argued to have a strong ToM component as it relies on the ability to represent someone else's false belief (the director believes the "big jar" is the one they can see, but there is a bigger jar on view to the participant). Both of these tasks would provide interesting ways of measuring the social components of VPT.

Kessler and Thomson (2009) developed a task in which they were able to examine the underlying spatial components present in perspective taking (termed spatial perspective taking, or SPT). Participants were presented with images of a human avatar seated at a table with an item to either side of them (a flower and a gun). The position of the avatar at the table was rotated to be more or less congruent with the position of the participant (providing changes in the angular disparity between the avatar and viewer). Participants had to make laterality judgments in regards to the placements of the items from the avatars viewpoint. The authors found that the larger the angular disparity between then avatar and the viewer, the longer participants took to respond. This demonstrated the underlying spatial transformation that the participant completed in order to put themselves in the place of the avatar, highlighting the importance of spatial mechanisms in perspective taking. These findings show that in order to take a first person perspective, an embodied transformation (where the viewer transforms their body to match that of the avatar or target viewpoint) is often necessary. Mazzarella et al. (2013) built upon these findings, investigating the neural underpinnings of spatial perspective taking with a similar experiment which examined SPT under fMRI. In this task participants were scanned whilst making egocentric (what item is on your left) vs. altercentric (which item is on their left) judgments about the placement of items on a table [using the same paradigm as Kessler and Thomson (2009)]. This was designed to tease apart the differences in transforming the self to a different position vs. transforming the self into someone else's position. The authors found that though both types of transformation show similar behavioral data patterns, there was a neural distinction between the areas engaged during egocentric and altercentric perspective taking. This suggests that multiple strategies may be used for putting the self in a different place. These tasks both provide clear mechanisms for teasing out the spatial components of VPT, as well as interesting avenues to explore in people with autism.

Recently, researchers have also begun to examine the link between autistic traits in TD individuals and how this affects perspective taking. As VPT is a sociocognitive ability which impacts on social interaction, it stands to reason that those with poorer social skills might also show poorer perspective taking ability. Three studies have examined this question. First, Kessler and Wang (2012) examined participants using the same task from Kessler and Thomson (2009). A measure of autistic traits in these participants was taken using the Autism Quotient (AQ, Baron-Cohen et al., 2001). The authors found that participants who scored higher on the AQ (Baron-Cohen et al., 2001) showed more difficulty with performing egocentric transformations in a VPT2 task than low AQ scorers. However these high AQ participants also showed quicker response times. The results further suggest that using an embodied perspective slowed participant's responses at higher angular disparities as it took longer for the participant to transform their body to match that of the target. Participants with poorer embodiment skills did not slow their response times, most likely due to the use of a non-embodied transformation strategy. Using a very similar task, Brunye et al. (2012) also found that high AQ scorers had difficulty with using an egocentric reference frame in VPT2, though in this study these participants showed slower response times. This suggested that these high AQ participants were attempting to use an embodied strategy, but found it more difficult. Finally, Shelton et al. (2012) also found a link between spatial skills and autistic traits. In their study participants were presented with a three mountains (Piaget and Inhelder, 1956) like scene, in which an array of three buildings were visible to participants. A doll was placed facing the array and participants had to respond to which point of view the doll would see. Their study showed that participants with high AQ scores were less accurate than those with low AQ scores.

Together, all these suggest that autistic traits (as well as autism itself) can influence a participant's ability to perform VPT2. These studies are important for two reasons. Firstly they demonstrate that autistic traits (not just a diagnosis of autism) impact on the ability to take another perspective. Secondly, they add weight to the argument that those who find it difficult to complete VPT2 using an embodied perspective may develop an alternative strategy. The findings from these studies provide a strong motivation for considering the types of participant samples used in VPT2 research and measuring traits which could affect performance alongside carefully designed paradigms and tasks.

## **CONCLUSIONS**

From the evidence presented in this review, the majority of studies suggest that whilst VPT1 may be intact in people with autism, VPT2 is impaired. We suggest that this is a result of the cognitive mechanisms involved in the different levels of VPT, with VPT2 drawing on embodied spatial transformations and triadic representations (Surtees et al., 2013) more than VPT1. Future studies should carefully consider the cognitive differences between VPT1 and VPT2. Furthermore, there is evidence to suggest that the ability to perform egocentric transformations (a process which can be seen as the first step in completing VPT2 (Yu and Zacks, 2010) could be impaired in autism, but may also be affected in people with high levels of autistic traits (Brunye et al., 2012; Kessler and Wang, 2012; Shelton et al., 2012). It is clear that more research is needed into the processes related to VPT2 in autism in order to clarify these suggestions. There is a strong case to be made for more inclusion of measures of general spatial ability in studies on VPT and the use of a "fine cuts" technique when designing studies. This will allow researchers to tease apart impairments in the spatial demands of a task vs. the social. The recommendations set out in this review provide a strong motivation for investigating VPT in autism and shed light on why findings so far are inconsistent.

## **REFERENCES**

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**Conflict of Interest Statement:** The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

*Received: 28 June 2013; accepted: 18 September 2013; published online: 08 October 2013.*

*Citation: Pearson A, Ropar D and Hamilton AF (2013) A review of visual perspective taking in autism spectrum disorder. Front. Hum. Neurosci. 7:652. doi: 10.3389/fnhum. 2013.00652*

*This article was submitted to the journal Frontiers in Human Neuroscience.*

*Copyright © 2013 Pearson, Ropar and Hamilton. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.*

**REVIEW ARTICLE** published: 10 September 2013 doi: 10.3389/fnhum.2013.00558

## The primacy of social over visual perspective-taking

## *Henrike Moll\* and Derya Kadipasaoglu*

*Department of Psychology, University of Southern California, Los Angeles, CA, USA*

#### *Edited by:*

*Klaus Kessler, University of Glasgow, UK*

#### *Reviewed by:*

*Ian Apperly, University of Birmingham, UK Mark Gardner, University of Westminster, UK*

#### *\*Correspondence:*

*Henrike Moll, Department of Psychology, University of Southern California, SGM 501, 3620 South McClintock Ave., Los Angeles, CA 90089, USA e-mail<EMAIL_ADDRESS>
In this article, we argue for the developmental primacy of social over visual perspective-taking. In our terminology, social perspective-taking involves some understanding of another person's preferences, goals, intentions etc. which can be discerned from temporally extended interactions, including dialog. As is evidenced by their successful performance on various reference disambiguation tasks, infants in their second year of life first begin to develop such skills. They can, for example, determine which of two or more objects another is referring to based on previously expressed preferences or the distinct quality with which these objects were jointly explored. The pattern of findings from developmental research further indicates that this ability emerges sooner than analogous forms of visual perspective-taking. Our explanatory account of this developmental sequence highlights the primary importance of joint attention and the formation of common ground with others. Before children can develop an awareness of what exactly is seen or how an object appears from a particular viewpoint, they must learn to share attention and build common "experiential" ground. Learning about others' as well as one's own "snapshot" perspectives in a literal, i.e., optical sense of the term, is a secondary step that affords an abstraction from all (prior) pragmatic involvement with objects.

**Keywords: referential communication, perspective-taking, joint attention, theory of mind (ToM), intersubjectivity**

Visual perspective-taking tasks typically entail another agent who embodies the spatial coordinates that the participant has to consider. They are thus at least minimally social in the sense that someone else is co-present and available for social interaction (see Schütz, 1932). In line with this, children with autism, whose difficulties are known to be first and foremost social in nature, struggle to detemine how others see things from their viewpoint (Reed, 2002; Hamilton et al., 2009; Yu et al., 2011; but see Hobson, 1984). At the same time, however, a "cold-cognitive" assessment or computation of how objects relate to one another in space is arguably less of a social affair than understanding another's affective, conceptual, or epistemic attitude toward a situation (see Fishbein et al., 1972).

In this article, we adopt the opposition of visuo-spatial and social perspective-taking employed by the editors. We will argue from a developmental approach that social perspective-taking is primary and precedes visual perspective-taking in human ontogeny. Our claim is that children first learn to take perspectives in situations that are not defined by differences in how self and other perceive objects visually but by differences in their experiential backgrounds, i.e., in what they did, witnessed, or heard. It might seem more complex to keep track of another's prior encounters and engagement with things than to compute his instantaneous visuo-spatial relation to an object in the room. Yet, it will become clear that infants readily note and update "experiential records" (Perner and Roessler, 2012, p. 522). Registering and remembering what others did, witnessed, or mentioned is less of a task demand for them than a helpful cue to others' goals and intentions. Per definition, no such cues from prior encounters are available in visual perspective-taking tasks that revolve entirely around momentary visuo-spatial relations.

First, we will review referential ambiguity tasks that are typically solved in the second year of life. It will become obvious that infants readily rely on others' previous expressions of attitude, their prior attentional engagements with objects, and previous discourse to solve the reference problem. These manifold abilities of infants to establish reference against the background of prior interactions are subsumed under "social perspectivetaking."

An overview of studies on visual perspective-taking will show that this ability has its onset noticably later. Again, it is generally taken for granted that perceptual perspective-taking precedes and serves as a foundation for the "deeper" forms of social perspective-taking (Kessler and Thomson, 2010). The same is suggested by accounts of mutual knowledge according to which physical co-presence is the easiest and least errorprone way to arrive at mutual knowledge (Clark and Marshall, 1981; Schiffer, 1972). These assumptions are seriously called into question by the empirical fact that visual perspectivetaking does not precede but follows social perspective-taking ontogenetically.

An excursion into the early development of graphic skills lends further support to the idea that knowledge of visual perspectives is a relatively late cognitive achievement that is derivative of social perspective-taking. We will conclude with a programmatic attempt to explain this developmental sequence with the social and cooperative nature that sets humans apart from other animals.

## **THE ROLE OF THE EXPERIENTIAL BACKGROUND**

#### **PRIOR AFFECTIVE EXPRESSIONS**

Affective displays are key indicators as to how people will behave toward objects. In a seminal study, 14− and 18-month-old infants were presented with two food items: crackers and broccoli (Repacholi and Gopnik, 1997). The infants opted for the crackers, whereas an adult displayed the opposite preference. When the adult, without looking at either dish, later requested food from the infants, the younger ones gave her what they themselves liked (crackers), whereas the older ones selected the broccoli.

As was made clear by Perner et al. (2005), understanding perspectives in sensu strictu, as evidenced by an explicit acknowledgment of different takes on the self-same thing ("I cannot stand broccoli, but she likes it!") is not necessary for this test. The infants just had to realize that the other and broccoli "go together," and so an understanding of objective "person-object couplings" suffices to pass this test. Nonetheless, the older infants were able to learn about the other's taste preference from her prior expressions. A study by Egyed et al. (2007) confirmed that, in the absence of ostensive cues (which gear infants toward more objectcentered interpretations such as "Broccoli is good"; see Gergely et al., 2007), 14-month-olds track specific persons' affective displays toward objects and expect them to behave in accordance with them later.

"Emotional eavesdropping" (Repacholi and Meltzoff, 2007) provides further support that infants act differently vis-à-vis others depending on their previously expressed affective attitudes. When 18-month-olds witness an adult reprimand another for performing a novel action, the infants later imitated the act less when the adult was present as opposed to when he was absent. Independently of their own desire or interest to perform an act, infants thus alter their behavior as a function of others' attitudes toward objects and actions.

#### **PRIOR ENGAGEMENT**

Infants use various other cues to disambiguate reference. A powerful one is the other's familiarity with or ignorance of objects and their locations (see O'Neill, 1996, for an influential study with 2− and 2–5-year-olds). In their modification of a word learning study (Akhtar et al., 1996), Tomasello and Haberl (2003) found that 1 year-olds knew which of three objects an adult requested from them based on her prior engagement with the objects. When the adult excitedly asked infants for a toy, 12-month-olds chose the one that was new for the adult because she failed to see it in the past. Even though the infants themselves were equally familiar with all toys, their responses showed that they knew what the other had and had not witnessed a few moments prior.

MacPherson and Moore (2010) directly contrasted what an adult knew with what the infant herself was familiar with. In their study, two objects were mutually familiar for adult and infant, a third object was new for the infant and a fourth was new for the adult, but "old" for the infant. When the adult later excitedly requested a toy, 13-month-olds egocentrically chose what was new for themselves, while 19-month-olds selected the toy that was new for the adult and not for them.

Many studies have not just confirmed that infants readily track others' experiential backgrounds but have also yielded insights into the scope and limits of this skill. Joint attention has been shown to play an important role in interactive test situations. Having observed as mere onlookers how an agent engages with objects was insufficient for 14-month-olds to identify what the agent requested from them based on his knowledge vs. ignorance of the different objects. When the infant and the agent jointly engaged around the objects, infants successfully determined which things the other did and did not know (Moll and Tomasello, 2007; Moll et al., 2007, 2008). In contrast to mere onlooking, joint attention makes the co-attenders' familiarity with the object "mutually transparent" (Eilan, 2005)—it leaves no room for doubt that the object has been registered. Furthermore, it seems that unless the questioner clearly conveys that her excitement is elicited by something that is new for her individually, infants have a general bias to point out what is mutually familiar and unifies self and other in prior bouts of shared experiences (Saylor and Ganea, 2007; Liebal et al., 2009, 2011).

In a study that aimed to test false belief understanding, infants saw an adult as striving for different goals depending on what he witnessed earlier (Buttelmann et al., 2009). After the adult had placed an object in a box, he either attentively watched it being moved to a different container (true belief) or failed to witness the transfer (false belief). When the adult later approached the box from which the object had been removed, 18-month-olds helped him to get the box open ("He must want something else from this box!") in the true belief, but retrieved the object from its new location in the false belief condition. Again, this demonstrates that infants take what others have witnessed into account when acting and responding toward them. They revert to the background constituted by past experiences and use it to inform them about an agent's desires, goals, and intentions.

Looking-time studies on false belief understanding further support this idea (e.g., Onishi and Baillargeon, 2005; Surian et al., 2007; Kovács et al., 2010). Even in their first year of life, infants look longer when they see an agent acting in a way that disaccords with his prior perceptual experiences (he acts as if he knows something he did not observe) than when they see him behave in ways that are consistent with what he observed. Whether belief understanding can be captured with this method remains the subject of an ongoing debate (Perner and Ruffman, 2005; Low and Perner, 2012), but what this research unequivocally demonstrates is that infants at a very young age are aware of what others have and have not registered perceptually. The findings also relativize the importance of joint attention suggested by interactive studies, because infants in looking-time tests usually do not jointly attend with the other and, in some cases, have not even reached the age at which they are able to do so. Joint attention might thus only play a critical role when infants have to directly respond to the agent in a communicative or cooperative act, which might require a more explicit understanding of knowledge and ignorance.

#### **PRIOR DISCOURSE**

To not talk past, but speak with each other, interlocutors must know what they can and cannot presuppose as mutually given. Part of what defines the mutually given is the shared prior discourse—what Clark and Marshall (1981) refer to as "linguistic co-presence" in their model of mutual knowledge formation. Anecdotal evidence of "egocentric speech" (Piaget, 1929, 1955) alongside experimental data questioned children's skills in communicative perspective-taking. Young children tend to use pronouns (e.g., O'Neill and Holmes, 2002) and definite articles (Maratsos, 1976; Power and dal Martello, 1986) without having provided the antecedent. Their descriptions are often not specific enough to allow the listener to discern reference—even after requests for clarification were made, thus challenging effortless communication (see Glucksberg and Krauss, 1967; Deutsch and Pechmann, 1982; Sonnenschein and Whitehurst, 1984). Generally, young children have a tendency to underestimate the informativeness that is needed to communicate effectively (Olson and Torrance, 1987).

At the same time, evidence accumulates that even infants adjust their (speech) behavior according to what has been shared linguistically. For example, 2-year-olds use more informative naming constructions when a referent is new than when it is given, in the sense that it was part of previous discourse. Matthews et al. (2006) had 2-year-olds watch a video of a character performing an action (e.g., a clown jumping) together with an assistant. The assistant mentioned the character to the child. Another adult, who had either participated in the discourse or not then asked children to narrate what happened. In their replies, the children referred to the character more often with a pronoun (instead of a full noun) when their interlocutor had participated in the prior discourse than when he was not part of this discourse (see Nayer and Graham, 2006, for similar results with 3-year-olds). In Clark and Marshall's (1981) terms, the children tailored their references to the linguistic copresence they shared with their particular interlocutor.

On the side of comprehension, even 1-year-olds are sensitive to what is and is not linguistically co-present. Ganea and Saylor (2007) found that 15- and 18-month-olds rely on a person's prior verbal reference to an absent object to determine what the same person is speaking of a few moments later. After an adult made clear that she was searching for a particular object (e.g., a puppy), she exclaimed that she knew where "it" was and led the infant to a cabinet. Two objects—the target (puppy) and a distractor were revealed, and the adult ambiguously asked "Can you get it for me?" Infants at both ages selected the target object, thus showing that they located the referent in the adult's prior speech. Echoing the findings on prior attentional engagement (e.g., Moll et al., 2008; Liebal et al., 2009), the infants also knew with which particular person they shared the linguistic background: When a different adult than the one who had searched articulated the request, the infants grasped objects randomly.

A further indication that infants keep track of and update records of linguistic co-presence is their appropriate use of elliptical constructions in discourse. In a study by Salomo et al. (2010), 2-year-olds were asked, "What's the agent doing now?" after watching and hearing verbal descriptions of videos showing either the same action performed on different patients (e.g., a frog feeding a duck vs. a ladybug) or different actions performed on the same patient (e.g., a frog feeding vs. washing a duck). In their answers, the children omitted reference to the patient when it remained the same and was thus given in the prior discourse. When the patient changed and was thus new, the same children made reference to it with a lexical noun. The children thus knew when null-references were and were not warranted given the discourse background. Additional evidence that 2-year-olds know which information is obligatory vs. optional in speech stems from observations of children who acquire "null-argument" languages; i.e., languages that allow the omission of subjects and objects given the appropriate discourse context (Serratrice, 2005).

Taken together, these findings clearly demonstrate that infants produce and understand gestures and speech acts against the background of their prior interactions with other persons (see Wittgenstein, 2001; Tomasello, 2008). What infuses the gestures and speech acts with meaning is the intersubjectively shared background of prior experiences. Through joint attention, infants construct a common ground (Clark, 1996) with specific other persons, and they discriminate between the dyadspecific common grounds, keeping track of what they have and have not shared with whom. In their attempts to secure reference, they naturally revert to these backgrounds, which becomes particularly obvious under conditions of potential ambiguity.

### **VISUAL PERSPECTIVE-TAKING: NO HELP FROM THE BACKGROUND**

None of the above is available in visual perspective-taking. All that is relevant here are instantaneous viewing angles and momentary spatial relations. The experiential background offers no help to solve referential ambiguity in these tests. In fact, a prerequisite that has to be met to guarantee the validity of these tests is that the candidate objects be "experientially neutral," i.e., that target and distractor cannot be distinguished by any distinct roles they played in prior interactions. The correct response has to depend entirely on the objects' visibility (level 1) or mode of presentation (level 2 perspective-taking, see e.g., Flavell, 1992, for the distinction of level 1 vs. level 2) from a particular viewpoint. We will limit our analysis to level 1 visual perspective-taking, i.e., the ability to determine what another can and cannot see. This level of perspective-taking emerges a couple of years prior to level 2, and is structurally similar to the tasks above, which dealt with children's understanding of what others desired, witnessed, or spoke about. Level 2 is a more effortful, qualitatively distinct (Kessler and Rutherford, 2010), phylogenetically recent (human-specific) skill, that requires an explicit understanding of perspectival differences and, in the absence of autism (see Hamilton et al., 2009), emerges between 4 and 5 years.

Children first exhibit an understanding of what others can and cannot see at around 2 years of age and older. For example, when 24-month-olds witness an adult searching for something, they preferably hand her an object that is blocked from the adult's view instead of a mutually visible one (Moll and Tomasello, 2006). In a similar task by Nurmsoo and Bloom (2008), 31-month-olds also mostly selected an object that was hidden from an adult's view when he pretended to be searching for something. (One should note that there was a confound with gaze direction in this study: The adult looked straight at the visible distractor object when asking "where" the referent was, allowing children to act on a simple heuristic that people do not search for things at which they are currently looking.)

In one of several tasks administered by Masangkay et al. (1974), children between 2 and 3 correctly judged that an adult sitting across from them could not see an apple depicted on the front of a card held between them. Hughes and Donaldson (1979) found that 3-year-olds knew where to place a doll in a house so that none of several policemen at various positions could see her. In another study, 2.5−, but not 2-year-olds, granted an adult visual access to an object he desired to see by either revealing the object from behind an occluder or moving away the occluder (Lempers et al., 1977). In an "analogy task" developed by Yaniv and Shatz (1990) 3.5-year-olds were able to place a duck so that a doll perceiver saw the same part or side (e.g., its back) of the duck as another doll that looked at an identical duck.

In sum, we find that level 1 perspective-taking as demonstrated by tests using interactive methods emerges between the second and third birthday. This ability comprises percept production (enabling another to see something), percept diagnosis (judging what another sees), and percept deprivation (hiding objects from another). In Clark and Marshall's (1981) terms, it is now that children have come to understand when mutual knowledge is and is not supported by immediate physical co-presence.

However, children at this age are far from being proficient at visual perspective-taking. On the contrary, striking limitations have been identified. Under the age of 3, children are unable to hide an object from an adult by placing a barrier between her and the object (Flavell et al., 1978; McGuigan and Doherty, 2002). Two-year-olds also struggle to select appropriate referring expressions depending on what their interlocutor can see. While the children in Matthews et al.'s (2006) above-mentioned study successfully tailored their expressions to the prior discourse, they did not adjust their speech accordingly when the adult's visual access to the video was manipulated. More concretely, they did not produce more full nouns (instead of the less informative pronouns) when the adult failed to see the video compared to when he saw it. In Yaniv and Shatz's (1990) study, 3-year-olds preferably positioned the duck facing the doll, even when asked to place it so that the doll would see its back. They thus exerted a bias to generate the canonical or good—in this case the frontal—view of the object, irrespective of the instruction (see Light and Nix, 1983; more on a similar phenomenon in children's drawings below).

## **A DEVELOPMENTAL LAG**

Taken together, these studies point at a developmental lag between social and visual perspective-taking. Infants rely on prior joint perceptual experiences including previously shared discourse at least 1 year before they take into account others' visuo-spatial relations to the things around them when they discern or establish reference. This is a significant décalage given the young age of these children. Contra Clark and Marshall (1981) and contra intuition, immediate physical co-presence does not necessarily facilitate the delineation of common ground. While it is true that physical co-presence often rightly signals that a given object figures in the common ground, the same co-presence can hampen children's ability to identify what is mutually given from what they have privileged access to as individuals. It can trick them into falsely assuming that an object they see is perceptually available to the other as well. The strong priority that is ascribed to an *ad-hoc* formation of mutual knowledge based on immediate or potential physical co-presence is thus called into question by this developmental sequence.

That the lag is real and robust becomes particularly obvious in studies in which an understanding of knowledge and ignorance is directly contrasted with visual perspective-taking. Moll et al. (2010) compared 2-year-olds' ability to detect an adult's ignorance due to absence vs. impeded vision. When the adult disengaged entirely from her interaction with the child by leaving after having shared two toys with her, the children later knew that the adult was unfamiliar with a third object that they were presented with. But when the adult remained co-present with her visual access to the third object blocked by a barrier as the child explored it, the children later acted as if the adult was familiar with this object. They failed to recognize the barrier's effect.

A very similar pattern emerged in Nurmsoo and Bloom's (2008) study. In their second experiment, 31-month-olds had no problem identifying what an adult was looking for when she had hidden one object but was absent when the other was hidden thus making her ignorant of the second object's location. By contrast, children this age found it relatively difficult to determine what the adult searched for when he had seen neither placement but was spatially positioned so that he could not see one of the objects (Experiment 1). Similarly, and as mentioned above, while 2-year-olds in Matthews et al.'s (2006) study readily switched to more informative references when an object was not shared in prior discourse with an adult, they failed to adjust the informativeness of their speech accordingly when the referent was blocked from the adult's sight. Taken as a whole, these studies clearly show that young children can draw the knowledge-ignorance distinction before they solve otherwise identical tests that tap visual perspective-taking.

The same gap has been identified with looking-time measures as well. Again, when this method is applied, infants as young as 7 months show a sensitivity to the manipulation of perceptually induced beliefs (Kovács et al., 2010). They look longer when an agent behaves in a way that is inconsistent with what she witnessed earlier than when her behavior matches her prior observations (someone looks for something where she last saw it). In contrast, the youngest age for which level 1 visual perspectivetaking has been documented with the looking-time technique is 13–16 months (Luo and Baillargeon, 2007; Sodian et al., 2007; Luo and Beck, 2010). For example, when 13-month-olds repeatedly see an adult reaching for one of two toys, they form an expectation that he will keep doing so—as evidenced by longer looks when he suddenly reaches for the previously ignored toy. But they only form this expectation when the agent is able to see the alternative object, and thus disprefers it. No extended looks were shown when the non-chosen toy was blocked from the agent's view, and so simply unseen.

Further indication that 13-month-olds have rudimentary skills in visual perspective-taking stems from a study that is purported to test false belief comprehension (Surian et al., 2007). In this looking-time experiment, a caterpillar's knowledge of his preferred object's location was manipulated by the presence/absence of a barrier impeding the caterpillar's, but not the child's, vision of the object. The authors do not interpret their results in terms of visual perspective-taking. But partly because looking-time measures involve no "task" (the child is not asked or prompted to respond to anything in particular), it remains open which aspect infants mainly reacted to or found harder to process: realizing the barrier's defeating effect on the agent's vision, or keeping track of what he did and did not witness.

In either case, the same developmental lag that is found with interactive response methods becomes manifest when looking times are applied, albeit at a younger age—reflecting the reduced task affordances of this method. The fact that the developmental order pervades different research methods shows its robustness. But it has to be emphasized that the lag is limited to level 1 visual perspective-taking and its corresponding counterparts in social perspective-taking. A more synchronous pattern is found at level 2, which affords an explicit knowledge of the possibility of alternative, and potentially false, views. This knowledge, which spans across visual and social perspectives alike, is formed between 4 and 5 years—supporting the idea of a common cognitive thread that runs through various perspective problems (see Perner et al., 2003; Moll and Meltzoff, 2012). The gap that calls for an explanation thus only exists in the early beginnings of perspective-taking, before a more abstract and uniform understanding of perspectives develops in late preschool.

The pressing question then is how the counterintuitive sequence of visual perspective-taking preceding social perspective-taking observed in the early years can be explained. We will make a first explanatory attempt by addressing the more specific question of why visual perspective-taking might pose a particular challenge (see Moll and Meltzoff, 2012).

#### **SHARED PERCEPTUAL SPACES**

We argue that young children have a proclivity to treat social interaction as a sufficient condition for shared perceptual availability: "When you and I are co-present and engaged, you should be able to perceive what I perceive." An impression of a shared perceptual space is induced, and only later overcome once children learn more about and attend more to the specific defeating conditions of perception, such as a blocked line of sight.

Support for the idea that co-presence and social engagement create an illusion of shared perception comes from experimental data with both children and adults. Glucksberg and Krauss (1967) report that preschoolers produced iconic gestures and used demonstratives ("It goes like this!") to describe objects to their conversational partner who sat across from an occluder. The work of Keysar and colleagues shows that even adults have a prepotent tendency to assume that others around them share their perceptual access to objects, even when this is not true (e.g., Keysar et al., 2003; Epley et al., 2004; Keysar, 2007). Consistent with what we know about children, adults are biased to overrather than underestimate what the other sees or knows (Keysar and Henly, 2002; see also Bernstein et al., 2007). Interestingly, the thicker or richer the common ground shared by two people, the more likely they are to overrate the success of their communicative attempts (Wu and Keysar, 2007). The more that is shared, the less prepared one is to identify when something is not shared. A vast overlap in what is perceptually accessible weakens the alertness to check if a particular object is mutually given or not. In support of this, it was found that people communicate less informatively to a concrete other person who "co-inhabits" their perceptual space than to a merely imagined interlocutor (Schober, 1993). This is much in line with our developmental finding that corporeal co-presence, and thus a high overlap in what can potentially be turned into an object of shared attention, hampens young children's ability to detect others' ignorance (Moll et al., 2010).

This overestimation effect also helps to explain young children's notoriously poor perspective-taking skills when speaking on the phone. It has long been known that children use manual gestures, demonstratives, and non-specific references during phone conversations (Bordeaux and Willbrand, 1987; Warren and Tate, 1992)—indicating that they are unaware of the fact that they and the things around them cannot be seen. In our interpretation, the shared discourse elicits the false impression of a generally shared perceptual space that spans across different sense modalities, including vision. That is, verbally established co-presence leads to the illusory impression of shared visual perception.

This idea, however, is called into question by experiments suggesting that others' viewpoints make their way into our considerations effortlessly and automatically (Qureshi et al., 2010). When asked how many items they see in a visual array, adults and school-age children are slower and less accurate in their judgments if their visual input mismatches that of another agent who is part of the scene they watch (Samson et al., 2010; Surtees and Apperly, 2012; see also Surtees et al., 2012). Two things can be said to reconcile these findings with our overestimation thesis. Firstly, it is conceivable that once level 1 visual perspectivetaking has been practiced for years, it becomes "second nature" or automated. Secondly, the participants' situation differs drastically between the studies. In those studies supporting the overestimation thesis, the child interacts with the other directly, which might let the perspectival differences between them dissolve "in the heat of the moment." In the tasks suggesting automatic perspectivetaking, participants have a contemplative, theoretical distance to the other, who figures in the array like an object. This theoretical distance could highlight the other's position in relation to the remaining items in the scene. The two sets of findings thus do not necessarily contradict each other.

#### **A GLANCE AT EARLY PICTURE-MAKING**

It was speculated that before children's perception is corrupted by language and thought, they ought to see the world with innocent, i.e., objective eyes (see Matisse, 1953) and even master perfectly the art of drawing in linear perspective (Bühler, 1930; Sully, 1895). But of course, by the time children have the motor skills and motivation to depict objects and events, they have long been language- and concept-using beings who have passed any hypothetical phase of innocent vision (see Costall, 1997, 2001).

When children begin to draw figuratively, they do not faithfully translate three-dimensional objects onto two-dimensional picture planes. They show no intention to depict things exactly the way they appear to them from one fixed point of observation. Drawing does not serve the goal of imitating visual experiences. As a famous dictum says, children "draw what they know, not what they see" (but see Arnheim, 1974, p. 164, for rightly criticizing the false opposition of seeing and knowing that is employed here)—exhibiting a style dubbed "intellectual realism" (Luquet, 1927). They include aspects and elements in their pictures that cannot be seen from their present perspective and may not be visible from any particular, single viewpoint. They create a "good" or ideal view of objects by depicting features they consider relevant or important and omitting what is irrelevant. The goal is not to produce a correct perspectival reconstruction but to show objects in their typical form and thus to capture their constitutive or essential features. For example, a cup will be depicted in canonical fashion with a handle on its side (ideal for grasping, see Cox, 1991). Likewise, humans are shown in their canonical frontal view with a face including two eyes (ideal for social interaction), whereas trunk, nose and other parts might be left out (Cox, 1997).

Also, young children mostly produce images spontaneously from memory and imagination (Golomb, 2004). When presented with a model to guide their drawing activity, they rarely look up to see what the object exactly looks like. The model serves as a source of inspiration—it provides a theme or motif and is relevant insofar it exemplifies a generic object (Luquet, 1927), but it is not adhered to as an original that ought to be replicated. Again, what this indicates is that children do not intend but fail to draw from a fixed perspective.

In his essay "Perspective as symbolic form," Panofsky (1927) pointed out that a faithful reconstruction of what is seen from a particular viewpoint affords a severe abstraction from the content of experience.  An individualistic and somewhat arbitrary factor thereby gets introduced, because one commits to showing the scene from a single, static point of observation. Any ordering according to what is regarded important or relevant has to make way for a strictly geometric ordering.

With this held in mind, it becomes much less puzzling why an awareness of visual perspectives emerges rather late—not just in history, but in ontogeny as well (see Gablik, 1977, for parallels between the history and genetic development of visual art). Though children at age 5 and older can be induced to draw what they see, it is not before 7 or 8 years that they spontaneously create view-dependent images (Davis, 1983; Cox, 1991). Even at this age, their advances are such that they acknowledge partial occlusion and draw only what is visible (e.g., the correct number of faces of a cube), but they still do not depict the visible parts precisely in the way they appear (e.g., with lines converging in a vanishing point; Bremner and Batten, 1991; Cox, 1991).

What is of primary importance to children is to share the world of those around them. Precisely how this shared world presents itself from one specific vantage point is secondary and does not become thematic in the very early stages. First and foremost, drawing serves to "make sense of the world" (Arnheim, 1969, p. 257)—and this is true ontogenetically as well. Young children draw to narrate events and give "shape and order" (Cox, 2005) to their experiences. We want to go further and argue that picturemaking primarily serves to make sense of the social world, as one of the first and most frequent motifs is the human figure (Maitland, 1895; Lark-Horovitz et al., 1939; see Cox, 1993, for an overview). But not just the themes or motifs are social; so is the process of drawing. It is an activity that is typically shown in the presence of another to whom the child narrates as she draws, and for whom she might create the picture as a gift. The graphic product in itself can hardly be interpreted without the accompanying speech in which children reconstruct their experiences and reveal what they intend to draw (Cox, 2005).

In either case, we find that the relatively late onset of taking others' visual perspectives is paralleled by a late emergence of the use of perspective in drawings. Young children's pictures document their inattention to specific visual perspectives. Just like there was no motivation to graphically capture objects from specific, transient viewpoints in the early history of visual art (Panofsky, 1927), so do children show no interest in representing things precisely the way they happen to see them. They ignore the contingent ways in which things appear momentarily for the sake of capturing what belongs to an object more generally. This also becomes manifest in perceptual self-reports. When preschoolers are asked to indicate how they perceive a visual array by choosing from among a set of different pictures, they often judge incorrectly and select a picture showing the ideal rather than their own view (Liben and Belknap, 1981; Light and Nix, 1983). The upshot is that children's drawings are one of several pieces of converging evidence that young children pay little attention to differences in visual perspective. Others are their faulty perceptual reports, their behavior during phone conversations, and, as we have seen, profound struggles with visual perspective-taking—neither of which require graphic skills.

### **CONCLUDING REMARKS**

Humans are extraordinarily *relational* and interdependent beings (MacMurray, 1961). They are adapted to rely on and cooperate with others in a way that is unparalleled in the animal kingdom (Gintis et al., 2003). Especially in the early beginnings, a human individual is entirely dependent on others' care, attention, and sharing of knowledge (Csibra and Gergely, 2011). What is crucial at this early stage is that the child comes to share the world of those around her. She accomplishes this by jointly attending to things with others. It is in these bouts of joint attention that the child learns about objects: their gestalts, functions, and labels etc. Importantly, these are perspective-invariant properties. The focus lies on the object and its qualities, not on the different perspectives from which each co-attender perceives it (Campbell, 2012; Moll and Meltzoff, 2012; Seemann, 2012). Only once it can be taken for granted that we attend to the same thing, is there room, in a second step, to "objectify" the different viewpoints from which each of us perceives the object. As Campbell (2012, p. 428) puts it, "The point is that a grasp of the different perspectives from which a thing may be experienced should not be allowed to take on a life of its own; this grasp of the different perspectives from which a thing may be experienced is always grounded in a prior knowledge of which thing is in question."

But this merely seems to explain why joint attention precedes knowledge of perspectives, not why children engage in social perspective-taking before visual perspective-taking. However, we think that these two things are related. In joint attention, one's knowledge of the object becomes mutually transparent and so does the expression of one's attitude toward it. While the focus of joint attention is the object itself, it simultaneously informs us of the other's knowledge of it as well as her take on it. Joint attention thus directly supports the forms of social perspectivetaking discussed in this article, which are critical for cooperative communication and other forms of collaborative activities.

The visuo-spatial positions of the co-attenders, in contrast, remain entirely in the background. Firstly, the viewing angles involved usually bear no significance with regard to the object, its qualities, or the other's attitude toward it. Secondly, given the dynamic character of joint attention, these perspectives rarely remain constant but tend to fluctuate over the course of exploration, as the object gets manipulated and/or the spatial positions changed. Joint attention thus directly paves the way to early forms of social, but not visual perspective-taking.

The picture looks very different for non-human primates that possess simple forms of visual perspective-taking. Chimpanzees have been shown to preferably approach food that is blocked from a dominant individual's sight (Hare et al., 2000), and to seek out locations and motion paths that hide their bodies from competitors (Whiten and Byrne, 1988; Hare et al., 2006). These behaviors are advantageous in potentially antagonistic and risky encounters with conspecifics or predators (Hare and Tomasello, 2004). They are evolutionarily adaptive for animals that are yoked much tighter into the here and now than humans and do not engage in shared intentionality and cooperation. We think that joint attention and cooperation bridge spatial distances between self and other and thus privilege social over visual perspective-taking. The competitive and individualistic mode of operating found in nonhuman primates, in contrast, makes an awareness of the visibility of resources and one's own body to others critical for survival.

Generally, visuo-spatial perspective-taking is seen as the most basic and embodied form of perspective-taking, that is expected to subserve and function as a model for more mental or highercognitive forms, such as imagining how others feel or think about

#### **REFERENCES**

a certain situation (as is also suggested by spatial metaphors such as "putting oneself in another's position/shoes," see Kessler and Thomson, 2010). The genetic primacy of social over visual perspective-taking that we argued and provided empirical support for is at odds with this idea of visual perspective-taking as the cradle for other kinds of perspective-taking. Being aware of and responsive to others' literal viewpoints can certainly be key in social interaction. To communicate effectively we often have to adjust our speech and non-verbal behavior according to what the other sees or how he sees things—e.g., when we direct him to an object outside of his visual field or ask him to move his left shoulder that is on our right as we stand facing him. But getting a grip on others' visual perspectives takes time ontogenetically, and is not the first skill of its type to emerge.

We tried to show in this article that before children come to know what is seen from which particular viewpoint, they not only bridge perspectival differences in acts of joint attention and deictic reference by the age of 9–12 months, allowing them to create a common ground of shared experience with others. They also readily track and update what others have witnessed, done, and said. This knowledge is foundational for effective communication and other forms of cooperation, as it constitutes the background against which gestures and speech acts are understood and produced. We cited empirical evidence that children develop an awareness of visual perspectives somewhat later. This is not only suggested by the relatively late onset of visual perspectivetaking, but is also reflected in children's aperspectival drawings and false perceptual judgments. In our attempt to explain the counterintuitive sequence from social to visual perspective-taking we highlighted the primary importance of forming experiential backgrounds with others for the sake of communication and cooperation. If the developmental trajectory that we traced is informative with regard to the relation between visual and social perspective-taking in cognitively mature human beings remains an open question.

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**Conflict of Interest Statement:** The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

*Received: 03 June 2013; accepted: 22 August 2013; published online: 10 September 2013.*

*Citation: Moll H and Kadipasaoglu D (2013) The primacy of social over visual perspective-taking. Front. Hum. Neurosci. 7:558. doi: 10.3389/fnhum. 2013.00558*

*This article was submitted to the journal Frontiers in Human Neuroscience.*

*Copyright © 2013 Moll and Kadipasaoglu. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.*

## Old cortex, new contexts: re-purposing spatial perception for social cognition

## *Carolyn Parkinson\* and ThaliaWheatley*

*Department of Psychological and Brain Sciences, Dartmouth College, Hanover, NH, USA*

#### *Edited by:*

*Antonia Hamilton, University of Nottingham, UK*

#### *Reviewed by:*

*Ivan Toni, Radboud University, Netherlands Anna M. Borghi, Institute of Cognitive Sciences and Technologies, University of Bologna, Rome, Italy*

#### *\*Correspondence:*

*Carolyn Parkinson, Department of Psychological and Brain Sciences, Dartmouth College, 6207 Moore Hall, Hanover, NH 03755, USA e-mail<EMAIL_ADDRESS>
Much of everyday mental life involves information that we cannot currently perceive directly, from contemplating the strengths of friendships to reasoning about the contents of other minds. Despite their primacy to everyday human functioning, and in particular, to human sociality, the mechanisms that support abstract thought are poorly understood. An explanatory framework that has gained traction recently in cognitive neuroscience is exaptation, or the re-purposing of evolutionarily old circuitry to carry out new functions. We argue for the utility of applying this concept to social cognition. Convergent behavioral and neuroscientific evidence suggests that humans co-opt mechanisms originally devoted to spatial perception for more abstract domains of cognition (e.g., temporal reasoning). Preliminary evidence suggests that some aspects of social cognition also involve the exaptation of substrates originally evolved for processing physical space. We discuss the potential for future work to test more directly if cortical substrates for spatial processing were exapted for social cognition, and in so doing, to improve our understanding of how humans evolved mechanisms for navigating an exceptionally complex social world.

**Keywords: exaptation, neural reuse, social neuroscience, metaphor, spatial cognition, perspective taking, social distance, posterior parietal cortex**

## **EXAPTATION AND HUMAN COGNITION**

Our thoughts often include information outside of the current sensory environment, from imagined futures to the contents of other minds. However, the mechanisms supporting abstract cognition remain poorly understood. An explanatory framework that has gained traction recently (Gallese and Lakoff, 2005; Dehaene and Cohen, 2007; Anderson, 2010) involves exaptation: co-opting existing morphological features for novel functions (Gould and Vrba, 1982). New cognitive capacities may have emerged over the course of evolution when brain regions originally devoted to specific functions were repurposed and recombined in novel ways to process additional kinds of information (Anderson, 2010). Analogous cortical recycling processes may occur during development whereby cultural inventions co-opt circuitry evolved for older aspects of cognition (Dehaene and Cohen, 2007). Exaptation and cortical recycling provide plausible neural bases for proposals that representational resources originally devoted to space were co-opted to process more abstract information (e.g., Boroditsky, 2011).

If our ability to reason about abstract concepts resulted from evolutionary "tinkering" (Jacob, 1977) with neural mechanisms originally developed for operating on physical space, then demanding that these mechanisms handle conflicting inputs pertaining to their new and old functions simultaneously should create response conflict. Further, evidence from clinical and neuroimaging studies should suggest shared substrates for these functions. Both kinds of evidence are accumulating with respect to several domains of abstract cognition, most widely in studies relating temporal and numerical processing to spatial cognition (Hubbard et al., 2005; Bonato et al., 2012). Here, we highlight the potential for our understanding of the mechanisms underlying abstract social cognition to benefit from a similar approach, and review evidence that these mechanisms may be best understood in terms of the kinds of computations (e.g., distance judgments, perspective taking), rather than the domains of knowledge, that they involve.

## **SOCIALITY AND HUMAN BRAIN EVOLUTION**

Humans come into the world seemingly hardwired to detect and connect with other minds (Wheatley et al., 2012), and maintaining this predisposition is closely tied to healthy development (Pavlova, 2012). Effectively perceiving and interpreting social cues is particularly crucial for humans, who must navigate an exceptionally flexible system of relationships with conspecifics (Fiske, 1991). The ability to meet the intensive computational demands of humans' complex social environment (e.g., forging alliances, sharing intentions, tactical deception; Harcourt, 1988, 1989; Tomasello et al., 2005) is thought to have been a driving force for cortical expansion during evolution (Dunbar, 1998). Consistent with this hypothesis, feats of social cognition presumed to be uniquely human, such as sharing intentions (Tomasello et al., 2005) and representing others' beliefs (representational theory of mind, RTOM; Call and Tomasello, 2008) involve cortical areas that underwent the most evolutionary expansion (e.g., lateral posterior parietal cortex, PPC;Van Essen et al., 2001; particularly the temporoparietal junction, TPJ; Saxe, 2006; Redcay et al., 2010). These aspects of social cognition (e.g., RTOM) tend to involve information that cannot be perceived directly (e.g., false beliefs), and are functionally (Gobbini et al., 2007) and structurally (Parkinson and Wheatley, 2012) dissociable from older social processes (e.g., motor resonance), suggesting they either involve entirely new structures or structures previously devoted to non-social functions. Gould and Vrba

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(1982) suggested that exaptation of complex traits would likely be followed by secondary adaptations to further support new functions. Consistent with PPC circuitry evolved for dealing with space having been exapted, then expanded, to support abstract social cognition, the PPC has an evolutionarily old role in spatial perception (it encodes space in our distant relatives, e.g., rats; Nitz, 2006), processes both social and spatial information in humans and other primates (Yamazaki et al., 2009), and has expanded (Van Essen et al., 2001) and formed new connections (Mantini et al., 2013) in humans as it came to support evermore abstract aspects of social cognition. Recent computational modeling experiments support the notion that human brain expansion was driven by the cognitive demands of human sociality (Dávid-Barrett and Dunbar, 2013). Importantly, large brain size has a great metabolic cost; the human brain accounts for 2% of body mass but requires 20% of the energy that we consume (Clark and Sokoloff, 1999). In order to outweigh the considerable metabolic cost of the larger brain that they require, the cognitive mechanisms supporting human sociality must have conferred substantial adaptive benefits.

However, compared to other domains of abstract cognition (e.g., mathematics; Hubbard et al., 2005), little is known about how social forms of abstract cognition (e.g., representing beliefs or one's place in a social network) relate to evolutionarily older aspects of cognition. This may be due to several factors. First, compared to cognitive neuroscience, social cognitive neuroscience is a young field (Ochsner, 2007); many aspects of social cognition have simply been studied less extensively than other aspects of cognition. Second, early social cognitive neuroscience research often assumed a modular view of the brain (Bergeron, 2007), and involved searching for encapsulated brain areas devoted to processing particular contents (Kihlstrom, 2010). If one understands an aspect of cognition to be supported by a domain-specific module, attempting to relate that aspect of cognition to other mental phenomena may not be considered a particularly worthwhile endeavor.  Consistent with the suggestion that social cognition and physical perception involve common computations (Zaki, 2013), the functional significance of brain areas involved in social cognition may often be best characterized in terms of the operations they perform across multiple domains of information.

#### **LINGUISTIC MAPPINGS BETWEEN ABSTRACT COGNITION AND SPATIAL PERCEPTION**

One window into the cognitive operations supporting abstract thought is the language we use to describe them (Lakoff and Johnson, 1980). The spatialization of form hypothesis (Lakoff, 1987) specifically highlights the widespread use of spatial words (e.g., "outside," "far") to describe conceptual relations, suggesting that spatial schemata structure mental representations. Abstract relations may be represented in terms of space because unlike spatial relationships, they must be imagined rather than observed (Evans, 2006). We can observe two people sitting close together, gaze direction, or moving a vehicle forward, but can only imagine

the closeness of a friendship, a belief, or moving a meeting forward (Casasanto et al., 2010). In this view, phrases like "close friendship" or "far from the truth" are not mere figures of speech, but rather, figures of thought that reveal the structure of mental representations (Lakoff, 1986). The extent to which representational overlap between space and abstract domains results from exaptation during evolution, metaphoric structuring acquired during development, or some combination of these processes, remains an open question. With respect to social processing, the recruitment of brain areas involved in reorienting visual attention (TPJ) while congenitally blind individuals perform RTOM tasks (Bedny et al., 2009) suggests that functional overlap between social and visuospatial processes may be an innately predisposed result of evolutionary exaptation that is now reflected in linguistic metaphors for mentalizing (e.g., "Try to see things from my point of view").

The domain of abstract cognition that has been studied most extensively in terms its relation to space is time. Cross-linguistic studies indicate that people around the world use spatial language to describe time (Boroditsky, 2011); the intuition to represent time analogously to space may be evolutionarily predisposed. Do all languages employ spatial language to describe social relationships (e.g., "close friend") and RTOM? Are mappings consistent across languages? Some cross-linguistic variability exists in spatiotemporal metaphors, but certain mappings (future = forward) are nearly ubiquitous, likely due to shared aspects of human physiology and experience. Similarly, some English spatial metaphors for social relationships (familiarity = closeness) may stem from the tendency to give personal space to others based on the "closeness" of relationships (Hayduk, 1983). To our knowledge, metaphoric mappings between spatial and social relationships or between visuospatial and social perspective taking have not been subjected to exhaustive cross-linguistic analysis. Thus, whether or not humans around the world use space to structure mental representations of the magnitude and traversal of social distances remains an open question.

#### **BEHAVIORAL EVIDENCE FOR MAPPINGS BETWEEN ABSTRACT COGNITION AND SPATIAL PERCEPTION**

Behavioral mappings between space and abstract cognition have been most extensively studied with respect to time and number. Number and space are associated implicitly; according to the spatial numerical association of response codes (SNARC) effect, people are faster to respond regarding small numbers on the left side of space, and large numbers on the right side of space, even for tasks unrelated to magnitude (Dehaene et al., 1993). Similar associations have been documented between number and elevation (Pecher and Boot, 2011; Lugli et al., 2013). Representational overlap between space and number appears to comprise a universal human intuition (Dehaene et al., 2008), and can be documented outside of the laboratory. When thinking about numbers, more than 10% of individuals report automatically accessing mental "number forms" consisting of spatial layouts (Seron et al., 1992). It has even been suggested that on the scale of motoric action, time, space, and quantity are processed by an analog magnitude system (Walsh, 2003), which was co-opted to process discrete number (Bueti and Walsh, 2009).

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Stimulus-response compatibility codes also exist for time (Ishihara et al., 2008; Sell and Kaschak, 2011). Additionally, people tend to spontaneously sway forward while imagining the future and backward while imagining the past, suggesting that representations of movement through space are automatically activated during imagined movement through time (Miles et al., 2010). Monkeys (Merritt et al., 2010) and infants without exposure to relevant linguistic or sensorimotor mappings (Srinivasan and Carey, 2010) exhibit representational overlap between spatial extent and temporal duration (but not all magnitudes), suggesting that spatiotemporal mappings originate from common processing mechanisms, independently of sensorimotor grounding or linguistic correspondences.

Social and spatial information are also behaviorally associated. Visual perspective taking and mentalizing abilities are positively correlated (Flavell et al., 1986; Hamilton et al., 2009). People readily convert judgments of social compatibility into physical distances (Yamakawa et al., 2009). Words characterizing close social distances (e.g., "us," "friend") are associated with close locations, and words characterizing remote social distances (e.g., "them," "enemy") are associated with far spatial locations (Bar-Anan et al., 2007). Additionally, consistent with the suggestion that out-group members are construed as being physically distant from oneself (except following threat, Xiao and Van Bavel, 2012), Jones et al. (1981) found that out-group members are rated as more homogenous (i.e., having a narrower range of personal characteristics) than in-group members. Similarly, powerful individuals, who see themselves as exceptionally distinctive, construe others as exceptionally distant and homogenous (Fiske, 1993; Lee and Tiedens, 2001). It may be parsimonious to represent social and spatial distances analogously: Construal level theory of psychological distance (Liberman and Trope, 2008) posits that spatial, temporal and social egocentric distance share a common psychological meaning – distance from the self in the here and now.

Although extant research highlights a possible relationship between mental representations of social and spatial information, more research is needed to explore this possibility, and address several remaining questions, such as: is there a hierarchy of egocentric psychological distance domains, in which some are more primary than others? Do we spontaneously access representations of moving through space when traversing"social"distances or perspective taking, like during mental time travel? Are spatial representations activated explicitly when thinking about social relationships in everyday life, as they are for many individuals when thinking about numbers? Exploring questions like these will lead to an improved understanding of the mechanisms involved in abstract social cognition.

#### **NEUROSCIENTIFIC EVIDENCE FOR MAPPINGS BETWEEN ABSTRACT COGNITION AND SPATIAL PERCEPTION**

If spatial processing were repurposed for abstract cognition, one would expect overlapping neural substrates. Past research suggests that PPC systems for sensorimotor control and cognition largely overlap (Creem-Regehr, 2009). As the PPC expanded in size over the course of human evolution (Van Essen et al., 2001), it appears to have expanded in function as well, leading to suggestions that mechanisms originally devoted to representing

peripersonal space were repurposed to perform analogous operations on new contents. According to this theory, mechanisms previously dedicated to representing spatial information about the current sensory environment were first co-opted to represent simulations of peripersonal space in the past and future to support episodic memory and prospection, and later, to represent information in increasingly abstract frames of reference (Yamazaki et al., 2009). A growing body of neuroimaging and neuropsychological evidence suggests that representations of spatial and abstract information, including aspects of social cognition, are associated in the PPC.

Functional magnetic resonance imaging (fMRI) studies in humans implicate the PPC in representing perceptual, temporal, social and conceptual frames of reference (Yamazaki et al., 2009). Importantly, most of these results are based on overlapping activations from univariate contrasts, which could reflect shared neural codes or nearby but distinct codes for different kinds of information (Peelen and Downing, 2007). Multivariate pattern analysis (MVPA), which compares distributed patterns of activity between experimental conditions, rather than regionally smoothed and averaged responses, may better characterize brain regions' representational contents (**Figure 1**). The few studies that have used MVPA to compare spatial and abstract cognition in the PPC support the suggestion that representations of spatial information "scaffold" those of more abstract information. A pattern classifier trained only to distinguish PPC responses to leftward vs. rightward saccades can distinguish mental addition from subtraction (Knops et al., 2009). Additionally, position and valence words can be decoded by a classifier trained only on patterns of PPC activity corresponding to visual elevation (Quadflieg et al., 2011). Because MVPA can reveal information about underlying cognitive structures (**Figure 1**), this approach will be valuable in elucidating whether use of spatial language in describing abstract social concepts reflects true representational similarities or linguistic bottlenecks that push people to use metaphors in the absence of adequate domain-specific terminology (such bottlenecks have been demonstrated in olfaction; Yeshurun and Sobel, 2010).

Further research is needed to characterize the relationship between the PPC's involvement in social and spatial cognition. For instance, the TPJ is recruited both when subjects reason about others' false beliefs and positions in space (Abraham et al., 2008), suggesting that this region may perform similar computations on visuospatial and social contents. MVPA could be used to more directly test this possibility. Similarly, judgments about hierarchy and social distance recruit areas of the PPC involved in self-referential physical distance processing (Chiao et al., 2009; Yamakawa et al., 2009). Does this brain region represent "high" social status and "close" social distances analogously to how it represents "high" spatial location and "close" spatial distances? Again, characterizing the representational structure of the PPC with MVPA could elucidate this question (**Figure 1**).

Neuropsychological data also suggests a close relationship between representations of spatial and abstract information in the PPC. Patients with left hemineglect following right PPC damage often also neglect the "left" side of the mental number line (Zorzi et al., 2002), whereas PPC lesion patients without neglect show no numerical deficits (Vuilleumier et al., 2004). Remarkably,

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#### **FIGURE 1 | Interpreting fMRI responses to social and spatial tasks.**

**(A)** Hypothetical responses from an 8-voxel region of interest (ROI) to stimuli depicting: high social status (blue), high spatial position (orange), low social status (green), and low spatial position (pink), as well as baseline (gray; fixation cross). **(B)** Comparing the magnitude of locally smoothed and averaged responses could reveal that this ROI responds robustly to all 4 conditions relative to baseline, suggesting that it is involved in both social and spatial processing. **(C)** The same data can be studied as multivoxel patterns; responses from an ROI containing *n* voxels can be analyzed as *n*-dimensional vectors. Examining response patterns using MVPA can reveal more detailed information regarding the representational content of an ROI, as illustrated in **(D–H)**. **(D)** Responses from voxels 1 and 2 from the patterns depicted in **(C)** for 10 examples of each stimulus category; two-dimensional patterns are presented for clarity of visualization. Each dot represents a response to an example of each experimental condition. Experimental conditions are indicated by dot color. Machine learning algorithms can be used to determine which distinctions a region contains information about (Norman et al., 2006).

Here, a linear classifier would accurately distinguish the 4 experimental conditions from baseline, as well as "high" social status and spatial position from "low" social status and spatial position, as would be expected from a brain region that represents social status analogously to spatial position. **(E–H)** Visualizations of possible representational similarity structures (Kriegeskorte et al., 2008) for responses that may not differ in average magnitude, as in **(B)**. Pairwise correlation distances between response patterns can be used to characterize pattern dissimilarity. Shorter distances between dots indicate greater pattern similarity; larger distances indicate greater pattern dissimilarity. Local response patterns within a region that is recruited for all 4 experimental conditions can contain information about domain (i.e., social vs. spatial) regardless of position (i.e., high vs. low spatial location or social status; **E**), position but not domain **(F)**, or about both domain and position **(G)**. Alternatively, such a region may not contain information useful in distinguishing either position or domain **(H)**. Thus, MVPA will be useful in testing whether overlapping fMRI activations for social and spatial tasks reflect shared or distinct processing mechanisms.

normal numerical processing is restored in neglect patients following interventions utilizing adaptation to leftward-shifting prism glasses that restore visual attention to the previously neglected side of space (Rossetti et al., 2004). Patients with hemispatial neglect exhibit analogous distortions of temporal processing, systematically overestimating temporal durations (Basso et al., 1996; Calabria et al., 2011). Spatiotemporal mappings appear to be supported by the PPC in healthy individuals, as they are diminished following transcranial magnetic stimulation to this region (Oliveri et al., 2009). Neuropsychological studies relating spatial and abstract cognition have focused primarily on non-social domains of abstract cognition (e.g., time, number) and space. However, Samson et al. (2004) reported impaired mentalizing in patients with focal lesions to the inferior PPC. To our knowledge, no studies have tested if PPC damage is associated with abnormal representations of one's social network.

One limitation of neuroscientific evidence relating space and other domains of cognition is that data are available only from individuals in industrialized societies, and many of the corresponding behavioral phenomena are malleable to cultural learning (Dehaene et al., 1993). Although the tendency to map various domains of knowledge onto spatial representations appears to

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comprise a universal intuition (Dehaene et al., 2008; Parkinson et al., 2012), the nature of these mappings is often subject to cultural variation (Hung et al., 2008; Boroditsky and Gaby, 2010). Even two weeks of tool use engenders white and gray matter changes in the macaque PPC (Hubbard et al., 2005; Iriki, 2005). Lifelong immersion in cultures emphasizing metaphors and analogical reasoning no doubt impacts neural representations. Although the work summarized here is drawn from studies conducted in several countries, more cross-cultural work, especially that involving direct cross-cultural comparisons, is required to better understand how representational overlap between spatial and social cognition arises in the brain.

## **COMPARING SPATIAL REPRESENTATIONS BETWEEN DOMAINS OF KNOWLEDGE**

Importantly, although multiple domains of abstract cognition appear to co-opt mechanisms for spatial processing, different exaptations could have arisen separately, and may operate differently. There is a paucity of research investigating how different domains of knowledge that use space as a "reference domain" relate to one another. Different processes may have independently come to co-opt circuitry originally for spatial computations because such an arrangement was efficient and likely given pre-existing anatomical and functional constraints (Cantlon et al., 2009). Consistent with this suggestion,

### **REFERENCES**

a recent study comparing spatial representations of number and pitch within individuals suggests that spatial representations are idiosyncratic to specific domains of knowledge (Beecham et al., 2009). Thus, although past work relating spatial cognition to non-social aspects of abstract cognition will be informative for future studies aimed at characterizing the relationship between spatial perception and social cognition, this will not be a trivial endeavor.

## **CONCLUSION**

Convergent evidence from behavior, neuropsychology, and neuroimaging suggest that humans use knowledge about space to scaffold mental representations of abstract information. Whereas most investigations have focused on non-social domains of abstract cognition, less work has explored the relationship between abstract aspects of social cognition (e.g., social distance evaluation, mentalizing) and spatial perception. Given the substantial progress that has stemmed from using this approach to characterize the mechanisms that support non-social domains of abstract cognition, we predict that relating abstract social cognition to spatial perception will be similarly fruitful. Further, given the centrality of sociality to human health and brain evolution (Dunbar, 1998), better understanding the mechanisms involved in social cognition is essential to understanding the human brain more generally.

group size: computational evidence for the cognitive costs of sociality. *Proc. Biol. Sci.* 280, 20131151. doi: 10.1098/rspb.2013.1151

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Rizzolatti (Cambridge: MIT Press), 253–272.

overlapping functional activations. *Trends Cogn. Sci.* 11, 4–5. doi: 10.1016/j.tics.2006.10.009

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monkeys and humans using surfacebased atlases. *Vis. Res.* 41, 1359– 1378. doi: 10.1016/S0042-6989(01) 00045-1

to unidimensional odor objects. *Annu. Rev. Psychol.* 61, 219–241. doi: 10.1146/annurev.psych.60.110707. 163639

**Conflict of Interest Statement:** The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

*Received: 15 July 2013; accepted: 17 September 2013; published online: 08 October 2013.*

*Citation: Parkinson C and Wheatley T (2013) Old cortex, new contexts: re-purposing spatial perception for social cognition. Front. Hum. Neurosci. 7:645. doi: 10.3389/fnhum.2013.00645*

*This article was submitted to the journal Frontiers in Human Neuroscience.*

*Copyright © 2013 Parkinson and Wheatley. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.*

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## Common brain areas engaged in false belief reasoning and visual perspective taking: a meta-analysis of functional brain imaging studies

## *Matthias Schurz 1,2\*, Markus Aichhorn1,2, Anna Martin1,2 and Josef Perner 1,2*

*<sup>1</sup> Center for Neurocognitive Research, University of Salzburg, Salzburg, Austria*

*<sup>2</sup> Department of Psychology, University of Salzburg, Salzburg, Austria*

#### *Edited by:*

*Sarah H. Creem-Regehr, University of Utah, USA*

#### *Reviewed by:*

*Christian Sorg, Klinikum rechts der Isar Technische Universität München, Germany Elliot Berkman, University of Oregon, USA*

#### *\*Correspondence:*

*Matthias Schurz, Center for Neurocognitive Research and Department of Psychology, University of Salzburg, Hellbrunnerstr. 34, 5020 Salzburg, Austria e-mail<EMAIL_ADDRESS>
We performed a quantitative meta-analysis of functional neuroimaging studies to identify brain areas which are commonly engaged in social and visuo-spatial perspective taking. Specifically, we compared brain activation for visual-perspective taking to activation for false belief reasoning, which requires awareness of perspective to understand someone's mistaken belief about the world which contrasts with reality. In support of a previous account by Perner and Leekam (2008), our meta-analytic conjunction analysis found common activation for false belief reasoning and visual perspective taking in the left but not the right dorsal temporo-parietal junction (TPJ). This fits with the idea that the left dorsal TPJ is responsible for representing different perspectives in a domain-general fashion. Moreover, our conjunction analysis found activation in the precuneus and the left middle occipital gyrus close to the putative Extrastriate Body Area (EBA). The precuneus is linked to mental-imagery which may aid in the construction of a different perspective. The EBA may be engaged due to imagined body-transformations when another's viewpoint is adopted.

**Keywords: neuroimaging meta-analysis, theory of mind, false belief, visual perspective taking, temporo-parietal junction**

## **INTRODUCTION**

Being able to adopt another person's perspective is an important feature of human social cognition. In the last decade and a half, functional neuroimaging studies have sought to identify the neural mechanisms underlying this ability. Two lines of research have emerged. One group of studies has looked at perspective relevant processes in the context of visuo-spatial cognition, typically by asking about the visual experience arising from a different point of view (visual perspective taking). Studies in this field can be divided into level 1 and 2 visual perspective taking (Masangkay et al., 1974; Flavell et al., 1981). Level 1 perspective taking refers to the ability to distinguish what people can and cannot see, e.g., that two persons looking at different sides of a piece of paper see different things. Level 2 perspective taking refers to the ability to understand that when two persons look at an object from different viewpoints or angles, they arrive at different and maybe contradictory descriptions. Besides research on visual perspective taking, another group of studies has looked at perspective relevant processing in social contexts. The terms "mentalizing", "mind reading" or "theory of mind" refer to our ability to think about the mental states—such as thoughts and beliefs—of ourselves and others (Premack and Woodruff, 1978). A way to test children's ability to attribute mental states to others is the false belief task. Children are told a story in which a character, Mistaken Max, fails to witness how his chocolate is unexpectedly transferred from one location to another. Therefore, he believes that the chocolate is still in its original location. Children have to predict whether he will look for the chocolate in its original or in its new location. To arrive at the correct answer—its original location—children have to take into account that Mistaken Max holds a false belief about the location of the chocolate, which contrasts with their own knowledge about its real location.

Developmental research showed that the ability to make correct level 2 visual perspective judgments emerges about 2 years later than the ability to master these judgments at level 1 (Masangkay et al., 1974). At the same time when children start to master level 2 judgments—at around 4 to 5 years of age—they also start to pass the false belief test (Wimmer and Perner, 1983). Hamilton et al. (2009) found that theory of mind performance (assessed with a set of tasks including the false belief task) significantly predicted performance on a level 2 visual perspective task in a sample of 4–8 year old children. In contrast, neither performance on a mental rotation task nor children's verbal mental age showed a relation to level 2 visual perspective taking. One explanation (e.g., Perner et al., 2003; Perner and Rössler, 2012) for this link between level 2 visual perspective and false belief understanding is that both tasks require an understanding of perspective, i.e., that different persons can have different views on/or beliefs about one and the same state of affairs. In addition, for both tasks children must be able to intentionally switch to another perspective.

Brain activation for false belief reasoning was mostly studied by presenting short stories to adult participants, and results show a consistent network of brain areas activated (see e.g., Saxe and Kanwisher, 2003; Perner et al., 2006; Saxe and Powell, 2006), including the medial prefrontal cortex (mPFC), bilateral temporal poles, the precuneus, and bilateral temporo-parietal junction (TPJ) areas. The mPFC was linked to the processing of socially and emotionally relevant information about other people that is contained in the stories, but not specifically linked to the processing of belief (Aichhorn et al., 2006; Saxe, 2006; Saxe and Powell, 2006). For example, an fMRI study found that the mPFC was equally engaged by stories about a person's thoughts and by stories about a person's physical appearance or bodily sensations (Saxe and Powell, 2006). The temporal poles were linked to the retrieval of social semantic knowledge from long-term memory, which takes place because participants read stories about persons in social situations (e.g., Gallagher and Frith, 2003; Ross and Olson, 2010). Based on its engagement in visuo-spatial mental imagery (e.g., Ghaem et al., 1997; Hanakawa et al., 2003), it was assumed that the precuneus subserves mental imagery to represent another person's perspective in theory of mind tasks (Cavanna and Trimble, 2006). Similarly, the TPJ areas were linked to the representation of mental and non-mental perspectives (Perner et al., 2006; Perner and Leekam, 2008). The right TPJ was specifically linked to the representation of beliefs, as it was found to respond more strongly when reading statements about a person's thoughts than when reading statements about physical appearance or bodily sensations (Saxe and Powell, 2006), and also compared to reading statements about a person's emotions and perceptions (Zaitchik et al., 2010). In another study, an interesting observation was made for the left TPJ. Perner et al. (2006) presented a novel condition—false sign stories—in addition to the standard false belief and photo control stories. An example for a false sign story is: "The sign to the monastery points to the path through the woods. While playing, the children make the sign point to the golf course. According to the sign the monastery is now in the direction of the ... golf course / woods". False sign stories present a very different problem than false belief stories which require figuring out an internal and unobservable mental state of another person. False sign stories simply require reflecting upon the external and directly observable world—the direction to where a sign is pointing. Nevertheless, Perner et al. (2006) found equally high activation for false sign stories as for false belief stories in the left TPJ (but not in the right TPJ). A significantly lower level of activation was found for photo control stories. These findings suggest that the left TPJ is responsible for an operation that is common to reasoning about false belief and false signs: processing of a perspective difference, regardless of whether it is an unobservable inner state (belief) or a visible state (where the sign points). Both in the case of false belief stories and false sign stories, two contrasting perspectives of one and the same state of affairs are involved: the belief of a person that contrasts with one's own knowledge of reality, or the location to which a sign is pointing that contrasts with one's own knowledge about the real location of a target.

In comparison to the detailed picture that has already emerged for the neural correlates of false belief reasoning, brain imaging evidence on visual perspective taking is relatively scattered and has been discussed less extensively. To our knowledge, no systematic review or meta-analysis of visual perspective studies has been done yet. When contrasting judgments about another person's perspective with judgments about one's own perspective (level 1 and 2 taken together) studies mainly found activation in three areas: (i) Lateral prefrontal cortices (e.g., Vogeley et al., 2004; Aichhorn et al., 2006; David et al., 2006, 2008; Dumontheil et al., 2010; Mazzarella et al., 2013), (ii) bilateral parietal and temporoparietal areas (Vogeley et al., 2004; David et al., 2006, 2008; Kaiser et al., 2008; Mazzarella et al., 2013) and (iii) the precuneus (Vogeley et al., 2004; Kaiser et al., 2008; Dumontheil et al., 2010). The lateral prefrontal cortices – in particular the inferior frontal gyri—are engaged by cognitive control in interference tasks, such as the color-word Stroop task or stimulus-response reversal studies (for review see Derrfuss et al., 2005). Likewise, researchers linked these areas to the inhibition of the irrelevant own perspective when making visual perspective judgments (McCleery et al., 2011; Ramsey et al., 2013). Activation in temporo-parietal areas was linked to the representation of perspectives, and in particular to the representation of differences in perspective and ownership of perspective (McCleery et al., 2011). In addition, Ramsey et al. (2013) suggested that superior parietal areas are engaged in perspective selection, i.e., in choosing the relevant over the irrelevant perspective. This was assumed to take place in cooperation with lateral prefrontal areas, forming a functional network that is sometimes referred to as the "fronto-parietal control network" (e.g., Vincent et al., 2008). The precuneus was rarely mentioned when discussing the neurocognitive processes subserving visual perspective taking, although it is implicated in multiple forms of visuo-spatial mental imagery (e.g., Ghaem et al., 1997; Hanakawa et al., 2003).

Our review of the neuroimaging literature on false belief reasoning and visual perspective taking showed that both discussed the left TPJ and the precuneus as candidate areas for representing perspectives and perspective differences. Only little functional imaging research has addressed this connection. To our knowledge, no study has directly compared activation for false belief reasoning to activation for visual perspective taking. Aichhorn et al. (2006) measured brain activation for level 2 visual perspective taking, and asked participants to judge the spatial arrangement of two objects (e.g., "the block is in front of the pole") from the viewpoint of an avatar. The authors found brain activation for level 2 perspective taking—compared to making the same judgments from one's own viewpoint—in an area of the left TPJ that was also activated in a number of earlier studies on theory of mind (e.g., Gallagher et al., 2000; Ruby and Decety, 2003; Saxe and Kanwisher, 2003). Aichhorn et al. (2006) therefore concluded that the left TPJ is responsible for representing different perspectives and is commonly engaged by tasks which require such processing. However, a more recent study provided evidence against this interpretation. David et al. (2008) asked participants to either make a visual perspective or a mentalizing (preference) judgment with respect to two objects in front of an avatar. The avatar was facing participants. In the level 2 perspective judgment, participants were asked which of the two objects (left or right) was elevated from the avatar's point of view. For example, if the elevated object was on the left from the avatar's point of view, this implied that it was shown on the right side of the image to participants. In the preference judgment, participants were asked to judge which object the avatar would prefer—based on his gestures (e.g., pointing at one object) and facial expression. During the judgments participants always indicated the object as seen from their own perspective. The comparison of brain activation between the tasks showed two completely distinct networks of brain activation and no overlap in the left TPJ. Therefore, David et al. (2008) concluded that visual perspective taking and mentalizing rely on different cortical mechanisms.

Studies that compared brain activation for visual perspective taking and mentalizing show contradictory results. However, these studies never directly compared activation for false belief reasoning with visual perspective taking. As we have outlined above, both developmental research and neurocognitive theories speak for a functional link between these tasks. The present study evaluates the functional overlap between false belief reasoning and visual perspective taking by means of a quantitative metaanalysis of brain imaging studies. To increase statistical power, we analyze both level 1 and 2 visual perspective taking studies in our meta-analysis. Based on the reviewed literature, we expect to find a functional overlap in the left TPJ and in the precuneus.

## **METHODS**

We performed key-word searches in the databases PubMed, Science Citation Index, and PsycInfo. The first criterion of our search was that studies included one of the key-words "neuroimaging" or "fMRI" or "PET". For our false belief metaanalysis, the second criterion was that studies further included the key-words "false belief" or "theory of mind". For our visual perspective taking meta-analysis, the second criterion was that studies included the key-words "perspective taking" or "visual perspective" or "viewer rotation"<sup>1</sup> . In a second step, we extended our literature samples by searching the reference lists of recent meta-analyses on theory of mind and social cognition (Mar, 2011; Bzdok et al., 2012; Denny et al., 2012; Murray et al., 2012) as well as the reference lists of most recent publications on visual perspective taking (Lambrey et al., 2012; Mazzarella et al., 2013; Ramsey et al., 2013).

We then applied a number of methodological selection-criteria to the literature identified by our search (see e.g., Radua et al., 2012). Studies were only selected if they had performed a whole brain analysis and reported activation coordinates in standard space (MNI or Talairach). We ensured that the same threshold throughout the whole brain was used within each included study, in order to avoid biases toward liberally thresholded brain regions. This does not mean that different studies should employ the same threshold. We included 25 studies (*N* = 419) in our meta-analysis on false belief and 14 studies (*N* = 216) in our meta-analysis on visual perspective taking. We used Effect-Size Signed Differential Mapping (ES-SDM) software, version 2.31 for meta-analysis (Radua et al., 2010, 2012; http://www.sdmproject.com). ES-SDM uses standard effect size and variance-based meta-analytic calculations. Based on the reported *t*-values and the sample size of a study, ES-SDM creates a map of effect-sizes (Hedge's *g* values) and their variances. Variance is estimated from the map of effect-sizes and the sample size of the study. Effect- sizes are exactly calculated for those voxels containing a peak reported in the results table of an original study. For the rest of the voxels, an effect-size is estimated depending on the distance to close peaks (<20 mm) by means of an unnormalized Gaussian kernel. In the present analysis, we used the recommended Gaussian kernel with a FWHM of 20 mm. A validation study which compared the results of coordinate based ES-SDM meta-analysis to the results of a standard voxel-wise GLM analysis of the same original data (Radua et al., 2012) found that this FWHM provided an optimal balance between sensitivity and specificity. For statistical-analysis, all foci were transformed to Talairach space which is the native space of the software, by using the matrix transformations proposed by Lancaster et al. (2007). We calculated a mean analysis for each task-group. Calculation of the meta-analytic mean map is implemented by a random-effects model in which each study is weighted by the inverse of the sum of its variance plus an estimate of between-study heterogeneity. The latter is obtained by the DerSimonian-Laird method (DerSimonian and Laird, 1986). This approach enables studies with larger sample size or lower variability to contribute more and that effects are assumed to randomly vary between samples. The statistical significance was assessed by a permutation test; 100 random maps were generated with the same number of input foci as included in the to-be-tested map (see Radua et al., 2012). Finally, the meta-analytic maps were thresholded using a voxel-level (height) threshold of *p* < 0.005 (uncorrected) and a cluster-level (extent) threshold of 10 voxels. This uncorrected threshold was found to optimally balance sensitivity and specificity, and to be an approximate equivalent to a corrected threshold of *p* < 0.05 in original neuroimaging studies (Radua et al., 2012). We performed a conjunction analysis (see **Figure 1B**) with the "image calculator" utility in SPM8 (www.fil.ion.ucl.ac.uk). Conjoint activation is determined by a voxel-wise combination of results by a logical AND function. For convenience, we report all activations in MNI-space.

#### **RESULTS**

#### **FALSE BELIEF REASONING**

Studies on false-belief reasoning mainly used two types of tasks. One group of studies contrasted stories about false belief with stories about an outdated photograph. We give some examples in **Table 1**. In total, we found 15 studies (reported in 14 publications) that relied on this type of contrast (Saxe and Kanwisher, 2003; Saxe and Wexler, 2005; Perner et al., 2006; Saxe and Powell, 2006; Saxe et al., 2006; Young et al., 2007, 2010, 2011; Kliemann et al., 2008; Mitchell, 2008; Aichhorn et al., 2009; Young and Saxe, 2009; Dodell-Feder et al., 2011; Lee et al., 2011). In the false belief story a short text passage is presented, which involves a person holding a false belief. A test question asks participants about the belief or its behavioral consequences. In the control task, a short text passage describes a photograph (or a similar physical representation) of the past, together with a note about how things shown on the photograph have changed by now. Participants are asked what is shown on the photo. Another more heterogeneous group of studies presented similar stories about false belief. In this group of studies, however, stories of different length and richness were presented, and different types of control stories were used.

<sup>1</sup>Viewer rotation' refers to an imagined change of one's own point of view, i.e., imagining oneself rotating around an object in space, arriving at a new viewpoint on it.

We give some examples for false belief studies of our second group in the lower part of **Table 1**. The common element of these studies is that they present a story (sentence or cartoon format) about a person that holds a false belief as activation tasks. Participants are asked a question which relates to the false belief of the person. In the control condition, again a story about a person is presented, but here the person does not hold a false belief. Participants are asked about non-mental state information in the story.  We pooled the two groups of tasks that present stories about false belief into one single meta-analysis (total *n* = 25).

We performed a meta-analysis on the reported activation maps for the contrast false belief stories > control stories. Results are shown in blue in **Figure 1A** and are listed in **Table 2**. The largest cluster of meta-analytic convergence was found in the mPFC, including parts of dorsal and ventral mPFC and the anterior cingulate gyrus. Another large cluster of convergence was found in precuneus and posterior cingulate gyrus bilaterally. Further clusters of convergent activation were found in bilateral temporoparietal areas, spanning across parts of middle and superior temporal gyri up to the inferior parietal lobule (up to *z* = 42). Two smaller clusters of convergence were found in anterior parts of the right temporal lobe.

#### **VISUAL PERSPECTIVE TAKING**

Compared to the large number of imaging studies on false belief reasoning, relatively few imaging studies on visual perspective taking exist. We identified three groups of visual perspective tasks in the literature: level 1 visual perspective taking (3 studies), level 2 visual perspective taking (5 studies), and level 2 imagined viewer rotation (6 studies). Due to the small sample-sizes of these taskgroups, it was not possible to perform individual meta-analyses. We therefore decided to merge the different visual perspective tasks into a pooled analysis, which gave us a large enough sample for quantitative meta-analytic calculations (*n* = 14). Later on (see section Region of interest based review), we provide a complementary results overview for individual task-types.

**Table 3** gives task-descriptions for all visual-perspective taking studies in our meta-analysis. Level 1 visual perspective taking studies typically present a scene with an avatar and a number of objects. Participants are asked how many of these objects the avatar can see (while some of the objects are behind the avatars' back). In the control conditions of level 1 visual perspective taking studies, participants are asked how many objects they can see themselves <sup>2</sup> . Level 2 visual perspective taking tasks also typically present a scene with an avatar and a number of objects. However, here the avatar is able to see all of the objects in the

<sup>2</sup>A recent level 1 visual perspective taking study (Ramsey et al., 2013) did not look at the contrast other > self, but at interactions between perspective taking (self vs. other) and the consistency of perspectives (i.e., do self and other perspectives differ in the task-response that they require?). Ramsey et al.'s (2013) results show that the consistency between perspectives is an important and previously ignored determinant of brain activation. However, these data go beyond the scope of the present meta-analysis and cannot be synthesized with results from other studies in our meta-analysis. Therefore, we did not include Ramsey et al.'s (2013) study in our analysis.

#### **Table 1 | Examples for false belief reasoning tasks.**

scene, but views them from a different angle. Participants are asked to indicate the relative position of one object from the avatar's viewpoint. In the control condition of level 2 visual perspective tasks, participants are asked about the relative location of one object from their own perspective. The last type of visualperspective taking tasks in our meta-analysis, level 2 imagined viewer rotation tasks, typically present an array of objects and ask to imagine viewing this array from a different angle. Then, participants are asked to indicate the relative position of one object from the imagined viewpoint. Two types of control tasks are frequently used in studies on imagined viewer rotation. In one type of control task, participants have to indicate the relative position of one object in the array as seen from their actual viewpoint (similar to the control conditions in level 2 visual perspective taking tasks). In another type of control task, a so-called object rotation task, participants are asked to imagine rotating the array around its vertical axis (e.g., with their right hand), and then indicate the current position of one object from their viewpoint.

We performed a meta-analysis on the reported activations for all three types of visual perspective taking compared to their respective control condition. **Figure 1A** shows clusters of reliable meta-analytic convergence for visual perspective taking in red, and results are listed in **Table 2**. The largest cluster of convergent activation was found in the left lateral prefrontal cortex, with its

#### **Table 2 | Results of meta-analyses for False Belief Reasoning and Visual Perspective Taking.**

peak in the left middle frontal gyrus. The cluster further included parts of the inferior frontal gyrus, the insula and the precentral gyrus. In the right hemisphere, lateral prefrontal activation was substantially smaller compared to the left. Two small clusters of activation were found, located in the right precentral gyrus and right insula. Larger clusters were found in the left inferior parietal lobule and in the precuneus. The left inferior parietal cluster included parts of the angular gyrus and the posterior middle temporal gyrus. The precuneus cluster spanned both hemispheres. In addition to the left inferior parietal area, two other clusters of convergence were found in left temporo-parietal areas. One was located in the left posterior middle temporal gyrus extending into

**Table 3 | ROI-based follow-up review: + signs denote that a study reported activation within 20 mm distance to a peak of our meta-analytic conjunction (20 mm corresponds to the smoothness of meta-analysis).**

*(Continued)*

**Table 3 | Continued**

*PREC* ... *Precuneus x* = *0, y* = −*53, z* = *52; ANG* ... *Angular Gyrus x* = −*41, y* = −*59, z* = *42; OCC* ... *Middle Occipital Gyrus x* = −*49, y* = −*72, z* = *13;*

*\*Dumontheil et al.'s (2010) study could also be classified as a level 2 perspective task. The picture stimuli used in the task show a level 1 perspective difference. However, the task also presents statements (e.g., "move the large ball up") that have to be interpreted from another person's perspective. A correct interpretation requires understanding that the other person has a different perspective of the entire scene (from his perspective, one particular ball is the largest of all, whereas from one's own point of view, another ball is the largest of all).*

the superior occipital gyrus; the other located in the left inferior and middle occipital gyri, near the location of the Extrastriate Body Area (EBA, Downing et al., 2001). Finally, a cluster of convergent activation was found in the left cerebellum (not visible in **Figure 1A** because of its location buried underneath the cerebellar surface).

#### **CONJUNCTION ANALYSIS**

Our conjunction analysis determined which brain areas showed convergent activation for both false belief reasoning and visual perspective taking. Results are listed in **Table 2** and illustrated in **Figure 1B**. The largest areas of convergence for both meta-analyses were found in bilateral precuneus, with a slightly larger cluster in the left compared to the right precuneus. Further conjoined clusters of convergence were found in the left TPJ (angular gyrus and the posterior middle temporal gyrus) and the left middle occipital gyrus corresponding to the EBA.

#### **REGION OF INTEREST BASED REVIEW**

We followed-up the findings of our meta-analytic conjunction by a region of interest (ROI) based review. This approach does not include a statistical comparison. However, it gives an overview of which visual perspective taking studies contributed to the metaanalytic findings. We selected three peaks from our meta-analytic conjunction as ROIs: precuneus (*x* = 0, *y* = −53, *z* = 52), left dorsal TPJ/angular gyrus (*x* = −41, *y* = −59, *z* = 42) and left middle occipital gyrus (*x* = −49, *y* = −72, *z* = 13). ROIs were created by a 20 mm spherical volume around the peak coordinates. This radius corresponds to the size of the smoothing (FWHM) used by our meta-analysis. The other peaks from our conjunction analysis (left posterior middle temporal gyrus, right precuneus) did not enter our ROI analysis because they were located at too close distance to the three other ROIs, and were therefore practically not separable from them.

For each study, we checked if any of the reported activation coordinates fell within the 20 mm sphere around the three peak coordinates in the left precuneus, the left angular gyrus, and the left middle occipital gyrus. **Table 3** summarizes the results of this review. It lists each study and indicates with a '+' symbol if a study reported activation within a ROI. Contributions to the metaanalytic peak activation in the left angular gyrus were balanced over the three types of visual perspective taking: level 1 visual perspective (2/3 studies), level 2 visual perspective (3/5 studies), and level 2 viewer rotation (2/6 studies). Contributions to the peak activation in the left middle occipital gyrus were relatively weak for level 1 visual perspective (1/3 studies) and level 2 visual perspective (1/5 studies), but more substantial for level 2 viewer rotation (4/6 studies). Contributions to the meta-analytic peak in the left precuneus were relatively strong for level 1 visual perspective (3/3 studies), moderate for 2 viewer rotation (3/6 studies), and completely absent for level 2 visual perspective (0/5 studies).

## **DISCUSSION**

We meta-analyzed brain activation for false-belief reasoning and visual perspective taking and looked for common brain areas engaged by these tasks with a conjunction analysis. We expected to find common activation in the left TPJ, based on our hypothesis that this area is implicated in processing perspective differences (Perner and Leekam, 2008). Our results confirm this expectation, as we found two clusters in the dorsal left TPJ (angular gyrus and posterior middle temporal gyrus) that were reliably engaged both in false belief and in visual perspective processing. In addition to these clusters, our meta-analysis revealed common areas in the left middle occipital gyrus and in the precuneus for false belief reasoning and visual perspective taking. In the next sections, we will discuss the potential functional roles of these locations of convergent brain activation.

#### **LEFT TEMPORO-PARIETAL JUNCTION**

Our meta-analytic conjunction found two clusters of conjoint activation for visual perspective taking and false belief reasoning in the left dorsal TPJ, one in the angular gyrus at *z* = 42 and another one in the left posterior middle temporal gyrus at *z* = 32. No overlap in activation was found for right TPJ areas. These findings support the functional account of TPJ areas reviewed in our introduction (Perner et al., 2006; Perner and Leekam, 2008). In this view, the right TPJ is mostly responsible for belief-desire reasoning. Accordingly, our meta-analysis found activation only for false belief reasoning here, and no activation for visual perspective taking. The left TPJ, on the other hand, is thought to be involved in processing of alternative perspectives in a domain-general way. In support of this idea, we found an overlap in brain activation between visual perspective taking and false belief reasoning here.