Allow me to begin with an anecdote. Flirt was one of the chimpanzees who I observed during my study of chimpanzees at Gombe National Park. During this time, Flirt had the habit of sneaking up behind me and another researcher, and very quietly trying to grab our hands. She was successful only once; completely surprising me, she managed to grab my hand. I knew this was wrong and let her hand go. As part of the protocol at Gombe, humans must always maintain a distance of at least 10 meters from the chimps and never physically interact with them, for health and safety reasons. However, I really enjoyed that stolen moment of holding Flirt’s hand.
This episode has remained in my memory for all these years, but it is only now that I am starting to understand its significance. There is something important about the way human primates use touch in social encounters; for example, consider greetings in airports (hugs vs. handshakes) and the way children push each other in a playground (a quick push to warn, a really hard one when it is serious!). Human primates use touch as a way of conveying a wide range of social information. In this chapter, I will argue that one of the best ways of understanding social cognition in nonhuman primates is through touch. Moreover, I will argue that if we would like to describe the evolutionary history of social cognition, touch is one of the ideal modes to operationalize social interaction across different kinds of primates. Flirt wanted to hold my hand and I understood perfectly well what that meant, because touch is the social language spoken among primates.
In their seminal paper, Scaife and Bruner (1975) designed an experiment examining mother-infant face-to-face social interactions in which the parent attempted to elicit gaze-following by turning her head. Because infants between 2–14 months old did follow their parents’ gaze, the authors interpreted their results as evidence that infants are capable of joint attention. Since then, joint-attention studies have focused on triadic interactions between two individuals who alternate their attention between an object in the environment that the partner is also looking at, and their partner. The way this triadic interaction takes place has been interpreted in different ways; however, one common element in the interpretations is that joint visual attention provides a context in which infants can acquire information about objects and about their social partners (MacPherson and Moore 2007). Researchers also use gaze-following as a way to operationalize joint attention in testing whether chimpanzees are capable of joint attention (see Tomasello, Carpenter, and Hobson 2005, for example).
Gaze-following has also been used to operationalize experiments in theory of mind. From the beginning, theory of mind has been defined as the ability to attribute mental states such as beliefs, intent and desires (among other mental states) to oneself and to others, and as the capacity to understand that others may have mental states and perspectives different from your own (Premack and Woodruff 1978). In chimpanzees, the majority of the research has focused on theory of mind in terms of vision; these experimental protocols test whether chimpanzees know what others have seen (or not), and whether this is an indication that they have some form of theory of mind (see Rosati, Santos, and Hare 2010 for a review).
Moreover, gaze-following has been used to understand certain disorders that limit the interactional capabilities of individuals, such as autism. For example, in his highly influential book Mindblindness, Baron-Cohen writes: “When I step back from the model of the mind reading system that I have proposed, EDD (Eye Direction-Detector) seems to stand out” (1995: 97).
The prevalence of using visual modes in the study of social cognition is also present in the study of emotions in primates. Most of the authors who adopt a basic approach to emotions argue for the existence of a basic set of discrete emotions or of families of emotions that is the product of evolution, and present in both human and nonhuman primates (see Tracy and Randles 2011 for a review). One of the most influential ways in which basic emotions have been studied is through the Facial Action Coding System (FACS) (Ekman and Friesen 1978); in this system, facial expressions are divided into segments, and specific configurations of these facial segments are identified with each basic emotion. This scoring system has been successfully applied to nonhuman primates. For example, in humans, great apes and monkeys, researchers have applied FACS to study the relationship between facial expression and taste (Steiner, Glaser, Hawilo, and Berridge 2001 in humans, chimpanzees, orangutans, gorillas, New World monkeys and Old World monkeys; Ueno, Ueno, and Tomonaga 2004 in macaques and chimpanzees). Preuschoft and van Hooff (1995) used FACS to study homology between the chimpanzee bared-teeth display and the human smile. Parr and colleagues (Vick et.al. 2007) created the Chimpanzee Facial Action Coding System (ChimpFACS), based on Ekman’s FACS, and have used it to validate the existing categories of facial expressions of chimpanzees (Waller et al. 2007). Caeiro and colleagues (2013) designed OrangFACS to study facial expressions in orangutans.
We see that the visual mode of interaction has been prevalent and highly successful as a way of operationalizing social cognition. The adoption of the visual mode has allowed us to understand many aspects of social cognition in primates; however, I believe that it is necessary to take a further step, recognize the limitations of the visual mode in understanding social cognition, and include other modes, such as touch.
It is problematic to use gaze-following as a paradigm of social cognition because using the visual mode to operationalize interaction limits our understanding to a single modality. For example, it would be impossible to even consider joint attention among blind individuals using this model. In the past, it was thought that blind children had severe deficits similar to those children in the Autism Spectrum Disorder (ASD). According to Bigelow (2003), research in these infants demonstrates that vision is not necessary for joint attention. Clearly these infants experience challenges in their development, such as understanding the spatial properties of objects, and as a result they experience delays when compared to other infants. However, throughout alternative modes of interaction (i.e. tactile and auditory) with their caregivers, these infants develop the same cognitive abilities as infants with vision, in particular joint attention (see Perez-Pereira and Conti-Ramsden 2013 for review). This example shows that if we are willing to shift modes of interaction, it is possible to understand how children who do not achieve milestones in the traditional way can achieve similar cognitive skills (in particular social referring) when compared to infants who follow a more traditional developmental path.
A second example can be found in studies of Theory of Mind in non-human primates. Researchers of social cognition in apes debate whether the experimental evidence on the knowledge that animals have about what others have seen (or not seen) shows that animals posses theory of mind (see Martin and Santos 2016 for a summary of this debate; and Lurz and Halina, Chapters 21 and 22, respectively, in this volume). Gaze also plays an important role in the debate about whether apes posses joint attention. For example, Carpenter and Call (2013) suggest that apes lack joint attention, and they criticize the way that intention behind an ape’s gaze-following behavior has been interpreted in other joint-attention studies (Gomez 2010). I think that this lack of agreement stems from the limitations of what we can learn from vision in apes. Researchers are setting themselves to fail if they look for social cognition in a modality in which the species doesn’t demonstrate social cognition, in the same way researchers were set to failure when looking for social cognition in visually impaired children using visual paradigms.
Why think that vision isn’t the modality that best demonstrates social cognitive capacities in great apes? Consider how wild apes live. While it is true that in the wild, mother and infant chimpanzees will gaze at each other (van Lawick-Goodall 1967), they rarely use prolonged gaze as a form of interaction (personal observation; for a similar finding in monkeys, see Perry and Manson 2008). Shortly after giving birth, chimpanzee mothers pay little visual attention to their babies except when they are grooming and cleaning them (Plooij 1984). Later in development, mothers are observed to “caress” their infants, by either gently stroking their fur or making grooming movements while gazing upon their babies. However, there are no reports of prolonged mutual gaze between mother and infant (van Lawick-Goodall 1967). The infants don’t appear to be interested in the mother’s face until around nine weeks of age (Plooij 1984), and it isn’t until the infant is four months old that the infant starts focusing on the mother’s face in communicative situations, such as begging for food. Before four months, chimpanzee infants typically take food from their mothers without looking at them (Plooij 1984).
These reports on wild populations seem to contradict observations of populations in captivity (Tomonaga et al. 2004). I would join others (Russell, Bard, and Adamson 1997) in arguing that the interactions between the human caregiver and the infant ape can modify the emergence of abilities in the social cognition of the ape, resulting in an inadequate model for understanding species-typical behavior in wild populations; mothers in the wild do not engage in the same kinds of behaviors as mothers in captivity, so the zone of proximal development is different in wild and captive apes. Moreover, the ecological conditions of captivity also influence the way mother and infant pairs interact. For example, Tomonaga and colleagues (2004)1 report that, during the first two months in the lives of the infants, three mother-infant pairs were observed increasing their engagement in mutual gaze, and that this increase in mutual gaze corresponded to a decrease in cradling behavior by the mothers. Tomonaga and colleagues conclude that the frequency of mutual gaze is negatively correlated with the frequency of physical contact between mother and infant. In contrast to mothers in the safe environment offered by captivity, it has been reported that mothers in the wild carry infants constantly from shortly after birth until the infants are three months old (van Lawick-Goodall 1967; Plooij 1984). According to Goodall (van Lawick-Goodall 1967), during the first months of life, the infant is protected from almost all contact with other individuals. This behavior is the mother’s response to the environmental conditions to which mothers and infants are exposed during the first months of the infant’s life; at this stage, the infant has to remain in constant physical contact with the mother because s/he is at constant risk of being killed by males during aggressive displays, by predators, and by attacks from other females. Thus, we should exercise caution when attempting to extrapolate observations done in captivity to general claims about the behavior of a species in the wild.
Finally, focusing on gaze as the modality through which researchers understand social cognition has similar consequences in the study of basic emotions in apes. One of the main problems when applying FACS to understand basic emotions in chimpanzees is that, even though chimpanzees and humans share much of the same facial musculature (Waller et. al. 2007), chimpanzees do not share some of the facial features that allow humans to easily detect facial expressions: because of skin pigmentation, reduced outer lip vermillion, and eye morphology, the chimpanzee face, unlike the human face, does not offer a salient contrast that facilitates the detection of facial movement (Vick et al. 2007). Thus, given the behavioral and morphological characteristics of apes, when researchers focus on vision to study theory of mind, joint attention and basic emotions, they are limiting what they can learn about social cognition.
There is growing evidence that touch plays an important role in human social cognition. It has been shown that touch, in the form of grooming, has effects in social interactions and social bonds (see, for example, Dunbar 1996; de Waal 1990). However, touch can be used in more complex ways in the development of social cognition in infant primates. The interaction that the human and nonhuman primate infant experiences from birth is one of the earliest modes of interaction that allows the infant to start understanding the kinds of interaction involved in social cognition.
To understand how touch is fundamental for the development of social cognition, it is necessary to understand that there are two different kinds of neurophysiological processes behind touch in humans: emotional (affective) and discriminative (sensory), depending on the site of the touch (Olausson et al. 2010). Hairy skin, such as on the arm, contains C-tactile (CT) afferents, which are fundamental for affective touch; CT afferents give rise to the pleasurable feelings experienced in interpersonal touch. Meanwhile, glabrous skin, such as in the palm of the hand, does not contain CT afferents and is linked to discriminative touch; glabrous skin is responsible for detecting, discriminating and identifying external stimuli that will serve as a guide for behavior. As a result, depending on the site, touch is experienced in different ways by humans. Moreover, these neurophysiological characteristics are shared among different species. Human CT afferents and animal C-fiber low-threshold mechanoreceptors (CLTMs) are both afferent types and are only found in hairy skin, in mice, cats and non-human primates (Nordin 1990; Vrontou et al. 2013).
To fully understand the role played by touch in social cognition, it is helpful to focus on affective touch perceived through CT afferents. Several authors (McGlone et al. 2007; Loken et al. 2009) have argued that CT afferents play an important role in the affective processing of interpersonal touch. Olausson and colleagues (2010) have developed the “affect touch hypothesis,” which predicts that the role of the CT system is to provide pleasurable feelings and increase the disposition to seek close contact with others. The function of this kind of touch is to serve as the foundation of affiliative behavior, provide a mechanism for the formation and maintenance of social bonds, and become a nonverbal means of communication of emotions (Morrison et al. 2011).
As evident in the ineffectuality of attempting to give oneself a hug, it is important to notice that this affective aspect of touch is mostly manifested in interpersonal touch. Ackerley et al. (2014) found that the touch of another is given higher positive emotional rating than self-touch. Furthermore, Gentsch and colleagues (2015) found that active stroking elicits more pleasure when this kind of touch is given to another than when it is given to one’s own skin. Participants in this experiment also judged the skin of another softer than their own. This “social softness illusion” appeared when the neurophysiological system for touch (i.e. CT afferents) was activated in the receiver. Given this evidence, the researchers suggest that touch is a mechanism for social bonding and affiliation.
In summary, these studies indicate that touch, specifically touch experienced through CT afferents, is a characteristic among different species that allows organisms to perceive that there are “others” who are different from them and to become affectively bonded to those others. Thus, the neurophysiology of touch suggests that, when infants experience touch from a young age, they can understand that there are others, social partners, different from themselves – and they can learn that it is pleasant to engage with these others. As a result, the infant has, through the mode of touch, the first motivation to engage with others in social interactions.
An example of this kind of interaction through touch in human primates is the pattern of communication found in breast feeding. Kaye (1982) describes how newborn infants stop sucking, even when they are not full or when the milk has not stopped flowing, and how human mothers across cultures respond by jiggling their infants after they have stopped sucking the mother’s breast or a bottle. This is the first instance of turn-taking that functions as a “conversation”; the infant “brings in” the mother when they pause, and the mother responds by jiggling in ways that adopt to the patterns of the individual infant.
Even though, to my knowledge, there are no equivalent studies of this kind of pattern in chimpanzees in wild populations, Goodall’s (1967) observations of mother-infant interaction suggest a similar pattern of mother-infant communication based on touch. According to Goodall, from the moment of birth through the infant’s first days of life, the mother’s hands and thighs support the infant almost continually. When the mother walks, she constantly keeps one hand under her baby’s back and shoulders, rounding her own back. After these initial days, during the first few weeks, the mother gradually supports her infant less frequently. The infant will continue to ride on the mother’s chest for the first 6–9 months, gripping her hair with flexed fingers and toes. Because of this, Goodall argues that in the first few months of a chimpanzee infant’s life, tactile signals play a major role in mother-infant coordination. The pressure of the infant’s body against the body of the mother and the intensity of “hair pull,” where the infant grasps the mother’s hair with their hands and feet, together with changes of intensity in either of these stimulations, function as signals. At the same time, the infant can perceive through touch (for example, through piloerection (when the hair stands on end) and elevated heartbeat the mother’s responses to the infant and the world.
The interaction that takes place between caregivers and young infants through the mode of touch opens the door for the infant’s development of social cognition in several ways: it can serve to communicate to young infants that there is an other, and that this other has a perspective that is different from the infant’s (a basic trait of joint attention and theory of mind); and it is a method for learning how to self-regulate one’s own emotions.
First, touch can convey that the perspective of a caregiver is different from the perspective of the infant. Hertenstein (2002) argues that tactile communication takes place when “there are systematic changes in another’s perceptions, thoughts, feelings, and/or behavior as a function of another’s touch in relation to the context in which it occurs” (2002: 72). He argues that touch may transmit the caregiver’s perceptions, thoughts and feelings to the infant (in a conscious or unconscious way), and that it is possible that the caregiver’s experience is transmitted to the infant without being generated in the infant. For example, Hertenstein asks us to imagine what is unconsciously transmitted through touch by a parent who had a stressful day, changing an infant’s diaper. Moreover, it is possible that the infant may perceive this stress but does not become stressed herself. Thus, through touch, primate infants can start understanding that there are others and that these others have a different perspective, two basic traits of joint attention and theory of mind (see Botero 2016 for how touch can be used to investigate joint attention in primates).
It may be argued that this kind of interaction can be characterized as the caregiver eliciting an emotion in the infant, but no actual information is transmitted through touch. However, according to Tronick (1995), tactile communication can transmit specific information to the infant, information such as the presence or absence of a caregiver and the identity of the person who touches the infant, through different types of touch; and according to Hertenstein and colleagues (2009), through touch, individuals can communicate eight distinct emotions (i.e. anger, fear, disgust, love, gratitude, sympathy, happiness and sadness).
Second, I believe that touch as a mode of interaction should be included in the study of social cognition because touch allows primates to learn how to regulate their emotions, and this regulation allows infants to be calm enough to pay attention to the world around them, including their social partners. Touch has a soothing effect that is so powerful that it may be used to overcome psychologically or physically stressful conditions in nonhuman primates. For example, in Harlow’s early studies, it was clear that primates, and in particular infants, had a preference for “touch” in the form of a “cloth-mother” (Harlow and Zimmerman 1959). Mason and Berkson (1962) showed that chimpanzee infants who received electric shocks emitted fewer stress vocalizations when held by humans than when left by themselves on a table, and exhibited higher thresholds before vocalizing when held by a human than when left alone on a table. It has been shown that among wild chimpanzees, the absence of the mother, who provides most of the touch to the infant, has profound effects on the infant’s social behavior and levels of anxiety (Botero et al. 2013).
Studies have shown that the touch provided by the caregiver to human primate infants has an effect on an infant’s levels of comfort, learning, exploration and attachment, and on the amount of crying or fussing (for a review on the effects of touch for well-being, see Field 2011). Moreover, human infants also use touch as a way to regulate their emotions in various contexts, such as maternal unavailability and exploration of new environments (Stack 2011). The interaction through the mode of touch allows infants to be calm enough and to engage in social exchanges.
These findings suggest that focusing on touch as a mode of interaction has two advantages in the study of social cognition in primates. First, non-glabrous touch is a mode that does not require use of the mode of vision or of highly visible and distinctive facial features, which means that touch is a mode that can be used easily by nonhuman primates. Second, touch is a mode that is used in affective exchanges where, given its pleasurable nature, it provides the organism with the motivation to engage with others. Third, a focus on touch allows us to study the development of social cognition in very young infants; that is, observing the caregiver-infant interaction through the mode of touch allows us to observe one of the first ways in which the infant is introduced to social cognition. In recent years, several measurements have been designed to capture the qualitative and quantitative aspects of touch in human primates (for an overview, see Brown et al. 2011). I hypothesize that these measurements could be adapted to the study of these forms of social cognition across nonhuman primates (see Botero 2014 for a discussion).
Most of the current research on social cognition in human and nonhuman primates has focused on vision as a way of operationalizing social cognition. I argue that to study social cognition across different kinds of primates, we should include touch as a mode of interaction. This mode will allow us to understand cognition in younger infant primates and will allow us to operationalize social cognition in nonhuman primates. Moreover, through touch, we can learn how nonhuman primates form and maintain social bonds in ways that correspond to their morphological and behavioral characteristics. In short, by focusing on touch, we can learn how social cognition emerges in nonhuman primates.
1 I would like to note that among various research projects on ape development, one of the most interesting methodological designs is the one developed by Tomonaga and colleagues at the Primate Research Institute (PRI) of Kyoto University, where researchers engage in longitudinal studies, attempting to emulate as closely as possible naturalistic conditions in order to follow the development of three infant chimpanzees born at PRI. For example, as opposed to other research sites, each of the mothers at PRI successfully held her baby and did not have to be separated from her baby (for the baby’s protection), as is common in captive settings. However, despite these advances, the difference between wild populations and captive population must be kept in mind.
Field, T. M. (1995). Touch in early development. Hoboken: Taylor and Francis, provides a multidisciplinary approach to the role played by touch in the development of human and nonhuman primates. Hertenstein, M.J., and Weiss, S. J. (2011). The Handbook of touch: Neuroscience, behavioral, and health perspectives. New York: Springer, is a good introduction to the variety of approaches and methodologies currently used in the study of touch. Flom, R., Lee, K., and Muir, D. (2007). Gaze-following: Its development and significance. Mahwah, NJ: Lawrence Erlbaum Associates, provides an insightful overview of the role that gaze has played in the study of social cognition. Finally, Tomasello, M. (2014). A natural history of human thinking. Cambridge, MA: Harvard University Press, presents a carefully and comprehensive account of the evolution of social cognition that emphasizes the differences between apes and humans.
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