Development and aging

The evolutionary origins of natural pedagogy: Rhesus monkeys show sustained attention following nonsocial cues versus social communicative signals

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Bettle, R. & Rosati, A.G. (2020). The evolutionary origins of natural pedagogy: Rhesus monkeys show sustained attention following nonsocial cues versus social communicative signals. Developmental Science.

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The natural pedagogy hypothesis proposes that human infants preferentially attend to communicative signals from others, facilitating rapid cultural learning. In this view, sensitivity to such signals are a uniquely human adaptation and as such nonhuman animals should not produce or utilize these communicative signals. We test these evolutionary predictions by examining sensitivity to communicative cues in 206 rhesus monkeys (Macaca mulatta) using an expectancy looking time task modeled on prior work with infants. Monkeys observed a human actor who either made eye contact and vocalized to the monkey (social cue), or waved a fruit in front of her face and produced a tapping sound (nonsocial cue). The actor then either looked at an object (referential look) or looked towards empty space (look away). We found that, unlike human infants in analogous situations, rhesus monkeys looked longer at events following nonsocial cues, regardless of the demonstrator’s subsequent looking behavior. Moreover, younger and older monkeys showed similar patterns of responses across development. These results provide support for the natural pedagogy hypothesis, while also highlighting evolutionary changes in human sensitivity to communicative signals.

Heterochrony in chimpanzee and bonobo spatial memory development

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Rosati, A.G. (2019). Heterochrony in chimpanzee and bonobo spatial memory development. American Journal of Physical Anthropology, 169: 302-321.

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Objectives: The emergence of human-unique cognitive abilities has been linked to our species’ extended juvenile period. Comparisons of cognitive development across species can provide new insights into the evolutionary mechanisms shaping cognition. This study examined the development of different components of spatial memory, cognitive mechanisms that support complex foraging, by comparing two species with similar life history that vary in wild ecology: bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). Materials and Methods: Spatial memory development was assessed using a cross-sectional experimental design comparing apes ranging from infancy to adulthood. Study 1 tested 73 sanctuary-living apes on a task examining recall of a single location after a one-week delay, compared to an earlier session. Study 2 tested their ability to recall multiple locations within a complex environment. Study 3 examined a subset of individuals from Study 2 on a motivational control task. Results: In Study 1, younger bonobos and chimpanzees of all ages exhibited improved performance in the test session compared to their initial learning experience. Older bonobos, in contrast, did not exhibit a memory boost in performance after the delay. In Study 2, older chimpanzees exhibited an improved ability to recall multiple locations, whereas bonobos did not exhibit any age-related differences. In Study 3, both species were similarly motivated to search for food in the absence of memory demands. Discussion: These results indicate that closely-related species with similar life history characteristics can exhibit divergent patterns of cognitive development, and suggests a role of socioecological niche in shaping patterns of cognition in Pan.

 

Developmental shifts in social cognition: socioemotional biases across the lifespan in rhesus monkeys

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Rosati, A.G., Arre, A.M., Platt, M.L., & Santos, L.R. (2018). Developmental shifts in social cognition: socioemotional biases across the lifespan in rhesus monkeys.Behavioral Ecology and Sociobiology, 72: 63.

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Humans exhibit a suite of developmental changes in social cognition across the lifespan. To what extent are these developmental patterns unique? We first review several social domains in which humans undergo critical ontogenetic changes in socio-cognitive processing, including social attention and theory of mind. We then examine whether one human developmental transition—a shift in socioemotional preferences—also occurs in nonhuman primates. Specifically, we experimentally measured socioemotional processing in a large population of rhesus macaques (Macaca mulatta) ranging from infancy to old age. We tested whether macaques, like humans, also exhibited developmental shifts from a negativity bias at younger ages, indicating preferential attention to negative socioemotional stimuli, to a positivity bias at older ages. We first assessed monkeys’ (n = 337) responses to negative socioemotional stimuli by comparing their duration of looking towards photos of negative conspecific signals (threat displays) versus matched neutral expressions. In contrast to the pattern observed in humans, we found that older monkeys were more attentive to negative emotional stimuli than were younger monkeys. In a second study, we used the same method to examine monkeys’ (n = 132) attention to positive (affiliative displays) versus matched neutral expressions. Monkeys did not exhibit an overall preference for positive stimuli, nor major age-related changes in their attention. These results indicate that while monkeys show robust ontogenetic shifts in social preferences, they differ from humans by exhibiting an increasing negativity bias with age. Studies of comparative cognitive development can therefore provide insight into the evolutionary origins of human socio-cognitive development.

Tolerant Barbary macaques maintain juvenile levels of social attention in old age, but despotic rhesus macaques do not

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Rosati, A. G., & Santos, L. R. (2017). Tolerant Barbary macaques maintain juvenile levels of social attention in old age, but despotic rhesus macaques do not. Animal Behaviour, 130, 199-207.

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Complex social life is thought to be a major driver of complex cognition in primates, but few studies have directly tested the relationship between a given primate species’ social system and their social cognitive skills. We experimentally compared lifespan patterns of a foundational social cognitive skill (following another’s gaze) in tolerant Barbary macaques, Macaca sylvanus, and despotic rhesus macaques, Macaca mulatta. Semi-free-ranging monkeys (N = 80 individuals from each species) followed gaze more in test trials where an actor looked up compared to control trials. However, species differed in ontogenetic trajectories: both exhibited high rates of gaze following as juveniles, but rhesus monkeys exhibited declines in social attention with age, whereas Barbary macaques did not. This pattern indicates that developmental patterns of social attention vary with social tolerance, and that diversity in social behaviour can lead to differences in social cognition across primates.

Understanding human gaze

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Bettle, R., & Rosati, A. G. (2016). Understanding human gaze. In: Encyclopedia of Evolutionary Psychological Science (T. Shackelford and V. Weekes-Shackelford, eds.). Springer, pp. 1-4.

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Social attention is a foundational component of human social behavior. Our ability to detect and think about the direction of other’s gaze involves the attribution of mental states to others and scaffolds the development of other complex cognitive skills. Gaze-following is also widespread among other primates, but the cognitive mechanisms underlying gaze-sensitive behaviors appear to differ across species. Understanding the evolutionary origins of human social attention capacities can reveal the roots of our species’ unique patterns of cognition and culture.

Rhesus monkeys show human-like changes in gaze following across the lifespan

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Rosati, A. G., Arre, A. M., Platt, M. L., & Santos, L. R. (2016). Rhesus monkeys show human-like changes in gaze following across the lifespan. Proceedings of the Royal Society B , 283, 20160376.

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Gaze following, or co-orienting with others, is a foundational skill for human social behaviour. The emergence of this capacity scaffolds critical human-specific abilities such as theory of mind and language. Non-human primates also follow others’ gaze, but less is known about how the cognitive mechanisms supporting this behaviour develop over the lifespan. Here we experimentally tested gaze following in 481 semi-free-ranging rhesus macaques (Macaca mulatta) ranging from infancy to old age. We found that monkeys began to follow gaze in infancy and this response peaked in the juvenile period—suggesting that younger monkeys were especially attuned to gaze information, like humans. After sexual maturity, monkeys exhibited human-like sex differences in gaze following, with adult females showing more gaze following than males. Finally, older monkeys showed reduced propensity to follow gaze, just as older humans do. In a second study (n = 80), we confirmed that macaques exhibit similar baseline rates of looking upwards in a control condition, regardless of age. Our findings indicate that—despite important differences in human and non-human primate life-history characteristics and typical social experiences—monkeys undergo robust ontogenetic shifts in gaze following across early development, adulthood and ageing that are strikingly similar to those of humans.

Context influences spatial frames of reference in bonobos (Pan paniscus)

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Rosati, A. G. (2015). Context influences spatial frames of reference in bonobos (Pan paniscus). Behaviour, 152, 375-406.

Reprinted in: Bonobo cognition and behavior (B. Hare & S. Yamamoto, eds.)

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Primates must solve complex spatial problems when foraging, such as finding patchy resources and navigating between different locations. However, the nature of the cognitive representations supporting these types of behaviors is currently unclear. In humans, there has been great debate concerning the relative importance of egocentric representations (which are viewer-dependent) versus allocentric representations (which are based on aspects of the external environment). Comparative studies of nonhuman apes can illuminate which aspects of human spatial cognition are shared with other primates, versus which aspects are unique to our lineage. The current studies therefore examined spatial cognitive development in one of our closest living relatives, bonobos (Pan paniscus) across contexts. The first study assessed how younger bonobos encode locations in a place-response task in which apes first learn that one of two locations is consistently baited with a reward, and then must approach the two locations from a flipped perspective. The second study examined how a larger age sample of bonobos responded to a spatial relations task in which they first experience that one location is baited, and then can generalize this learning to a new set of targets. Results indicated that while bonobos exhibited a predominantly allocentric strategy in the first study, they consistently exhibited an egocentric strategy in the second. Together, these results show that bonobos can use both strategies to encode spatial information, and illuminate the complementary contributions to cognition made by egocentric and allocentric representations.

Comparative developmental psychology: How is human cognitive development unique?

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Rosati, A. G., Wobber, V., Hughes, K., & Santos, L. R. (2014). Comparative developmental psychology: How is human cognitive development unique?. Evolutionary Psychology, 12, 448-473.

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The fields of developmental and comparative psychology both seek to illuminate the roots of adult cognitive systems. Developmental studies target the emergence of adult cognitive systems over ontogenetic time, whereas comparative studies investigate the origins of human cognition in our evolutionary history. Despite the long tradition of research in both of these areas, little work has examined the intersection of the two: the study of cognitive development in a comparative perspective. In the current article, we review recent work using this comparative developmental approach to study non-human primate cognition. We argue that comparative data on the pace and pattern of cognitive development across species can address major theoretical questions in both psychology and biology. In particular, such integrative research will allow stronger biological inferences about the function of developmental change, and will be critical in addressing how humans come to acquire species-unique cognitive abilities.

Chimpanzees and bonobos exhibit divergent spatial memory development

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Rosati, A. G., & Hare, B. (2012). Chimpanzees and bonobos exhibit divergent spatial memory development. Developmental Science, 15, 840-853.

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Spatial cognition and memory are critical cognitive skills underlying foraging behaviors for all primates. While the emergence of these skills has been the focus of much research on human children, little is known about ontogenetic patterns shaping spatial cognition in other species. Comparative developmental studies of nonhuman apes can illuminate which aspects of human spatial development are shared with other primates, versus which aspects are unique to our lineage. Here we present three studies examining spatial memory development in our closest living relatives, chimpanzees (Pan troglodytes) and bonobos (P. paniscus). We first compared memory in a naturalistic foraging task where apes had to recall the location of resources hidden in a large outdoor enclosure with a variety of landmarks (studies 1 and 2). We then compared older apes using a matched memory choice paradigm (study 3). We found that chimpanzees exhibited more accurate spatial memory than bonobos across contexts, supporting predictions from these species’ different feeding ecologies. Furthermore, chimpanzees—but not bonobos—showed developmental improvements in spatial memory, indicating that bonobos exhibit cognitive paedomorphism (delays in developmental timing) in their spatial abilities relative to chimpanzees. Together, these results indicate that the development of spatial memory may differ even between closely related species. Moreover, changes in the spatial domain can emerge during nonhuman ape ontogeny, much like some changes seen in human children.

Early social cognition: How psychological mechanism can inform models of decision-making

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Warneken, F., & Rosati, A. G. (2012). Early social cognition: How psychological mechanism can inform models of decision-making. In: Evolving the Mechanisms of Decision Making: Toward a Darwinian Decision Theory, Strüngmann Forum Reports, vol. 11 (P. Hammerstein and J. R. Stevens, eds.). Cambridge, MA: MIT Press, pp. 288-289.

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Many approaches to understanding social decision-making use formalized models that account for costs and benefits to predict how individuals should choose. While these types of models are appropriate for describing social behavior at the ultimate level—accounting for the fitness consequences of different patterns of behavior—they do not necessarily reflect the proximate mechanisms used by decision-makers. We argue that a focus on psychological mechanisms is essential for understanding the causes of decision making in a social context. We particularly focus on the behavior of human children to elucidate the psychological capacities that are foundational for the developmental emergence of social decision-making in humans. In particular, we present evidence that across a wide range of contexts, young children appear to focus on the underlying psychological states of potential social partners in cooperative contexts. This suggests that many types of social decisions may be driven by intention-attribution, not explicit utility calculations. We propose that a comprehensive theory of social decision-making has to address both questions about ultimate function, as well as integrate empirical studies of the psychological instantiation of these processes. Developmental approaches are particularly informative, as they elucidate the origins of decision-making, as well as the factors that shape them into their mature form seen in adults.

Primate social cognition: Thirty years after Premack and Woodruff

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Rosati, A. G., Santos, L. R., & Hare, B. (2010). Primate social cognition: Thirty years after Premack and Woodruff. In: Primate Neuroethology (A. Ghazanfar and M. Platt, eds.). Oxford: Oxford University Press, pp. 117-143.

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Since Darwin declared the mind as the province of biology as well as psychology, the human intellect has been a major challenge for evolutionary biologists, with some researchers emphasizing the continuity between humans and other animals, and others emphasizing seemingly unique aspects of our psychological makeup. Research over the past ten years has revealed that at least some primates have some capability to assess the psychological states of others—while simultaneously showing striking differences between the social-cognitive capacities of humans and other primates. Here we address two aspects of primate social cognition—understanding of intentional, goal-directed action, and understanding perceptions, knowledge, and beliefs—focusing on newest comparative research since the last major reviews were written on the topic over a decade ago. We first review evidence suggesting that diverse species of primates understand the actions of others in terms of goals and intentions, and furthermore can reason about some, but probably not all, kinds of psychological states. We then examine the hypothesis that primates show their most complex social skills in competitive contexts, and suggest that inquiry into other aspects of primate social life, such as during cooperative interactions, may prove to be the next important step for experimental inquiries into primate social-cognitive skills. Finally, we examine primate social cognition in a broader evolutionary context that may allow us to better understand both primate and human cognitive skills.