Development and aging

Predictions about reward outcomes in rhesus monkeys

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Huang, Y., Chang, H., Santos, L.R. & Rosati, A.G. (2024). Predictions about reward outcomes in rhesus monkeys. Behavioral Neuroscience, 138: 43-58

[PDF] [Supplementary] [Study Videos] [Publisher’s version]Abstract
Human infants and nonhuman animals respond to surprising events by looking longer at unexpected than expected situations. These looking responses provide core cognitive evidence that nonverbal minds make predictions about possible outcomes and detect when these predictions fail to match reality. We propose that this phenomenon has crucial parallels with the processes of reward prediction error, indexing the difference between expected and actual reward outcomes. Most work on reward prediction errors to date involves neurobiological techniques that cannot be implemented in many relevant populations, so we developed a novel behavioral task to assess monkeys’ predictions about reward outcomes using looking time responses. In Study 1, we tested how semi-free-ranging monkeys (n = 210) responded to positive error (more rewards than expected), negative error (less rewards than expected), and a number control. We found that monkeys looked longer at a given reward when it was unexpectedly large or small, compared to when the same quantity was expected. In Study 2, we compared responses in the positive error condition in monkeys ranging from infancy to old age (n = 363), to assess lifespan changes in sensitivity to reward predictions. We found that adolescent monkeys showed heightened responses to unexpected rewards, similar to patterns seen in humans, but showed no changes during aging. These results suggest that monkeys’ looking responses can be used to track their predictions about rewards, and that monkeys share some developmental signatures of reward sensitivity with humans, providing a new approach to access cognitive processes underlying reward-based decision making.

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Advancing methods for the biodemography of aging within social contexts

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Hernández-Pacheco, R., Steiner, U.K., Rosati, A.G., Tuljapurka, S. (2023). Advancing methods for the biodemography of aging within social contexts. Neuroscience and BioBehavioral Reviews, 153: 105400.

[PDF] [Publisher’s version]Abstract
Several social dimensions including social integration, status, early-life adversity, and their interactions across the life course can predict health, reproduction, and mortality in humans. Accordingly, the social environment plays a fundamental role in the emergence of phenotypes driving the evolution of aging. Recent work placing human social gradients on a biological continuum with other species provides a useful evolutionary context for aging questions, but there is still a need for a unified evolutionary framework linking health and aging within social contexts. Here, we summarize current challenges to understand the role of the social environment in human life courses. Next, we review recent advances in comparative biodemography and propose a biodemographic perspective to address socially driven health phenotype distributions and their evolutionary consequences using a nonhuman primate population. This new comparative approach uses evolutionary demography to address the joint dynamics of populations, social dimensions, phenotypes, and life history parameters. The long-term goal is to advance our understanding of the link between individual social environments, population-level outcomes, and the evolution of aging.

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Distinct developmental trajectories for risky and impulsive decision-making in chimpanzees

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Rosati, A.G., Emery Thompson, M., Atencia, R., & Buckholtz, J.W. (2023). Distinct developmental trajectories for risky and impulsive decision-making in chimpanzees. Journal of Experimental Psychology: General, 152: 1551–1564.

[PDF][Supplementary][Publisher’s version] Abstract
Human adolescence is characterized by a suite of changes in decision-making and emotional regulation that promote risky and impulsive behavior. Accumulating evidence suggests that behavioral and physiological shifts seen in human adolescence are shared by some primates, yet it is unclear if the same cognitive mechanisms are recruited. We examined developmental changes in risky choice, intertemporal choice, and emotional responses to decision outcomes in chimpanzees, our closest-living relatives. We found that adolescent chimpanzees were more risk-seeking than adults, as in humans. However, chimpanzees showed no developmental change in intertemporal choice, unlike humans, although younger chimpanzees did exhibit elevated emotional reactivity to waiting compared to adults. Comparisons of cortisol and testosterone indicated robust age-related variation in these biomarkers, and patterns of individual differences in choices, emotional reactivity, and hormones also supported a developmental dissociation between risk and choice impulsivity. These results show that some but not all core features of human adolescent decision-making are shared with chimpanzees.

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Sensitivity to line-of-sight in tolerant versus despotic macaques (Macaca sylvanus and Macaca mulatta)

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Bettle, R. & Rosati, A.G. (2022) Sensitivity to line-of-sight in tolerant versus despotic macaques (Macaca sylvanus and Macaca mulatta). Journal of Comparative Psychology, 136: 93–104.

[PDF] [Supplementary] [Study Video] [Publisher’s version] [Commentary] Abstract
Complex social life is considered important to the evolution of cognition in primates. One key aspect of primate social interactions concerns the degree of competition that individuals face in their social group. To examine how social tolerance versus competition shapes social cognition, we experimentally assessed capacities for flexible gaze-following in more tolerant Barbary macaques (Macaca sylvanus) and compared to previous data from despotic rhesus macaques (Macaca mulatta). Monkeys experienced one of two possible conditions. In the barrier condition, they observed an actor look upwards into an overheard barrier, so they could not directly see the target of the actor’s gaze without reorienting. In the no barrier condition, they observed an actor look upwards without a barrier blocking her line-of-sight, so they could observe the target of the actor’s gaze by also looking upwards. Both species (N = 58 Barbary macaques, 64 rhesus macaques) could flexibly modulate their gaze responses to account for the demonstrator’s line of sight, looking up more often when no barrier was present, and this flexible modulation declined with age in both species. However, neither species preferentially approached to look inside the barrier when their view of the target location was obscured, although rhesus macaques approached more overall. This pattern suggests that both tolerant and despotic macaques exhibit similar capacities to track other’s line of sight and do not preferentially reorient their bodies to observe what an actor looks at in this situation. This contrasts with other work indicating that competitive primates are especially adept at some aspects of theory of mind. Thus, it is important to understand both the similarities and differences in the social–cognitive abilities of primates with different social styles.

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Children show economic trust for both ingroup and outgroup partners

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Grueneisen, S., Rosati, A.G., Warneken, F. (2021) Children show economic trust for both ingroup and outgroup partners. Cognitive Development, 59: 101077

[PDF] [Publisher’s version] Abstract
Trust is a critical aspect of human cooperation, allowing individuals to overcome the risks posed by such interactions because of others’ presumed cooperative inclinations. Adults sometimes mitigate these risks by preferentially trusting members of their own social group, yet it is currently unclear if the early emergence of children’s trust in others’ cooperative tendencies is affected by their intergroup psychology. Here we tested whether group membership impacts two key aspects of trust-based cooperation in young children – their trust in others’ willingness to reciprocate an investment (assessed using the Investment Game, Study 1), and their trust in others’ generosity (assessed using the Faith Game, Study 2). In both studies, children assigned to novel and otherwise arbitrary groups demonstrated general preferences for ingroup members on several measures. However, group membership did not influence their decisions about economic trust. In Study 1, 4- and 6-year-old children showed high levels of trust in both ingroup and outgroup members’ tendency to reciprocate an investment. In Study 2, 6- to 7-year-old children similarly showed high levels of trust in ingroup and outgroup members’ generosity, and they did so regardless of whether their group membership was a matter of common knowledge between themselves and the trustee. These findings show that young children’s preferences for ingroup members do not result in bias due to shared group membership when making economic trust decisions. Rather, children tend to exhibit trust in the cooperativeness of others regardless of group membership.

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The primate origins of human social cognition

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Bettle, R. & Rosati, A.G. (2021). The primate origins of human social cognition. Language Learning and Development, 17: 96-127

[PDF] [Publisher’s version] Abstract
The ability to understand the mental states of other individuals is central to human social behavior, yet some theory of mind capacities are shared with other species. Comparisons of theory of mind skills across humans and other primates can provide a critical test of the cognitive prerequisites necessary for different theory of mind skills to emerge. A fundamental difference between humans and non-humans is language: while language may scaffold some developing theory of mind skills in humans, other species do not have similar capacities for or immersion in language. Comparative work can therefore provide a new line of evidence to test the role of language in the emergence of complex social cognition. Here we first provide an overview of the evidence for shared aspects of theory of mind in other primates, and then examine the evidence for apparently human-unique aspects of theory of mind that may be linked to language. We finally contrast different evolutionary processes, such as competition and cooperation, that may have been important for primate social cognition versus human-specific forms of theory of mind. We argue that this evolutionary perspective can help adjudicate between different proposals on the link between human-specific forms of social cognition and language.

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Variation in primate decision-making under uncertainty and the roots of human economic behaviour

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De Petrillo, F. & Rosati, A.G. (2021). Variation in primate decision-making under uncertainty and the roots of human economic behaviour. Philosophical Transactions of the Royal Society B, 376: 20190671

[PDF] [Supplementary] [Publisher’s version] Abstract
Uncertainty is a ubiquitous component of human economic behaviour, yet people can vary in their preferences for risk across populations, individuals, and different points in time. As uncertainty also characterizes many aspects of animal decision-making, comparative research can help evaluate different potential mechanisms that generates this variation, including the role of biological differences or maturational change versus cultural learning, as well as identify human-unique components of economic decision-making. Here we examine decision-making under risk across primates, our closest relatives. We first review theoretical approaches and current methods for understanding decision-making in animals. We then assess current evidence for variation in animal preferences between species and populations; between individuals based on personality, sex, and age; and finally, between different contexts and individual states. We then use this primate data to evaluate the processes that can shape human decision-making strategies and identify the primate foundations of human economic behaviour.

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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. (2021). The evolutionary origins of natural pedagogy: Rhesus monkeys show sustained attention following nonsocial cues versus social communicative signals. Developmental Science, 24: e12987.

[PDF] [Supplementary] [Videos] [Publisher’s version] Abstract
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.

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Social selectivity in aging wild chimpanzees

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Rosati, A.G., Hagberg, L., Enigk, D.K., Otali, E., Emery Thompson, M., Muller, M.N., Wrangham, R.W. & Machanda, Z.P. (2020), Social selectivity in aging wild chimpanzees. Science, 370: 473-476.

[PDF] [Supplementary] [Publisher’s Version] [Commentary] Abstract

Humans prioritize close, positive relationships during aging, and socioemotional selectivity theory proposes that this shift causally depends on capacities for thinking about personal future time horizons. To examine this theory, we tested for key elements of human social aging in longitudinal data on wild chimpanzees. Aging male chimpanzees have more mutual friendships characterized by high, equitable investment, whereas younger males have more one-sided relationships. Older males are more likely to be alone, but they also socialize more with important social partners. Further, males show a relative shift from more agonistic interactions to more positive, affiliative interactions over their life span. Our findings indicate that social selectivity can emerge in the absence of complex future-oriented cognition, and they provide an evolutionary context for patterns of social aging in humans.

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Healthy cardiovascular biomarkers across the lifespan in wild-born chimpanzees (Pan troglodytes)

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Cole, M.F., Cantwell, A., Rukundo, J. Ajarova, L., Fernandez-Navarro, S., Atencia, R. & Rosati, A.G. (2020). Healthy cardiovascular biomarkers across the lifespan in wild-born chimpanzees (Pan troglodytes).Philosophical Transactions of the Royal Society B, 375: 20190609.

[PDF] [Supplementary] [Publisher’s version] Abstract
Chimpanzees (Pan troglodytes) are a crucial model for understanding the evolution of human health and longevity. Cardiovascular disease is a major source of mortality during aging in humans and therefore a key issue for comparative research. Current data indicates that compared to humans, chimpanzees have proatherogenic blood lipid profiles, an important risk factor for cardiovascular disease in humans. However, most work to date on chimpanzee lipids come from laboratory-living populations where lifestyles diverge from a wild context. Here we examined cardiovascular profiles in chimpanzees living in African sanctuaries, who semi-free-range in large forested enclosures, consume a naturalistic diet, and generally experience conditions more similar to a wild chimpanzee lifestyle. We measured blood lipids, body weight, and body fat in 75 sanctuary chimpanzees and compared them to publicly-available data from laboratory-living chimpanzees from the Primate Aging Database. We found that semi-free-ranging chimpanzees exhibited lower body weight and lower levels of lipids that are risk factors for human cardiovascular disease, and that some of these disparities increased with age. Our findings support the hypothesis that lifestyle can shape health indices in chimpanzees, similar to effects observed across human populations, and contribute to an emerging understanding of human cardiovascular health in evolutionary context.

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Insights from evolutionarily-relevant models for human ageing

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Emery Thompson, M., Rosati, A.G., Snyder-Mackler, N. (2020). Insights from evolutionarily-relevant models for human ageing. Philosophical Transactions of the Royal Society B, 375: 20190605.

[PDF] [Publisher’s version] Abstract

As the world confronts the health challenges of an aging population, there has been dramatically increased interest in the science of aging. This research has overwhelmingly focused on age-related disease, particularly in industrialized human populations and short-lived laboratory animal models. However, it has become clear that humans and long-lived primates age differently than many typical model organisms, and that many of the diseases causing death and disability in the developed world are greatly exacerbated by modern lifestyles. As such, research on how the human aging process evolved is vital to understanding the origins of prolonged human lifespan and factors increasing vulnerability to degenerative disease. In this issue, we highlight emerging comparative research on primates, highlighting the physical, physiological, behavioural, and cognitive processes of aging. This work comprises data and theory on non-human primates, as well as underrepresented data on humans living in small-scale societies, which help elucidate how environment shapes senescence. Component papers address (1) the critical processes that comprise senescence in long-lived primates; (2) the social, ecological, or individual characteristics that predict variation in the pace of aging; and (3) the complicated relationship between aging trajectories and disease outcomes. Collectively, this work provides essential comparative, evolutionary data on aging and demonstrates its unique potential to inform our understanding of the human aging process.

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Shifting sociality during primate ageing

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Machanda, Z.P. & Rosati, A.G. (2020). Shifting sociality during primate ageing. Philosophical Transactions of the Royal Society B, 375: 20190620.

[PDF] [Supplementary] [Publisher’s version] Abstract

Humans exhibit major age-related shifts in social relationships along with changes in social and emotional psychological processes that underpin these behavioral shifts. Does social aeging in nonhuman primates follow similar patterns, and if so, what are the ultimate evolutionary consequences of these social shifts? Here we synthesize empirical evidence for shifts in social behavior and underlying psychological processes across species. Focusing on three elements of social behavior and cognition that are important for humans—propensities to engage with others, the positive versus negative valence of these interactions, and capabilities to influence others, we find evidence for wide variation in the trajectories of these characteristics across primates. Based on this, we identify potential modulators of the primate social ageing process, including social organization, sex, and dominance status. Finally, we discuss how comparative research can contextualize human social ageing.

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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.

[PDF] [Supplementary] [Videos] [Publisher’s Version] Abstract
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.

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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.

[PDF] [Video] [Supplementary] [Publisher’s Version] Abstract
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.

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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.

[PDF]  [Supplementary]  [Publisher’s Version]  Abstract

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.

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