Decision-making and cognitive control

Early emergence of metacognition in rhesus monkeys

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Huang, Y. & Rosati, A.G. (2025). Early emergence of metacognition in rhesus monkeys. Developmental Science, 28: e70012. [PDF] [Supplementary] [Study Video] [Publisher’s version]

Abstract
Metacognition, or monitoring and controlling one’s knowledge, is a key feature of human cognition. Accumulating evidence shows that foundational forms of metacognition are already present in young infants and then scaffold later-emerging skills.
Although many animals exhibit cognitive processes relevant to metacognition, it is unclear if other species share the developmental
trajectories seen in humans. Here, we examine the emergence of metacognitive information-seeking in rhesus monkeys (Macaca
mulatta). We presented a large sample of semi-free-ranging monkeys, ranging from juvenility to adulthood, with a one-shot task
where they could seek information about a food reward by bending down to peer into a center vantage point in an array of tubes.
In the hidden condition, information-seeking was necessary as no food was visible on the apparatus, whereas in the visible control,
condition information-seeking was not necessary to detect the location of the reward. Monkeys sought information at the center
vantage point more often when it was necessary than in the control condition, and younger monkeys already showed competency
similar to adults. We also tracked additional monkeys who voluntarily chose not to approach to assess monkeys’ ability to actively
infer opportunities for information-seeking, and again found similar performance in juveniles and adults. Finally, we found that
monkeys were overall slower to make metacognitive inferences than to approach known reward, and that younger monkeys were
specifically slower to detect opportunities for information-seeking compared to adults. These results indicate that many features of
mature metacognition are already detectable in young monkeys, paralleling evidence for “core metacognition” in infant humans.

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Flexible information-seeking in chimpanzees

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Rosati, A.G., Felsche, E., Cole, M.F., Atencia, R., & Rukundo, J. (2024). Flexible information-seeking in chimpanzees. Cognition, 251: 105898. [PDF] [Supplementary] [Study Videos] [Publisher’s version]

Abstract
Humans can flexibly use metacognition to monitor their own knowledge and strategically acquire new information when needed. While humans can deploy these skills across a variety of contexts, most evidence for metacognition in animals has focused on simple situations, such as seeking out information about the location of food. Here, we examine the flexibility, breadth, and limits of this skill in chimpanzees. We tested semi-free-ranging chimpanzees on a novel task where they could seek information by standing up to peer into different containers. In Study 1, we tested n = 47 chimpanzees to assess if chimpanzees would spontaneously engage in information-seeking without prior experience, as well as to characterize individual variation in this propensity. We found that many chimpanzees engaged in information-seeking with minimal experience, and that younger chimpanzees and females were more likely to do so. In two subsequent studies, we then further tested chimpanzees who initially showed robust information-seeking on new variations of this task, to disentangle the cognitive processing shaping their behaviors. In Study 2, we examined how a subset of n = 12 chimpanzees applied these skills to seek information about the location versus the identity of rewards, and found that chimpanzees were equally adept at seeking out location and identity information. In Study 3, we examined whether a subset of n = 6 chimpanzees could apply these skills to make more efficacious decisions when faced with uncertainty about reward payoffs. Chimpanzees were able to use information-seeking to resolve risk and choose more optimally when faced with uncertain payoffs, although they often also engaged in information-seeking when it was not strictly necessary. These results identify core features of flexible metacognition that chimpanzees share with humans, as well as constraints that may represent key evolutionary shifts in human cognition.

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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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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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The evolution of cognitive control in lemurs

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De Petrillo, F., Nair, P., Cantwell, A., & Rosati, A.G. (2022). The evolution of cognitive control in lemurs. Psychological Science, 33: 1408-1422.

[PDF] [Supplementary] [Publisher’s version] Abstract
Cognitive control, or executive function, is a key feature of human cognition, allowing individuals to plan, acquire new information, or adopt new strategies when the circumstances change. Yet it is unclear which factors promote the evolution of more sophisticated executive-function abilities such as those possessed by humans. Examining cognitive control in nonhuman primates, our closest relatives, can help to identify these evolutionary processes. Here, we developed a novel battery to experimentally measure multiple aspects of cognitive control in primates: temporal discounting, motor inhibition, short-term memory, reversal learning, novelty responses, and persistence. We tested lemur species with targeted, independent variation in both ecological and social features (ruffed lemurs, Coquerel’s sifakas, ring-tailed lemurs, and mongoose lemurs; N = 39) and found that ecological rather than social characteristics best predicted patterns of cognitive control across these species. This highlights the importance of integrating cognitive data with species’ natural history to understand the origins of complex cognition.

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The origins of cognitive flexibility in chimpanzees

Cantwell, A., Buckholtz, J.W., Atencia, R., & Rosati, A.G. (2022). The origins of cognitive flexibility in chimpanzees. Developmental Science, 25: e13266.

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

Cognitive flexibility is a core component of executive function, a suite of cognitive capacities that enables individuals to update their behavior in dynamic environments. Human executive functions are proposed to be enhanced compared to other species, but this inference is based primarily on neuroanatomical studies. To address this, we examined the nature and origins of cognitive flexibility in chimpanzees, our closest living relatives. Across three studies, we examined different components of cognitive flexibility using reversal learning tasks where individuals first learned one contingency and then had to shift responses when contingencies flipped. In Study 1, we tested n = 82 chimpanzees ranging from juvenility to adulthood on a spatial reversal task, to characterize the development of basic shifting skills. In Study 2, we tested how n = 24 chimpanzees use spatial versus arbitrary perceptual information to shift, a proposed difference between human and nonhuman cognition. In Study 3, we tested n = 40 chimpanzees on a probabilistic reversal task. We found an extended developmental trajectory for basic shifting and shifting in response to probabilistic feedback—chimpanzees did not reach mature performance until late in ontogeny. Additionally, females were faster to shift than males were. We also found that chimpanzees were much more successful when using spatial versus perceptual cues, and highly perseverative when faced with probabilistic versus consistent outcomes. These results identify both core features of chimpanzee cognitive flexibility that are shared with humans, as well as constraints on chimpanzee cognitive flexibility that may represent evolutionary changes in human cognitive development.

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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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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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Decision-making in animals: rational choices and adaptive strategies

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De Petrillo, F. & Rosati, A.G. (2021). Decision-making in animals: rational choices and adaptive strategies. In: Cambridge Handbook of Animal Cognition (A. Kaufman, J. Call, & J. Kaufman, eds.) Cambridge: Cambridge University Press, pp. 770-791.

[PDF] [Publisher’s version] Abstract
Humans face a myriad of choices every day, from simple decisions about what to eat for lunch or how much time to spend on leisure versus work, to more complex decisions like selecting between competitive jobs offers or deciding whether or not get married. How do we make these choices? This question has spurred research in decision science across fields including economics, psychology, and biology, and has led to the development of several normative theories and models predicting how decision-makers should act to choose optimally.

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Logical inferences from visual and auditory information in ruffed lemurs and sifakas

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De Petrillo, F. & Rosati, A.G. (2020). Logical inferences from visual and auditory information in ruffed lemurs and sifakas. Animal Behaviour, 164: 193-204

[PDF] [Videos] [Publisher’s Version] Abstract
Inference by exclusion, or the ability to select a correct course of action by systematically excluding other potential alternatives, is a form of logical inference that allow individuals to solve problems without complete information. Current comparative research shows that several bird, mammal, and primate species can find hidden food through inference by exclusion. Yet there is also wide variation in how successful different species are, as well kinds of sensory information they can use to do so. An important question is therefore why some species are better at engaging in logical inference than others. Here, we investigate the evolution of logical reasoning abilities by comparing two strepsirrhine primate species that vary in dietary ecology: frugivorous ruffed lemur (Varecia spp.) and folivorous Coquerel’s sifakas (Propithecus coquereli). Across two studies, we examined their abilities to locate food using direct information versus inference from exclusion and using both visual and auditory information. In Study 1, we assessed whether these lemurs could make inferences when full visual and auditory information about the two potential locations of food were provided. In Study 2, we then compared their ability to make direct inferences versus inferences by exclusion in both the visual and auditory domains. We found that both lemur species can use visual information to find food, but that only ruffed lemurs were also able to use auditory cues, mirroring differences in the complexity of their wild ecology. We further found that, unlike many anthropoid species tested to date, both strepsirrhine species failed to make inferences by exclusion. These results highlight the importance of natural history in understanding the evolution of logical inference, and help reconstruct the deeper phylogeny of primate cognition.

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Economic trust in young children

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Rosati, A.G., Benjamin, N., Pieloch, K., Warneken, F. (2019). Economic trust in young children. Proceedings of the Royal Society B, 286: 20190822.

[PDF] [Supplementary] [Supplementary Scripts] [Publisher’s Version] Abstract
Mutually beneficial interactions often require trust that others will reciprocate. Such interpersonal trust is foundational to evolutionarily unique aspects of human social behaviour, such as economic exchange. In adults, interpersonal trust is often assessed using the ‘trust game’, in which a lender invests resources in a trustee who may or may not repay the loan. This game captures two crucial elements of economic exchange: the potential for greater mutual benefits by trusting in others, and the moral hazard that others may betray that trust. While adults across cultures can trust others, little is known about the developmental origins of this crucial cooperative ability. We developed the first version of the trust game for use with young children that addresses these two components of trust. Across three experiments, we demonstrate that 4- and 6-year-olds recognize opportunities to invest in others, sharing more when reciprocation is possible than in a context measuring pure generosity. Yet, children become better with age at investing in trustworthy over untrustworthy partners, indicating that this cooperative skill emerges later in ontogeny. Together, our results indicate that young children can engage in complex economic exchanges involving judgements about interpersonal trust and show increasing sensitivity to appropriate partners over development.

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Rhesus macaques use probabilities to predict future events

De Petrillo, F. & Rosati, A.G. (2019). Rhesus macaques use probabilities to predict future events. Evolution and Human Behavior, 40: 436-446.

[PDF] [Videos] [Publisher’s Version]Abstract
Humans can use an intuitive sense of statistics to make predictions about uncertain future events, a cognitive skill that underpins logical and mathematical reasoning. Recent research shows that some of these abilities for statistical inferences can emerge in preverbal infants and non-human primates such as apes and capuchins. An important question is therefore whether animals share the full complement of intuitive reasoning abilities demonstrated by humans, as well as what evolutionary contexts promote the emergence of such skills. Here, we examined whether free-ranging rhesus macaques (Macaca mulatta) can use probability information to infer the most likely outcome of a random lottery, in the first test of whether primates can make such inferences in the absence of direct prior experience. We developed a novel expectancy-violation looking time task, adapted from prior studies of infants, in order to assess the monkeys’ expectations. In Study 1, we confirmed that monkeys (n = 20) looked similarly at different sampled items if they had no prior knowledge about the population they were drawn from. In Study 2, monkeys (n = 80) saw a dynamic ‘lottery’ machine containing a mix of two types of fruit outcomes, and then saw either the more common fruit (expected trial) or the relatively rare fruit (unexpected trial) fall from the machine. We found that monkeys looked longer when they witnessed the unexpected outcome. In Study 3, we confirmed that this effect depended on the causal relationship between the sample and the population, not visual mismatch: monkeys (n = 80) looked equally at both outcomes if the experimenter pulled the sampled item from her pocket. These results reveal that rhesus monkeys spontaneously use information about probability to reason about likely outcomes, and show how comparative studies of nonhumans can disentangle the evolutionary history of logical reasoning capacities.

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Ecological rationality: convergent decision-making in apes and capuchins

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De Petrillo, F. & Rosati, A.G. (2019). Ecological rationality: convergent decision-making in apes and capuchins. Behavioural Processes, 164: 201-213.

[PDF] [Publisher’s Version] Abstract
Humans and other animals appear to defy many principles of economic ‘rationality’ when making decisions. Here, we use an ecological rationality framework to examine patterns of decision-making across species to illu- minate the origins of these strategies. We argue that examples of convergent evolution—the independent emergence of similar traits in species facing similar environments—can provide a crucial test for evolutionary theories of decision-making. We first review theoretical work from evolutionary biology proposing that many economically-puzzling patterns of decision-making may be biologically adaptive when considering the en- vironment in which they are made. We then focus on convergence in ecology, behavior, and cognition of apes and capuchin monkeys as an example of how to apply this ecological framework across species. We review evidence that wild chimpanzees and capuchins, despite being distantly related, both exploit ecological niches characterized by costly extractive foraging and risky hunting behaviors. We then synthesize empirical studies comparing these species’ decision preferences. In fact, both capuchins and chimpanzees exhibit high tolerance for delays in inter-temporal choice tasks, as well as a preference for risky outcomes when making decisions under uncertainty. Moreover, these species exhibit convergent psychological mechanisms for choices, including emotional responses to decision outcomes and sensitivity to social context. Finally, we argue that identifying the evolutionary pressures driving the emergence of specific decision strategies can shed light into the adaptive nature of human economic preferences.

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Chimpanzee cooperation is fast and independent from self-control

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Rosati, A.G., DiNicola, L.M., & Buckholtz, J.W. (2018). Chimpanzee cooperation is fast and independent from self-control. Psychological Science, 29: 1832-1845.

[PDF] [Supplementary] [Videos] [Publisher’s Version] Abstract
Large-scale cooperation is a hallmark of our species that appears unique amongst primates. Yet the evolutionary mechanisms that drove the emergence of human-like patterns of cooperation remain unclear. Studying the cognitive processes underlying cooperative behavior in apes, our closest living relatives, can help identify these mechanisms. Accordingly, we employed a novel test battery to assess the willingness of forty chimpanzees to donate resources, instrumentally help others, and punish a culpable thief. We found that chimpanzees were faster to make prosocial than selfish choices, and that more prosocial individuals made the fastest responses. Further, two measures of self-control did not predict variation in prosocial responding, and individual performance across cooperative tasks did not covary. These results show that chimpanzees and humans share key cognitive processes for cooperation, despite differences in the scope of their cooperative behaviors.

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Chimpanzee cognition and the roots of the human mind

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Rosati, A.G. (2017). Chimpanzee cognition and the roots of the human mind. In: Chimpanzees and Human Evolution (M. Muller, R. Wrangham & D. Pilbeam, eds.). Cambridge: The Belknap Press of Harvard University Press, pp. 703-745.

[PDF] Abstract
The origins of the human mind have been a puzzle ever since Darwin (1871, 1872). Despite striking continuities in the behavior of humans and nonhumans, our species also exhibits a suite of abilities that diverge from the rest of the animal kingdom: we create and utilize complex technology, pass cultural knowledge from generation to generation, and cooperate across numerous and diverse contexts. Why do humans exhibit these abilities, but other animals (mostly) do not? This is a fundamental question in biology, psychology, and philosophy. This puzzle involves two main parts. The first is concerned with identifying the psychological capacities that are unique to humans. This phylogenetic question can be addressed through careful comparisons of humans and other animals to pinpoint the cognitive traits that are likely derived in our species. The second is concerned with the function of these capacities, and the context in which they arose. This evolutionary question examines why, from an ultimate perspective, we evolved these specialized capacities in the first place. Solving these puzzles poses a special challenge because it is only possible to directly measure the cognition of living animals. The bodies of extinct species leave traces in the fossil record, and even some behavioral traits exhibit well-understood relationships with physical traits—such as relationships between dentition and dietary ecology, or mating system and sexual size dimorphism. These relationships provide important benchmarks when biologists infer the behavior of extinct species. Unfortunately, cognition does not fossilize, and neither do the brains that generate cognitive abilities. Even those features of neuroanatomy that do leave some trace in the fossil record—such as brain size or particular anatomical landmarks—are often related to the kinds of complex cognitive capacities potentially unique to humans in a coarse fashion. As such, identifying derived human cognitive traits requires reconstructing the mind of the last common ancestor of chimpanzees (Pan troglodytes), bonobos (Pan paniscus), and humans (Homo sapiens). This reconstruction then can be used to infer what cognitive characteristics have changed in the human lineage.

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