Disentangling perceptual awareness from nonconscious processing in rhesus monkeys (Macaca mulatta).

Scholars have long debated whether animals, which display impressive intelligent behaviors, are consciously aware or not. Yet, because many complex human behaviors and high-level functions can be performed without conscious awareness, it was long considered impossible to untangle whether animals are aware or just conditionally or nonconsciously behaving. Here, we developed an empirical approach to address this question. We harnessed a well-established cross-over double dissociation between nonconscious and conscious processing, in which people perform in completely opposite ways when they are aware of stimuli versus when they are not. To date, no one has explored if similar performance dissociations exist in a nonhuman species. In a series of seven experiments, we first established these signatures in humans using both known and newly developed nonverbal double-dissociation tasks and then identified similar signatures in rhesus monkeys (Macaca mulatta). These results provide robust evidence for two distinct modes of processing in nonhuman primates. This empirical approach makes it feasible to disentangle conscious visual awareness from nonconscious processing in nonhuman species; hence, it can be used to strip away ambiguity when exploring the processes governing intelligent behavior across the animal kingdom. Taken together, these results strongly support the existence of both nonconscious processing as well as functional human-like visual awareness in nonhuman animals.

Macaque species with varying social tolerance show no differences in understanding what other agents perceive.

A growing body of work demonstrates that a species' socioecology can impact its cognitive abilities. Indeed, even closely related species with different socioecological pressures often show different patterns of cognitive performance on the same task. Here, we explore whether major differences in social tolerance in two closely related macaque species can impact a core sociocognitive ability, the capacity to recognize what others see. Specifically, we compared the performance of Barbary macaques (Macaca sylvanus, n = 80) and rhesus macaques (Macaca mulatta, n = 62) on a standard test of visual perspective understanding. In contrast to the difference in performance, one might expect from these species' divergent socioecologies that our results show similar performance across Barbary and rhesus macaques, with both species forming expectations about how another agent will act based on that agent's visual perspective. These results suggest that differences in socioecology may not play as big of a role in the evolution of some theory of mind capacities as they do in other decision-making or foraging contexts.

Training differences predict dogs' (Canis lupus familiaris) preferences for prosocial others.

Humans evaluate other agents' behavior on a variety of different dimensions, including morally, from a very early age. For example, human infants as young as 6-months old prefer prosocial over antisocial others and demonstrate negative evaluations of antisocial others in a variety of paradigms (Hamlin et al. in Nature 450(7169):557, 2007; Dev Sci 13(6):923-929, 2010; Proc Natl Acad Sci 108(50):19931-19936, 2011). While these tendencies are well documented in the human species, less is known about whether similar preference emerge in non-human animals. Here, we explore this question by testing prosocial preferences in one non-human species: the domestic dog (Canis lupus familiaris). Given the ubiquity of dog-human social interactions, it is possible that dogs display human-like social evaluation tendencies. Unfortunately, prior research examining social evaluation in dogs has produced mixed results. To assess whether differences in methodology or training differences account for these contrasting results, we tested two samples of dogs with different training histories on an identical social evaluation task. Trained agility dogs approached a prosocial actor significantly more often than an antisocial actor, while untrained pet dogs showed no preference for either actor. These differences across dogs with different training histories suggest that while dogs may demonstrate preferences for prosocial others in some contexts, their social evaluation abilities are less flexible and less robust compared to those of humans.

Psychopaths fail to automatically take the perspective of others.

Psychopathic individuals display a chronic and flagrant disregard for the welfare of others through their callous and manipulative behavior. Historically, this behavior is thought to result from deficits in social-affective processing. However, we show that at least some psychopathic behaviors may be rooted in a cognitive deficit, specifically an inability to automatically take another person's perspective. Unlike prior studies that rely solely on controlled theory of mind (ToM) tasks, we employ a task that taps into automatic ToM processing. Controlled ToM processes are engaged when an individual intentionally considers the perspective of another person, whereas automatic ToM processes are engaged when an individual unintentionally represents the perspective of another person. In a sample of incarcerated offenders, we find that psychopathic individuals are equally likely to show response interference under conditions of controlled ToM, but lack a common signature of automatic ToM known as altercentric interference. We also demonstrate that the magnitude of this dysfunction in altercentric interference is correlated with real-world callous behaviors (i.e., number of assault charges). These findings suggest that psychopathic individuals have a diminished propensity to automatically think from another's perspective, which may be the cognitive root of their deficits in social functioning and moral behavior.

Do young rhesus macaques know what others see?: A comparative developmental perspective.

Humans undergo robust ontogenetic shifts in the theory of mind capabilities. Are these developmental changes unique to human development or are they shared with other closely related non-human species? To explore this issue, we tested the development of the theory of mind capacities in a population of 236 infant and juvenile rhesus macaques (Macaca mulatta). Using a looking-time method, we examined what developing monkeys know about others' perceptions. Specifically, we tested whether younger monkeys predict that a person will reach for an object where she last saw it. Overall, we found a significant interaction between a monkey's age and performance on this task (p = .014). Juvenile monkeys (between two and 5 years of age) show a nonsignificant trend towards human infant-like patterns of performance, looking longer during the unexpected condition as compared to the expected condition, though this difference is nonsignificant (p = .09). However, contrary to findings in human infants, infant rhesus macaques show a different trend. Infant monkeys on average look slightly longer on average during the expected condition than the unexpected condition, though this pattern was not significant (p = .06). Our developmental results in monkeys provide some hints about the development of the theory of mind capacities in non-humans. First, young rhesus macaques appear to show some interest in the perception of other agents. Second, young rhesus seems able to make predictions based on the visual perspective of another agent, though the developmental pattern of this ability is not as clear nor as robust as in humans. As such, though an understanding of others' perceptions is early-emerging in human infants, it may require more experience interacting with other social agents in our non-human relatives.

The Influence of Interactions with Dogs on Affect, Anxiety, and Arousal in Children.

Interactions with animals represent a promising way to reduce the burden of childhood mental illness on a large scale. However, the specific effects of child-animal interactions are not yet well-established. This study provides a carefully controlled demonstration that unstructured interactions with dogs can improve clinically relevant symptoms in children. Seventy-eight children (55.1% female, 44.9% male) ages 10 to 13 (M = 12.01, SD = 1.13) completed the Trier Social Stress Test for Children, followed by (a) interaction with a dog, (b) a tactile-stimulation control condition, or (c) a waiting control condition. The Positive and Negative Affect Schedule for Children, Short Form and the State/Trait Anxiety Inventory for Children were completed at baseline and posttest, and salivary cortisol was assessed at 5 time points. Adjusting for baseline scores, participants in the experimental condition showed higher scores on the Positive Affect scale than participants in both control conditions and lower scores on the State/Trait Anxiety Inventory for Children than participants in the waiting control condition at posttest. Negative affect was not assessed reliably, and we detected no effect of the interactions on salivary cortisol, as measured by area under the curve with respect to ground. Brief, unstructured interactions with dogs boosted children's positive emotions and reduced anxiety. Additional research is needed to further clarify which features of the interactions produce these benefits and the extent to which interactions with animals offer benefits that exceed the effects of other common coping strategies, activities, and interventions.

Dogs do not demonstrate a human-like bias to defer to communicative cues.

Human children and domesticated dogs learn from communicative cues, such as pointing, in highly similar ways. In two experiments, we investigate whether dogs are biased to defer to these cues in the same way as human children. We tested dogs on a cueing task similar to one previously conducted in human children. Dogs received conflicting information about the location of a treat from a Guesser and a Knower, who either used communicative cues (i.e., pointing; Experiments 1 and 2), non-communicative physical cues (i.e., a wooden marker; Experiment 1), or goal-directed actions (i.e., grasping; Experiment 2). Although human children tested previously struggled to override inaccurate information provided by the Guesser when she used communicative cues, in contrast to physical cues or goal-directed actions, dogs were more likely to override the Guesser's information when she used communicative cues or goal-directed actions than when she used non-communicative physical cues. Given that dogs did not show the same selective bias towards the Guesser's information in communicative contexts, these findings provide clear evidence that dogs do not demonstrate a human-like bias to defer to communicative cues. Instead, dogs may be more likely to critically evaluate information presented via communicative cues than either physical or non-communicative cues.

Capuchins (Cebus apella) fail to show an asymmetric dominance effect.

The asymmetric dominance effect (ADE) occurs when the introduction of a partially dominated decoy option increases the choice share of its dominating alternative. The ADE is a violation of regularity and the constant-ratio rule, which are two derivations of the independence of irrelevant alternatives axiom, a core tenant of rational choice. The ADE is one of the most widely reported human choice phenomena, leading researchers to probe its origins by studying a variety of non-human species. We examined the ADE in brown capuchin monkeys (Cebus apella), a species that displays many other decision biases. In Experiment 1, we used a touchscreen method to elicit choice-based preferences for food rewards in asymmetrically dominated choice sets. In Experiments 2 and 3, we distinguished between different types of judgments and used a free selection task to elicit consumption-based preferences for juice rewards. However, we found no evidence for the ADE through violations of regularity or the constant-ratio rule, despite the similarity of our stimuli to other human and non-human experiments. While these results appear to conflict with existing literature on the ADE in non-human species, we point out methodological differences-notably, the distinction between value-based and perception-based stimuli-that have led to a collection of phenomena that are difficult to understand under a unitary theoretical framework. In particular, we highlight key differences between the human and non-human research and provide a series of steps that researchers could take to better understand the ADE.

Exploring the evolutionary origins of overimitation: a comparison across domesticated and non-domesticated canids.

When learning from others, human children tend to faithfully copy - or 'overimitate' - the actions of a demonstrator, even when these actions are irrelevant for solving the task at hand. We investigate whether domesticated dogs (Canis familiaris) and dingoes (Canis dingo) share this tendency to overimitate in three experiments. In Experiment 1, dogs and dingoes had the opportunity to solve a puzzle after watching an ostensive demonstrator who used both a relevant action and an irrelevant action. We find clear evidence against overimitation in both species. In contrast to human children (Horner & Whiten, 2005), dogs and dingoes used the irrelevant action less often across trials, suggesting that both species were filtering out the irrelevant action as they gained experience with the puzzle (like chimpanzees; Horner & Whiten, 2005). Experiments 2 and 3 provide further evidence against overimitation, demonstrating that both species' behavior is better characterized by individual exploration than overimitation. Given that both species, particularly dogs, show human-like social learning in other contexts, these findings provide additional evidence that overimitation may be a unique aspect of human social learning. A video abstract of this article can be viewed at: https://youtu.be/g2mRniJZ7aU.

The evolution of self-control.

Cognition presents evolutionary research with one of its greatest challenges. Cognitive evolution has been explained at the proximate level by shifts in absolute and relative brain volume and at the ultimate level by differences in social and dietary complexity. However, no study has integrated the experimental and phylogenetic approach at the scale required to rigorously test these explanations. Instead, previous research has largely relied on various measures of brain size as proxies for cognitive abilities. We experimentally evaluated these major evolutionary explanations by quantitatively comparing the cognitive performance of 567 individuals representing 36 species on two problem-solving tasks measuring self-control. Phylogenetic analysis revealed that absolute brain volume best predicted performance across species and accounted for considerably more variance than brain volume controlling for body mass. This result corroborates recent advances in evolutionary neurobiology and illustrates the cognitive consequences of cortical reorganization through increases in brain volume. Within primates, dietary breadth but not social group size was a strong predictor of species differences in self-control. Our results implicate robust evolutionary relationships between dietary breadth, absolute brain volume, and self-control. These findings provide a significant first step toward quantifying the primate cognitive phenome and explaining the process of cognitive evolution.

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

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.

Spontaneous Metacognition in Rhesus Monkeys.

Metacognition is the ability to think about thinking. Although monitoring and controlling one's knowledge is a key feature of human cognition, its evolutionary origins are debated. In the current study, we examined whether rhesus monkeys (Macaca mulatta; N = 120) could make metacognitive inferences in a one-shot decision. Each monkey experienced one of four conditions, observing a human appearing to hide a food reward in an apparatus consisting of either one or two tubes. The monkeys tended to search the correct location when they observed this baiting event, but engaged in information seeking-by peering into a center location where they could check both potential hiding spots-if their view had been occluded and information seeking was possible. The monkeys only occasionally approached the center when information seeking was not possible. These results show that monkeys spontaneously use information about their own knowledge states to solve naturalistic foraging problems, and thus provide the first evidence that nonhumans exhibit information-seeking responses in situations with which they have no prior experience.

The evolutionary roots of human decision making.

Humans exhibit a suite of biases when making economic decisions. We review recent research on the origins of human decision making by examining whether similar choice biases are seen in nonhuman primates, our closest phylogenetic relatives. We propose that comparative studies can provide insight into four major questions about the nature of human choice biases that cannot be addressed by studies of our species alone. First, research with other primates can address the evolution of human choice biases and identify shared versus human-unique tendencies in decision making. Second, primate studies can constrain hypotheses about the psychological mechanisms underlying such biases. Third, comparisons of closely related species can identify when distinct mechanisms underlie related biases by examining evolutionary dissociations in choice strategies. Finally, comparative work can provide insight into the biological rationality of economically irrational preferences.

A decade of theory of mind research on Cayo Santiago: Insights into rhesus macaque social cognition.

Over the past several decades, researchers have become increasingly interested in understanding how primates understand the behavior of others. One open question concerns whether nonhuman primates think about others' behavior in psychological terms, that is, whether they have a theory of mind. Over the last ten years, experiments conducted on the free-ranging rhesus monkeys (Macaca mulatta) living on Cayo Santiago have provided important insights into this question. In this review, we highlight what we think are some of the most exciting results of this body of work. Specifically we describe experiments suggesting that rhesus monkeys may understand some psychological states, such as what others see, hear, and know, but that they fail to demonstrate an understanding of others' beliefs. Thus, while some aspects of theory of mind may be shared between humans and other primates, others capacities are likely to be uniquely human. We also discuss some of the broader debates surrounding comparative theory of mind research, as well as what we think may be productive lines for future research with the rhesus macaques of Cayo Santiago.

Another way to learn about teaching: What dogs can tell us about the evolution of pedagogy.

Kline argues that it is crucial to isolate the respective roles of teaching and learning in order to understand how pedagogy has evolved. We argue that doing so requires testing species that learn from pedagogy but that rarely teach themselves. Here, we review how one previously neglected species - domesticated dogs (Canis familiaris) - may allow researchers to do just that.

Capuchins' (Cebus apella) sensitivity to others' goal-directed actions in a helping context.

As humans, our ability to help others effectively is at least in part dependent upon our capacity to infer others' goals in a variety of different contexts. Several species of nonhuman primate have demonstrated that they will also help others in some relatively simple situations, but it is not always clear whether this helping is based on an understanding of another agent's goals. Although the results of a number of different studies support the hypothesis that chimpanzees represent others' goals in various helping contexts and are sensitive to these goals when actually helping others, less work has addressed whether more distantly related species actively represent goals when helping. To explore the cognitive mechanisms underlying helping behaviors in species less closely related to humans, we tested whether a species of New World monkey-the brown capuchin (Cebus apella)-would provide an experimenter with a desired out-of-reach object more often than an alternative object when the experimenter attempted to obtain the former object only. We found that capuchins reliably helped by providing the experimenter's goal object (Experiment 1) and that explanations based on the use of several less sophisticated strategies did not account for the overall pattern of data (Experiments 2-4). Results are thus consistent with the hypothesis that capuchins help others based on an understanding of their goals although more work is needed to address the possibility that capuchins may be responding to gestural and postural factors alone.

Understanding the role of mirror neurons in action understanding will require more than a domain-general account.

Cook et al. propose that mirror neurons emerge developmentally through a domain-general associative mechanism. We argue that experience-sensitivity does not rule out an adaptive or genetic argument for mirror neuron function, and that current evidence suggests that mirror neurons are more specialized than the authors' account would predict. We propose that future work integrate behavioral and neurophysiological techniques used with primates to examine the proposed functions of mirror neurons in action understanding.

Predictions about reward outcomes in rhesus monkeys.

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. (PsycInfo Database Record (c) 2024 APA, all rights reserved).

The influence of interactions with pet dogs on psychological distress.

Many people, including nearly half of American households, own a pet dog. Previous work has found that therapy dog interactions reduce distress, but little work to date has empirically established the mood-enhancing effects of interaction with one's own pet dog. In this study, dog owners (N = 73; 86.3% female, 13.7% male; age 25-77 years) underwent a stress-inducing task followed by random assignment to either (a) interacting with their dog (n = 24), (b) an expectancy control (n = 25; "stress-reducing" coloring books), or (c) a waiting control (n = 24). We compared the effects of each condition on affect and state anxiety. Participants assigned to the dog interaction showed greater increases in positive affect, as well as greater reductions in anxiety compared to both expectancy and waiting controls (ds > 0.72, ps < .018). No significant reductions in negative affect were detected. Second, we found that self-reported experiences with animals, attitudes toward animals, or bondedness with their dog did not differentially predict the condition's impact on the owner's mood. Finally, we coded participants' degree of engagement (e.g., time spent playing) with the dog and found that higher engagement predicted reduced negative affect. Overall, interacting with one's own pet dog reduced owners' distress. Such interactions, which occur commonly in daily life, may have the potential to alleviate distress at a large scale. Precisely how this works and for whom it is especially well suited remain intriguing open questions. (PsycInfo Database Record (c) 2024 APA, all rights reserved).

Solving small spaces: investigating the use of landmark cues in brown capuchins (Cebus apella).

Some researchers have recently argued that humans may be unusual among primates in preferring to use landmark information when reasoning about some kinds of spatial problems. Some have explained this phenomenon by positing that our species' tendency to prefer landmarks stems from a human-unique trait: language. Here, we test this hypothesis-that preferring to use landmarks to solve such tasks is related to language ability-by exploring landmark use in a spatial task in one non-human primate, the brown capuchin monkey (Cebus apella). We presented our subjects with the rotational displacement task, in which subjects attempt to relocate a reward hidden within an array of hiding locations which are subsequently rotated to a new position. Over several experiments, we varied the availability and the salience of a landmark cue within the array. Specifically, we varied (1) visual access to the array during rotation, (2) the type of landmark, (3) the consistency of the landmark qualities, and (4) the amount of exposure to the landmark. Across Experiments 1 through 4, capuchins did not successfully use landmarks cues, suggesting that non-linguistic primates may not spontaneously use landmarks to solve some spatial problems, as in this case of a small-scale dynamic spatial task. Importantly, we also observed that capuchins demonstrated some capacity to learn to use landmarks in Experiment 4, suggesting that non-linguistic creatures may be able to use some landmarks cues in similar spatial tasks with extensive training.