Advanced Cognitive Abilities Research Articles

Group service in macaques (Macaca fuscata), capuchins (Cebus apella) and marmosets (Callithrix jacchus): A comparative approach to identifying proactive prosocial motivations.

Proactive, that is, spontaneous, prosociality reflects a psychological interest in the welfare of others and has been reported in callitrichid monkeys, capuchin monkeys (Cebus apella), and humans, but not in chimpanzees. One explanation for the co-occurrence of proactive prosociality in these species is that it is linked to shared infant care (cooperative breeding); alternatively, it might merely reflect unusually high social tolerance or be mediated by advanced cognitive abilities. To date, distinguishing between these alternative explanations is difficult, partly because available evidence is restricted to only a handful of species and partly because methodological differences thwart comparisons across studies. Here, we present an experimental paradigm called group service, which allows estimation of both social tolerance and proactive prosociality in group settings. Its simplicity makes it intuitively plausible to subjects and allows testing a broad variety of species, including in zoos. We applied the test to independently breeding Japanese macaques (Macaca fuscata), cooperatively breeding common marmosets (Callithrix jacchus), and capuchin monkeys with an intermediate breeding system. Social tolerance was slightly higher in marmosets than capuchins and much higher in both compared to macaques, but only marmosets provided a service to other group members. Furthermore, we validated the group service paradigm in the common marmosets by comparing their performance to earlier data. Although our results are consistent with the cooperative breeding hypothesis, a comprehensive evaluation requires adding data from additional groups and species, which should be facilitated by the group service approach.

Spontaneous innovation in tool manufacture and use in a Goffin’s cockatoo

Summary Accounts of complex tool innovations in animals, particularly in species not adaptively specialized for doing so, are exceedingly rare and often linked to advanced cognitive abilities in the physical domain [1], even though the relation between such capabilities and intelligence is poorly understood [2]. For this reason, discoveries of such capabilities transcend anecdotal value and contribute significantly to comparative cognition [3–5]. Among birds, there are several reports of tool innovations in corvids, but very few documented records in other families (for example [1,3–7]). Here, we report a case of spontaneous tool innovation in the Goffin's cockatoo ( Cacatua goffini ), a species endemic to the Tanimbar archipelago in Indonesia. Like most corellas, they live in social groups (∼10–100) in tropical dry forests, roost in simple tree holes, and feed mainly on a seed based diet (which occasionally causes interference with agriculture) [8]. There are no records of tool-related behavior in the wild. We report how a captive male named Figaro successfully, reliably and repeatedly made and used stick-type tools to rake in food, manufacturing them from two different materials and displaying different steps and techniques.

Group hunting within the Carnivora: physiological, cognitive and environmental influences on strategy and cooperation

Cooperative hunting is believed to have important implications for the evolution of sociality and advanced cognitive abilities. Variation in the level of hunt organisation amongst species and how their cognitive, behavioural and athletic adaptations may contribute to observed patterns of cooperative hunting behaviour, however, are poorly understood. We, therefore, reviewed the literature for evidence of different levels of hunt organisation and cooperation in carnivorans and examined their social and physical adaptations for hunting. Descriptions of group hunting were scarce for many species and often of insufficient detail for us to be able to classify the level of hunt organisation involved. However, despite this, reports of behaviour fitting the description of collaboration, the most advanced level of hunt organisation, were found in over half the carnivorans reported to hunt cooperatively. There was no evidence that this behaviour would require advanced cognitive abilities. However, there was some evidence that both social mechanisms reducing aggression between group members and information transfer amongst individuals may aid cooperative hunting. In general, the cooperative strategies used seemed to depend partly on the species’ locomotor abilities and habitat. There was some evidence that individuals take on consistent roles during cooperative hunts in some species, but it was not clear if this reflects individuals’ physical differences, social factors or life experiences. Better understanding of the social, cognitive and physical mechanisms underlying cooperative hunting, and indeed establishing to what degree it exists in the first instance, will require more data for multiple individuals and species over many hunts.

Cooperation and the evolution of intelligence.

The high levels of intelligence seen in humans, other primates, certain cetaceans and birds remain a major puzzle for evolutionary biologists, anthropologists and psychologists. It has long been held that social interactions provide the selection pressures necessary for the evolution of advanced cognitive abilities (the ‘social intelligence hypothesis’), and in recent years decision-making in the context of cooperative social interactions has been conjectured to be of particular importance. Here we use an artificial neural network model to show that selection for efficient decision-making in cooperative dilemmas can give rise to selection pressures for greater cognitive abilities, and that intelligent strategies can themselves select for greater intelligence, leading to a Machiavellian arms race. Our results provide mechanistic support for the social intelligence hypothesis, highlight the potential importance of cooperative behaviour in the evolution of intelligence and may help us to explain the distribution of cooperation with intelligence across taxa.

The Nexus between Neurodegeneration and Advanced Cognitive Abilities

The Nexus between Neurodegeneration and Advanced Cognitive Abilities

Ontogeny of Social Relations and Coalition Formation in Common Ravens (Corvus corax)

The social intelligence hypothesis, originally developed for primates to explain their high intelligence and large relative brain size, assumes that challenges posed by social life in complex societies with many group members lead to the evolution of advanced cognitive abilities. In birds, pair-bonded species have larger brains than non-pair bonded species, indicating that the quality of social relationships better predicts social complexity than group size. Ravens are a long-term monogamous and territorial species, renowned for their sophisticated socio-cognitive skills and complex social relationships. Notably, during their early years they live in fission-fusion-like non-breeder societies in which social relationships could be of particular importance. Here we observed the development of dominance and affiliative relationships in 12 hand-raised captive ravens, examining the influence of age, sex and kinship on social interactions. Furthermore, we investigated at which developmental step a stable hierarchy emerged, whether third-party interventions played a role and how selectively birds intervened in others' conflicts. At 4-5 months post-fledging, we found an increase in socio-positive behaviour and a decrease in aggression, along with the establishment of a linear dominance rank hierarchy. In line with kin selection theory, siblings exhibited a greater degree of tolerance and engaged in more socio-positive behaviour. In their first few months, ravens frequently intervened in others' conflicts but supported mainly the aggressor; later on, their support became more selective towards kin and close social partners. These findings indicate that ravens engage in sophisticated social behaviours and form stable relationships already in their first year of life.

No observable relationship between the 12 genes of nervous system and reasoning skill in a young Chinese Han population.

Reasoning skill is an advanced cognitive ability which is needed for drawing inferences from given information. It is well known that the ability depends on the neural network of the frontal and parietal brain regions. In this study, we hypothesized that some genes involved in neurotransmitter systems were related to reasoning skill. To confirm this hypothesis, we examined the effects of 13 genes (BDNF, NRSF, COMT, DBH, DRD(2), DRD(3), DAT(1), MAOA, GRM(1), GRIN2B, TPH(2), 5-HT(2A), and 5-HT(6)) in neurotransmitter systems on the non-verbal reasoning and verbal reasoning skills. The results indicated there were on significant effects of the 17 functional variants of these genes on the performance of non-verbal reasoning and verbal analogical reasoning skills (χ(2) > 3.84, df = 1, P > 0.05). This study suggests that some of the functional variations in BDNF, COMT, DBH, DRD(2), DRD(3), MAOA, 5-HT(2A), 5-HT(6), GRM(1), and GRIN2B have no observable effects on the certain reasoning skills in a young healthy Chinese Han population.

Inertia: the discrepancy between individual and common good in dispersal and prospecting behaviour

The group selection debate of the 1960s made it clear that evolution does not necessarily increase population performance. Individuals can be selected to have traits that diminish a common good and make population persistence difficult. At the extreme, the discrepancy between levels of selection is predicted to make traits evolve towards values at which a population can no longer persist (evolutionary suicide). Dispersal and prospecting are prime examples of traits that have a strong influence on population persistence under environmental and demographic stochasticity. Theory predicts that an 'optimal' dispersal strategy from a population point of view can differ considerably from that produced by individual-level selection. Because dispersal is frequently risky or otherwise costly, individuals are often predicted to disperse less than would be ideal for population performance (persistence or size). We define this discrepancy as 'inertia' and examine current knowledge of its occurrence and effects on population dynamics in nature. We argue that inertia is potentially widespread but that a framework is currently lacking for predicting precisely the extent to which it has a real influence on population persistence. The opposite of inertia, 'hypermobility' (more dispersal by individuals than would maximize population performance) remains a possibility: it is known that highest dispersal rates do not lead to best expected population performance, and examples of such high dispersal evolving exist at least in the theoretical literature. We also show, by considering prospecting behaviour, that similar issues arise in species with advanced cognitive and learning abilities. Individual prospecting strategies and the information acquired during dispersal are known to influence the decisions and therefore the fate of individuals and, as a corollary, populations. Again, the willingness of individuals to sample environments might evolve to levels that are not optimal for populations. This conflict can take intriguing forms. For example, better cognitive abilities of individuals may not always lead to better population-level performance. Simulation studies have found that 'blind' dispersal can lead to better connected metapopulations than cognitively more advanced habitat choice rules: the latter can lead to too many individuals sticking to nearby safe habitat. The study of the mismatch between individual and population fitness should not be a mere intellectual exercise. Population managers typically need to take a population-level view of performance, which may necessitate human intervention if it differs from what is selected for. We conclude that our knowledge of inertia and hypermobility would advance faster if theoretical studies--without much additional effort--quantified the population consequences of the evolving traits and compared this with hypothetical (not selectively favoured) dispersal rules, and if empirical studies were similarly conducted with the differing levels of selection in mind.

Tool‐like behavior in the sixbar wrasse, Thalassoma hardwicke (Bennett, 1830)

There are only a few documented cases of the use of either tools or substrates (anvils) as pseudotools in fishes. Described here is an anvil behavior of a labrid fish, Thalassoma hardwicke, observed under aquarium conditions. This fish was fed with pellets that are too large to swallow and too hard to break up into manageable bits using jaws only. The observed individual carried a pellet to an anvil to break it up into pieces small enough to be swallowed. This feeding behavior was frequently repeated (observed in detail about 15 times), nearly always successful, and remarkably consistent, suggesting that the rock selected for an anvil is remembered and its functional qualities or other factors may play a part in its choice. These observations agree with evidence for other advanced cognitive abilities in members of the genus Thalassoma and suggest that, for welfare demand, rocks with rough surfaces should be provided to these fish, especially when they receive hard food for variety.

Cooperation among non-relatives evolves by state-dependent generalized reciprocity

For decades, attempts to understand cooperation between non-kin have generated substantial theoretical and empirical interest in the evolutionary mechanisms of reciprocal altruism. There is growing evidence that the cognitive limitations of animals can hinder direct and indirect reciprocity because the necessary mental capacity is costly. Here, we show that cooperation can evolve by generalized reciprocity (help anyone, if helped by someone) even in large groups, if individuals base their decision to cooperate on a state variable updated by the outcome of the last interaction with an anonymous partner. We demonstrate that this alternative mechanism emerges through small evolutionary steps under a wide range of conditions. Since this state-based generalized reciprocity works without advanced cognitive abilities it may help to understand the evolution of complex social behaviour in a wide range of organisms.

Cognitive Processes Associated with Sequential Tool Use in New Caledonian Crows

BackgroundUsing tools to act on non-food objects—for example, to make other tools—is considered to be a hallmark of human intelligence, and may have been a crucial step in our evolution. One form of this behaviour, ‘sequential tool use’, has been observed in a number of non-human primates and even in one bird, the New Caledonian crow (Corvus moneduloides). While sequential tool use has often been interpreted as evidence for advanced cognitive abilities, such as planning and analogical reasoning, the behaviour itself can be underpinned by a range of different cognitive mechanisms, which have never been explicitly examined. Here, we present experiments that not only demonstrate new tool-using capabilities in New Caledonian crows, but allow examination of the extent to which crows understand the physical interactions involved.Methodology/Principal FindingsIn two experiments, we tested seven captive New Caledonian crows in six tasks requiring the use of up to three different tools in a sequence to retrieve food. Our study incorporated several novel features: (i) we tested crows on a three-tool problem (subjects were required to use a tool to retrieve a second tool, then use the second tool to retrieve a third one, and finally use the third one to reach for food); (ii) we presented tasks of different complexity in random rather than progressive order; (iii) we included a number of control conditions to test whether tool retrieval was goal-directed; and (iv) we manipulated the subjects' pre-testing experience. Five subjects successfully used tools in a sequence (four from their first trial), and four subjects repeatedly solved the three-tool condition. Sequential tool use did not require, but was enhanced by, pre-training on each element in the sequence (‘chaining’), an explanation that could not be ruled out in earlier studies. By analyzing tool choice, tool swapping and improvement over time, we show that successful subjects did not use a random probing strategy. However, we find no firm evidence to support previous claims that sequential tool use demonstrates analogical reasoning or human-like planning.Conclusions/SignificanceWhile the ability of subjects to use three tools in sequence reveals a competence beyond that observed in any other species, our study also emphasises the importance of parsimony in comparative cognitive science: seemingly intelligent behaviour can be achieved without the involvement of high-level mental faculties, and detailed analyses are necessary before accepting claims for complex cognitive abilities.

What You See Is What You Get? Exclusion Performances in Ravens and Keas

BackgroundAmong birds, corvids and parrots are prime candidates for advanced cognitive abilities. Still, hardly anything is known about cognitive similarities and dissimilarities between them. Recently, exclusion has gained increasing interest in comparative cognition. To select the correct option in an exclusion task, one option has to be rejected (or excluded) and the correct option may be inferred, which raises the possibility that causal understanding is involved. However, little is yet known about its evolutionary history, as only few species, and mainly mammals, have been studied.Methodology/Principal FindingsWe tested ravens and keas in a choice task requiring the search for food in two differently shaped tubes. We provided the birds with partial information about the content of one of the two tubes and asked whether they could use this information to infer the location of the hidden food and adjust their searching behaviour accordingly. Additionally, this setup allowed us to investigate whether the birds would appreciate the impact of the shape of the tubes on the visibility of food. The keas chose the baited tube more often than the ravens. However, the ravens applied the more efficient strategy, choosing by exclusion more frequently than the keas. An additional experiment confirmed this, indicating that ravens and keas either differ in their cognitive skills or that they apply them differently.ConclusionTo our knowledge, this is the first study to demonstrate that corvids and parrots may perform differently in cognitive tasks, highlighting the potential impact of different selection pressures on the cognitive evolution of these large-brained birds.

Imitation and the development of infant learning, memory, and categorisation

The ability to copy the actions of others is present from birth in both infant humans and chimpanzees and provides a method for the social transmission of knowledge. For this type of learning to have an impact over the long-term, the infant must be able to encode, store, and retrieve the information they receive for use at a later date. Here we review the literature with the deferred imitation paradigm to demonstrate that by at least 6 months of age, human infants are capable of these comparatively advanced cognitive abilities, which are thought to involve the declarative memory system and the hippocampal formation. Across early development there are dramatic changes in the duration over which information can be retained and the ability of infants to retrieve and express their memories in a flexible manner, which enables them to solve new problems. Research with the deferred imitation paradigm therefore provides important insight into our understanding of social and cognitive development as well as brain development.

Electrophysiological correlates for response inhibition in intellectually gifted children: A Go/NoGo study

Superior response inhibition is an essential component of the advanced cognitive abilities of gifted children. This study investigated response inhibition in intellectually gifted children by recording event-related brain potentials (ERPs) during a Go/NoGo task. Fifteen intellectually gifted children and 15 intellectually average children participated. Our present findings showed that intellectually gifted children had shorter Go-P3 latency, indicating faster processing of Go stimuli, a finding consistent with previous studies. We focused on the two inhibition-related components, NoGo-N2 and NoGo-P3. The results showed that NoGo-P3 latency was shorter for intellectually gifted children compared to their average peers. N2 latency did not indicate the intelligence difference. These results suggested that intellectually gifted children showed faster inhibition when dealing with NoGo stimuli, and this superiority came from the later stages of inhibition, i.e., response evaluation or the success of inhibiting a response, as indexed by the shorter P3 latency.

Self-medication as adaptive plasticity: increased ingestion of plant toxins by parasitized caterpillars.

Self-medication is a specific therapeutic behavioral change in response to disease or parasitism. The empirical literature on self-medication has so far focused entirely on identifying cases of self-medication in which particular behaviors are linked to therapeutic outcomes. In this study, we frame self-medication in the broader realm of adaptive plasticity, which provides several testable predictions for verifying self-medication and advancing its conceptual significance. First, self-medication behavior should improve the fitness of animals infected by parasites or pathogens. Second, self-medication behavior in the absence of infection should decrease fitness. Third, infection should induce self-medication behavior. The few rigorous studies of self-medication in non-human animals have not used this theoretical framework and thus have not tested fitness costs of self-medication in the absence of disease or parasitism. Here we use manipulative experiments to test these predictions with the foraging behavior of woolly bear caterpillars (Grammia incorrupta; Lepidoptera: Arctiidae) in response to their lethal endoparasites (tachinid flies). Our experiments show that the ingestion of plant toxins called pyrrolizidine alkaloids improves the survival of parasitized caterpillars by conferring resistance against tachinid flies. Consistent with theoretical prediction, excessive ingestion of these toxins reduces the survival of unparasitized caterpillars. Parasitized caterpillars are more likely than unparasitized caterpillars to specifically ingest large amounts of pyrrolizidine alkaloids. This case challenges the conventional view that self-medication behavior is restricted to animals with advanced cognitive abilities, such as primates, and empowers the science of self-medication by placing it in the domain of adaptive plasticity theory.

TATIANA IVANOVNA ALEKSEYEVA

Neuroscience and artificial intelligence (AI) share a long history of collaboration. Advances in neuroscience, alongside huge leaps in computer processing power over the last few decades, have given rise to a new generation of in silico neural networks inspired by the architecture of the brain. These AI systems are now capable of many of the advanced perceptual and cognitive abilities of biological systems, including object recognition and decision making. Moreover, AI is now increasingly being employed as a tool for neuroscience research and is transforming our understanding of brain functions. In particular, deep learning has been used to model how convolutional layers and recurrent connections in the brain’s cerebral cortex control important functions, including visual processing, memory, and motor control. Excitingly, the use of neuroscience-inspired AI also holds great promise for understanding how changes in brain networks result in psychopathologies, and could even be utilized in treatment regimes. Here we discuss recent advancements in four areas in which the relationship between neuroscience and AI has led to major advancements in the field; (1) AI models of working memory, (2) AI visual processing, (3) AI analysis of big neuroscience datasets, and (4) computational psychiatry.

Comparing responses to novel objects in wild baboons (Papio ursinus) and geladas (Theropithecus gelada)

Behavioral flexibility is considered by some to be one of the hallmarks of advanced cognitive ability. One measure of behavioral flexibility is how subjects respond to novel objects. Despite growing interest in comparative cognition, no comparative research on neophilia in wild primates has been conducted. Here, we compare responses to novel objects in wild chacma baboons (Papio ursinus) and geladas (Theropithecus gelada). Baboons and geladas are closely related taxa, yet they differ in their ecology and degree of social tolerance: (1) baboons are habitat and dietary generalists, whereas geladas have one of the most specialized primate diets (90% grass); (2) baboons exhibit an aversion toward extra-group individuals, whereas geladas typically exhibit an attraction toward them. Using subjects of all age and sex classes, we examined responses to three different objects: a plastic doll, a rubber ball, and a metal can. Overall, baboon subjects exhibited stronger responses to the objects (greater neophilia and exploration) than gelada subjects, yet we found no evidence that the geladas were afraid of the objects. Furthermore, baboons interacted with the objects in the same way they might interact with a potential food item. Responses were unrelated to sex, but immatures showed more object exploration than adults. Results corroborate novel object research conducted in captive populations and suggest that baboons and geladas have differences in behavioral flexibility (at least in this cognitive domain) that have been shaped by ecological (rather than social) differences between the two species.

Reconstructing elements and processes of human cognitive evolution in monkey brain

Based on evidence that a particular behavioral history can modify neural connectivity in subjects, I propose a comparative approach for studying a possible course of human cognitive evolution in nonhuman species. This is exemplified by our research on “sensory tool use” in Japanese monkeys. Monkeys were trained to use a sensory tool that was used to obtain sensory information, with the aim of inducing human-specific tool use. Training started with a use of a motor-tool for substituting for motor effectors. By means of systematic shaping techniques, monkeys successfully acquired complete use of the sensory tool (a kind of endoscope attached to a rake) to explore the entire table to find food. This induction of sensory tool use in a monkey species offers a novel comparative framework to the study of the evolution of advanced cognitive abilities in humans through a recursive interaction between individual and environment.

Other-regarding preferences in a non-human primate: common marmosets provision food altruistically.

Human cooperation is unparalleled in the animal world and rests on an altruistic concern for the welfare of genetically unrelated strangers. The evolutionary roots of human altruism, however, remain poorly understood. Recent evidence suggests a discontinuity between humans and other primates because individual chimpanzees do not spontaneously provide food to other group members, indicating a lack of concern for their welfare. Here, we demonstrate that common marmoset monkeys (Callithrix jacchus) do spontaneously provide food to nonreciprocating and genetically unrelated individuals, indicating that other-regarding preferences are not unique to humans and that their evolution did not require advanced cognitive abilities such as theory of mind. Because humans and marmosets are cooperative breeders and the only two primate taxa in which such unsolicited prosociality has been found, we conclude that these prosocial predispositions may emanate from cooperative breeding.

Mesial Temporal Lobe Epilepsy Impairs Advanced Social Cognition

Although memory, language, and executive functions have been extensively studied in patients with mesial temporal lobe epilepsy (MTLE), investigations into advanced social cognitive abilities have been neglected. In the present study, we investigated the ability to detect social faux pas and studied possible mediating clinical and demographic variables in patients with MTLE compared with patients with an epilepsy not originating within the MTLE and healthy controls. The 27 MTLE patients (16 were investigated pre- and 11 postoperatively), 27 patients with an extramesiotemporal epilepsy (except frontal lobe epilepsy), and 12 healthy controls performed a shortened version of the faux-pas test. Additionally, we used standardized tests to measure intelligence. Only patients with intact reading-comprehension abilities were included in the study. MTLE patients, both pre- and postoperative, performed the faux-pas test significantly worse than patients with extramesiotemporal lobe epilepsy and healthy controls. The latter two groups showed comparable performance. No statistical association was found between the MTLE patients' deficit in recognizing a faux pas and the variables IQ, age, age at seizure onset, and duration of epilepsy. We report for the first time that patients with MTLE are specifically impaired in recognizing faux pas, suggesting that MTLE as such is a specific etiology of deficits in higher-order social cognition.