Gaze following in Archosauria-Alligators and palaeognath birds suggest dinosaur origin of visual perspective taking.

Taking someone else's visual perspective marks an evolutionary shift in the formation of advanced social cognition. It enables using others' attention to discover otherwise hidden aspects of the surroundings and is foundational for human communication and understanding of others. Visual perspective taking has also been found in some other primates, a few songbirds, and some canids. However, despite its essential role for social cognition, visual perspective taking has only been fragmentedly studied in animals, leaving its evolution and origins uncharted. To begin to narrow this knowledge gap, we investigated extant archosaurs by comparing the neurocognitively least derived extant birds-palaeognaths-with the closest living relatives of birds, the crocodylians. In a gaze following paradigm, we showed that palaeognaths engage in visual perspective taking and grasp the referentiality of gazes, while crocodylians do not. This suggests that visual perspective taking originated in early birds or nonavian dinosaurs-likely earlier than in mammals.

The selfish preen: absence of allopreening in Palaeognathae and its socio-cognitive implications.

Preening behaviours are widespread in extant birds. While most birds appear to autopreen (self-directed preening), allopreening (preening directed at conspecifics) seems to have emerged only in certain species, but across many families. Allopreening has been hypothesised to reinforce mutual relationships and cooperation between individuals, and to underpin various socio-cognitive abilities. Palaeognathae is a bird group exhibiting neurocognitively plesiomorphic traits compared to other birds. They share many features with non-avian paravian dinosaurs and are thus important for the study of cognitive evolution in birds. Despite this, and the important correlation of allopreening with many complicated social behaviours, allopreening has not been systematically studied in Palaeognathae. Therefore, we examined the preening behaviours in four species of palaeognaths: common ostriches (Struthio camelus), greater rheas (Rhea americana), emus (Dromaius novaehollandiae), and elegant crested tinamous (Eudromia elegans). We compared findings with common ravens (Corvus corax), a neognath species known for its allopreening and complex social cognition. We found autopreening, but no allopreening, in the palaeognath species, while both autopreening and allopreening was found in common ravens. The absence of allopreening in Palaeognathae suggests an emergence of this behaviour within Neognathae. We contextualise our results in relation to the socio-cognitive underpinnings of allopreening and its implications for the understanding of the evolution of socio-cognitive abilities in non-avian paravian dinosaurs and early birds.

Differential responses to con- and allospecific visual cues in juvenile ravens (Corvus corax): the ontogeny of gaze following and social predictions.

Gaze following refers to the ability to co-orient with others' gaze directions. Ontogenetic studies on gaze following in animals have predominantly used human experimenters as demonstrators. It is, however, likely that developing animals are initially more attuned to individuals from their own species, which might result in differences in the ontogenetic onset of gaze following with human and conspecific demonstrators. "Checking back" is a signature behaviour in the gaze following repertoires of humans, apes, and some Old world monkeys. It is commonly interpreted as a representation of the referentiality of gaze and is thus diagnostic of social predictions. Recently, "checking back" has been discovered in four avian species, suggesting a shared skill among birds. To investigate effects of con- and allospecific demonstrators on gaze following responses, we studied visual co-orientations of four hand-raised juvenile common ravens (Corvus corax) with human and conspecific gaze cues. Moreover, we for the first time investigated "checking back" in ravens and compared the effects of con- and allospecific demonstrators on this behaviour. Ravens followed human and conspecific gaze with no apparent differences in ontogenetic onset, but after significantly longer latencies with human demonstrators. Subjects moreover already checked back at 30 days old and did so significantly more often with conspecific demonstrators. Our findings suggest differences in processing speed and social predictions of human and conspecific gazes, indicating an underlying neurocognitive mechanism attuned to social information gathering from conspecifics. We propose more studies using conspecific demonstrators to reveal the full gaze following potential of a species.

Gaze following: A socio-cognitive skill rooted in deep time.

Social gaze has received much attention in social cognition research in both human and non-human animals. Gaze following appears to be a central skill for acquiring social information, such as the location of food and predators, but can also draw attention to important social interactions, which in turn promotes the evolution of more complex socio-cognitive processes such as theory of mind and social learning. In the past decades, a large number of studies has been conducted in this field introducing differing methodologies. Thereby, various factors influencing the results of gaze following experiments have been identified. This review provides an overview of the advances in the study of gaze following, but also highlights some limitations within the research area. The majority of gaze following studies on animals have focused on primates and canids, which limits evolutionary interpretations to only a few and closely related evolutionary lineages. This review incorporates new insights gained from previously understudied taxa, such as fishes, reptiles, and birds, but it will also provide a brief outline of mammal studies. We propose that the foundations of gaze following emerged early in evolutionary history. Basic, reflexive co-orienting responses might have already evolved in fishes, which would explain the ubiquity of gaze following seen in the amniotes. More complex skills, such as geometrical gaze following and the ability to form social predictions based on gaze, seem to have evolved separately at least two times and appear to be correlated with growing complexity in brain anatomy such as increased numbers of brain neurons. However, more studies on different taxa in key phylogenetic positions are needed to better understand the evolutionary history of this fundamental socio-cognitive skill.

Goffin's Cockatoos (Cacatua goffiniana) Can Solve a Novel Problem After Conflicting Past Experiences.

Novel problems often partially overlap with familiar ones. Some features match the qualities of previous situations stored in long-term memory and therefore trigger their retrieval. Using relevant, while inhibiting irrelevant, memories to solve novel problems is a hallmark of behavioral flexibility in humans and has recently been demonstrated in great apes. This capacity has been proposed to promote technical innovativeness and thus warrants investigations of such a mechanism in other innovative species. Here, we show that proficient tool-users among Goffin's cockatoos-an innovative tool-using species-could use a relevant previous experience to solve a novel, partially overlapping problem, even despite a conflicting, potentially misleading, experience. This suggests that selecting relevant experiences over irrelevant experiences guides problem solving at least in some Goffin's cockatoos. Our result supports the hypothesis that flexible memory functions may promote technical innovations.

Great apes selectively retrieve relevant memories to guide action.

Memory allows us to draw on past experiences to inform behaviour in the present. However, memories rarely match the situation at hand exactly, and new situations regularly trigger multiple related memories where only some are relevant to act upon. The flexibility of human memory systems is largely attributed to the ability to disregard irrelevant, but salient, memories in favour of relevant ones. This is considered an expression of an executive function responsible for suppressing irrelevant memories, associated with the prefrontal cortex. It is unclear to what extent animals have access to this ability. Here, we demonstrate, in a series of tool-use tasks designed to evoke conflicting memories, that chimpanzees and an orangutan suffer from this conflict but overcome it in favour of a more relevant memory. Such mnemonic flexibility is among the most advanced expressions of executive function shown in animals to date and might explain several behaviours related to tool-use, innovation, planning and more.

Investigating information seeking in ravens (Corvus corax).

Measuring the responses of non-human animals to situations of uncertainty is thought to shed light on an animal's metacognitive processes; namely, whether they monitor their own knowledge states. For example, when presented with a foraging task, great apes and macaques selectively seek information about the location of a food item when they have not seen where it was hidden, compared to when they have. We presented this same information seeking task to ravens, in which a food item was hidden in one of three containers, and subjects could either watch where the food was hidden, infer its location through visual or auditory clues, or were given no information. We found that unlike several ape species and macaques, but similar to capuchin monkeys, the ravens looked inside at least one tube on every trial, but typically only once, inside the baited tube, when they had either witnessed it being baited or could visually infer the reward's location. In contrast, subjects looked more often within trials in which they had not witnessed the baiting or were provided with auditory cues about the reward's location. Several potential explanations for these ceiling levels of looking are discussed, including how it may relate to the uncertainty faced by ravens when retrieving food caches.

A theory stuck in evolutionary and historical time.

We argue that the two temporal cognition systems are conceptually too confined to be helpful in understanding the evolution of temporal cognition. In fact, we doubt there are two systems. In relation to this, we question that the authors did not describe the results of our planning study on ravens correctly, as this is of consequence to their theory.

Cats Parallel Great Apes and Corvids in Motor Self-Regulation - Not Brain but Material Size Matters.

The inhibition of unproductive motor movements is regarded as a fundamental cognitive mechanism. Recently it has been shown that species with large absolute brain size or high numbers of pallial neurons, like great apes and corvids, show the highest performance on a task purportedly measuring this mechanism: the cylinder task. In this task the subject must detour a perpendicularly oriented transparent cylinder to reach a reward through a side opening, instead of directly reaching for it and bumping into the front, which is regarded as an inhibitory failure. Here we test domestic cats, for the first time, and show that they can reach the same levels as great apes and corvids on this task, despite having much smaller brains. We tested subjects with apparatuses that varied in size (cylinder length and diameter) and material (glass or plastic), and found that subjects performed best on the large cylinders. As numbers of successes decreased significantly when the cylinders were smaller, we conducted additionally two experiments to discern which properties (length of the transparent surface, goal distance from the surface, size of the side opening) affects performance. We conclude that sensorimotor requirements, which differ between species, may have large impact on the results in such seemingly simple and apparently comparable tests. However, we also conclude that cats have comparably high levels of motor self-regulation, despite the differences between tests.

Comparing chimpanzees' preparatory responses to known and unknown future outcomes.

When humans plan for the future, we recognize not only that one particular event may occur, but that the future can have different, mutually exclusive possible outcomes. A recent study by Suddendorf et al (Suddendorf 2017 Biol. Lett.13, 20170170 (doi:10.1098/rsbl.2017.0170)) suggests that young children (less than 3 years) and apes lack this capacity, as demonstrated by their failure to cover each of two tube openings to ensure catching an object that would drop randomly from one of the tubes. Before drawing conclusions based on these negative results, however, it is important to assess subjects' failures and test the reliability of the task itself. To explore whether the apes' performance resulted from an inability to represent mutually exclusive futures or from extraneous factors related to the task, we replicated the methods of Suddendorf et al (Suddendorf 2017 Biol. Lett.13, 20170170 (doi:10.1098/rsbl.2017.0170)) with a group of six chimpanzees but included a key control condition in which subjects were expected to cover both tubes on every trial (i.e. the rewards would consistently emerge from both tubes). We show that even in this straightforward condition in which the outcome of the trial was known, only four of the six subjects ever covered both tubes, typically doing so after a minimum of 17 trials, and often reverting back to covering one tube on later trials. We conclude that this task is not valid for testing the ability to represent mutually exclusive futures. We discuss what potential factors may explain the results and outline a new suggested method to continue testing for this capacity in the future.

The detour paradigm in animal cognition.

In this paper, we review one of the oldest paradigms used in animal cognition: the detour paradigm. The paradigm presents the subject with a situation where a direct route to the goal is blocked and a detour must be made to reach it. Often being an ecologically valid and a versatile tool, the detour paradigm has been used to study diverse cognitive skills like insight, social learning, inhibitory control and route planning. Due to the relative ease of administrating detour tasks, the paradigm has lately been used in large-scale comparative studies in order to investigate the evolution of inhibitory control. Here we review the detour paradigm and some of its cognitive requirements, we identify various ecological and contextual factors that might affect detour performance, we also discuss developmental and neurological underpinnings of detour behaviors, and we suggest some methodological approaches to make species comparisons more robust.

The Development of Motor Self-Regulation in Ravens.

Inhibitory control refers to the ability to stop impulses in favor of more appropriate behavior, and it constitutes one of the underlying cognitive functions associated with cognitive flexibility. Much attention has been given to cross-species comparisons of inhibitory control; however, less is known about how and when these abilities develop. Mapping the ontogeny of inhibitory control in different species may therefore reveal foundational elements behind cognitive processes and their evolution. In this study, we tested the development of motor self-regulation in raven chicks (Corvus corax), using two detour tasks that required inhibition of motor impulses to directly reach for a visible reward behind a barrier. One task included a mesh barrier, which partly occluded the reward, and the other task used a completely transparent barrier, the cylinder task. The results suggest that the more visible a reward is, the more difficult it is to inhibit motor impulses toward it, and further, that this inhibitory challenge gradually decreases during development. The mesh barrier is reliably detoured before the animals pass the task with the wholly transparent cylinder. As the majority of the birds begun testing as nestlings, and as we provided them with experiences they normally would not receive in a nest, it is likely that they showed the earliest possible onset of these skills. A control subject, tested at a later age, showed that the mesh detours required no particular training, but that tasks including complete transparency likely require more specific experiences. Adult ravens without explicit training are highly proficient in inhibitory detour tasks, and, together with chimpanzees, they are the best performers of all tested species in the cylinder task. Our results suggest that their skills develop early in life, around their third month. Their developmental pattern of inhibitory skills for detours resembles that of children and rhesus macaques, albeit the pace of development is markedly faster in ravens. Investigating the development of cognition is crucial to understanding its foundations within and across species.

Are parrots poor at motor self-regulation or is the cylinder task poor at measuring it?

The ability to inhibit unproductive motor responses triggered by salient stimuli is a fundamental inhibitory skill. Such motor self-regulation is thought to underlie more complex cognitive mechanisms, like self-control. Recently, a large-scale study, comparing 36 species, found that absolute brain size best predicted competence in motor inhibition, with great apes as the best performers. This was challenged when three Corvus species (corvids) were found to parallel great apes despite having much smaller absolute brain sizes. However, new analyses suggest that it is the number of pallial neurons, and not absolute brain size per se, that correlates with levels of motor inhibition. Both studies used the cylinder task, a detour-reaching test where food is presented behind a transparent barrier. We tested four species from the order Psittaciformes (parrots) on this task. Like corvids, many parrots have relatively large brains, high numbers of pallial neurons, and solve challenging cognitive tasks. Nonetheless, parrots performed markedly worse than the Corvus species in the cylinder task and exhibited strong learning effects in performance and response times. Our results suggest either that parrots are poor at controlling their motor impulses, and hence that pallial neuronal numbers do not always correlate with such skills, or that the widely used cylinder task may not be a good measure of motor inhibition.

Ravens parallel great apes in flexible planning for tool-use and bartering.

The ability to flexibly plan for events outside of the current sensory scope is at the core of being human and is crucial to our everyday lives and society. Studies on apes have shaped a belief that this ability evolved within the hominid lineage. Corvids, however, have shown evidence of planning their food hoarding, although this has been suggested to reflect a specific caching adaptation rather than domain-general planning. Here, we show that ravens plan for events unrelated to caching-tool-use and bartering-with delays of up to 17 hours, exert self-control, and consider temporal distance to future events. Their performance parallels that seen in apes and suggests that planning evolved independently in corvids, which opens new avenues for the study of cognitive evolution.

Affective forecasting in an orangutan: predicting the hedonic outcome of novel juice mixes.

Affective forecasting is an ability that allows the prediction of the hedonic outcome of never-before experienced situations, by mentally recombining elements of prior experiences into possible scenarios, and pre-experiencing what these might feel like. It has been hypothesised that this ability is uniquely human. For example, given prior experience with the ingredients, but in the absence of direct experience with the mixture, only humans are said to be able to predict that lemonade tastes better with sugar than without it. Non-human animals, on the other hand, are claimed to be confined to predicting-exclusively and inflexibly-the outcome of previously experienced situations. Relying on gustatory stimuli, we devised a non-verbal method for assessing affective forecasting and tested comparatively one Sumatran orangutan and ten human participants. Administered as binary choices, the test required the participants to mentally construct novel juice blends from familiar ingredients and to make hedonic predictions concerning the ensuing mixes. The orangutan's performance was within the range of that shown by the humans. Both species made consistent choices that reflected independently measured taste preferences for the stimuli. Statistical models fitted to the data confirmed the predictive accuracy of such a relationship. The orangutan, just like humans, thus seems to have been able to make hedonic predictions concerning never-before experienced events.

A novel tool-use mode in animals: New Caledonian crows insert tools to transport objects.

New Caledonian crows (Corvus moneduloides) rely heavily on a range of tools to extract prey. They manufacture novel tools, save tools for later use, and have morphological features that facilitate tool use. We report six observations, in two individuals, of a novel tool-use mode not previously reported in non-human animals. Insert-and-transport tool use involves inserting a stick into an object and then moving away, thereby transporting both object and tool. All transported objects were non-food objects. One subject used a stick to transport an object that was too large to be handled by beak, which suggests the tool facilitated object control. The function in the other cases is unclear but seems to be an expression of play or exploration. Further studies should investigate whether it is adaptive in the wild and to what extent crows can flexibly apply the behaviour in experimental settings when purposive transportation of objects is advantageous.

Ravens, New Caledonian crows and jackdaws parallel great apes in motor self-regulation despite smaller brains.

Overriding motor impulses instigated by salient perceptual stimuli represent a fundamental inhibitory skill. Such motor self-regulation facilitates more rational behaviour, as it brings economy into the bodily interaction with the physical and social world. It also underlies certain complex cognitive processes including decision making. Recently, MacLean et al. (MacLean et al. 2014 Proc. Natl Acad. Sci. USA 111, 2140-2148. (doi:10.1073/pnas.1323533111)) conducted a large-scale study involving 36 species, comparing motor self-regulation across taxa. They concluded that absolute brain size predicts level of performance. The great apes were most successful. Only a few of the species tested were birds. Given birds' small brain size-in absolute terms-yet flexible behaviour, their motor self-regulation calls for closer study. Corvids exhibit some of the largest relative avian brain sizes-although small in absolute measure-as well as the most flexible cognition in the animal kingdom. We therefore tested ravens, New Caledonian crows and jackdaws in the so-called cylinder task. We found performance indistinguishable from that of great apes despite the much smaller brains. We found both absolute and relative brain volume to be a reliable predictor of performance within Aves. The complex cognition of corvids is often likened to that of great apes; our results show further that they share similar fundamental cognitive mechanisms.

Putting flexible animal prospection into context: escaping the theoretical box.

The debate on non-human future-oriented cognition has long revolved around the question whether such cognition at all occurs. Closer inspection reveals just how much cognition in general-down to its simplest forms-is geared toward predicting the future in a bid to maintain homeostasis and fend off entropy. Over the course of life's existence on Earth, evolution and natural selection have, through a series of evolutionary arms races, gotten increasingly good at achieving this. Prospection has reached its current pinnacle based partly on a system for episodic cognition that-as research increasingly is showing-is not limited principally to human beings. Nevertheless, and despite some notable recent defections, many researchers remain convinced of the merits of the Bischof-Köhler Hypothesis with its claim that no species other than human beings is able to anticipate future needs or otherwise live in anything other than the immediate present moment. What might, at first, appear to be empirical disputes turn out to reveal largely unquestioned theoretical divides. Without due care, one risks setting out conditions for 'true' future orientation that are irrelevant for describing human cognition. In sorting out the theoretical and terminological muddle framing contemporary debate, this article makes a plea for moving beyond past dogmas while putting animal prospection research into the context of evolution and contemporary cognitive science. For further resources related to this article, please visit the WIREs website.