Intelligence in Corvids and Apes: A Case of Convergent Evolution?

Intelligence is suggested to have evolved in primates in response to complexities in the environment faced by their ancestors. Corvids, a large-brained group of birds, have been suggested to have undergone a convergent evolution of intelligence [ Emery & Clayton (2004) Science , Vol. 306, pp. 1903–1907 ]. Here we review evidence for the proposal from both ultimate and proximate perspectives. While we show that many of the proposed hypotheses for the evolutionary origin of great ape intelligence also apply to corvids, further study is needed to reveal the selective pressures that resulted in the evolution of intelligent behaviour in both corvids and apes. For comparative proximate analyses we emphasize the need to be explicit about the level of analysis to reveal the type of convergence that has taken place. Although there is evidence that corvids and apes solve social and physical problems with similar speed and flexibility, there is a great deal more to be learned about the representations and algorithms underpinning these computations in both groups. We discuss recent comparative work that has addressed proximate questions at this level, and suggest directions for future research.     

Episodic-like memory in the rat

A fundamental question in comparative cognition is whether animals remember unique, personal past experiences. It has long been argued that memories for specific events (referred to as episodic memory) are unique to humans. Recently, considerable evidence has accumulated to show that food-storing birds possess critical behavioral elements of episodic memory, referred to as episodic-like memory in acknowledgment of the fact that behavioral criteria do not assess subjective experiences. Here we show that rats have a detailed representation of remembered events and meet behavioral criteria for episodic-like memory. We provided rats with access to locations baited with distinctive (e.g., grape and raspberry) or nondistinctive (regular chow) flavors. Locations with a distinctive flavor replenished after a long but not a short delay, and locations with the nondistinctive flavor never replenished. One distinctive flavor was devalued after encoding its location by prefeeding that flavor (satiation) or by pairing it with lithium chloride (acquired taste aversion), while the other distinctive flavor was not devalued. The rats selectively decreased revisits to the devalued distinctive flavor but not to the nondevalued distinctive flavor. The present studies demonstrate that rats selectively encode the content of episodic-like memories.     

Hippocampal synaptic activity, pattern separation and episodic-like memory: implications for mouse models of Alzheimer's disease pathology

The present review summarizes converging evidence from animal and human studies that an early target of amyloid pathology is synaptic activity in the DG (dentate gyrus)/CA3 network. We briefly review the computational significance of the DG/CA3 network in the encoding of episodic memory and present new evidence that the CA3/DG pattern of activation is compromised in a mouse model of amyloid pathology. In addition, we present a new behavioural method to test the prediction that amyloid-related synaptic pathology will disrupt the formation of an integrated episodic-like (what, where and when) memory in mice.     

Handedness in great apes: A review of findings

We present data on hand preference in great apes and discuss them in the context of theoretical models of hand preference in nonhuman primates presented by MacNeilageet al. (1987) and by Fagot and Vauclair (1991). We also discuss several methodological and statistical issues as they pertain to the assessment of hand preference in great apes and other primate species. Finally, we present a comparative framework for the study of hand preference, emphasizing the importance of studies with great apes in developing evolutionary models of hemispheric specialization.     

Do rhesus monkeys recognize themselves in mirrors?

Self-recognition continues to attract attention because of the evidence of a striking difference between the great apes and humans, on the one hand, and all other primates; the former are capable of self recognition,whereas no compelling evidence exists for prosimians, monkeys, or lesser apes. This is inspite of numerous attempts to facilitate mirror self-recognition in other primates. Although all previous attempts to find self-recognition in rhesus macaques have failed, a recent article [Rajala et al., PLoS One9:e12865, 2010] claimed the opposite—that adult male rhesus monkeys did recognize their own image in a mirror. We critically examine this claim, and conclude that the article fails to provide acceptable evidence for self-recognition in rhesus monkeys.     

Elements of episodic-like memory in animal models

Representations of unique events from one’s past constitute the content of episodic memories. A number of studies with non-human animals have revealed that animals remember specific episodes from their past (referred to as episodic-like memory). The development of animal models of memory holds enormous potential for gaining insight into the biological bases of human memory. Specifically, given the extensive knowledge of the rodent brain, the development of rodent models of episodic memory would open new opportunities to explore the neuroanatomical, neurochemical, neurophysiological, and molecular mechanisms of memory. Development of such animal models holds enormous potential for studying functional changes in episodic memory in animal models of Alzheimer’s disease, amnesia, and other human memory pathologies. This article reviews several approaches that have been used to assess episodic-like memory in animals. The approaches reviewed include the discrimination of what, where, and when in a radial arm maze, dissociation of recollection and familiarity, object recognition, binding, unexpected questions, and anticipation of a reproductive state. The diversity of approaches may promote the development of converging lines of evidence on the difficult problem of assessing episodic-like memory in animals.     

Mirror-induced behavior in the magpie (Pica pica): evidence of self-recognition

Comparative studies suggest that at least some bird species have evolved mental skills similar to those found in humans and apes. This is indicated by feats such as tool use, episodic-like memory, and the ability to use one's own experience in predicting the behavior of conspecifics. It is, however, not yet clear whether these skills are accompanied by an understanding of the self. In apes, self-directed behavior in response to a mirror has been taken as evidence of self-recognition. We investigated mirror-induced behavior in the magpie, a songbird species from the crow family. As in apes, some individuals behaved in front of the mirror as if they were testing behavioral contingencies. When provided with a mark, magpies showed spontaneous mark-directed behavior. Our findings provide the first evidence of mirror self-recognition in a non-mammalian species. They suggest that essential components of human self-recognition have evolved independently in different vertebrate classes with a separate evolutionary history.     

Mental time travel: animals anticipate the future

Recent behavioral experiments with scrub jays and nonhuman primates indicate they can anticipate and plan for future needs not currently experienced. Combined with accumulating evidence for episodic-like memory in animals, these studies suggest that some animals can mentally time travel into both the past and future.     

Cognitive ornithology: the evolution of avian intelligence

Comparative psychologists interested in the evolution of intelligence have focused their attention on social primates, whereas birds tend to be used as models of associative learning. However, corvids and parrots, which have forebrains relatively the same size as apes, live in complex social groups and have a long developmental period before becoming independent, have demonstrated ape-like intelligence. Although, ornithologists have documented thousands of hours observing birds in their natural habitat, they have focused their attention on avian behaviour and ecology, rather than intelligence. This review discusses recent studies of avian cognition contrasting two different approaches; the anthropocentric approach and the adaptive specialization approach. It is argued that the most productive method is to combine the two approaches. This is discussed with respects to recent investigations of two supposedly unique aspects of human cognition; episodic memory and theory of mind. In reviewing the evidence for avian intelligence, corvids and parrots appear to be cognitively superior to other birds and in many cases even apes. This suggests that complex cognition has evolved in species with very different brains through a process of convergent evolution rather than shared ancestry, although the notion that birds and mammals may share common neural connectivity patterns is discussed.     

Rooks perceive support relations similar to six-month-old babies

Some corvids have demonstrated cognitive abilities that rival or exceed those of the great apes; for example, tool use in New Caledonian crows, and social cognition, episodic-like memory and future planning in Western scrub-jays. Rooks appear to be able to solve novel tasks through causal reasoning rather than simple trial-and-error learning. Animals with certain expectations about how objects interact would be able to narrow the field of candidate causes substantially, because some causes are simply ‘impossible’. Here we present evidence that rooks hold such expectations and appear to possess perceptual understanding of support relations similar to that demonstrated by human babies, which is more comprehensive than that of chimpanzees.     

Can animals recall the past and plan for the future?

According to the 'mental time travel hypothesis' animals, unlike humans, cannot mentally travel backwards in time to recollect specific past events (episodic memory) or forwards to anticipate future needs (future planning). Until recently, there was little evidence in animals for either ability. Experiments on memory in food-caching birds, however, question this assumption by showing that western scrub-jays form integrated, flexible, trial-unique memories of what they hid, where and when. Moreover, these birds can adjust their caching behaviour in anticipation of future needs. We suggest that some animals have elements of both episodic-like memory and future planning.     

Episodic-like memory in animals: psychological criteria, neural mechanisms and the value of episodic-like tasks to investigate animal models of neurodegenerative disease

The question of whether any non-human species displays episodic memory is controversial. Associative accounts of animal learning recognize that behaviour can change in response to single events but this does not imply that animals need or are later able to recall representations of unique events at a different time and place. The lack of language is also relevant, being the usual medium for communicating about the world, but whether it is critical for the capacity to represent and recall events is a separate matter. One reason for suspecting that certain animals possess an episodic-like memory system is that a variety of learning and memory tasks have been developed that, even though they do not meet the strict criteria required for episodic memory, have an 'episodic-like' character. These include certain one-trial learning tasks, scene-specific discrimination learning, multiple reversal learning, delayed matching and non-matching tasks and, most recently, tasks demanding recollection of 'what, where and when' an event happened. Another reason is that the neuronal architecture of brain areas thought to be involved in episodic memory (including the hippocampal formation) are substantially similar in mammals and, arguably, all vertebrates. Third, our developing understanding of activity-dependent synaptic plasticity (which is a candidate neuronal mechanism for encoding memory traces) suggests that its expression reflects certain physiological characteristics that are ideal components of a neuronal episodic memory system. These include the apparently digital character of synaptic change at individual terminals and the variable persistence of potentiation accounted for by the synaptic tag hypothesis. A further value of studying episodic-like memory in animals is the opportunity it affords to model certain kinds of neurodegenerative disease that, in humans, affect episodic memory. An example is recent work on a transgenic mouse that over-expresses a mutation of human amyloid precursor protein (APP) that occurs in familial Alzheimer's disease, under the control of platelet derived (PD) growth factor promoter (the PDAPP mouse). A striking age- and amyloid plaque-related deficit is seen using a task in which the mice have to keep changing their memory representation of the world rather than learn a single fact.     

Neural systems underlying episodic memory: insights from animal research

Two strategies used to uncover neural systems for episodic-like memory in animals are discussed: (i) an attribute of episodic memory (what? when? where?) is examined in order to reveal the neuronal interactions supporting that component of memory; and (ii) the connections of a structure thought to be central to episodic memory in humans are studied at a level of detail not feasible in humans. By focusing on spatial memory (where?) and the hippocampus, it has proved possible to bring the strategies together. A review of lesion, disconnection and immediate early-gene studies in animals reveals the importance of interactions between the hippocampus and specific nuclei in the diencephalon (most notably the anterior thalamic nuclei) for spatial memory. Other parts of this extended hippocampal system include the mammillary bodies and the posterior cingulate (retrosplenial) cortex. Furthermore, by combining lesion and immediate early-gene studies it is possible to show how the loss of one component structure or tract can influence the remaining regions in this group of structures. The validity of this convergent approach is supported by new findings showing that the same set of regions is implicated in anterograde amnesia in humans.     

Frequency and timing of scaphoid-centrale fusion in hominoids

Fusion between the os centrale and the scaphoid has played a central role in many functional and phylogenetic interpretations of hominoid evolution. In particular, scaphoid-centrale fusion shared among African apes and humans has been interpreted as an adaptation in knuckle-walkers, an exaptation in hominins, and has been offered as evidence for a knuckle-walking origin of bipedalism. However, discrepancies in the literature concerning the taxa in which this scaphoid-centrale fusion occurs, as well as the timing and/or frequency of this fusion, have confounded the significance of this trait. This study provides an historical review of the literature on scaphoid-centrale fusion in primates and the first formal investigation into the timing and frequency of this character among primates, with a focus on extant hominoids. Results indicate that there is a significant difference in the timing and frequency of scaphoid-centrale fusion in African apes and humans compared to Asian apes, suggesting that prenatal or early postnatal fusion among hominines is a synapomorphy. Scaphoid-centrale fusion does not occur randomly within primates. Instead, only Homininae and some members of Lemuroidea show consistent and ontogenetically early fusion of these carpals. The consistent occurrence of this trait within only two primate clades and a clear heterochronic trend in timing and frequency of scaphoid-centrale fusion among hominines suggest that this character is primarily phylogenetically controlled. We could not falsify the hypothesis that scaphoid-centrale fusion in African apes is indeed related to midcarpal stability in knuckle-walking, but neither were we able to find direct biomechanical or kinematic evidence to support this hypothesis. A more definitive answer to the question of the functional significance of scaphoid-centrale fusion will have to await more detailed analyses of great ape wrist kinematics.     

A developmental approach to the origins of self-recognition in great apes

In this paper I present an hypothesis to explain the presence of mirror self-recognition (MSR) in great apes and human infants, and the absence of MSR in monkeys. This hypothesis is based on the following elements: 1) review of Gallupian studies of MSR in monkeys and apes; 2) review of Lewis & Brooks-Gunn's study for self-recognition in human infants; 3) application of the human model to comparative data on MSR in nonhuman primates; 4) discussion of cognitive correlates of MSR in human infants; 5) analysis of the cognitive correlates of MSR absence in monkeys, and MSR presence in apes; 6) comparative analysis of the modalities of occurrence of imitation and understanding of causality in monkeys and apes; and 7) a cladistic reconstruction of the evolution of MSR.     

Problems faced by food-caching corvids and the evolution of cognitive solutions

The scatter hoarding of food, or caching, is a widespread and well-studied behaviour. Recent experiments with caching corvids have provided evidence for episodic-like memory, future planning and possibly mental attribution, all cognitive abilities that were thought to be unique to humans. In addition to the complexity of making flexible, informed decisions about caching and recovering, this behaviour is underpinned by a motivationally controlled compulsion to cache. In this review, we shall first discuss the compulsive side of caching both during ontogeny and in the caching behaviour of adult corvids. We then consider some of the problems that these birds face and review the evidence for the cognitive abilities they use to solve them. Thus, the emergence of episodic-like memory is viewed as a solution for coping with food perishability, while the various cache-protection and pilfering strategies may be sophisticated tools to deprive competitors of information, either by reducing the quality of information they can gather, or invalidating the information they already have. Finally, we shall examine whether such future-oriented behaviour involves future planning and ask why this and other cognitive abilities might have evolved in corvids.     

Hand preferences for coordinated bimanual actions in 777 great apes: implications for the evolution of handedness in hominins

Whether or not nonhuman primates exhibit population-level handedness remains a topic of considerable scientific debate. Here, we examined handedness for coordinated bimanual actions in a sample of 777 great apes including chimpanzees, bonobos, gorillas, and orangutans. We found population-level right-handedness in chimpanzees, bonobos and gorillas, but left-handedness in orangutans. Directional biases in handedness were consistent across independent samples of apes within each genus. We suggest that, contrary to previous claims, population-level handedness is evident in great apes but differs among species as a result of ecological adaptations associated with posture and locomotion. We further suggest that historical views of nonhuman primate handedness have been too anthropocentric, and we advocate for a larger evolutionary framework for the consideration of handedness and other aspects of hemispheric specialization among primates.     

Laterality in Maternal Cradling and Infant Positional Biases: Implications for the Development and Evolution of Hand Preferences in Nonhuman Primates

Left-sided maternal cradling has been widely reported in human populations. In this paper, I review the evidence of laterality in maternal cradling and infant positional biases in non-human primates. The review revealed some evidence of population-left sided cradling in great apes but little consistency in bias was found among Old and New World monkeys. Very little data have been reported in prosimians. I further describe how asymmetries in either maternal cradling or infant positional biases may explain individual and species differences in hand preference.     

Development of the Laryngeal Air Sac in Chimpanzees

Though many nonhuman primates possess a laryngeal sac, the great apes are unique in their great size. Though an enlarged sac probably arose in their common ancestor, its functional adaptations remain a matter of debate. Its development in extant great apes is likely to provide valuable information to clarify the issue. We used magnetic resonance imaging to examine the development of the laryngeal sac in 3 living chimpanzees, age 4 mo–5 yr, and identified 2 distinct growth phases of the sac. A gradual growth of the sac in early infancy results in a configuration so that it occupies the ventral region of the neck; many adult nonhominoid primates having a sac show the configuration. The subsequent rapid expansion of the sac in late infancy causes the final configuration in chimpanzees, wherein the sac expands into the pectoral, clavicular, and axillary regions. The latter phase possibly arose at latest in the last common ancestor of extant great apes and contributed to the evolution of the enlarged sac, despite the later evolutionary diversification in adult sac anatomy and growth. As many studies have advocated, the enlarged sac probably plays a role in vocalization in adults. However, physiological modifications in the laryngeal region during infancy are likely to provide valuable information to evaluate the functional adaptations of the enlarged sac in the great apes.     

How humans evolved large brains: Comparative evidence

The human brain is about three times as large as that of our closest living relatives, the great apes. Overall brain size is a good predictor of cognitive performance in a variety of tests in primates. 1 , 2 Therefore, hypotheses explaining the evolution of this remarkable difference have attracted much interest. In this review, we give an overview of the current evidence from comparative studies testing these hypotheses. If cognitive benefits are diverse and ubiquitous, it is possible that most of the variation in relative brain size among extant primates is explained by variation in the ability to avoid the fitness costs of increased brain size (allocation trade‐offs and increased minimum energy needs). This is indeed what we find, suggesting that an energetic perspective helps to complement approaches to explain variation in brain size that postulate cognitive benefits. The expensive brain framework also provides a coherent scenario for how these factors may have shaped early hominin brain expansion.