For decades, the cognitive and neural sciences have benefitted greatly from a separation of mind and brain into distinct functional domains. The tremendous success of this approach notwithstanding, it is self-evident that such a view is incomplete. Goal-directed behaviour of an organism requires the joint functioning of perception, memory and sensorimotor control. A prime candidate for achieving integration across these functional domains are attentional processes. Consequently, this Theme Issue brings together studies of attentional selection from many fields, both experimental and theoretical, that are united in their quest to find overreaching integrative principles of attention between perception, memory and action. In all domains, attention is understood as combination of competition and priority control (‘bias’), with the task as a decisive driving factor to ensure coherent goal-directed behaviour and cognition. Using vision as the predominant model system for attentional selection, many studies of this Theme Issue focus special emphasis on eye movements as a selection process that is both a fundamental action and serves a key function in perception. The Theme Issue spans a wide range of methods, from measuring human behaviour in the real word to recordings of single neurons in the non-human primate brain. We firmly believe that combining such a breadth in approaches is necessary not only for attentional selection, but also to take the next decisive step in all of the cognitive and neural sciences: to understand cognition and behaviour beyond isolated domains.
attention; biased competition; task; real world; priority; vision
The goal of this review is to introduce a theory of task-driven visual attention and working memory (TRAM). Based on a specific biased competition model, the ‘theory of visual attention’ (TVA) and its neural interpretation (NTVA), TRAM introduces the following assumption. First, selective visual processing over time is structured in competition episodes. Within an episode, that is, during its first two phases, a limited number of proto-objects are competitively encoded—modulated by the current task—in activation-based visual working memory (VWM). In processing phase 3, relevant VWM objects are transferred via a short-term consolidation into passive VWM. Second, each time attentional priorities change (e.g. after an eye movement), a new competition episode is initiated. Third, if a phase 3 VWM process (e.g. short-term consolidation) is not finished, whereas a new episode is called, a protective maintenance process allows its completion. After a VWM object change, its protective maintenance process is followed by an encapsulation of the VWM object causing attentional resource costs in trailing competition episodes. Viewed from this perspective, a new explanation of key findings of the attentional blink will be offered. Finally, a new suggestion will be made as to how VWM items might interact with visual search processes.
visual attention; visual working memory; biased competition; short-term consolidation; attentional blink; eye movements
For natural scenes, attention is frequently quantified either by performance during rapid presentation or by gaze allocation during prolonged viewing. Both paradigms operate on different time scales, and tap into covert and overt attention, respectively. To compare these, we ask some observers to detect targets (animals/vehicles) in rapid sequences, and others to freely view the same target images for 3 s, while their gaze is tracked. In some stimuli, the target's contrast is modified (increased/decreased) and its background modified either in the same or in the opposite way. We find that increasing target contrast relative to the background increases fixations and detection alike, whereas decreasing target contrast and simultaneously increasing background contrast has little effect. Contrast increase for the whole image (target + background) improves detection, decrease worsens detection, whereas fixation probability remains unaffected by whole-image modifications. Object-unrelated local increase or decrease of contrast attracts gaze, but less than actual objects, supporting a precedence of objects over low-level features. Detection and fixation probability are correlated: the more likely a target is detected in one paradigm, the more likely it is fixated in the other. Hence, the link between overt and covert attention, which has been established in simple stimuli, transfers to more naturalistic scenarios.
gaze; eye movements; recognition; salience; free-viewing
Wildlife reintroductions select or treat individuals for good health with the expectation that these individuals will fare better than infected animals. However, these individuals, new to their environment, may also be particularly susceptible to circulating infections and this may result in high morbidity and mortality, potentially jeopardizing the goals of recovery. Here, using the reintroduction of the grey wolf (Canis lupus) into Yellowstone National Park as a case study, we address the question of how parasites invade a reintroduced population and consider the impact of these invasions on population performance. We find that several viral parasites rapidly invaded the population inside the park, likely via spillover from resident canid species, and we contrast these with the slower invasion of sarcoptic mange, caused by the mite Sarcoptes scabiei. The spatio-temporal patterns of mange invasion were largely consistent with patterns of host connectivity and density, and we demonstrate that the area of highest resource quality, supporting the greatest density of wolves, is also the region that appears most susceptible to repeated disease invasion and parasite-induced declines. The success of wolf reintroduction appears not to have been jeopardized by infectious disease, but now shows signs of regulation or limitation modulated by parasites.
wildlife reintroduction; parasite invasion; enemy release; Sarcoptes scabiei; sarcoptic mange; canine distemper virus
To devise and implement effective health policy, we must define the problem, choose the tools, craft the policy, build consensus, set goals and deadlines, raise funds and take action. Success or failure depends on the perception of risk, the strength of the underlying science, the efficacy of the technology, ownership and intellectual property, the conflict between individual and public health, the choice of weaker (guidelines) and stronger (law) policy instruments, the level of public interest, political opportunity, institutional inertia, mechanisms for enforcement and who foots the bill. All these things considered, this paper is a brief policy-making guide by example, illustrating some achievements and disappointments with reference to cholera, drug-resistant tuberculosis, HIV/AIDS and rabies.
cholera; drug resistance; HIV/AIDS; international health regulations; rabies; tuberculosis
Finch trichomonosis, caused by the protozoal parasite Trichomonas gallinae, was first recognized as an emerging infectious disease of British passerines in 2005. The first year of seasonal epidemic mortality occurred in 2006 with significant declines of greenfinch Carduelis chloris and chaffinch Fringilla coelebs populations. Here, we demonstrate that large-scale mortality, principally of greenfinch, continued in subsequent years, 2007–2009, with a shifting geographical distribution across the British Isles over time. Consequent to the emergence of finch trichomonosis, the breeding greenfinch population in Great Britain has declined from ca 4.3 million to ca 2.8 million birds and the maximum mean number of greenfinches (a proxy for flock size) visiting gardens has declined by 50 per cent. The annual rate of decline of the breeding greenfinch population within England has exceeded 7 per cent since the initial epidemic. Although initially chaffinch populations were regionally diminished by the disease, this has not continued. Retrospective analyses of disease surveillance data showed a rapid, widespread emergence of finch trichomonosis across Great Britain in 2005 and we hypothesize that the disease emerged by T. gallinae jumping from columbiforms to passeriforms. Further investigation is required to determine the continuing impact of finch trichomonosis and to develop our understanding of how protozoal diseases jump host species.
Trichomonas gallinae; trichomonosis; greenfinch; Carduelis chloris; emerging infectious disease; population decline
Invading infectious diseases can, in theory, lead to the extinction of host populations, particularly if reservoir species are present or if disease transmission is frequency-dependent. The number of historic or prehistoric extinctions that can unequivocally be attributed to infectious disease is relatively small, but gathering firm evidence in retrospect is extremely difficult. Amphibian chytridiomycosis and Tasmanian devil facial tumour disease (DFTD) are two very different infectious diseases that are currently threatening to cause extinctions in Australia. These provide an unusual opportunity to investigate the processes of disease-induced extinction and possible management strategies. Both diseases are apparently recent in origin. Tasmanian DFTD is entirely host-specific but potentially able to cause extinction because transmission depends weakly, if at all, on host density. Amphibian chytridiomycosis has a broad host range but is highly pathogenic only to some populations of some species. At present, both diseases can only be managed by attempting to isolate individuals or populations from disease. Management options to accelerate the process of evolution of host resistance or tolerance are being investigated in both cases. Anthropogenic changes including movement of diseases and hosts, habitat destruction and fragmentation and climate change are likely to increase emerging disease threats to biodiversity and it is critical to further develop strategies to manage these threats.
extinction; disease; amphibian chytrid fungus; Tasmanian devil facial tumour
This paper addresses the question of how the brain of an animal achieves cognitive integration—that is to say how it manages to bring its fullest resources to bear on an ongoing situation. To fully exploit its cognitive resources, whether inherited or acquired through experience, it must be possible for unanticipated coalitions of brain processes to form. This facilitates the novel recombination of the elements of an existing behavioural repertoire, and thereby enables innovation. But in a system comprising massively many anatomically distributed assemblies of neurons, it is far from clear how such open-ended coalition formation is possible. The present paper draws on contemporary findings in brain connectivity and neurodynamics, as well as the literature of artificial intelligence, to outline a possible answer in terms of the brain's most richly connected and topologically central structures, its so-called connective core.
animal cognition; brain networks; computational neuroscience
We are often asked whether some apes are smarter than others. Here we used two individual-based datasets on cognitive abilities to answer this question and to elucidate the structure of individual differences. We identified some individuals who consistently scored well across multiple tasks, and even one individual who could be classified as exceptional when compared with her conspecifics. However, we found no general intelligence factor. Instead, we detected some clusters of certain abilities, including inferences, learning and perhaps a tool-use and quantities cluster. Thus, apes in general and chimpanzees in particular present a pattern characterized by the existence of some smart animals but no evidence of a general intelligence factor. This conclusion contrasts with previous studies that have found evidence of a g factor in primates. However, those studies have used group-based as opposed to the individual-based data used here, which means that the two sets of analyses are not directly comparable. We advocate an approach based on testing multiple individuals (of multiple species) on multiple tasks that capture cognitive, motivational and temperament factors affecting performance. One of the advantages of this approach is that it may contribute to reconcile the general and domain-specific views on primate intelligence.
individual differences; animal cognition; g factor; apes; temperament
Darwin's claim ‘that the difference in mind between man and the higher animals … is certainly one of degree and not of kind’ is at the core of the comparative study of cognition. Recent research provides unprecedented support for Darwin's claim as well as new reasons to question it, stimulating new theories of human cognitive uniqueness. This article compares and evaluates approaches to such theories. Some prominent theories propose sweeping domain-general characterizations of the difference in cognitive capabilities and/or mechanisms between adult humans and other animals. Dual-process theories for some cognitive domains propose that adult human cognition shares simple basic processes with that of other animals while additionally including slower-developing and more explicit uniquely human processes. These theories are consistent with a modular account of cognition and the ‘core knowledge’ account of children's cognitive development. A complementary proposal is that human infants have unique social and/or cognitive adaptations for uniquely human learning. A view of human cognitive architecture as a mosaic of unique and species-general modular and domain-general processes together with a focus on uniquely human developmental mechanisms is consistent with modern evolutionary-developmental biology and suggests new questions for comparative research.
cognitive evolution; human uniqueness; modularity; dual process theories
A fundamental and frequently overlooked aspect of animal learning is its reliance on compatibility between the learning rules used and the attentional and motivational mechanisms directing them to process the relevant data (called here data-acquisition mechanisms). We propose that this coordinated action, which may first appear fragile and error prone, is in fact extremely powerful, and critical for understanding cognitive evolution. Using basic examples from imprinting and associative learning, we argue that by coevolving to handle the natural distribution of data in the animal's environment, learning and data-acquisition mechanisms are tuned jointly so as to facilitate effective learning using relatively little memory and computation. We then suggest that this coevolutionary process offers a feasible path for the incremental evolution of complex cognitive systems, because it can greatly simplify learning. This is illustrated by considering how animals and humans can use these simple mechanisms to learn complex patterns and represent them in the brain. We conclude with some predictions and suggested directions for experimental and theoretical work.
evolution of learning; comparative cognition; language acquisition; learning of structured data; data acquisition; innate template
Animal cognition experiments frequently reveal striking individual variation but rarely consider its causes and largely ignore its potential consequences. Studies often focus on a subset of high-performing subjects, sometimes viewing evidence from a single individual as sufficient to demonstrate the cognitive capacity of a species. We argue that the emphasis on demonstrating species-level cognitive capacities detracts from the value of individual variation in understanding cognitive development and evolution. We consider developmental and evolutionary interpretations of individual variation and use meta-analyses of data from published studies to examine predictors of individual performance. We show that reliance on small sample sizes precludes robust conclusions about individual abilities as well as inter- and intraspecific differences. We advocate standardization of experimental protocols and pooling of data between laboratories to improve statistical rigour. Our analyses show that cognitive performance is influenced by age, sex, rearing conditions and previous experience. These effects limit the validity of comparative analyses unless developmental histories are taken into account, and complicate attempts to understand how cognitive traits are expressed and selected under natural conditions. Further understanding of cognitive evolution requires efforts to elucidate the heritability of cognitive traits and establish whether elevated cognitive performance confers fitness advantages in nature.
cognition; development; evolution; individual differences; meta-analysis; reproductive fitness
To understand how complex, or ‘advanced’ various forms of cognition are, and to compare them between species for evolutionary studies, we need to understand the diversity of neural–computational mechanisms that may be involved, and to identify the genetic changes that are necessary to mediate changes in cognitive functions. The same overt cognitive capacity might be mediated by entirely different neural circuitries in different species, with a many-to-one mapping between behavioural routines, computations and their neural implementations. Comparative behavioural research needs to be complemented with a bottom-up approach in which neurobiological and molecular-genetic analyses allow pinpointing of underlying neural and genetic bases that constrain cognitive variation. Often, only very minor differences in circuitry might be needed to generate major shifts in cognitive functions and the possibility that cognitive traits arise by convergence or parallel evolution needs to be taken seriously. Hereditary variation in cognitive traits between individuals of a species might be extensive, and selection experiments on cognitive traits might be a useful avenue to explore how rapidly changes in cognitive abilities occur in the face of pertinent selection pressures.
brain; convergent evolution; homology; intelligence; neural circuits
With the exception of a few model species, individual differences in cognition remain relatively unstudied in non-human animals. One intriguing possibility is that variation in cognition is functionally related to variation in personality. Here, we review some examples and present hypotheses on relationships between personality (or behavioural syndromes) and individual differences in cognitive style. Our hypotheses are based largely on a connection between fast–slow behavioural types (BTs; e.g. boldness, aggressiveness, exploration tendency) and cognitive speed–accuracy trade-offs. We also discuss connections between BTs, cognition and ecologically important aspects of decision-making, including sampling, impulsivity, risk sensitivity and choosiness. Finally, we introduce the notion of cognition syndromes, and apply ideas from theories on adaptive behavioural syndromes to generate predictions on cognition syndromes.
animal personalities; behavioural syndromes; cognition; speed–accuracy trade-off
Using cooperation in chimpanzees as a case study, this article argues that research on animal minds needs to steer a course between ‘association-blindness’—the failure to consider associative learning as a candidate explanation for complex behaviour—and ‘simple-mindedness’—the assumption that associative explanations trump more cognitive hypotheses. Association-blindness is challenged by the evidence that associative learning occurs in a wide range of taxa and functional contexts, and is a major force guiding the development of complex human behaviour. Furthermore, contrary to a common view, association-blindness is not entailed by the rejection of behaviourism. Simple-mindedness is founded on Morgan's canon, a methodological principle recommending ‘lower’ over ‘higher’ explanations for animal behaviour. Studies in the history and philosophy of science show that Morgan failed to offer an adequate justification for his canon, and subsequent attempts to justify the canon using evolutionary arguments and appeals to simplicity have not been successful. The weaknesses of association-blindness and simple-mindedness imply that there are no short-cuts to finding out about animal minds. To decide between associative and yet more cognitive explanations for animal behaviour, we have to spell them out in sufficient detail to allow differential predictions, and to test these predictions through observation and experiment.
animal cognition; associative learning; chimpanzee; cooperation; Morgan's canon; parsimony
A traditional view of cognition is that it involves an internal process that represents, tracks or predicts an external process. This is not a general characteristic of all complex neural processing or feedback control, but rather implies specific forms of processing giving rise to specific behavioural capabilities. In this paper, I will review the evidence for such capabilities in insect navigation and learning. Do insects know where they are, or do they only know what to do? Do they learn what stimuli mean, or do they only learn how to behave?
insect; robot; perception; learning; navigation
Associative learning plays a variety of roles in the study of animal cognition from a core theoretical component to a null hypothesis against which the contribution of cognitive processes is assessed. Two developments in contemporary associative learning have enhanced its relevance to animal cognition. The first concerns the role of associatively activated representations, whereas the second is the development of hybrid theories in which learning is determined by prediction errors, both directly and indirectly through associability processes. However, it remains unclear whether these developments allow associative theory to capture the psychological rationality of cognition. I argue that embodying associative processes within specific processing architectures provides mechanisms that can mediate psychological rationality and illustrate such embodiment by discussing the relationship between practical reasoning and the associative-cybernetic model of goal-directed action.
animal cognition; associationism; associative learning; psychological rationality
Do we fully understand the structure of the problems we present to our subjects in experiments on animal cognition, and the information required to solve them? While we currently have a good understanding of the behavioural and neurobiological mechanisms underlying associative learning processes, we understand much less about the mechanisms underlying more complex forms of cognition in animals. In this study, we present a proposal for a new way of thinking about animal cognition experiments. We describe a process in which a physical cognition task domain can be decomposed into its component parts, and models constructed to represent both the causal events of the domain and the information available to the agent. We then implement a simple set of models, using the planning language MAPL within the MAPSIM simulation environment, and applying it to a puzzle tube task previously presented to orangutans. We discuss the results of the models and compare them with the results from the experiments with orangutans, describing the advantages of this approach, and the ways in which it could be extended.
comparative cognition; mechanism; function; modelling; planning; artificial intelligence
Differences between individuals are the raw material from which theories of the evolution and ontogeny of cognition are built. For example, when 4-year-old children pass a test requiring them to communicate the content of another's falsely held belief, while 3-year-olds fail, we know that something must change over the course of the third year of life. In the search for what develops or evolves, the typical route is to probe the extents and limits of successful individuals' ability. Another is to focus on those that failed, and find out what difference or lack prevented them from passing the task. Recent research in developmental psychology has harnessed individual differences to illuminate the cognitive mechanisms that emerge to enable success. We apply this approach to explaining some of the failures made by chimpanzees when using tools to solve problems. Twelve of 16 chimpanzees failed to discriminate between a complete and a broken tool when, after being set down, the ends of the broken one were aligned in front of them. There was a correlation between performance on this aligned task and another in which after being set down, the centre of both tools was covered, suggesting that the limiting factor was not the representation of connection, but memory or attention. Some chimpanzees that passed the aligned task passed a task in which the location of the broken tool was never visible but had to be inferred.
chimpanzees; tool-use; representation; executive function
ocean acidification; climate change; ecology
Reversible protein phosphorylation is a major mechanism in the regulation of fundamental signalling events in all living organisms. Bacteria have been shown to possess a versatile repertoire of protein kinases, including histidine and aspartic acid kinases, serine/threonine kinases, and more recently tyrosine and arginine kinases. Tyrosine phosphorylation is today recognized as a key regulatory device of bacterial physiology, linked to exopolysaccharide production, virulence, stress response and DNA metabolism. However, bacteria have evolved tyrosine kinases that share no resemblance with their eukaryotic counterparts and are unique in exploiting the ATP/GTP-binding Walker motif to catalyse autophosphorylation and substrate phosphorylation on tyrosine. These enzymes, named BY-kinases (for Bacterial tYrosine kinases), have been identified in a majority of sequenced bacterial genomes, and to date no orthologues have been found in Eukarya. The aim of this review was to present the most recent knowledge about BY-kinases by focusing primarily on their evolutionary origin, structural and functional aspects, and emerging regulatory potential based on recent bacterial phosphoproteomic studies.
tyrosine kinase; bacteria; protein phosphorylation; biological role; structure
The switch between the Krebs cycle and the glyoxylate bypass is controlled by isocitrate dehydrogenase kinase/phosphatase (AceK). AceK, a bifunctional enzyme, phosphorylates and dephosphorylates isocitrate dehydrogenase (IDH) with its unique active site that harbours both the kinase and ATP/ADP-dependent phosphatase activities. AceK was the first example of prokaryotic phosphorylation identified, and the recent characterization of the structures of AceK and its complex with its protein substrate, IDH, now offers a new understanding of both previous and future endeavours. AceK is structurally similar to the eukaryotic protein kinase superfamily, sharing many of the familiar catalytic and regulatory motifs, demonstrating a close evolutionary relationship. Although the active site is shared by both the kinase and phosphatase functions, the catalytic residues needed for phosphatase function are readily seen when compared with the DXDX(T/V) family of phosphatases, despite the fact that the phosphatase function of AceK is strictly ATP/ADP-dependent. Structural analysis has also allowed a detailed look at regulation and its stringent requirements for interacting with IDH.
kinase; phosphatase; AceK; isocitrate dehydrogenase; phosphorylation
Eukaryotic protein kinases belong to a large superfamily with hundreds to thousands of copies and are components of essentially all cellular functions. The goals of this study are to classify protein kinases from 25 plant species and to assess their evolutionary history in conjunction with consideration of their molecular functions. The protein kinase superfamily has expanded in the flowering plant lineage, in part through recent duplications. As a result, the flowering plant protein kinase repertoire, or kinome, is in general significantly larger than other eukaryotes, ranging in size from 600 to 2500 members. This large variation in kinome size is mainly due to the expansion and contraction of a few families, particularly the receptor-like kinase/Pelle family. A number of protein kinases reside in highly conserved, low copy number families and often play broadly conserved regulatory roles in metabolism and cell division, although functions of plant homologues have often diverged from their metazoan counterparts. Members of expanded plant kinase families often have roles in plant-specific processes and some may have contributed to adaptive evolution. Nonetheless, non-adaptive explanations, such as kinase duplicate subfunctionalization and insufficient time for pseudogenization, may also contribute to the large number of seemingly functional protein kinases in plants.
plant protein kinase; gene family evolution; lineage-specific expansion; comparative genomics
The advantageous chemical properties of the phosphate ester linkage were exploited early in evolution to generate the phosphate diester linkages that join neighbouring bases in RNA and DNA (Westheimer 1987 Science
235, 1173–1178). Following the fixation of the genetic code, another use for phosphate ester modification was found, namely reversible phosphorylation of the three hydroxyamino acids, serine, threonine and tyrosine, in proteins. During the course of evolution, phosphorylation emerged as one of the most prominent types of post-translational modification, because of its versatility and ready reversibility. Phosphoamino acids generated by protein phosphorylation act as new chemical entities that do not resemble any natural amino acid, and thereby provide a means of diversifying the chemical nature of protein surfaces. A protein-linked phosphate group can form hydrogen bonds or salt bridges either intra- or intermolecularly, creating stronger hydrogen bonds with arginine than either aspartate or glutamate. The unique size of the ionic shell and charge properties of covalently attached phosphate allow specific and inducible recognition of phosphoproteins by phosphospecific-binding domains in other proteins, thus promoting inducible protein–protein interaction. In this manner, phosphorylation serves as a switch that allows signal transduction networks to transmit signals in response to extracellular stimuli.
phosphate; ester; protein; phosphorylation; kinase; evolution