Functional imaging of numerical processing in adults and 4-y-old children

Adult humans, infants, pre-school children, and non-human animals appear to share a system of approximate numerical processing for non-symbolic stimuli such as arrays of dots or sequences of tones. Behavioral studies of adult humans implicate a link between these non-symbolic numerical abilities and symbolic numerical processing (e.g., similar distance effects in accuracy and reaction-time for arrays of dots and Arabic numerals). However, neuroimaging studies have remained inconclusive on the neural basis of this link. The intraparietal sulcus (IPS) is known to respond selectively to symbolic numerical stimuli such as Arabic numerals. Recent studies, however, have arrived at conflicting conclusions regarding the role of the IPS in processing non-symbolic, numerosity arrays in adulthood, and very little is known about the brain basis of numerical processing early in development. Addressing the question of whether there is an early-developing neural basis for abstract numerical processing is essential for understanding the cognitive origins of our uniquely human capacity for math and science. Using functional magnetic resonance imaging (fMRI) at 4-Tesla and an event-related fMRI adaptation paradigm, we found that adults showed a greater IPS response to visual arrays that deviated from standard stimuli in their number of elements, than to stimuli that deviated in local element shape. These results support previous claims that there is a neurophysiological link between non-symbolic and symbolic numerical processing in adulthood. In parallel, we tested 4-y-old children with the same fMRI adaptation paradigm as adults to determine whether the neural locus of non-symbolic numerical activity in adults shows continuity in function over development. We found that the IPS responded to numerical deviants similarly in 4-y-old children and adults. To our knowledge, this is the first evidence that the neural locus of adult numerical cognition takes form early in development, prior to sophisticated symbolic numerical experience. More broadly, this is also, to our knowledge, the first cognitive fMRI study to test healthy children as young as 4 y, providing new insights into the neurophysiology of human cognitive development.     

Common and divergent psychobiological mechanisms underlying maternal behaviors in non-human and human mammals

Maternal interactions with young occupy most of the reproductive period for female mammals and are absolutely essential for offspring survival and development. The hormonal, sensory, reward-related, emotional, cognitive and neurobiological regulators of maternal caregiving behaviors have been well studied in numerous subprimate mammalian species, and some of the importance of this body of work is thought to be its relevance for understanding similar controls in humans. We here review many of the important biopsychological influences on maternal behaviors in the two best studied non-human animals, laboratory rats and sheep, and directly examine how the conceptual framework established by some of the major discoveries in these animal “models” do or do not hold for our understanding of human mothering. We also explore some of the limits for extrapolating from non-human animals to humans. We conclude that there are many similarities between non-human and human mothers in the biological and psychological factors influencing their early maternal behavior and that many of the differences are due to species-characteristic features related to the role of hormones, the relative importance of each sensory system, flexibility in what behaviors are exhibited, the presence or absence of language, and the complexity of cortical function influencing caregiving behaviors.     

Monkeys match the number of voices they hear to the number of faces they see

Convergent evidence demonstrates that adult humans possess numerical representations that are independent of language [1, 2, 3, 4, 5 and 6]. Human infants and nonhuman animals can also make purely numerical discriminations, implicating both developmental and evolutionary bases for adult humans' language-independent representations of number [7 and 8]. Recent evidence suggests that the nonverbal representations of number held by human adults are not constrained by the sensory modality in which they were perceived [9]. Previous studies, however, have yielded conflicting results concerning whether the number representations held by nonhuman animals and human infants are tied to the modality in which they were established [10, 11, 12, 13, 14 and 15]. Here, we report that untrained monkeys preferentially looked at a dynamic video display depicting the number of conspecifics that matched the number of vocalizations they heard. These findings suggest that number representations held by monkeys, like those held by adult humans, are unfettered by stimulus modality.     

On the pursuit of the brain network for proto-syntactic learning in non-human primates: conceptual issues and neurobiological hypotheses

Songbirds have become impressive neurobiological models for aspects of human verbal communication because they learn to sequence their song elements, analogous, in some ways, to how humans learn to produce spoken sequences with syntactic structure. However, mammals such as non-human primates are considered to be at best limited-vocal learners and not able to sequence their vocalizations, although some of these animals can learn certain 'artificial grammar' sequences. Thus, conceptual issues have slowed the progress in exploring potential neurobiological homologues to language-related processes in species that are taxonomically closely related to humans. We consider some of the conceptual issues impeding a pursuit of, as we define them, 'proto-syntactic' capabilities and their neuronal substrates in non-human animals. We also discuss ways to better bridge comparative behavioural and neurobiological data between humans and other animals. Finally, we propose guiding neurobiological hypotheses with which we aim to facilitate the future testing of the level of correspondence between the human brain network for syntactic-learning and related neurobiological networks present in other primates. Insights from the study of non-human primates and other mammals are likely to complement those being obtained in birds to further our knowledge of the human language-related network at the cellular level.     

恒河猴在生殖生物学中的应用进展

目的非人灵长类动物在生殖生物学研究领域是一种非常重要的实验动物。人类利用非人灵长类动物与人的生物学等方面相似的特征,开展了生殖生物学、生理学、药理学、毒理学以及生育调节等方面的研究工作,为生殖生物学基础研究以及人类健康和疾病问题的基础研究和临床前研究提供了理想的动物模型。随着生命科学的发展,对非人灵长类实验动物质量提出了更高的要求,人们认识到实验时,应用健康的优质非人灵长类动物的重要性。本文简要概括了非人灵长类动物恒河猴的生物学特性,阐述了非人灵长类动物恒河猴在生殖生物学中的应用研究。     

Culture in humans and other animals

The study of animal culture is a flourishing field, with culture being recorded in a wide range of taxa, including non-human primates, birds, cetaceans, and rodents. In spite of this research, however, the concept of culture itself remains elusive. There is no universally assented to concept of culture, and there is debate over the connection between culture and related concepts like tradition and social learning. Furthermore, it is not clear whether culture in humans and culture in non-human animals is really the same thing, or merely loose analogues that go by the same name. The purpose of this paper is to explicate core desiderata for a concept of culture and then to construct a concept that meets these desiderata. The paper then applies this concept in both humans and non-human animals.     

Character phylogeny of the primate forelimb superficial venous system.

The ontogeny and comparative anatomy of the forelimb superficial veins were investigated in humans, non-human primates and other mammals. Adult humans and the orangutan (Pongo) possess two autonomous forelimb veins, one on the lateral (preaxial) margin of the limb, the other on the medial (postaxial) margin. All other adult primates and mammals examined possess a lateral vein alone. In African apes (Pan and Gorilla) and in 24% of human forelimbs the lateral vein is short, being essentially confined to the antebrachial region, whereas in other mammals and in 76% of human limbs the lateral vein runs from the carpus to the clavicular region. In humans the medial vein develops before the lateral vein, whereas in the rabbit and the pig the medial vein is present in early embryos but is subsequently lost. We propose that in humans, and probably also in the orangutan, the possession of a medial vein is a neotenic retention of a primitive tetrapod condition. These animals, which retain their medial vein, are united by losing a late stage in their ontogeny. Other animals subsequently pass through a stage in which the medial vein is lost, but Pongo and Homo retain this vein to adulthood. The loss of an ontogenetic stage can arise independently, and the presence of a medial vein therefore affords only weak evidence for a close phylogenetic relationship between humans and the orangutan. The polymorphic lateral vein of humans may be a character state that is intermediate between the derived (short) lateral vein of the African apes and the primitive long lateral vein of other non-human primates and mammals.     

Evidence for two numerical systems that are similar in humans and guppies

Background

Humans and non-human animals share an approximate non-verbal system for representing and comparing numerosities that has no upper limit and for which accuracy is dependent on the numerical ratio. Current evidence indicates that the mechanism for keeping track of individual objects can also be used for numerical purposes; if so, its accuracy will be independent of numerical ratio, but its capacity is limited to the number of items that can be tracked, about four. There is, however, growing controversy as to whether two separate number systems are present in other vertebrate species.

Methodology/Principal Findings

In this study, we compared the ability of undergraduate students and guppies to discriminate the same numerical ratios, both within and beyond the small number range. In both students and fish the performance was ratio-independent for the numbers 1–4, while it steadily increased with numerical distance when larger numbers were presented.

Conclusions/Significance

Our results suggest that two distinct systems underlie quantity discrimination in both humans and fish, implying that the building blocks of uniquely human mathematical abilities may be evolutionarily ancient, dating back to before the divergence of bony fish and tetrapod lineages.     

Infants' knowledge of their own species

Recognition of individuals at first sight is important for social species and can be achieved by attending to facial or body information. Previous research suggests that infants possess a perceptual template for evolutionarily relevant stimuli, which may include humans, dangerous animals (e.g. snakes), but not non-dangerous animals. To be effective, such a mechanism should result in a systematic preference for attending to humans over non-dangerous animals. Using a preferential looking paradigm, the present studies investigated the nature of infants' early representation of humans. We show that 3.5- and six-month-old infants attend more to human beings than non-human primates (a gorilla or monkey) which are examplars of non-dangerous animals. This occurred when infants were presented with head or body information in isolation, as well as when both are presented simultaneously. This early preference for humans by 3.5 months of age suggests that there is a basic representation for humans, which includes both head and/or body information. However, neonates demonstrated a preference only for human faces over non-human primate faces, not for humans over non-human primates when the stimuli were presented with both head and body simultaneously. The results show that although neonates display a preference for human faces over others, preference for the human body only develops later, in the first few months of life. This suggests that infants have acquired some knowledge about the human body at 3.5 months of age that may have developed from their privileged experience with other humans in the first few months of life, rather than an innate ability to detect humans in their entirety.     

A model of social grooming among adult female monkeys.

Grooming networks among adult female monkeys exhibit two similar features across a number of different species. High-ranking animals receive more grooming than others, and the majority of grooming occurs between females of adjacent rank. A theoretical model which duplicates these features is presented, and the properties of the model are used to explain the possible causation and function of female grooming behaviour. The model illustrates how relatively simple principles governing the behaviour of individuals may be used to explain more complex aspects of the social structure of non-human primate groups.     

Transitive inference in non-human animals: an empirical and theoretical analysis

Transitive inference has long been considered one of the hallmarks of human deductive reasoning. Recent reports of transitive-like behaviors in non-human animals have prompted a flourishing empirical and theoretical search for the mechanism(s) that may mediate this ability in non-humans. In this paper, I begin by describing the transitive inference tasks customarily used with non-human animals and then review the empirical findings. Transitive inference has been demonstrated in a wide variety of species, and the signature effects that usually accompany transitive inference in humans (the serial position effect and the symbolic distance effect) have also been found in non-humans. I then critically analyze the most prominent models of this ability in non-human animals. Some models are cognitive, proposing for instance that animals use the rules of formal logic or form mental representations of the premises to solve the task, others are based on associative mechanisms such as value transfer and reinforcement and non-reinforcement. Overall, I argue that the reinforcement-based models are in a much better empirical and theoretical position. Hence, transitive inference in non-human animals should be considered a property of reinforcement history rather than of inferential processes. I finalize by shedding some light on some promising lines of research.     

Effects of development and enculturation on number representation in the brain

A striking way in which humans differ from non-human primates is in their ability to represent numerical quantity using abstract symbols and to use these 'mental tools' to perform skills such as exact calculations. How do functional brain circuits for the symbolic representation of numerical magnitude emerge? Do neural representations of numerical magnitude change as a function of development and the learning of mental arithmetic? Current theories suggest that cultural number symbols acquire their meaning by being mapped onto non-symbolic representations of numerical magnitude. This Review provides an evaluation of this contention and proposes hypotheses to guide investigations into the neural mechanisms that constrain the acquisition of cultural representations of numerical magnitude.     

Comparative psychology and the grand challenge of drug discovery in psychiatry and neurodegeneration

Drug discovery for brain disorders is undergoing a period of upheaval. Faced with an empty drug pipeline and numerous failures of potential new drugs in clinical trials, many large pharmaceutical companies have been shrinking or even closing down their research divisions that focus on central nervous system (CNS) disorders. In this paper, we argue that many of the difficulties facing CNS drug discovery stem from a lack of robustness in pre-clinical (i.e., non-human animal) testing. There are two main sources for this lack of robustness. First, there is the lack of replicability of many results from the pre-clinical stage, which we argue is driven by a combination of publication bias and inappropriate selection of statistical and experimental designs. Second, there is the frequent failure to translate results in non-human animals to parallel results in humans in the clinic. This limitation can only be overcome by developing new behavioral tests for non-human animals that have predictive, construct, and etiological validity. Here, we present these translational difficulties as a “grand challenge” to researchers from comparative cognition, who are well positioned to provide new methods for testing behavior and cognition in non-human animals. These new experimental protocols will need to be both statistically robust and target behavioral and cognitive processes that allow for better connection with human CNS disorders. Our hope is that this downturn in industrial research may represent an opportunity to develop new protocols that will re-kindle the search for more effective and safer drugs for CNS disorders.     

Creative or created: using anecdotes to investigate animal cognition

In non-human animals, creative behaviour occurs spontaneously only at low frequencies, so is typically missed by standardised observational methods. Experimental approaches have tended to rely overly on paradigms from child development or adult human cognition, which may be inappropriate for species that inhabit very different perceptual worlds and possess quite different motor capacities than humans. The analysis of anecdotes offers a solution to this impasse, provided certain conditions are met. To be reliable, anecdotes must be recorded immediately after observation, and only the records of scientists experienced with the species and the individuals concerned should be used. Even then, interpretation of a single record is always ambiguous, and analysis is feasible only when collation of multiple records shows that a behaviour pattern occurs repeatedly under similar circumstances. This approach has been used successfully to study a number of creative capacities of animals: the distribution, nature and neural correlates of deception across the primate order; the occurrence of teaching in animals; and the neural correlates of several aptitudes--in birds, foraging innovation, and in primates, innovation, social learning and tool-use. Drawing on these approaches, we describe the use of this method to investigate a new problem, the cognition of the African elephant, a species whose sheer size and evolutionary distance from humans renders the conventional methods of comparative psychology of little use. The aim is both to chart the creative cognitive capacities of this species, and to devise appropriate experimental methods to confirm and extend previous findings.     

Evolutionary foundations of number: spontaneous representation of numerical magnitudes by cotton-top tamarins

Although animals of many species have been shown to discriminate between visual-spatial arrays or auditory-temporal sequences based on numerosity, most of the evidence for numerosity discrimination derives from experiments involving extensive laboratory training. Under these conditions, animals' discrimination of two numerosities depends on their ratio and is independent of their absolute value. It is an open question whether any untrained non-human animal spontaneously represents number in this way, as do human children and adults. We present the results of familiarization-discrimination experiments on cotton-top tamarin monkeys (Saguinus oedipus) that provide evidence for numerosity discrimination in the absence of training. Presented with auditory stimuli (speech syllables) controlled for the continuous variables of sequence duration, item duration, inter-stimulus interval and overall energy, tamarins readily discriminated sequences of 4 versus 8, 4 versus 6, and 8 versus 12 syllables. By contrast, tamarins failed to discriminate sequences of 4 versus 5 and 8 versus 10 syllables, providing evidence that their numerosity discrimination is approximate and shows the ratio signature of numerosity discrimination in humans and trained non-human animals. These results provide strong support for the hypothesis that representations of large, approximate numerosity are evolutionarily ancient and spontaneously available to non-human animals.     

Epidemiology and Molecular Characterization of Cryptosporidium spp. in Humans,Wild Primates,and Domesticated Animals in the Greater Gombe Ecosystem,Tanzania

Cryptosporidium is an important zoonotic parasite globally. Few studies have examined the ecology and epidemiology of this pathogen in rural tropical systems characterized by high rates of overlap among humans, domesticated animals, and wildlife. We investigated risk factors for Cryptosporidium infection and assessed cross-species transmission potential among people, non-human primates, and domestic animals in the Gombe Ecosystem, Kigoma District, Tanzania. A cross-sectional survey was designed to determine the occurrence and risk factors for Cryptosporidium infection in humans, domestic animals and wildlife living in and around Gombe National Park. Diagnostic PCR revealed Cryptosporidium infection rates of 4.3% in humans, 16.0% in non-human primates, and 9.6% in livestock. Local streams sampled were negative. DNA sequencing uncovered a complex epidemiology for Cryptosporidium in this system, with humans, baboons and a subset of chimpanzees infected with C. hominis subtype IfA12G2; another subset of chimpanzees infected with C. suis; and all positive goats and sheep infected with C. xiaoi. For humans, residence location was associated with increased risk of infection in Mwamgongo village compared to one camp (Kasekela), and there was an increased odds for infection when living in a household with another positive person. Fecal consistency and other gastrointestinal signs did not predict Cryptosporidium infection. Despite a high degree of habitat overlap between village people and livestock, our results suggest that there are distinct Cryptosporidium transmission dynamics for humans and livestock in this system. The dominance of C. hominis subtype IfA12G2 among humans and non-human primates suggest cross-species transmission. Interestingly, a subset of chimpanzees was infected with C. suis. We hypothesize that there is cross-species transmission from bush pigs (Potaochoerus larvatus) to chimpanzees in Gombe forest, since domesticated pigs are regionally absent. Our findings demonstrate a complex nature of Cryptosporidium in sympatric primates, including humans, and stress the need for further studies.     

The function of nonlinear phenomena in meerkat alarm calls

Nonlinear vocal phenomena are a ubiquitous feature of human and non-human animal vocalizations. Although we understand how these complex acoustic intrusions are generated, it is not clear whether they function adaptively for the animals producing them. One explanation is that nonlinearities make calls more unpredictable, increasing behavioural responses and ultimately reducing the chances of habituation to these call types. Meerkats (Suricata suricatta) exhibit nonlinear subharmonics in their predator alarm calls. We specifically tested the ‘unpredictability hypothesis’ by playing back naturally occurring nonlinear and linear medium-urgency alarm call bouts. Results indicate that subjects responded more strongly and foraged less after hearing nonlinear alarm calls. We argue that these findings support the unpredictability hypothesis and suggest this is the first study in animals or humans to show that nonlinear vocal phenomena function adaptively.     

Punishment and cooperation in nature

Humans use punishment to promote cooperation in laboratory experiments but evidence that punishment plays a similar role in non-human animals is comparatively rare. In this article, we examine why this may be the case by reviewing evidence from both laboratory experiments on humans and ecologically relevant studies on non-human animals. Generally, punishment appears to be most probable if players differ in strength or strategic options. Although these conditions are common in nature, punishment (unlike other forms of aggression) involves immediate payoff reductions to both punisher and target, with net benefits to punishers contingent on cheats behaving more cooperatively in future interactions. In many cases, aggression yielding immediate benefits may suffice to deter cheats and might explain the relative scarcity of punishment in nature.     

Adult human brain cell culture for neuroscience research

Studies of the brain have progressed enormously through the use of in vivo and in vitro non-human models. However, it is unlikely such studies alone will unravel the complexities of the human brain and so far no neuroprotective treatment developed in animals has worked in humans. In this review we discuss the use of adult human brain cell culture methods in brain research to unravel the biology of the normal and diseased human brain. The advantages of using adult human brain cells as tools to study human brain function from both historical and future perspectives are discussed. In particular, studies using dissociated cultures of adult human microglia, astrocytes, oligodendrocytes and neurons are described and the applications of these types of study are evaluated. Alternative sources of human brain cells such as adult neural stem cells, induced pluripotent stem cells and slice cultures of adult human brain tissue are also reviewed. These adult human brain cell culture methods could benefit basic research and more importantly, facilitate the translation of basic neuroscience research to the clinic for the treatment of brain disorders.