Preserved neural dynamics across animals performing similar behaviour.

Animals of the same species exhibit similar behaviours that are advantageously adapted to their body and environment. These behaviours are shaped at the species level by selection pressures over evolutionary timescales. Yet, it remains unclear how these common behavioural adaptations emerge from the idiosyncratic neural circuitry of each individual. The overall organization of neural circuits is preserved across individuals1 because of their common evolutionarily specified developmental programme2-4. Such organization at the circuit level may constrain neural activity5-8, leading to low-dimensional latent dynamics across the neural population9-11. Accordingly, here we suggested that the shared circuit-level constraints within a species would lead to suitably preserved latent dynamics across individuals. We analysed recordings of neural populations from monkey and mouse motor cortex to demonstrate that neural dynamics in individuals from the same species are surprisingly preserved when they perform similar behaviour. Neural population dynamics were also preserved when animals consciously planned future movements without overt behaviour12 and enabled the decoding of planned and ongoing movement across different individuals. Furthermore, we found that preserved neural dynamics extend beyond cortical regions to the dorsal striatum, an evolutionarily older structure13,14. Finally, we used neural network models to demonstrate that behavioural similarity is necessary but not sufficient for this preservation. We posit that these emergent dynamics result from evolutionary constraints on brain development and thus reflect fundamental properties of the neural basis of behaviour.

Variation in personality can substitute for social feedback in coordinated animal movements.

Collective movements are essential for the effective function of animal societies, but are complicated by the need for consensus among group members. Consensus is typically assumed to arise via feedback mechanisms, but this ignores inter-individual variation in behavioural tendency ('personality'), which is known to underpin the successful function of many complex societies. In this study, we use a theoretical approach to examine the relative importance of personality and feedback in the emergence of collective movement decisions in animal groups. Our results show that variation in personality dramatically influences collective decisions and can partially or completely replace feedback depending on the directionality of relationships among individuals. The influence of personality increases with the exaggeration of differences among individuals. While it is likely that both feedback and personality interact in nature, our findings highlight the potential importance of personality in driving collective processes.

Researchers Keep Rejecting Grandmother Cells after Running the Wrong Experiments: The Issue Is How Familiar Stimuli Are Identified.

There is widespread agreement in neuroscience and psychology that the visual system identifies objects and faces based on a pattern of activation over many neurons, each neuron being involved in representing many different categories. The hypothesis that the visual system includes finely tuned neurons for specific objects or faces for the sake of identification, so-called "grandmother cells", is widely rejected. Here it is argued that the rejection of grandmother cells is premature. Grandmother cells constitute a hypothesis of how familiar visual categories are identified, but the primary evidence against this hypothesis comes from studies that have failed to observe neurons that selectively respond to unfamiliar stimuli. These findings are reviewed and it is shown that they are irrelevant. Neuroscientists need to better understand existing models of face and object identification that include grandmother cells and then compare the selectivity of these units with single neurons responding to stimuli that can be identified.

Perturbing low dimensional activity manifolds in spiking neuronal networks.

Several recent studies have shown that neural activity in vivo tends to be constrained to a low-dimensional manifold. Such activity does not arise in simulated neural networks with homogeneous connectivity and it has been suggested that it is indicative of some other connectivity pattern in neuronal networks. In particular, this connectivity pattern appears to be constraining learning so that only neural activity patterns falling within the intrinsic manifold can be learned and elicited. Here, we use three different models of spiking neural networks (echo-state networks, the Neural Engineering Framework and Efficient Coding) to demonstrate how the intrinsic manifold can be made a direct consequence of the circuit connectivity. Using this relationship between the circuit connectivity and the intrinsic manifold, we show that learning of patterns outside the intrinsic manifold corresponds to much larger changes in synaptic weights than learning of patterns within the intrinsic manifold. Assuming larger changes to synaptic weights requires extensive learning, this observation provides an explanation of why learning is easier when it does not require the neural activity to leave its intrinsic manifold.

Infrared thermal imaging: Positive and negative emotions modify the skin temperatures of monkey and ape faces.

Facial thermography has enabled researchers to noninvasively and continuously measure the changes of a range of emotional states in humans. The present work used this novel technology to study the effect of positive and negative emotions in nonhuman primates by focusing on four facial areas (the peri-orbital area, the nose bridge, the nose tip, and the upper lip). Monkeys and apes were examined for positive emotions (during interactions with toys and during tickling) and for negative emotions (during food delay and teasing). For the combined toy and tickling condition, the results indicated a drop in the nose tip temperature and a tendency of an increase in the peri-orbital temperature. For the combined food delay and teasing condition, the results also revealed a rise in the upper lip temperature of the subjects. These different effects on the facial temperatures in monkeys and apes most likely reflect distinctive physiological reactions of a primordial primate emotion system. We conclude that facial thermal imaging represents a promising physiologically grounded technology to noninvasively and continuously obtain reliable data on emotional states in nonhuman primates, which may help modernize research on emotions in nonhuman primates and enhance our understanding of the evolution of human emotions.

A probabilistic, distributed, recursive mechanism for decision-making in the brain.

Decision formation recruits many brain regions, but the procedure they jointly execute is unknown. Here we characterize its essential composition, using as a framework a novel recursive Bayesian algorithm that makes decisions based on spike-trains with the statistics of those in sensory cortex (MT). Using it to simulate the random-dot-motion task, we demonstrate it quantitatively replicates the choice behaviour of monkeys, whilst predicting losses of otherwise usable information from MT. Its architecture maps to the recurrent cortico-basal-ganglia-thalamo-cortical loops, whose components are all implicated in decision-making. We show that the dynamics of its mapped computations match those of neural activity in the sensorimotor cortex and striatum during decisions, and forecast those of basal ganglia output and thalamus. This also predicts which aspects of neural dynamics are and are not part of inference. Our single-equation algorithm is probabilistic, distributed, recursive, and parallel. Its success at capturing anatomy, behaviour, and electrophysiology suggests that the mechanism implemented by the brain has these same characteristics.

A metacognitive illusion in monkeys.

Like humans, monkeys can make accurate judgements about their own memory by reporting their confidence during cognitive tasks. Some have suggested that animals use associative learning to make accurate confidence judgements, while others have suggested animals directly access and estimate the strength of their memories. Here we test a third, non-exclusive possibility: perhaps monkeys, like humans, base metacognitive inferences on heuristic cues. Humans are known to use cues like perceptual fluency (e.g. how easy something is to see) when making metacognitive judgements. We tested monkeys using a match-to-sample task in which the perceptual fluency of the stimuli was manipulated. The monkeys made confidence wagers on their accuracy before or after each trial. We found that monkeys' wagers were affected by perceptual fluency even when their accuracy was not. This is novel evidence that animals are susceptible to metacognitive illusions similar to those experienced by humans.

A random-matrix theory of the number sense.

Number sense, a spontaneous ability to process approximate numbers, has been documented in human adults, infants and newborns, and many other animals. Species as distant as monkeys and crows exhibit very similar neurons tuned to specific numerosities. How number sense can emerge in the absence of learning or fine tuning is currently unknown. We introduce a random-matrix theory of self-organized neural states where numbers are coded by vectors of activation across multiple units, and where the vector codes for successive integers are obtained through multiplication by a fixed but random matrix. This cortical implementation of the 'von Mises' algorithm explains many otherwise disconnected observations ranging from neural tuning curves in monkeys to looking times in neonates and cortical numerotopy in adults. The theory clarifies the origin of Weber-Fechner's Law and yields a novel and empirically validated prediction of multi-peak number neurons. Random matrices constitute a novel mechanism for the emergence of brain states coding for quantity.This article is part of a discussion meeting issue 'The origins of numerical abilities'.

Do monkeys have a theory of mind? How to answer the question?

Since Premack and Woodruf (1978), the study of mindreading abilities in nonhumans, especially primates, has been thoroughly investigated. But attempts to understand the evolution of this aspect of human intelligence have mainly focused on comparisons between apes and human infants, while relatively little is known about the abilities of monkeys. This lack of data on monkeys seems mainly due to the hypothesis of a cognitive "gap" between apes and monkeys. However, in recent years monkeys have been featuring more prominently in the landscape of social cognition research, and some of these systematic studies appear promising. This paper reviews i) current knowledge about monkeys' socio-cognitive abilities, especially regarding gaze processing, attention and intention reading, and perspective-taking, ii) alternative hypotheses regarding the underlying mechanisms of such complex behaviors, and iii) potential new perspectives and future directions for studying ToM in monkeys.

Marmosets: A Neuroscientific Model of Human Social Behavior.

The common marmoset (Callithrix jacchus) has garnered interest recently as a powerful model for the future of neuroscience research. Much of this excitement has centered on the species' reproductive biology and compatibility with gene editing techniques, which together have provided a path for transgenic marmosets to contribute to the study of disease as well as basic brain mechanisms. In step with technical advances is the need to establish experimental paradigms that optimally tap into the marmosets' behavioral and cognitive capacities. While conditioned task performance of a marmoset can compare unfavorably with rhesus monkey performance on conventional testing paradigms, marmosets' social behavior and cognition are more similar to that of humans. For example, marmosets are among only a handful of primates that, like humans, routinely pair bond and care cooperatively for their young. They are also notably pro-social and exhibit social cognitive abilities, such as imitation, that are rare outside of the Apes. In this Primer, we describe key facets of marmoset natural social behavior and demonstrate that emerging behavioral paradigms are well suited to isolate components of marmoset cognition that are highly relevant to humans. These approaches generally embrace natural behavior, which has been rare in conventional primate testing, and thus allow for a new consideration of neural mechanisms underlying primate social cognition and signaling. We anticipate that through parallel technical and paradigmatic advances, marmosets will become an essential model of human social behavior, including its dysfunction in neuropsychiatric disorders.

"Zeroing" in on mathematics in the monkey brain.

A new study documented that monkeys showed selective neuronal responding to the concept of zero during a numerical task, and that there were two distinct classes of neurons that coded the absence of stimuli either through a discrete activation pattern (zero or not zero) or a continuous one for which zero was integrated with other numerosities in the relative rate of activity. These data indicate that monkeys, like humans, have a concept of zero that is part of their analog number line but that also may have unique properties compared to other numerosities.

The visual cliff's forgotten menagerie: rats, goats, babies, and myth-making in the history of psychology.

Eleanor Gibson and Richard Walk's famous visual cliff experiment is one of psychology's classic studies, included in most introductory textbooks. Yet the famous version which centers on babies is actually a simplification, the result of disciplinary myth-making. In fact the visual cliff's first subjects were rats, and a wide range of animals were tested on the cliff, including chicks, turtles, lambs, kid goats, pigs, kittens, dogs, and monkeys. The visual cliff experiment was more accurately a series of experiments, employing varying methods and a changing apparatus, modified to test different species. This paper focuses on the initial, nonhuman subjects of the visual cliff, resituating the study in its original experimental logic, connecting it to the history of comparative psychology, Gibson's interest in comparative psychology, as well as gender-based discrimination. Recovering the visual cliff's forgotten menagerie helps to counter the romanticization of experimentation by focusing on the role of extrascientific factors, chance, complexity, and uncertainty in the experimental process.

Incisor crown bending strength correlates with diet and incisor curvature in anthropoid primates.

Anthropoid incisors are large relative to the postcanine dentition and function in the preprocessing of food items. Previous analyses of anthropoid incisor allometry and shape demonstrate that incisor morphology is correlated with preferred foods and that more frugivorous anthropoids have larger and more curved incisors. Although the relationship between incisal crown curvature and preferred foods has been well documented in extant and fossil anthropoids, the functional significance of curvature variation has yet to be conclusively established. Given that an increase in crown curvature will increase maximum linear crown dimensions, and bending resistance is a function of linear crown dimensions, it is hypothesized that incisor crown curvature functons to increase incisor crown resistance to bending forces. This study uses beam theory to calculate the mesiodistal and labiolingual bending strengths of the maxillary and mandibular incisors of hominoid and platyrrhine taxa with differing diets and variable degrees of incisal curvature. Results indicate that bending strength correlates with incisal curvature and that frugivores have elevated incisor bending resistance relative to folivores. Maxillary central incisor bending strengths further discriminate platyrrhine and hominoid hard- and soft-object frugivores suggesting this crown is subjected to elevated occlusal loading relative to other incisors. These results are consistent with the hypothesis that incisor crown curvature functions to increase incisor crown resistance to bending forces but does not preclude the possibility that incisor bending strength is a composite function of multiple dentognathic variables including, but not limited to, incisor crown curvature.

Insight em macacos-prego (Sapajus spp) com diferentes contextos de treino das habilidades pré-requisitos / Insight in Capuchin-monkeys (Sapajus spp) with different contexts of training of prerequisite abilities

Insight, na Psicologia Experimental, indica, tradicionalmente, a resolução súbita e espontânea de um determinado problema. O presente estudo verificou a ocorrência de resolução súbita em macacos-prego (Sapajus spp.) a partir do treino de habilidades pré-requisitos de uma tarefa. Adicionalmente o estudo avaliou se a manipulação do local de treino altera a topografia de solução do problema. Dois sujeitos foram treinados a: a) encaixar objetos e b) pescar objetos fora do alcance utilizando uma ferramenta. O treino das duas habilidades se deu de forma independente e em diferentes contextos. A tarefa final consistiiu em pescar um alimento fora do alcance encaixando um par de ferramentas nunca antes manuseado. Os dois sujeitos resolveram a tarefa, entretanto, nenhum apresentou um desempenho tipicamente de insight, na medida em que as resoluções foram pouco fluidas, com pausas entre suas etapas, e aparentemente sem direcionamento. Discute-se o papel do treino das habilidades pré-requisitos em ambientes diferenciados como um fator que dificulta a resolução da tarefa (AU)

Insight em macacos-prego (Sapajus spp) com diferentes contextos de treino das habilidades pré-requisitos / Insight in Capuchin-monkeys (Sapajus spp) with different contexts of training of prerequisite abilities

Insight, na Psicologia Experimental, indica, tradicionalmente, a resolução súbita e espontânea de um determinado problema. O presente estudo verificou a ocorrência de resolução súbita em macacos-prego (Sapajus spp.) a partir do treino de habilidades pré-requisitos de uma tarefa. Adicionalmente o estudo avaliou se a manipulação do local de treino altera a topografia de solução do problema. Dois sujeitos foram treinados a: a) encaixar objetos e b) pescar objetos fora do alcance utilizando uma ferramenta. O treino das duas habilidades se deu de forma independente e em diferentes contextos. A tarefa final consistiiu em pescar um alimento fora do alcance encaixando um par de ferramentas nunca antes manuseado. Os dois sujeitos resolveram a tarefa, entretanto, nenhum apresentou um desempenho tipicamente de insight, na medida em que as resoluções foram pouco fluidas, com pausas entre suas etapas, e aparentemente sem direcionamento. Discute-se o papel do treino das habilidades pré-requisitos em ambientes diferenciados como um fator que dificulta a resolução da tarefa

Insight, in Experimental Psychology, traditionally refers a sudden and spontaneous solution of a specific problem. The present study aims to verify the occurrence of sudden problem resolution in capuchin monkeys (Sapajus spp.) based on explicit training of two pre-requisite repertoires. Additionally, we examined if the manipulation of the context of training alters the topography of the problem solution response. Two subjects were trained to: a) join objects, and b) to rake objects with a tool. The training of the two repertoires was independent and was carried out in different contexts. The final task consists in raking a piece of food with a joinable tool that was never seen before. The two subjects solved the task, but the topography of solution was not clearly compatible with insight interpretation. The solutions had pauses between steps, and the behavior was not goal directed. The negative effects of different contexts for the training of the pre-requisite repertoires are discussed

A translational neuroscience approach to understanding the development of social anxiety disorder and its pathophysiology.

This review brings together recent research from molecular, neural circuit, animal model, and human studies to help understand the neurodevelopmental mechanisms underlying social anxiety disorder. Social anxiety disorder is common and debilitating, and it often leads to further psychopathology. Numerous studies have demonstrated that extremely behaviorally inhibited and temperamentally anxious young children are at marked risk of developing social anxiety disorder. Recent work in human and nonhuman primates has identified a distributed brain network that underlies early-life anxiety including the central nucleus of the amygdala, the anterior hippocampus, and the orbitofrontal cortex. Studies in nonhuman primates have demonstrated that alterations in this circuit are trait-like in that they are stable over time and across contexts. Notably, the components of this circuit are differentially influenced by heritable and environmental factors, and specific lesion studies have demonstrated a causal role for multiple components of the circuit. Molecular studies in rodents and primates point to disrupted neurodevelopmental and neuroplastic processes within critical components of the early-life dispositional anxiety neural circuit. The possibility of identifying an early-life at-risk phenotype, along with an understanding of its neurobiology, provides an unusual opportunity to conceptualize novel preventive intervention strategies aimed at reducing the suffering of anxious children and preventing them from developing further psychopathology.

Frequency of behavior witnessed and conformity in an everyday social context.

Conformity is thought to be an important force in human evolution because it has the potential to stabilize cultural homogeneity within groups and cultural diversity between groups. However, the effects of such conformity on cultural and biological evolution will depend much on the particular way in which individuals are influenced by the frequency of alternative behavioral options they witness. In a previous study we found that in a natural situation people displayed a tendency to be 'linear-conformist'. When visitors to a Zoo exhibit were invited to write or draw answers to questions on cards to win a small prize and we manipulated the proportion of text versus drawings on display, we found a strong and significant effect of the proportion of text displayed on the proportion of text in the answers, a conformist effect that was largely linear with a small non-linear component. However, although this overall effect is important to understand cultural evolution, it might mask a greater diversity of behavioral responses shaped by variables such as age, sex, social environment and attention of the participants. Accordingly we performed a further study explicitly to analyze the effects of these variables, together with the quality of the information participants' responses made available to further visitors. Results again showed a largely linear conformity effect that varied little with the variables analyzed.

Inferences about the location of food in lemurs (Eulemur macaco and Eulemur fulvus): a comparison with apes and monkeys.

The ability of black and brown lemurs (Eulemur macaco and Eulemur fulvus) to make inferences about hidden food was tested using the same paradigm as in Call's (J Comp Psycol 118:232-241, 2004) cup task experiment. When provided with either visual or auditory information about the content of two boxes (one empty, one baited), lemurs performed better in the auditory condition than in the visual one. When provided with visual or auditory information only about the empty box, one subject out of four was above chance in the auditory condition, implying inferential reasoning. No subject was successful in the visual condition. This study reveals that (1) lemurs are capable of inferential reasoning by exclusion and (2) lemurs make better use of auditory than visual information. The results are compared with the performances recorded in apes and monkeys under the same paradigm.