Systems Neuroscience of Natural Behaviors in Rodents.

Animals evolved in complex environments, producing a wide range of behaviors, including navigation, foraging, prey capture, and conspecific interactions, which vary over timescales ranging from milliseconds to days. Historically, these behaviors have been the focus of study for ecology and ethology, while systems neuroscience has largely focused on short timescale behaviors that can be repeated thousands of times and occur in highly artificial environments. Thanks to recent advances in machine learning, miniaturization, and computation, it is newly possible to study freely moving animals in more natural conditions while applying systems techniques: performing temporally specific perturbations, modeling behavioral strategies, and recording from large numbers of neurons while animals are freely moving. The authors of this review are a group of scientists with deep appreciation for the common aims of systems neuroscience, ecology, and ethology. We believe it is an extremely exciting time to be a neuroscientist, as we have an opportunity to grow as a field, to embrace interdisciplinary, open, collaborative research to provide new insights and allow researchers to link knowledge across disciplines, species, and scales. Here we discuss the origins of ethology, ecology, and systems neuroscience in the context of our own work and highlight how combining approaches across these fields has provided fresh insights into our research. We hope this review facilitates some of these interactions and alliances and helps us all do even better science, together.

Rage Against the Machine: Advancing the study of aggression ethology via machine learning.

RATIONALE: Aggression, comorbid with neuropsychiatric disorders, exhibits with diverse clinical presentations and places a significant burden on patients, caregivers, and society. This diversity is observed because aggression is a complex behavior that can be ethologically demarcated as either appetitive (rewarding) or reactive (defensive), each with its own behavioral characteristics, functionality, and neural basis that may transition from adaptive to maladaptive depending on genetic and environmental factors. There has been a recent surge in the development of preclinical animal models for studying appetitive aggression-related behaviors and identifying the neural mechanisms guiding their progression and expression. However, adoption of these procedures is often impeded by the arduous task of manually scoring complex social interactions. Manual observations are generally susceptible to observer drift, long analysis times, and poor inter-rater reliability, and are further incompatible with the sampling frequencies required of modern neuroscience methods. OBJECTIVES: In this review, we discuss recent advances in the preclinical study of appetitive aggression in mice, paired with our perspective on the potential for machine learning techniques in producing automated, robust scoring of aggressive social behavior. We discuss critical considerations for implementing valid computer classifications within behavioral pharmacological studies. KEY RESULTS: Open-source automated classification platforms can match or exceed the performance of human observers while removing the confounds of observer drift, bias, and inter-rater reliability. Furthermore, unsupervised approaches can identify previously uncharacterized aggression-related behavioral repertoires in model species. DISCUSSION AND CONCLUSIONS: Advances in open-source computational approaches hold promise for overcoming current manual annotation caveats while also introducing and generalizing computational neuroethology to the greater behavioral neuroscience community. We propose that currently available open-source approaches are sufficient for overcoming the main limitations preventing wide adoption of machine learning within the context of preclinical aggression behavioral research.

Traditional knowledge and perception of birds in the Parnaíba Delta environmental protection area, Northeast Brazil

Local inhabitants retain a vast knowledge about the bird richness surrounding them, as well as many of their ethological and ecological aspects, and can identify the importance of those birds to the maintenance of ecosystem integrity. The present study sought to document the traditional knowledge retained by members of the Labino community concerning the avifauna of the Delta do Rio Parnaíba Environmental Protection Area (APA), Piauí State, Brazil. We interviewed 76 male (51% of the sample) and 74 female (49%) residents. The interviewees indicated the occurrence of 97 bird species belonging to 21 orders and 40 families. Men could identify more bird species than women. Older individuals recognize more bird species than younger members of the community. Individuals with less schooling demonstrated greater knowledge of species richness than those with more formal educations. A very significant percentage (45%, n = 68) of the interviewees reported consuming native birds, principally Aramides cajaneus, Columbina squammata, and Zenaida auriculata. A total of 48 species were perceived as having their populations reduced in recent years, principally Mimus gilvus, Icterus jamacaii, Aramides cajaneus, Turdus rufiventris, and Cacicus cela. The residents of the Labino community were therefore found to have a detailed knowledge of the local avifauna and perceived impacts caused mainly by hunting in the Parnaiba River Delta region.

Electric fish genomics: Progress, prospects, and new tools for neuroethology.

Electric fish have served as a model system in biology since the 18th century, providing deep insight into the nature of bioelectrogenesis, the molecular structure of the synapse, and brain circuitry underlying complex behavior. Neuroethologists have collected extensive phenotypic data that span biological levels of analysis from molecules to ecosystems. This phenotypic data, together with genomic resources obtained over the past decades, have motivated new and exciting hypotheses that position the weakly electric fish model to address fundamental 21st century biological questions. This review article considers the molecular data collected for weakly electric fish over the past three decades, and the insights that data of this nature has motivated. For readers relatively new to molecular genetics techniques, we also provide a table of terminology aimed at clarifying the numerous acronyms and techniques that accompany this field. Next, we pose a research agenda for expanding genomic resources for electric fish research over the next 10years. We conclude by considering some of the exciting research prospects for neuroethology that electric fish genomics may offer over the coming decades, if the electric fish community is successful in these endeavors.

From classic ethology to modern neuroethology: overcoming the three biases in social behavior research.

A typical current study investigating the neurobiology of animal behavior is likely restricted to male subjects, of standard inbred mouse strains, tested in simple behavioral assays under laboratory conditions. This approach enables the use of advanced molecular tools, alongside standardization and reproducibility, and has led to tremendous discoveries. However, the cost is a loss of genetic and phenotypic diversity and a divergence from ethologically-relevant behaviors. Here we review the pros and cons in behavioral neuroscience studies of the new era, focusing on reproductive behaviors in rodents. Recent advances in molecular technology and behavioral phenotyping in semi-natural conditions, together with an awareness of the critical need to study both sexes, may provide new insights into the neural mechanisms underlying social behaviors.

Trends in the Brazilian journal Revista de Etologia: a review from 1998 to 2014 / Tendências no periódico brasileiro Revista de Etologia: uma revisão de 1998 a 2014

Revista de Etologia (RE) is a Brazilian journal aimed at publishing scientific articles in the field of Ethology (Animal Behavior). Recently, RE was renamed to "Current Ethology", and some of its publishing policies were changed. A survey of the published articles in the journal while still named RE was carried out with the purpose of recognizing publication trends and patterns. The journal was regularly published during two periods: from 1998 to 2006 and from 2010 to 2014. Recent years have seen a reduction in the number of volumes published, but studies listed as "Observational" were prevalent in almost all volumes. Class "Mammalia" was the most studied taxon in the RE reports. Southeast Brazil has the highest number of empirical investigations and of publishing institutions. RE also contains publications from 12 countries. These trends are discussed taking into account the development of Ethology in Brazil and the current state of the country's biodiversity cataloging. The low number of studies on animal behavior in most regions of Brazil is pointed out and a suggestion for further research is mentioned

A Revista de Etologia (RE) é um periódico brasileiro destinado à publicação de artigos científicos no campo da Etologia (Comportamento Animal) em geral. Recentemente, a RE foi renomeada Current Ethology, e algumas de suas políticas de publicação foram alteradas. Neste trabalho foi feito o levantamento dos artigos no periódico ainda como RE com o objetivo de indicar tendências e padrões nos trabalhos publicados. Houve regularidade nas publicações em dois períodos: de 1998 a 2006, e de 2010 a 2014. Os anos recentes foram menos prolíficos, e estudos identificados como "Observacionais" predominaram em todos os volumes. A classe "Mammalia" foi o táxon mais estudado nos artigos da RE. Instituições da região Sudeste do Brasil foram responsáveis pelo maior número de publicações no periódico estudado. A RE contém artigos de 12 países. Essas tendências são discutidas levando-se em conta o desenvolvimento da Etologia no Brasil e o estado atual da catalogação da biodiversidade do país. O número reduzido de estudos sobre comportamento animal na maior parte das regiões do Brasil é apontado, e sugestões para pesquisas adicionais são fornecidas

Toward a science of computational ethology.

The new field of "Computational Ethology" is made possible by advances in technology, mathematics, and engineering that allow scientists to automate the measurement and the analysis of animal behavior. We explore the opportunities and long-term directions of research in this area.

Decision making: the neuroethological turn.

Neuroeconomics applies models from economics and psychology to inform neurobiological studies of choice. This approach has revealed neural signatures of concepts like value, risk, and ambiguity, which are known to influence decision making. Such observations have led theorists to hypothesize a single, unified decision process that mediates choice behavior via a common neural currency for outcomes like food, money, or social praise. In parallel, recent neuroethological studies of decision making have focused on natural behaviors like foraging, mate choice, and social interactions. These decisions strongly impact evolutionary fitness and thus are likely to have played a key role in shaping the neural circuits that mediate decision making. This approach has revealed a suite of computational motifs that appear to be shared across a wide variety of organisms. We argue that the existence of deep homologies in the neural circuits mediating choice may have profound implications for understanding human decision making in health and disease.

Toward an organismal neurobiology: integrative neuroethology.

Overt behavior is generated in response to a palette of external and internal stimuli and internal drives. Rarely are these variables introduced in isolation. This creates challenges for the organism to sort inputs that frequently favor conflicting behaviors. Under these conditions, the nervous system relies on established and flexible hierarchies to produce appropriate behavioral changes. The pteropod mollusc Clione limacina is used as an example to illustrate a variety of behavioral interactions that alter a baseline behavioral activity: slow swimming. The alterations include acceleration within the slow swimming mode, acceleration from the slow to fast swimming modes, whole body withdrawal (and inhibition of swimming), food acquisition behavior (with a feeding motivational state), and a startle locomotory response. These examples highlight different types of interaction between the baseline behavior and the new behaviors that involve external stimuli and two types of internal drives: a modular arousal system and a motivational state. The investigation of hierarchical interactions between behavioral modules is a central theme of integrative neuroethology that focuses on an organismal level of understanding of the neural control of behavior.

Complex echo classification by echo-locating bats: a review.

Echo-locating bats constantly emit ultrasonic pulses and analyze the returning echoes to detect, localize, and classify objects in their surroundings. Echo classification is essential for bats' everyday life; for instance, it enables bats to use acoustical landmarks for navigation and to recognize food sources from other objects. Most of the research of echo based object classification in echo-locating bats was done in the context of simple artificial objects. These objects might represent prey, flower, or fruit and are characterized by simple echoes with a single up to several reflectors. Bats, however, must also be able to use echoes that return from complex structures such as plants or other types of background. Such echoes are characterized by superpositions of many reflections that can only be described using a stochastic statistical approach. Scientists have only lately started to address the issue of complex echo classification by echo-locating bats. Some behavioral evidence showing that bats can classify complex echoes has been accumulated and several hypotheses have been suggested as to how they do so. Here, we present a first review of this data. We raise some hypotheses regarding possible interpretations of the data and point out necessary future directions that should be pursued.

Controlled studies of chimpanzee cultural transmission.

Following the first long-term field studies of chimpanzees in the 1960s, researchers began to suspect that chimpanzees from different African populations varied in their behavior, and that some of these variations were transmitted through social learning, thus suggesting culture. Additional reports of chimpanzee culture have since accumulated, which involve an increasing amount of behavioral variation that has no obvious ecological or genetic explanation. To date, close to 50 cultural variants have been reported, including subsistence behavior, tool-use, communication signals, and grooming patterns. Nevertheless, field studies lack the experimental controls and manipulations necessary to conclusively demonstrate that the observed variation results from differential invention and social transmission of behavior. This would require that behavioral variants have been learned from others, a question best addressed in a controlled experimental setting. The following chapter details a series of experimental studies at Yerkes National Primate Research Center of Emory University. In each case, the behavior of two captive groups (each N=12 individuals) was compared before and after the introduction of a novel foraging behavior by a trained conspecific "inventor." The studies were designed to investigate (i) the conditions under which chimpanzees learn from one another, (ii) how behaviors are transmitted, (iii) how cultures are maintained over generations. The results emphasize the importance of integrating both fieldwork and experimental approaches. Previous studies have reported deficits in chimpanzees' cultural capacities, but did so after testing them with human models, which are largely irrelevant to the problem at hand. A representative understanding of culture can only be gained when efforts are made to create a naturalistic learning environment in which chimpanzees have opportunities to learn spontaneously from conspecifics in a familiar social setting.

Aquatic animals, cognitive ethology, and ethics: questions about sentience and other troubling issues that lurk in turbid water.

In this general, strongly pro-animal, and somewhat utopian and personal essay, I argue that we owe aquatic animals respect and moral consideration just as we owe respect and moral consideration to all other animal beings, regardless of the taxonomic group to which they belong. In many ways it is more difficult to convince some people of our ethical obligations to numerous aquatic animals because we do not identify or empathize with them as we do with animals with whom we are more familiar or to whom we are more closely related, including those species (usually terrestrial) to whom we refer as charismatic megafauna. Many of my examples come from animals that are more well studied but they can be used as models for aquatic animals. I follow Darwinian notions of evolutionary continuity to argue that if we feel pain, then so too do many other animals, including those that live in aquatic environs. Recent scientific data ('science sense') show clearly that many aquatic organisms, much to some people's surprise, likely suffer at our hands and feel their own sorts of pain. Throughout I discuss how cognitive ethology (the study of animal minds) is the unifying science for understanding the subjective, emotional, empathic, and moral lives of animals because it is essential to know what animals do, think, and feel as they go about their daily routines. Lastly, I argue that when we are uncertain if we are inflicting pain due to our incessant, annoying, and frequently unnecessary intrusions into the lives of other animals as we go about 'redecorating nature' (removing animals or moving them from place to place), we should err on the side of the animals and stop engaging in activities that cause pain and suffering.

Ethological and temporal analyses of anxiety-like behavior: the elevated plus-maze model 20 years on.

As well as being considered a reliable measurement instrument of animal anxiety-like behavior, the elevated plus-maze (EPM) is also used as a post-hoc test to evaluate emotionality in genetically modified rodents. The present review considers factors which may further improve the validity (predictive/face/construct) of the EPM model: (1) the importance of measuring defensive patterns of response such as risk assessment in addition to traditional measures such as open arm time; (2) other methodological refinements such as min-by-min scoring and use of a test/retest protocol; and (3) the identification and control of major sources of variability in this test. To estimate whether current use of the EPM by researchers takes the above factor into account, a survey of the recent literature was conducted. Results showed that the majority of studies have not yet assimilated these important considerations into their use of the EPM. For example, although risk assessment measures may be more sensitive to anxiety modulating drugs than traditional measures, only a quarter of studies have adopted them. It is hoped that this review can provide insights into the optimal use of the EPM, a simple task that can be very complex in terms of behavioral analysis.