An in‐field experimental test of pinniped behavioral types

There has been extensive recent interest in the concepts of behavioral types, behavioral syndromes, and personalities in nonhuman animal species. Evidence for behavioral types now exists from a wide range of taxa, from mollusks to mammals. However, marine mammals are poorly represented in this literature. Here, we describe an in‐field experimental test of behavioral types in breeding gray seals, using a remotely controlled vehicle to deliver a standardized test stimulus to target individuals. We report on the design and implementation of this test and on the behavioral responses of individuals. Analysis of behavioral responses from both males and females revealed consistent individual differences across tests, suggesting that this is a practical and viable technique for determining individual variation in behavioral type in the field. Despite extensive literature on behavioral types, studies of behavioral types in wild populations remain rare. It is, therefore, important to develop ways to identify and quantify the existence of behavioral types in natural populations, because only by doing this, can we hope to ascertain the ecological and evolutionary relevance of behavioral types.     

The genetic contribution to canine personality

The domestic dog may be exceptionally well suited for behavioral genetic studies owing to its population history and the striking behavior differences among breeds. To explore to what extent and how behavioral traits are transmitted between generations, heritabilities and genetic correlations for behavioral traits were estimated in a cohort containing over 10,000 behaviorally tested German shepherd and Rottweiler dogs. In both breeds, the pattern of co-inheritance was found to be similar for the 16 examined behavioral traits. Furthermore, over 50% of the additive genetic variation of the behavioral traits could be explained by one underlying principal component, indicating a shared genetic component behind most of the examined behavioral traits. Only aggression appears to be inherited independently of the other traits. The results support a genetic basis for a broad personality trait previously named shyness-boldness dimension, and heritability was estimated to be 0.25 in the two breeds. Therefore, breeds of dogs appear to constitute a valuable resource for behavioral genetic research on the normal behavioral differences in broad personality traits.     

Are shy individuals less behaviorally variable? Insights from a captive population of mouse lemurs

Increasingly, individual variation in personality has become a focus of behavioral research in animal systems. Boldness and shyness, often quantified as the tendency to explore novel situations, are seen as personality traits important to the fitness landscape of individuals. Here we tested for individual differences within and across contexts in behavioral responses of captive mouse lemurs (Microcebus murinus) to novel objects, novel foods, and handling. We report consistent differences in behavioral responses for objects and handling. We also found that the responses to handling and novel objects were correlated and repeatable. Lastly, we show that shyer individuals may show less variability in their behavioral responses. This study provides new information on the potential for behavioral syndromes in this species and highlights differences in the degree to which behavioral types (e.g., shy/bold) vary in their behavioral responses.     

Why Evolutionary Issues are Reviving Interest in Proximate Behavioral Mechanisms

Information about proximate behavioral mechanisms is requiredto answer a variety of important questions about the evolutionof behavioral and other traits. For instance, theoretical studiesof maternal effects indicate that the behavior of parents mayhave profound effects on the evolution of phenotypic traitsin their offspring, and that maternal effects may provide nongeneticpathways for the inheritance of both behavioral and nonbehavioraltraits. Similarly, the recent emphasis on genetic correlationsamong traits cautions that correlations among behavioral traitsmay have surprising effects on behavioral evolution, and providesfurther impetus for studies of the proximate bases of behavioraltrait syndromes. Finally, the literature on information acquisitionsuggests that the behavioral processes used in assessment mayaffect the evolution of behavioral and other traits. For instance,if information is costly to obtain, individuals may prefer familiarto unfamiliar situations. In a social context, a preferencefor familiar individuals could have a variety of effects onthe evolution of social and nonsocial behavior patterns. Theseand other examples suggest that interest in behavioral processeswill continue to grow during the next decade, and that proximateand ultimate approaches to behavioral problems will be moreclosely integrated than was true in the past.     

Individual differences in temperament and behavioral management practices for nonhuman primates

Effective behavioral management plans are tailored to unique behavioral patterns of each individual species. However, even within a species behavioral needs of individuals can vary. Factors such as age, sex, and temperament can affect behavioral needs of individuals. While some of these factors, such as age and sex, are taken into account, other factors, such as an individual's temperament, are rarely specifically provided for in behavioral management plans. However, temperament may affect how animals respond to socialization, positive reinforcement training and other forms of enrichment. This review will examine how individual differences in temperament might affect, or be affected by, behavioral management practices for captive primates. Measuring temperament may help us predict outcome of social introductions. It can also predict which animals may be difficult to train using traditional methods. Further, knowledge of temperament may be able to help identify individuals at risk for development of behavioral problems. Taken together, understanding individual differences in temperament of captive primates can help guide behavioral management decisions.     

On our best behavior: optimality models in human behavioral ecology

This paper discusses problems associated with the use of optimality models in human behavioral ecology. Optimality models are used in both human and non-human animal behavioral ecology to test hypotheses about the conditions generating and maintaining behavioral strategies in populations via natural selection. The way optimality models are currently used in behavioral ecology faces significant problems, which are exacerbated by employing the so-called ‘phenotypic gambit’: that is, the bet that the psychological and inheritance mechanisms responsible for behavioral strategies will be straightforward. I argue that each of several different possible ways we might interpret how optimality models are being used for humans face similar and additional problems. I suggest some ways in which human behavioral ecologists might adjust how they employ optimality models; in particular, I urge the abandonment of the phenotypic gambit in the human case.     

Behavioral planning in the prefrontal cortex

Recent studies have presented evidence that the prefrontal cortex plays a crucial role in every aspect of the cognitive processes necessary for behavioral planning: processing and integration of perceived or memorized information, associative learning, reward-based behavioral control, behavioral selection/decision-making and behavioral guidance. We propose that the creation of novel information is the means by which the prefrontal cortex operates to achieve executive control over behavioral planning. The prefrontal cortex is the site of operation of nodal points, where neural circuits integrate currently available or memorized information to generate the information that is necessary to perform an action. The prefrontal cortex also regulates the flow of information through multiple nodes to meet behavioral demands.     

Behavioral barcoding in the cloud: embracing data-intensive digital phenotyping in neuropharmacology

For decades, studying the behavioral effects of individual drugs and genetic mutations has been at the heart of efforts to understand and treat nervous system disorders. High-throughput technologies adapted from other disciplines (e.g., high-throughput chemical screening, genomics) are changing the scale of data acquisition in behavioral neuroscience. Massive behavioral datasets are beginning to emerge, particularly from zebrafish labs, where behavioral assays can be performed rapidly and reproducibly in 96-well, high-throughput format. Mining these datasets and making comparisons across different assays are major challenges for the field. Here, we review behavioral barcoding, a process by which complex behavioral assays are reduced to a string of numeric features, facilitating analysis and comparison within and across datasets.     

Behavioral management of recurrent headache: three decades of experience and empiricism

In the past three decades, behavioral interventions (chiefly relaxation, biofeedback, and stress-management) have become standard components of the armamentarium for management of migraine and tension-type headaches. Meta-analytic literature reviews of these behavioral interventions have consistently identified clinically significant reductions in recurrent headache. Across studies, behavioral interventions have yielded approximately 35–50% reduction in migraine and tension-type headache activity. Although we have only recently begun to directly compare standard drug and nondrug treatments for headache, the available evidence suggests that the level of headache improvement with behavioral interventions may rival those obtained with widely used pharmacologic therapies in representative patient samples. In recent years, some attempts have been made to increase the availability and cost effectiveness of behavioral interventions through alternative delivery formats and mass communications. Recent developments within diagnosis and classification are summarized, pointing out implications for behavioral researchers. Select future directions are discussed, which include impact of the triptans, cost and cost effectiveness, and integration of behavioral treatments into primary care settings, the place where the great majority of headache sufferers receive treatment.     

Analyzing gene expression data in mice with the Neuro Behavior Ontology

We have applied the Neuro Behavior Ontology (NBO), an ontology for the annotation of behavioral gene functions and behavioral phenotypes, to the annotation of more than 1,000 genes in the mouse that are known to play a role in behavior. These annotations can be explored by researchers interested in genes involved in particular behaviors and used computationally to provide insights into the behavioral phenotypes resulting from differences in gene expression. We developed the OntoFUNC tool and have applied it to enrichment analyses over the NBO to provide high-level behavioral interpretations of gene expression datasets. The resulting increase in the number of gene annotations facilitates the identification of behavioral or neurologic processes by assisting the formulation of hypotheses about the relationships between gene, processes, and phenotypic manifestations resulting from behavioral observations.     

Different strokes: Can managing behavioral types increase post-release success?

Re-introduction programs for endangered animals operate under the hope that protected habitats can sustain viable populations that rely little on humans. The goal of these programs is to supply animals with the resources and skills they need to succeed in the modern wild. However, predicting the set of skills necessary to respond to unpredictable selection events is difficult and efforts sometimes fail as animals respond inappropriately to environmental variation because they lack behavioral flexibility. Population resilience to environmental change may be enhanced if all members of a population do not exhibit the same response when selection pressures change. In many species individual animals express behavioral types that exhibit alternative responses to the same stimuli. Yet when animals are prepared for release to the wild, there is rarely consideration of consistent behavioral variation between individuals. Since experience influences both behavioral and physiological responses to varied stimuli and can shape the future behavioral type of captive animals, pre-release environmental enrichment may be successful in facilitating the expression of varied behavioral types in populations slated for release. This approach to environmental enrichment requires a departure from a ‘one size fits all’ strategy and may also involve exposure to increased challenge and competition. In addition, there is a need for empirical evidence to better understand the role of environmental enrichment and behavioral types on post-release success. The zoo environment provides an excellent arena for examining the development and expression of behavioral types and for taking a novel functional approach to environmental enrichment research that may prove to be very important to re-introduction efforts.     

A Proposed Test Battery and Constellations of Specific Behavioral Paradigms to Investigate the Behavioral Phenotypes of Transgenic and Knockout Mice

Behavioral phenotyping of transgenic and knockout mice requires rigorous, formal analyses. Well-characterized paradigms can be chosen from the established behavioral neuroscience literature. This review describes (1) a series of neurological and neuropsychological tests which are effectively used as a first screen for behavioral abnormalities in mutant mice, and (2) a series of specific behavioral paradigms, clustered by category. Included are multiple paradigms for each category, including learning and memory, feeding, analgesia, aggression, anxiety, depression, schizophrenia, and drug abuse models. Examples are given from the experiences of the authors, in applying these experimental designs to transgenic and knockout mice. Extensive references for each behavioral paradigm are provided, to allow new investigators to access the relevant literature on behavioral methodology.     

Differentiall behavioral and adrenocortical responses to stress among three macaque species

Behavioral and adrenocortical responses of rhesus (Macaca mulatta), bonnet (M. radiata), and crabeating (M. fascicularis) macaques were compared in their home cages, during exposure to novelty and during physical restraint. Both behavioral and adrenocortical responses differentiated species in each condition. In all conditions, post-test corticosteroid levels were highest for crabeaters and lowest for rhesus. Rhesus were the most active behaviorally, and bonnets were the most passive, while crabeaters exhibited the greatest signs of behavioral disturbance. Relationships between adrenocortical and behavioral responses varied between groups. Both adrenocortical and behavioral profiles were in accord with the behavior of these three species under more natural conditions. The role of psychophysiological responses in general behavioral dispositions toward the environment is discussed. It is concluded that behavioral dispositions, inclusive of psychophysiological responses, may vary qualitatively even among closely related primate species.     

Behavioral management of chimpanzees in biomedical research facilities: the state of the science

The current status of the behavioral management of chimpanzees housed in US research facilities is examined, and recent advances are described. Behavioral management includes the application of environmental enrichment, animal training, and environmental design for improving animal welfare. Authors surveyed the six major chimpanzee holding facilities and found that the vast majority of chimpanzees are housed socially, with access to the outdoors. The institutions currently invest in behavioral scientists, enrichment specialists, and, most recently, chimpanzee trainers to implement and study chimpanzee behavioral management. This review is based on the substantial scientific literature related to managing social behavior, identifying the behavioral effects of restricted socialization, evaluating various forms of enrichment, and describing positive reinforcement animal training. Authors outline recent accomplishments in behavioral management, summarize behavioral issues that have been evaluated, and identify issues for future consideration. It is proposed that the enhanced application of behavioral management techniques, including training, could significantly reduce chimpanzee stress that is generally associated with experimental manipulations, and could improve animal welfare and the quality of biomedical research. The next challenge is to implement effectively and thoroughly the approaches that have been shown to be beneficial.     

The genetic architecture of sucrose responsiveness in the honeybee (Apis mellifera L.)

One of the best examples of a natural behavioral syndrome is the pollen-hoarding syndrome in honeybees that ties together multiple behavioral phenotypes, ranging from foraging behavior to behavioral ontogeny and learning performance. A central behavioral factor is the bees' responsiveness to sucrose, measured as their proboscis extension reflex. This study examines the genetics of this trait in diploid worker and haploid male honeybees (drones) to learn more about the genetic architecture of the overall behavioral syndrome, using original strains selected for pollen-hoarding behavior. We show that a significant proportion of the phenotypic variability is determined by genotype in males and workers. Second, our data present overwhelming evidence for pleiotropic effects of previously identified quantitative trait loci for foraging behavior (pln-QTL) and epistatic interactions among them. Furthermore, we report on three genomic QTL scans (two reciprocal worker backcrosses and one drone hybrid population) derived from our selection strains. We present at least one significant and two putative new QTL directly affecting the sucrose response of honeybees. Thus, this study demonstrates the modular genetic architecture of behavioral syndromes in general, and elucidates the genetic architecture of the pollen-hoarding behavioral syndrome in particular. Understanding this behavioral syndrome is important for understanding the division of labor in social insects and social evolution itself.     

Stimulus-response relationships of insect olfaction: Correlations among neurophysiological and behavioral measures of response

The inter-relationships among parameters of odorant concentration, the responses evoked in single olfactory receptor neurons, the whole-animal behavioral threshold, and the intensity of the behavioral response are examined for insect olfaction from the perspective of a new phenomenological model of the perceived intensity of single odorants. Electrophysiological and behavioral data compiled from diverse insect studies are analyzed in detail to determine the utility of the model for interpreting these studies and for designing new studies. The analysis of electrophysiological data indicates that the response of olfactory receptor neurons can be expressed as a power function of the odorant concentration. The behavioral thresholds to sex pheromone, predicted by the model from direct calculations using phenomenological parameters, are in good agreement with thresholds measured by bioassay. It is also shown that the interpretation of behavioral bioassay data in terms of concepts introduced by the model provides more information about the behavioral response than provided by the currently popular probit analysis. In addition, aspects of the physiological significance of power functions are discussed, and new methods are presented for distinguishing background activity from activity evoked in single olfactory neurons by an odor at threshold levels.     

GABA and the behavioral effects of anxiolytic drugs

Much recent research has shown that benzodiazepine binding sites in the central nervous system are associated with GABA receptors. It is therefore possible that the pharmacological and therapeutic effects of benzodiazepines and drugs with similar profiles are mediated through GABAergic mechanisms. In this paper the evidence is considered for a possible involvement of GABA in the behavioral effects of anxiolytic drugs. There are a number of reports that the behavioral actions of anxiolytics can be antagonised by GABA antagonists such as bicuculline or picrotoxin but there are many contradictory findings and these drugs are difficult to use effectively in behavioral studies. In general, GABA agonists do not exert anxiolytic-like behavioral effects after systemic injection but intracerebral administration of muscimol has been shown to produce benzodiazepine-like actions. Although a number of questions remain unanswered, current evidence does not provide strong support for a role for GABA in the behavioral effects of anxiolytic drugs.     

Modification of cockroach behavior to environmental humidity change by dehydration (Dictyoptera: Blattidae)

Effects of dehydration on the behavioral response to humidity have been examined in the cockroach, Periplaneta americanaL. Under normal conditions cockroaches prefer lower humidity, but the preference is reversed by dehydration. Dehydrated cockroaches can distinguish smaller differences between two air streams compared with normal individuals. Cockroach behavioral responses to humidification include swing of antennae and locomotion. The period from onset of humidification to behavioral response decreases with increasing dehydration, indicating that the humidity threshold required for behavioral response decreases. Observed modulations of the behavioral response are discussed in relation to the contribution of the antennal hygroreceptors.     

Attentional enhancement via selection and pooling of early sensory responses in human visual cortex

The computational processes by which attention improves behavioral performance were characterized by measuring visual cortical activity with functional magnetic resonance imaging as humans performed a contrast-discrimination task with focal and distributed attention. Focal attention yielded robust improvements in behavioral performance accompanied by increases in cortical responses. Quantitative analysis revealed that if performance were limited only by the sensitivity of the measured sensory signals, the improvements in behavioral performance would have corresponded to an unrealistically large reduction in response variability. Instead, behavioral performance was well characterized by a pooling and selection process for which the largest sensory responses, those most strongly modulated by attention, dominated the perceptual decision. This characterization predicts that high-contrast distracters that evoke large responses should negatively impact behavioral performance. We tested and confirmed this prediction. We conclude that attention enhanced behavioral performance predominantly by enabling efficient selection of the behaviorally relevant sensory signals.