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FUNCTIONAL MRI IN AWAKE DOGS PREDICTS SUITABILITY FOR ASSISTANCE WORK

The overall goal of this work was to measure the efficacy of fMRI for predicting whether a dog would be a successful service dog. The training and imaging were performed in 50 dogs entering advanced training at 17-21 months of age. FMRI responses were measured while each dog observed hand signals indicating either reward or no reward and given by both a familiar handler and a stranger. 49 dogs successfully completed fMRI training and scanning. Of these, 33 eventually completed service training and were matched with a person, while 10 were released for behavioral reasons. Using anatomically defined regions-of-interest in the ventral caudate, amygdala, and visual cortex, we developed a classifier based on the dogs' outcomes. We found that responses in the stranger condition were sufficient to develop an accurate brain-based classifier. On all data, the classifier had a positive predictive value of 96% with 10% false positives. The area under the receiver operating characteristic curve was 0.90 (0.79 with 4-fold cross-validation, P=0.02), indicating a significant diagnostic capability. Within the stranger condition, the differential response to [reward - no reward] in ventral caudate was positively correlated with a successful outcome, while the differential response in the amygdala was negatively correlated to outcome. These results show that successful service dogs transfer knowledge to strangers as indexed by ventral caudate activity without excessive arousal as measured in the amygdala.

Animal Behavior and Cognition

Loss of the habenula neuromodulator Kisspeptin1 disrupts learning

Learning how to actively avoid a predictable aversive stimulus involves two steps: recognizing the cue that predicts upcoming punishment, and learning a behavioral response that will lead to avoidance. In zebrafish, ventral habenula (vHb) neurons have been proposed to participate in both steps by encoding the expected aversiveness of a stimulus. vHb neurons increase their firing rate as expectation of punishment grows, but reduce their activity as avoidance learning occurs. How the change in vHb activity occurs is not known. Here, we ask whether the neuromodulator kisspeptin1, which is expressed in the ventral habenula, could be involved. Kiss1 mutants were generated with Cas9 using guide RNAs targeted to the signal sequence. Mutants, which have a stop codon upstream of the kisspeptin1 peptide, have a deficiency in learning to avoid a shock that is predicted by light. Electrophysiology indicates that kisspeptin1 has a concentration-dependent effect on vHb neurons: depolarizing at low concentrations and hyperpolarizing at high concentrations. These data suggest that as the fish learns to cope with a threat, kisspeptin1 may differentially modulate vHb neurons. This implies that learning a behavioral strategy to overcome a stressor is accompanied by physiological change in habenula neurons.\n\nSignificance statementLearning to deal with adversity can positively affect ones ability to cope with challenges in the immediate future. Control thus causes short-term change in the brain. Here, we show that the neuromodulator kisspeptin1 is required to learn to avoid a punishment. Expression and electrophysiological recordings suggest that this molecule functions by controlling the ventral habenula, a region of the brain that mediates fear by regulating serotonin release. Kisspeptin1 may be a potential player in resilience developed as a result of control, extending previous findings that it can reduce fear.

animal behavior and cognition

Putting bandits into context: How function learning supports decision making

We introduce the contextual multi-armed bandit task as a framework to investigate learning and decision making in uncertain environments. In this novel paradigm, participants repeatedly choose between multiple options in order to maximise their rewards. The options are described by a number of contextual features which are predictive of the rewards through initially unknown functions. From their experience with choosing options and observing the consequences of their decisions, participants can learn about the functional relation between contexts and rewards and improve their decision strategy over time. In three experiments, we explore participants behaviour in such learning environments. We predict participants behaviour by context-blind (mean-tracking, Kalman filter) and contextual (Gaussian process and linear regression) learning approaches combined with different choice strategies. Participants are mostly able to learn about the context-reward functions and their behaviour is best described by a Gaussian process learning strategy which generalizes previous experience to similar instances. In a relatively simple task with binary features, they seem to combine this learning with a \"probability of improvement\" decision strategy which focuses on alternatives that are expected to lead to an improvement upon a current favourite option. In a task with continuous features that are linearly related to the rewards, participants seem to more explicitly balance exploration and exploitation. Finally, in a difficult learning environment where the relation between features and rewards is non-linear, some participants are again well-described by a Gaussian process learning strategy, whereas others revert to context-blind strategies.

animal behavior and cognition

Modelling avoidance in pathologically anxious humans using reinforcement-learning

Serious and debilitating symptoms of anxiety are the most common mental health problem worldwide, accounting for around 5% of all adult years lived with disability in the developed world. Avoidance behaviour -avoiding social situations for fear of embarrassment, for instance-is a core feature of such anxiety. However, as for many other psychiatric symptoms, the biological mechanisms underlying avoidance remain unclear. Reinforcement-learning models provide formal and testable characterizations of the mechanisms of decision-making; here, we examine avoidance in these terms. One hundred and one healthy and pathologically anxious individuals completed an approach-avoidance go/no-go task under stress induced by threat of unpredictable shock. We show an increased reliance in the anxious group on a parameter of our reinforcement-learning model that characterizes a prepotent (Pavlovian) bias to withhold responding in the face of negative outcomes. This was particularly the case when the anxious individuals were under stress. This formal description of avoidance within the reinforcement-learning framework provides a new means of linking clinical symptoms with biophysically plausible models of neural circuitry and, as such, takes us closer to a mechanistic understanding of pathological anxiety.

animal behavior and cognition

The Drosophila pheromone Z4-11Al is encoded together with habitat olfactory cues and mediates species-specific communication

Mate recognition in animals evolves during niche adaptation and involves habitat and social olfactory signals. Drosophila melanogaster is attracted to fermenting fruit for feeding and egg-laying. We show that, in addition, female flies release a pheromone (Z)4-undecenal (Z4-11Al), that elicits flight attraction in both sexes. The biosynthetic precursor of Z4-11Al is the cuticular hydrocarbon (Z,Z)-7,11-heptacosadiene (7,11-HD), which is known to afford reproductive isolation between D. melanogaster and D. simulans. A pair of alternatively spliced receptors, Or69aB and Or69aA, is tuned to Z4-11Al and to food olfactory cues, respectively. These receptors are co-expressed in the same olfactory sensory neurons, and feed into a neural circuit mediating species-specific, long-range communication: the close relative D. simulans does not respond. That Or69aA and Or69aB have adopted dual olfactory traits highlights the interplay of habitat and social signals in mate finding. These olfactory receptor genes afford a collaboration between natural and sexual selection, which has the potential to drive phylogenetic divergence.

animal behavior and cognition

Cultural transmission and biological markets

Active cultural transmission of fitness-enhancing behavior can be seen as a costly strategy, one whose evolutionary stability poses a Darwinian puzzle. In this article, we offer a biological market model of cultural transmission that substitutes or complements existing kin-selection based theories for the evolution of cultural capacities. We explicitly formulate how a biological market can account for the evolution of deference and prestige-related phenomena, as well as how it can affect the dynamics of cumulative culture. We show that, under certain conditions, teaching evolves even when innovations are not sufficiently opaque and can be acquired by emulators via inadvertent transmission. Furthermore, teaching in a biological market is a precondition for enhanced individual learning abilities.

animal behavior and cognition

Unexpected diversity in socially synchronized rhythms of shorebirds

The behavioural rhythms of organisms are thought to be under strong selection, influenced by the rhythmicity of the environment1-4. Such behavioural rhythms are well studied in isolated individuals under laboratory conditions1,5, but free-living individuals have to temporally synchronize their activities with those of others, including potential mates, competitors, prey and predators6-10. Individuals can temporally segregate their daily activities (e.g. prey avoiding predators, subordinates avoiding dominants) or synchronize their activities (e.g. group foraging, communal defence, pairs reproducing or caring for offspring)6-9,11. The behavioural rhythms that emerge from such social synchronization and the underlying evolutionary and ecological drivers that shape them remain poorly understood5-7,9. Here, we address this in the context of biparental care, a particularly sensitive phase of social synchronization12 where pair members potentially compromise their individual rhythms. Using data from 729 nests of 91 populations of 32 biparentally-incubating shorebird species, where parents synchronize to achieve continuous coverage of developing eggs, we report remarkable within- and between-species diversity in incubation rhythms. Between species, the median length of one parents incubation bout varied from 1 - 19 hours, while period length-the time in which a parents probability to incubate cycles once between its highest and lowest value - varied from 6 - 43 hours. The length of incubation bouts was unrelated to variables reflecting energetic demands, but species relying on crypsis (the ability to avoid detection by other animals) had longer incubation bouts than those that are readily visible or actively protect their nest against predators. Rhythms entrainable to the 24-h light-dark cycle were less prevalent at high latitudes and absent in 18 species. Our results indicate that even under similar environmental conditions and despite 24-h environmental cues, social synchronization can generate far more diverse behavioural rhythms than expected from studies of individuals in captivity5-7,9. The risk of predation, not the risk of starvation, may be a key factor underlying the diversity in these rhythms.

animal behavior and cognition

Social ecology of a woodland songbird community: from individual movements to the emergence of population social structure

Social structure can have profound evolutionary and ecological implications for animal populations. Structure can arise and be maintained via social preferences or be indirectly shaped by habitat structure. Understanding how social structure emerges is important for understanding the potential links between social structure and evolutionary and ecological processes. Here, we study a large community of wild birds fitted with uniquely-coded passive integrated transponder (PIT) tags and recorded on a grid of automated feeders fitted with radio frequency identification (RFID) antennae. We show that both large-scale and fine-scale network communities are consistent across years in this population, despite high generational turn-over. Studying the process that generates community structure, here the movement of individual birds across the woodland, suggests an important role of habitat geometry in shaping population-level social community structure. Our study highlights how relatively simple factors can produce apparent emergent social structure at the population scale, which has widespread implications for understanding eco-evolutionary dynamics.

animal behavior and cognition

Inducible nitric oxide synthase (NOS2) knockout mice as a model of trichotillomania

Trichotillomania (TTM) is an impulse control disorder characterized by repetitive hair pulling/trimming. Barbering behavior (BB) has been observed in laboratory animals and proposed as TTM model. The neurobiological basis of TTM is not clear, but it seems to involve striatal hyperactivity parallel to hypoactivation of prefrontal cortex. In this study we observed that knockout mice to the inducible isoform of nitric oxide synthase (NOS2) exhibit exacerbated BB following the 4th week of age, as well as increased repetitive movements compared to wild-type mice (WT). These behaviors are associated to decreased levels of NMDA receptor subunit (NR1) in prefrontal cortex, while an increase was observed in striatum of NOS2KO compared to WT. Striatal neurons from NOS2KO also exhibited increased number of branches compared to WT. The repeated treatment with clomipramine, a clinically approved drug to treat TTM in humans, or memantine, an antagonist of NMDA receptors, as well as partial rescue of NOS2 expression in haploinsufficient animals, attenuated the expression of BB. The silencing of NOS2 expression reduced the MAP2 (microtubule-associated protein 2) levels in activity-induced differentiated PC12 cells. Our data led us to propose that NOS2 regulates the neuronal maturation of the inhibitory afferent pathways to striatum during neurodevelopment, and such inadequate inhibition of striatal motor programs might be associated to the observed phenotype.

animal behavior and cognition

Neuromodulatory circuit effects on Drosophila feeding behaviour and metabolism

Animals have evolved to maintain homeostasis in a changing external environment by adapting their internal metabolism and feeding behaviour. Metabolism and behaviour are coordinated by neuromodulation; a number of the implicated neuromodulatory systems are homologous between mammals and the vinegar fly, an important neurogenetic model. We investigated whether silencing fly neuromodulatory networks would elicit coordinated changes in feeding, behavioural activity and metabolism. We employed transgenic lines that allowed us to inhibit broad cellular sets of the dopaminergic, serotonergic, octopaminergic, tyraminergic and neuropeptide F systems. The genetically-manipulated animals were assessed for changes in their overt behavioural responses and metabolism by monitoring eleven parameters: activity; climbing ability; individual feeding; group feeding; food discovery; both fed and starved respiration; fed and starved lipid content; and fed/starved body weight. The results from these 55 experiments indicate that individual neuromodulatory system effects on feeding behaviour, motor activity and metabolism are dissociated.

animal behavior and cognition

Ultraviolet and yellow reflectance but not fluorescence is important for visual discrimination of conspecifics by Heliconius erato

Toxic Heliconius butterflies have yellow hindwing bars that - unlike their closest relatives - reflect ultraviolet (UV) and long wavelength light, and also fluoresce. The pigment in the yellow scales is 3-hydroxy-DL-kynurenine (3-OHK), found also in the hair and scales of a variety of animals. In other butterflies including pierids, which similarly display wing colors that vary in both the UV and the human-visible range, behavioral experiments have indicated that only the UV component is most relevant to mate choice. Whether in Heliconius butterflies it is the UV, the human-visible yellow, and/or the fluorescent component of yellow wing coloration that is relevant to mate choice is unknown. In field studies with butterfly paper models we show that both UV and 3-OHK yellow act as signals for H. erato but attack rates by birds do not differ significantly between the models. Furthermore, measurement of the quantum yield and reflectance spectra of 3-OHK indicates that fluorescence does not contribute to the visual signal under broad-spectrum illumination. Our results suggest that the use of 3-OHK pigmentation instead of ancestral yellow was driven by sexual selection rather than predation.\n\nSummary statementHeliconius butterflies use a co-opted yellow pigment for communication, while predators are fooled by non-Heliconius mimics using ancestral yellow pigments.

animal behavior and cognition

Confirmation bias in human reinforcement learning: evidence from counterfactual feedback processing

Previous studies suggest that factual learning, that is learning from obtained outcomes, is biased, such that participants preferentially take into account positive, as compared to negative, prediction errors. However, whether or not the prediction error valence also affects counterfactual learning, that is, learning from forgone outcomes, is unknown. To address this question, we analysed the performance of two cohorts of participants on reinforcement learning tasks using a computational model that was adapted to test if prediction error valance influences learning. Concerning factual learning, we replicated previous findings of a valence-induced bias, whereby participants learned preferentially from positive, relative to negative, prediction errors. In contrast, for counterfactual learning, we found the opposite valence-induced bias: negative prediction errors were preferentially taken into account relative to positive ones. When considering valence-induced bias in the context of both factual and counterfactual learning, it appears that people tend to preferentially take into account information that confirms their current choice. By documenting these valence-induced learning biases, our findings demonstrate the presence of a confirmation bias in human reinforcement learning.

animal behavior and cognition

A new law of human perception

Perception is a subjective experience that depends on the expectations and beliefs of an observer1. Psychophysical measures provide an objective yet indirect characterization of this experience by describing the dependency between the physical properties of a stimulus and the corresponding perceptually guided behavior2. Two fundamental psychophysical measures characterize an observers perception of a stimulus: how well the observer can discriminate the stimulus from similar ones (discrimination threshold) and how strongly the observers perceived stimulus value deviates from the true stimulus value (perceptual bias). It has long been thought that these two perceptual characteristics are independent3. Here we demonstrate that discrimination threshold and perceptual bias show a surprisingly simple mathematical relation. The relation, which we derived from assumptions of optimal sensory encoding and decoding4, is well supported by a wide range of reported psychophysical data5-16 including perceptual changes induced by spatial17,18 and temporal19-23 context, and attention24. The large empirical support suggests that the proposed relation represents a new law of human perception. Our results imply that universal rules govern the computational processes underlying human perception.

animal behavior and cognition

Localizing hidden regularities with known temporal structure in the EEG evoked response data

In this paper we describe a novel data driven spatial filtering technique that can be applied to the ERP analysis in order to find statistically significant hidden differential activations in the EEG data. The technique is based on the known morphological characteristics of the response. Underlying optimization problem is formulated as a generalized Rayleigh quotient maximization problem. We supply our tech-nique with a relevant randomization-based statistical test to assess the significance of the discovered phenomenon. Furthermore, we describe an application of the proposed method to the EEG data acquired in the study devoted to the analysis of the auditory neuroplasticity. We show how the mismatch negativity component, a tiny and short-lasting negative response that hallmarks the novel stimuli activating primary error-detection mechanisms, can be detected after filtration.

animal behavior and cognition

ISCA1 and CRY4: An improbable proposition

This manuscript was submitted to Nature Materials on December 15th 2015.\n\nIn their recent manuscript Xie and colleagues argue that the pigeon ISCA1/CRY4 complex acts as a magnetic protein biocompass having unambiguously proved that these two proteins interact forming a complex with unique biophysical features (1). We do not think the evidence presented in the manuscript supports this conclusion. Firstly, the authors provide no data (such as a reciprocal co-immunoprecipitation from retinal tissue) that demonstrates that ISCA1 and CRY4 interact in vivo, instead the conclusions are based primarily on overexpression in E.coli and in vitro reconstitution experiments. Secondly, their experiments have not employed the correct full length version of CRY4. The CRY4 protein expressed by Xie and colleagues was only 497 amino acids in length. We extracted mRNA from the pigeon retina (Invitrogen, 610.11), generated cDNA (Clontech, 121311), and performed rap ...

animal behavior and cognition

A tutorial on Gaussian process regression with a focus on exploration-exploitation scenarios

This tutorial introduces the reader to Gaussian process regression as an expressive tool to model, actively explore and exploit unknown functions. Gaussian process regression is a powerful, non-parametric Bayesian approach towards regression problems that can be utilized in exploration and exploitation scenarios. This tutorial aims to provide an accessible introduction to these techniques. We will introduce Gaussian processes which generate distributions over functions used for Bayesian non-parametric regression, and demonstrate their use in applications and didactic examples including simple regression problems, a demonstration of kernel-encoded prior assumptions and compositions, a pure exploration scenario within an optimal design framework, and a bandit-like exploration-exploitation scenario where the goal is to recommend movies. Beyond that, we describe a situation modelling risk-averse exploration in which an additional constraint (not to sample below a certain threshold) needs to be accounted for. Lastly, we summarize recent psychological experiments utilizing Gaussian processes. Software and literature pointers are also provided.

animal behavior and cognition

Looking at my own Face: Visual Processing Strategies in Physical Self-representation

We live in an age of selfies. Yet, how we look at our own faces has seldom been systematically investigated. In this study we test if visual processing of self-faces is different from other faces, using psychophysics and eye-tracking. Specifically, the association between the psychophysical properties of self-face representation and visual processing strategies involved in self-face recognition was tested. Thirty-three adults performed a self-face recognition task from a series of self-other face morphs with simultaneous eye-tracking. Participants were found to look at lower part of the face for longer duration for self-face compared to other-face. Participants with a reduced overlap between self and other face representations, as indexed by a steeper slope of the psychometric response curve for self-face recognition, spent a greater proportion of time looking at the upper regions of faces identified as self. Additionally, the association of autism-related traits with self-face processing metrics was tested, since autism has previously been associated with atypical self-processing, particularly in the psychological domain. Autistic traits were associated with reduced looking time to both self and other faces. However, no self-face specific association was noted with autistic traits, suggesting that autism-related features may be related to self-processing in a domain specific manner.

animal behavior and cognition

Familiarity with companions aids recovery from fear inzebrafish

Interaction with social partners during or after a stressful episode aids recovery in humans and other mammals. We asked if a comparable phenomenon exists in zebrafish (Danio rerio) that live in shoals in the wild. In the first experiment, we observed that most quantifiable parameters of swimming behavior were similar when zerbafish swam alone or with companions. However, after exposure to an alarm substance (Schreckstoff), individuals recovering alone continued to display behaviors associated with fear after removal of the stimulus, while those recovering with companions did not. In the next two experiments, we examined the role of familiarity of companions. Subjects spent more time in the vicinity of familiar companions in a two-choice assay. While both familiar and unfamiliar companions reduced behavioral signs of distress, familiar companions additionally modulated cortisol and endogenous isotocin in subjects. Shortly after being united with familiar companions, isotocin spiked followed by a dampening of circulating cortisol levels. These results suggest that zebrafish experience fear attenuation in the presence of others and familiar companions are more effective at buffering the stress associated with escaping predation. Changes in behavior, circulating cortisol and isotocin levels due to social partners are reminiscent of changes due to amelioration of fear in some mammalian species in the presence of companions. The two phenomena may be related.

animal behavior and cognition