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bioRxiv2015

Behavioral flexibility and problem solving in an invasive bird

Behavioral flexibility is considered an important trait for adapting to environmental change, but it is unclear what it is, how it works, and whether it is a problem solving ability. I investigated behavioral flexibility and problem solving abilities experimentally in great-tailed grackles, an invasive species and thus a likely candidate for possessing behavioral flexibility. I found that grackles are behaviorally flexible and good problem solvers, they vary in behavioral flexibility across contexts, flexibility did not correlate with problem solving ability, and those that are more flexible did not necessarily use more learning strategies. It appears that behavioral flexibility can be an independent trait that varies across contexts. Maintaining such a high level of variation could be a mechanism underlying successful species invasions. These results highlight the need to investigate how individuals use behavior to react to changing environments.

Animal Behavior and Cognition↗

bioRxiv2015

Social context modulates idiosyncrasy of behaviour in the gregarious cockroach Blaberus discoidalis

Individuals are different, but they can work together to perform adaptive collective behaviours. Despite emerging evidence that individual variation strongly affects group performance, it is less clear to what extent individual variation is modulated by participation in collective behaviour. We examined light avoidance (negative phototaxis) in the gregarious cockroach Blaberus discoidalis, in both solitary and group contexts. Cockroaches in groups exhibit idiosyncratic light-avoidance performance that persists across days, with some individual cockroaches avoiding a light stimulus 75% of the time, and others avoiding the light just above chance (i.e. ~50% of the time). These individual differences are robust to group composition. Surprisingly, these differences do not persist when individuals are tested in isolation, but return when testing is once again done with groups. During the solo testing phase cockroaches exhibited individually consistent light-avoidance tendencies, but these differences were uncorrelated with performance in any group context. Therefore, we have observed not only that individual variation affects group-level performance, but also that whether or not a task is performed collectively can have a significant, predictable effect on how an individual behaves. That individual behavioural variation is modulated by whether a task is performed collectively has major implications for understanding variation in behaviours that are facultatively social, and it is essential that ethologists consider social context when evaluating individual behavioural differences.\n\nAbbreviations: DLP: digital light processing; MP: megapixels; ANOVA: analysis of variance, ICC: intraclass correlation coefficient, CI: confidence interval.

Animal Behavior and Cognition↗

bioRxiv2015

Hierarchical compression of C. elegans locomotion reveals phenotypic differences in the organisation of behaviour

Regularities in animal behaviour offer insight into the underlying organisational and functional principles of nervous systems and automated tracking provides the opportunity to extract features of behaviour directly from large-scale video data. Yet how to effectively analyse such behavioural data remains an open question. Here we explore whether a minimum description length principle can be exploited to identify meaningful behaviours and phenotypes. We apply a dictionary compression algorithm to behavioural sequences from the nematode worm Caenorhabditis elegans freely crawling on an agar plate both with and without food and during chemotaxis. We find that the motifs identified by the compression algorithm are rare but relevant for comparisons between worms in different environments, suggesting that hierarchical compression can be a useful step in behaviour analysis. We also use compressibility as a new quantitative phenotype and find that the behaviour of wild-isolated strains of C. elegans is more compressible than that of the laboratory strain N2 as well as the majority of mutant strains examined. Importantly, in distinction to more conventional phenotypes such as overall motor activity or aggregation behaviour, the increased compressibility of wild isolates is not explained by the loss of function of the gene npr-1, which suggests that erratic locomotion is a laboratory-derived trait with a novel genetic basis. Because hierarchical compression can be applied to any sequence, we anticipate that compressibility can offer insight into the organisation of behaviour in other animals including humans.

Animal Behavior and Cognition↗

bioRxiv2015

Generalized Regressive Motion: a Visual Cue to Collision

Brains and sensory systems evolved to guide motion. Central to this task is controlling the approach to stationary obstacles and detecting moving organisms. Looming has been proposed as the main monocular visual cue for detecting the approach of other animals and avoiding collisions with stationary obstacles. Elegant neural mechanisms for looming detection have been found in the brain of insects and vertebrates. However, looming has not been analyzed in the context of collisions between two moving animals. We propose an alternative strategy, generalized regressive motion (GRM), which is consistent with recently observed behavior in fruit flies. Geometric analysis proves that GRM is a reliable cue to collision among conspecifics, whereas agent-based modeling suggests that GRM is a better cue than looming as a means to detect approach, prevent collisions and maintain mobility.

Animal Behavior and Cognition↗

bioRxiv2015

Shared generative rules of locomotor behavior in arthropods and vertebrates

The discovery of shared behavioral processes across phyla is an essential step in the establishment of a comparative study of behavior. We use immobility as an origin and reference for the measurement of locomotor behavior; speed, direction of walking and direction of facing as the three degrees of freedom shaping fly locomotor behavior; and cocaine as the parameter inducing a progressive transition in and out of immobility. In this way we expose and quantify the generative rules that shape part of fruit fly locomotor behavior, bringing about a gradual buildup of freedom during the transition from immobility to normal behavior and a precisely opposite narrowing down during the transition into immobility. During buildup the fly exhibits enhancement and then reduction to normal values of movement along each degree of freedom: first, body rotation in the horizontal plane, then path curvature and then speed of translation. Transition into immobility unfolds by narrowing down of the repertoire in the opposite sequential order, showing reciprocal relations during both buildup and narrowing down. The same generative rules apply to vertebrate locomotor behavior in a variety of contexts involving transition out and into immobility. Recent claims for deep homology between the arthropod central complex and the vertebrate basal ganglia provide an opportunity to examine whether the generative rules we discovered also share common descent. Neurochemical processes mediating the buildup of locomotor behavior in vertebrates could guide the search for equivalent processes in arthropods. The measurement methodology we use prompts the discovery of candidate behavioral homologies.\n\nSignificance StatementDo flies and mice share the same behavior? By defining immobility as an intrinsic reference point for locomotor behavior we show that the rules that generate the transition from immobility to full blown normal behavior, and from full blown behavior to immobility are shared by fruit flies and mice. These rules constitute a much desired aim of evolutionary biology: the discovery of behavioral homologies across distant phyla. The methodology we use facilitates the discovery of cross-phyletic behavioral homologies, shedding light on the problem of the evolution of behavior.

Animal Behavior and Cognition↗

bioRxiv2015

A quantitative interaction between signal detection in attention and reward/aversion behavior

This study examines how processes such as reward/aversion and attention, which are often studied as independent processes, in fact interact at a systems level. We operationalize attention with a continuous performance task and variables from signal detection theory, and reward/aversion with a keypress task using variables from relative preference theory. We find that while the relationship between reward/aversion and attention is functionally invariant, a power law formulation akin to the Cobb-Douglas production function in economics provides the best model fit and theoretical explanation for the interaction. These results indicate that a decreasing signal-to-noise with signal detection results in higher loss aversion. Furthermore, the estimated exponents for the multiplicative power law suggest capacity constraints to processing for attention and reward/aversion. These results demonstrate a systemic interaction of attention and reward/aversion across subjects, with a quantitative schema raising the hypothesis that mechanistic inference may be possible at the level of behavior alone.

Animal Behavior and Cognition↗

bioRxiv2015

Drosophila learn efficient paths to a food source

Elucidating the genetic, and neuronal bases for learned behavior is a central problem in neuroscience. A leading system for neurogenetic discovery is the vinegar fly Drosophila melanogaster; fly memory research has identified genes and circuits that mediate aversive and appetitive learning. However, methods to study adaptive food-seeking behavior in this animal have lagged decades behind rodent feeding analysis, largely due to the challenges presented by their small scale. There is currently no method to dynamically control flies access to food. In rodents, protocols that use dynamic food delivery are a central element of experimental paradigms that date back to the influential work of Skinner. This method is still commonly used in the analysis of learning, memory, addiction, feeding, and many other subjects in experimental psychology. The difficulty of microscale food delivery means this is not a technique used in fly behavior. In the present manuscript we describe a microfluidic chip integrated with machine vision and automation to dynamically control defined liquid food presentations and sensory stimuli. Strikingly, repeated presentations of food at a fixed location produced improvements in path efficiency during food approach. This shows that improved path choice is a learned behavior. Active control of food availability using this microfluidic system is a valuable addition to the methods currently available for the analysis of learned feeding behavior in flies.

Animal Behavior and Cognition↗

bioRxiv2015

Proprioceptive feedback determines visuomotor gain in Drosophila

Multisensory integration is a prerequisite for effective locomotor control in most animals. Especially the impressive aerial performance of insects relies on rapid and precise integration of multiple sensory modalities that provide feedback on different time scales. In flies, continuous visual signalling from the compound eyes is fused with phasic proprioceptive feedback to ensure precise neural activation of wing steering muscles within narrow temporal phase bands of the stroke cycle. This phase-locked activation relies on mechanoreceptors distributed over wings and gyroscopic halteres. Here we investigate visual steering performance of tethered flying fruit flies with reduced haltere and wing feedback signalling. Using a flight simulator, we evaluated visual object fixation behaviour, optomotor altitude control, and saccadic escape reflexes. The behavioural assays show an antagonistic effect of wing and haltere signalling on visuomotor gain during flight. Compared to controls, suppression of haltere feedback attenuates while suppression of wing feedback enhances the animals wing steering range. Our results suggest that the generation of motor commands owing to visual perception is dynamically controlled by proprioception. We outline a potential physiological mechanism based on the biomechanical properties of wing steering muscles and sensory integration processes at the level of motoneurons. Collectively, the findings contribute to our general understanding how moving animals integrate sensory information with dynamically changing temporal structure.

Animal Behavior and Cognition↗

bioRxiv2016

The Computational Nature of Memory Modification

Retrieving a memory can modify its influence on subsequent behavior. Whether this phenomenon arises from modification of the contents of the memory trace or its accessibility is a matter of considerable debate. We develop a computational theory that incorporates both mechanisms. Modification of the contents of the memory trace occurs through classical associative learning, but which memory trace is accessed (and thus made eligible for modification) depends on a structure learning mechanism that discovers the units of association by segmenting the stream of experience into statistically distinct clusters (latent causes). New memories are formed when the structure learning mechanism infers that a new latent cause underlies current sensory observations. By the same token, old memories are modified when old and new sensory observations are inferred to have been generated by the same latent cause. We derive this framework from probabilistic principles, and present a computational implementation. Simulations demonstrate that our model can reproduce the major experimental findings from studies of memory modification in the Pavlovian conditioning literature, including dependence on the strength and age of memories, the interval between memory retrieval and extinction, and prediction errors following retrieval.

Animal Behavior and Cognition↗

bioRxiv2016

Search calls long duration puts the bat on the tympanate moth's radar. A new perspective on how Noctuoidea's auditory cells drive evasive manoeuvres

The auditory stimulation method used in experiments on moth A cell(s) is generally believed to be adequate to characterise the encoding of echolocation signals. The stimulation method hosts, though, several bias. Their compounded effects can explain a range of discrepancies between the reported electrophysiological recordings and significantly alter the current interpretation. To test the hypothesis that the bias may significantly alter our current understanding of the moths auditory transducer characteristics, papers using the same auditory stimulation method and reporting on either spiking threshold or spiking activity of the moths A cells were analysed. The consistency of the reported data was assessed. A range of corrections issued from best practices and theoretical background were applied to the data in an attempt to re-interpret the data. We found that it is not possible to apply a posteriori corrections to all data and bias. However the corrected data indicates that the A cells spiking may be (i) independent of the repetition rate, (ii) maximum when detecting the long and low intensity pulses of the bat in searching mode, and (iii) steadily reduce as the bat closes on the moth. These observations raise the possibility that a fixed action pattern drives the mothss erratic evasive manoeuvres until the final moment. In depth investigation of the potential bias also suggest that the auditory transducers response may be constant for a larger frequency range than thought so far, and provide clues to explain the negative taxis in response to the searching batss calls detection.

Animal Behavior and Cognition↗

bioRxiv2016

DAVID: An open-source platform for real-time emotional speech transformation. With 25 applications in the behavioral sciences

We present an open-source software platform that transforms the emotions expressed by speech signals using audio effects like pitch shifting, inflection, vibrato, and filtering. The emotional transformations can be applied to any audio file, but can also run in real-time (with less than 20-millisecond latency), using live input from a microphone. We anticipate that this tool will be useful for the study of emotions in psychology and neuroscience, because it enables a high level of control over the acoustical and emotional content of experimental stimuli in a variety of laboratory situations, including real-time social situations. We present here results of a series of validation experiments showing that transformed emotions are recognized at above-chance levels in the French, English, Swedish and Japanese languages, with a naturalness comparable to natural speech. Then, we provide a list of twenty-five experimental ideas applying this new tool to important topics in the behavioral sciences.

Animal Behavior and Cognition↗

bioRxiv2016

Singing above the chorus: cooperative Princess cichlid fish (Neolamprologus pulcher) has high pitch

Teleost fishes not only communicate with well-known visual cues, but also olfactory and acoustic signals. Communicating with sound has advantages, as signals propagate fast, omnidirectionally, around obstacles, and over long distances. Heterogeneous environments might favour multimodal communication, especially in socially complex species, as combination of modalities strengths helps overcome their individual limitations. Cichlid fishes are known to be vocal, but a recent report suggests that this is not the case for the socially complex Princess cichlid Neolamprologus pulcher from Lake Tanganyika. Here we further investigated acoustic communication in this species. Wild and captive N. pulcher produced high frequency sounds (mean: 12 kHz), when stimulated by mirror images. In laboratory experiments, N. pulcher produced distinct two-pulsed calls mostly, but not exclusively, associated with agonistic displays. Our results suggest that male N. pulcher produce more sounds at greater durations than females. Thus, we confirm that the Princess cichlid does not produce low frequency sounds, but does produce high frequency sounds, both in combination with and independent from visual displays, suggesting that sounds are not a by-product of displays. Further studies on the hearing abilities of N. pulcher are needed to clarify if the high-frequency sounds are used in intra-or inter-specific communication.

Animal Behavior and Cognition↗

bioRxiv2016

Detailed temporal structure of communication networks in groups of songbirds

Animals in groups often exchange calls, in patterns whose temporal structure may be influenced by contextual factors such as physical location and the social network structure of the group. We introduce a model-based analysis for temporal patterns of animal call timing, originally developed for networks of firing neurons. This has advantages over cross-correlation analysis in that it can correctly handle common-cause confounds and provides a generative model of call patterns with explicit parameters for the influences between individuals. It also has advantages over standard Markovian analysis in that it incorporates detailed temporal interactions which affect timing as well as sequencing of calls. Further, a fitted model can be used to generate novel synthetic call sequences. We apply the method to calls recorded from groups of domesticated zebra finch (Taenopyggia guttata) individuals. We find that the communication network in these groups has stable structure that persists from one day to the next, and that \"kernels\" reflecting the temporal range of influence have a characteristic structure for a calling individuals effect on itself, its partner, and on others in the group. We further find characteristic patterns of influences by call type as well as by individual.

Animal Behavior and Cognition↗

bioRxiv2016

Infection avoidance behaviour: female fruit flies adjust foraging effort in response to internal and external cues of viral infection

Infection avoidance behaviours are the first line of defence against pathogenic encounters. Behavioural plasticity in response to internal or external cues can therefore generate potentially significant heterogeneity in infection. We tested whether Drosophila melanogaster exhibits infection avoidance behaviour during foraging, and whether this behaviour is modified by prior exposure to Drosophila C Virus (DCV) and by the risk of DCV encounter. We examined two measures of infection avoidance: (1) the motivation to feed in the presence of an infection risk and (2) the preference to feed on a clean food source over a potentially infectious source. While we found no clear evidence for preference of clean food sources over potentially infectious ones, female flies were less motivated to feed when presented with a risk of encountering DCV, but only if they had been previously exposed to the virus. We discuss the relevance of behavioural plasticity during foraging for host fitness and pathogen spread.

Animal Behavior and Cognition↗

bioRxiv2016

Contributions of hippocampus and striatum to memory-guided behavior depend on past experience

The hippocampal and striatal memory systems operate independently and in parallel in supporting spatial and response learning, respectively, when animals are explicitly trained in one task. Here, we investigated whether this principle continues to hold when animals are concurrently trained in two types of tasks. Rats were trained on a plus maze in either a spatial navigation or a cue response task (individual training), while a third set of rats acquired both (concurrent training). Subsequently, the rats underwent either sham surgery or neurotoxic lesions of the hippocampus (HPC), medial dorsal striatum (DSM) or lateral dorsal striatum (DSL), followed by retention testing. Finally, rats in the individual training condition also acquired the novel other task. When rats learned one task, HPC and DSL selectively supported spatial navigation cue response, respectively. However, when rats learned both tasks, HPC and DSL additionally supported the behavior incongruent with the processing style of the corresponding memory system. DSM significantly contributed to performance regardless of task or training procedure. Experience with the cue response task facilitated subsequent spatial learning, while experience with spatial navigation delayed both simultaneous and subsequent response learning. These findings suggest that multiple principles govern the interactions among memory systems.\n\nSignificance StatementCurrently, we distinguish among several types of memories, each supported by a distinct neural circuit. The memory systems are thought to operate independently and in parallel. Here, we demonstrate that the hippocampus and the dorsal striatum memory systems indeed operate independently and in parallel when rats learn one type of task at a time, but interact co-operatively and in synergism when rats concurrently learn two types of tasks. Furthermore, new learning is modulated by past experiences. These results can be explained by a model in which independent and parallel information processing that occurs in the separate memory-related neural circuits is supplemented by information transfer between the memory systems at the level of the cortex.

Animal Behavior and Cognition↗

bioRxiv2016

Anxiolytic treatment impairs helping behavior in rats

Despite decades of research with humans, the biological mechanisms that motivate an individual to help others remain poorly understood. In order to investigate the roots of pro-sociality in mammals, we established the helping behavior test, a paradigm in which rats are faced with a conspecific trapped in a restrainer that can only be opened from the outside. Over the course of repeated test sessions, rats exposed to a trapped cagemate learn to open the door to the restrainer, thereby helping the trapped rat to escape (Ben-Ami Bartal et al., 2011). The discovery of this natural behavior provides a unique opportunity to probe the motivation of rodent helping behavior, leading to a deeper understanding of biological influences on human pro-sociality.\n\nTo determine if an affective response motivates door-opening, rats received midazolam, a benzodiazepine anxiolytic, and tested in the helping behavior test. Midazolam-treated rats showed less helping behavior than saline-treated rats or rats receiving no injection. Yet, midazolam-treated rats opened a restrainer containing chocolate, highlighting the socially specific effects of the anxiolytic. To determine if midazolam interferes with helping through a sympatholytic effect, the peripherally restricted beta-adrenergic receptor antagonist nadolol was administered; nadolol did not interfere with helping.\n\nThe corticosterone response of rats exposed to a trapped cagemate was measured and compared to the rats subsequent helping behavior. Rats with the greatest corticosterone responses showed the least helping behavior and those with the smallest responses showed the most consistent helping at the shortest latency. These results are discussed in terms of their implications for the interaction between stress and pro-social behavior.\n\nFinally, we observed that door-opening appeared to be reinforcing. A novel analytical tool was designed to interrogate the pattern of door-opening for signs that a rats behavior on one session influenced his behavior on the next session. Results suggest that helping a trapped rat has a greater motivational value than does chocolate.\n\nIn sum, this series of experiments clearly demonstrates the fundamental role of affect in motivating pro-social behavior in rodents and the need for a helper to resonate with the affect of a victim.

Animal Behavior and Cognition↗

bioRxiv2016

Neural mechanisms for reward-modulated vector learning and navigation: from social insects to embodied agents

Despite their small size, insect brains are able to produce robust and efficient navigation in complex environments. Specifically in social insects, such as ants and bees, these navigational capabilities are guided by orientation directing vectors generated by a process called path integration. During this process, they integrate compass and odometric cues to estimate their current location as a vector, called home vector for guiding them back home on a straight path. They further acquire and retrieve path integration-based vector memories anchored globally to the nest or visual landmarks. Although existing computational models reproduced similar behaviors, they largely neglected evidence for possible neural substrates underlying the generated behavior. Therefore, we present here a model of neural mechanisms in a modular closed-loop control - enabling vector navigation in embodied agents. The model consists of a path integration mechanism, reward-modulated global and local vector learning, random search, and action selection. The path integration mechanism integrates compass and odometric cues to compute a vectorial representation of the agents current location as neural activity patterns in circular arrays. A reward-modulated learning rule enables the acquisition of vector memories by associating the local food reward with the path integration state. A motor output is computed based on the combination of vector memories and random exploration. In sim-ulation, we show that the neural mechanisms enable robust homing and localization, even in the presence of external sensory noise. The proposed learning rules lead to goal-directed navigation and route formation performed under realistic conditions. This provides an explanation for, how view-based navigational strategies are guided by path integration. Consequently, we provide a novel approach for vector learning and navigation in a simulated embodied agent linking behavioral observations to their possible underlying neural substrates.\n\nAuthor SummaryDesert ants survive under harsh conditions by foraging for food in temperatures over 60{degrees} C. In this extreme environment, they cannot, like other ants, use pheromones to track their long-distance journeys back to their nests. Instead they apply a computation called path integration, which involves integrating skylight compass and odometric stimuli to estimate its current position. Path integration is not only used to return safely to their nests, but also helps in learning so-called vector memories. Such memories are sufficient to produce goal-directed and landmark-guided navigation in social insects. How can small insect brains generate such complex behaviors? Computational models are often useful for studying behavior and their underlying control mechanisms. Here we present a novel computational framework for the acquisition and expression of vector memories based on path integration. It consists of multiple neural networks and a reward-based learning rule, where vectors are represented by the activity patterns of circular arrays. Our model not only reproduces goal-directed navigation and route formation in a simulated agent, but also offers predictions about neural implementations. Taken together, we believe that it demonstrates the first complete model of vector-guided navigation linking observed behaviors of navigating social insects to their possible underlying neural mechanisms.

Animal Behavior and Cognition↗

bioRxiv2016

Persistent vulnerability to relapse despite complete extinction of cocaine craving

Craving often precedes relapse into cocaine addiction. This explains why considerable research effort is being expended to try to develop anti-craving strategies for relapse prevention. Recently, we discovered using the classic reinstatement model of cocaine craving that the reinstating or priming effect of cocaine can be extinguished with repeated priming in rats - a phenomenon dubbed extinction of cocaine priming. Here we sought to measure the potential beneficial effect of this novel extinction strategy on subsequent relapse (i.e., return to the pre-extinction pattern of cocaine self-administration once the drug is made again available after extinction). Overall and contrary to our initial hope, extensive and complete extinction of cocaine priming had no major impact on relapse. This lack of effect occurred despite evidence for post-extinction loss of neuronal responses to cocaine priming in brain regions critically involved in cocaine-induced reinstatement (i.e., the dorsomedial prefrontal cortex and the core of the nucleus accumbens). An effect of extinction of cocaine priming on relapse was only observed when cocaine was available for self-administration under more demanding conditions. However, this effect was modest and short-lived. Finally, we succeeded to trace the origin of our failure to prevent relapse to a persistent, extinction-resistant form of operant behavior that is not directly induced by cocaine. This extinction-resistant behavior is commonly reported, though generally ignored as causally irrelevant, in many other reinstatement studies. We propose that this behavior should become both a novel marker for long-term vulnerability to relapse and a novel target for preclinical development of potential relapse prevention interventions.

Animal Behavior and Cognition↗