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bioRxiv2018

Transcriptional variation and divergence of host-finding behaviour in Steinernema carpocapsae infective juveniles

Steinernema carpocapsae is an entomopathogenic nematode that employs nictation and jumping behaviours to find host insects. We aimed to investigate the transcriptional basis of variant host-finding behaviours in the infective juvenile (IJ) stage of three S. carpocapsae strains (ALL, Breton and UK1). RNA-seq analysis revealed that whilst up to 28% of the S. carpocapsae transcriptome was differentially expressed (P<0.0001) between strains, remarkably few of the most highly differentially expressed genes (>2 log2 fold change, P<0.0001) were from neuronal gene families. S. carpocapsae Breton displays increased chemotaxis toward the laboratory host Galleria mellonella, relative to the other strains. This correlates with the up-regulation of four srsx chemosensory GPCR genes, and a sodium transporter gene, asic-2, relative to both ALL and UK1 strains. The UK1 strain exhibits a decreased nictation phenotype relative to ALL and Breton strains, which correlates with co-ordinate up-regulation of neuropeptide like protein 36 (nlp-36), and down-regulation of an srt family GPCR gene, and a distinct asic-2-like sodium channel paralogue. To further investigate the link between transcriptional regulation and behavioural variation, we sequenced microRNAs across IJs of each strain. We have identified 283 high confidence microRNA genes, yielding 321 isomiR variants in S. carpocapsae, and find that up to 36% of microRNAs are differentially expressed (P<0.0001) between strains. Many of the most highly differentially expressed microRNAs (>2 log2 fold, P<0.0001) are predicted to regulate a variety of neuronal genes that may contribute to variant host-finding behaviours. We have also found evidence for differential gene isoform usage between strains, which alters predicted microRNA interactions, and could contribute to the diversification of behaviour. These data provide deeper insight to the transcriptional landscape of behavioural variation in S. carpocapsae, underpinning efforts to functionally dissect the parasite host-finding apparatus.\n\nAuthor summarySteinernema carpocapsae is a lethal parasite of insects. In order to find and invade a host insect, the S. carpocapsae infective juvenile will typically stand upright, waving its anterior in the air as it searches for host-specific cues. When the infective juvenile senses insect volatile compounds and movement (both signals are required), it will attempt to jump towards the source of those stimuli. Whilst the jumping behaviour is unique to Steinernema species nematodes, nictation is a host-finding behaviour shared with other important parasites of medical and veterinary importance. We have found that different strains of S. carpocpsae use modified host-finding strategies, and that these behavioural differences correlate with gene expression patterns, identifying genes that may be crucial in regulating aspects of host-finding. We also assessed the complement of microRNAs, which are small non-coding RNAs that regulate target gene expression. We found a surprising difference in the abundance of shared microRNAs between strains of S. carpocapsae; these differences also reveal expression differences that correlate with behavioural variation. Predicted microRNA target genes suggest that microRNA variation could significantly influence the behaviour of nematodes. Broadly, this study provides insight to the relationship between gene expression and behaviour, paving the way for detailed studies on gene function.

animal behavior and cognition↗

bioRxiv2018

Ontogeny of familiarity with foraging landscape and foraging abilities in the tropical social wasp Ropalidia marginata

Possessing spatial familiarity with their foraging landscape may enable animals to reduce foraging effort without compromising on foraging benefits. For animals inhabiting feature-rich landscapes, spatial familiarity can increase with increasing age/experience. To check whether this holds for individually foraging tropical social wasp Ropalidia marginata, we recorded the number and duration of all foraging trips, the identity of the materials brought to the nest (building material, water or food) and the directions of outbound and inbound flights (respective to their nests) of known-age foragers from three natural colonies, each for three consecutive days. The average trip duration and time spent daily in foraging increased rapidly until about first four weeks of their life, during which they rarely brought food to their nest, although many of them brought building material and water. Thereafter, their average as well as per day duration of foraging trip started decreasing gradually. Nevertheless, their foraging efficiency and success for food kept on increasing monotonically with age. These results suggest that older wasps were more efficient in foraging despite spending less time doing so. With increasing age, wasps developed individual preferences for the direction of their outbound flights, increased directionality of their inbound trips as well as the angular difference between their outbound and subsequent inbound flights, indicating development of spatial memory. We conclude that wasps acquire familiarity with their foraging landscape in their initial foraging phase and gradually develop robust memory for rewarding sites and routes to those sites, which enables them to increase their foraging capabilities.\n\nSUMMARY STATEMENTContrary to insects inhabiting less-featured landscapes, tropical social wasps invest weeks to get familiar with foraging landscapes during their early foraging lives. This eventually enables them to increase foraging gain with reduced effort.

animal behavior and cognition↗

bioRxiv2018

The Educage: an automated platform for studying auditory perceptual learning in mice

Auditory perceptual learning of pure tones causes tonotopic map expansion in the primary auditory cortex (A1), but the function this plasticity sub-serves is unclear. We developed an automated training platform called the Educage, which was used to train mice on a go/no-go auditory discrimination task to their perceptual limits, for difficult discriminations among pure tones or natural sounds. Spiking responses of excitatory and inhibitory L2/3 neurons in mouse A1 revealed learning-induced overrepresentation of the learned frequencies, in accordance with previous literature. Using a novel computational model to study auditory tuning curves we show that overrepresentation does not necessarily improve discrimination performance of the network to the learned tones. In contrast, perceptual learning of natural sounds induced sparsening and decorrelation of the neural response, and consequently improving discrimination of these complex sounds. The signature of plasticity in A1 highlights its central role in coding natural sounds as compared to pure tones.

animal behavior and cognition↗

bioRxiv2018

Small differences in learning speed for different food qualities can drive efficient collective foraging in ant colonies

Social insects frequently make important collective decisions, such as selecting the best food sources. Many collective decisions are achieved via communication, for example by differential recruitment depending on resource quality. However, even species without recruitment can respond to a changing environment on collective level by tracking food source quality.\n\nWe hypothesised that an apparent collective decision to focus on the highest quality food source can be explained by differential learning of food qualities. Ants may learn the location of higher quality food faster, with most ants finally congregating at the best food source.\n\nTo test the effect of reward quality and motivation on learning in Lasius niger, we trained individual ants to find a reward of various sucrose molarities on one arm of a T-maze in spring and in autumn after one or four days of starvation.\n\nAs hypothesised, ants learned fastest in spring and lowest in autumn, with reduced starvation leading to slower learning. Surprisingly, the effect of food quality and motivation on the learning speed of individuals which persisted in visiting the feeders was small. However, persistence rates varied dramatically: All ants in spring made all (6) return visits to all food qualities, in contrast to 33% of ants in autumn under low starvation.\n\nFitting the empirical findings into an agent-based model revealed that even a tendency of ants to memorise routes to high quality food sources faster can result in ecologically sensible colony-level behaviour. Low motivation colonies are also choosier, due to increasing sensitivity to food quality.\n\nSignificance statementCollective decisions of insects are often achieved via communication and/or other interactions between individuals. However, animals can also make collective decisions in the absence of communication.\n\nWe show that foraging motivation and food quality can affect both route memory and the likelihood to return to the food source and thus mediate selective food exploitation. An agent-based model, implemented with our empirical findings, demonstrates that, at the collective level, even small differences in learning lead to ecologically sensible behaviour: mildly starved colonies are selective for high quality food while highly starved colonies exploit all food sources equally.\n\nWe therefore suggest that non-interactive factors such as individual learning and the foraging motivation of a colony can mediate or even drive group level behaviour. Instead of accounting collective behaviour exclusively to social interactions, possible contributing individual processes should also be considered.

animal behavior and cognition↗

bioRxiv2018

Chimpanzees but not orangutans display aversive reactions toward their partner receiving a superior reward

Fairness judgment is a fundamental aspect of human cooperation. By carefully balancing the payoffs and efforts with cooperating partner (s) we could either avoid or punish cheaters and stably maintain cooperation. Recent studies investigating the origin of this fairness sentiment have demonstrated that this psychological trait is not unique to humans, but also can be observed in other group-living primates, such as chimpanzees and capuchins, suggesting a convergent evolution of a sense of fairness, with cooperative social life being the selective pressure for it. The current study was designed to test this hypothesis by directly comparing the response to the outcome inequity in two of our closest living relatives, chimpanzees and orangutans, having different social systems, i.e. solitary and patrilocal multi-male multi-female groups. Unlike other inequity experiments, we used a prosocial choice apparatus with different reward distributions (advantageous / disadvantageous) to give subjects an active role of not-sharing foods if they considered it unfair. In addition to the choice, we also recorded the behavioral responses of the apes to the inequity. Throughout the experiments aversive emotional responses toward the disadvantageous inequity were only found in chimpanzees, but not in orangutans, supporting the convergent (or domain-specific) evolution of a sense of fairness. However, this aversion to the inequity did not lead the chimpanzees to actually make selfish choices, indirectly supporting the previous findings that chimpanzees employ a partner choice strategy rather than a punishment for fair cooperation. We also found that hierarchy seems to play an important role in the expression of aversion to inequity and prosocial tendency in chimpanzees.

animal behavior and cognition↗

bioRxiv2018

Immediate early gene activation throughout the brain is associated with dynamic changes in social context

Social competence is dependent on successful processing of social context information. The social opportunity paradigm is a methodology in which dynamic shifts in social context are induced through removal of the alpha male in a dominance hierarchy, leading to rapid ascent in the hierarchy of the beta male and of other subordinate males in the social group. In the current study, we use the social opportunity paradigm to determine what brain regions respond to this dynamic change in social context, allowing an individual to recognize the absence of the alpha male and subsequently perform status-appropriate social behaviors. Replicating our previous work, we show that following removal of the alpha male, beta males rapidly ascend the social hierarchy and attain dominant status by increasing aggression towards more subordinate individuals. Analysis of patterns of Fos immunoreactivity throughout the brain indicates that in individuals undergoing social ascent, there is increased activity in regions of the social behavior network, as well as the infralimbic and prelimbic regions of the prefrontal cortex and areas of the hippocampus. Our findings demonstrate that male mice are able to respond to changes in social context and provide insight into the how the brain processes these complex behavioral changes.

animal behavior and cognition↗

bioRxiv2018

Behavioral phenotyping of an improved mouse model of Phelan-McDermid Syndrome with a complete deletion of the Shank3 gene

AbstractPhelan-McDermid Syndrome (PMS) is a rare genetic disorder in which one copy of the SHANK3 gene is missing or mutated, leading to a global developmental delay, intellectual disability, and autism. Multiple intragenic promoters and alternatively spliced exons are responsible for the formation of numerous isoforms. Many genetically-modified mouse models of PMS have been generated but most disrupt only some of the isoforms. In contrast, the vast majority of known SHANK3 mutations found in patients involve deletions that disrupt all isoforms. Here, we report the production and thorough behavioral characterization of a new mouse model in which all Shank3 isoforms are disrupted. Our mice are more severely affected than previously published models. While the deficits were typically more pronounced in homozygotes, an intermediate phenotype was observed for heterozygotes in many paradigms. As in other Shank3 mouse models, stereotypies, including increased grooming, were observed. Additionally, both sensory and motor deficits were detected in neonatal and adult mice. While social behaviors were not strongly impacted, Shank3-deficient mice displayed a strong escape behavior and avoidance of inanimate objects indicating increased novelty-induced anxiety. Similarly, increased freezing was observed during fear conditioning training and amygdala-dependent cued retrieval. Finally, deficits were observed in both initial training and reversal in the Barnes maze and in contextual fear memory that are memory tasks involving hippocampal-prefrontal circuits. This new mouse model of PMS, engineered to most closely represent human mutations, recapitulates core symptoms of PMS providing improvements for both construct and face validity, compared to previous models.\n\nSignificant statementPhelan-McDermid syndrome, caused by happloinsufficiency of Shank3, is a severe and complex neurodevelopmental disorder. This study investigates the behavioral consequences of a disruption of all Shank3 isoforms in neonatal and adult mice using a detailed battery of tests tailored to investigate core symptoms and usual comorbidities of PMS. We found that our new model is more severely affected than previously published mouse models with only partial deletions of Shank3 and more closely recapitulates symptoms of PMS thus providing improvements for both construct and face validity. Our results highlight the significance of using a mouse model with a complete deletion of Shank3 for studying mechanisms underlying autism spectrum disorder and PMS, carrying preclinical studies and testing test novel therapeutic approaches.

animal behavior and cognition↗

bioRxiv2018

Distinguishing the roles of dorsolateral and anterior PFC in visual metacognition

Visual metacognition depends on regions within the prefrontal cortex. Two areas in particular have been repeatedly implicated: the dorsolateral prefrontal cortex (DLPFC) and the anterior prefrontal cortex (aPFC). However, it is still unclear what the function of each of these areas is and how they differ from each other. To establish the specific roles of DLPFC and aPFC in metacognition, we employed online transcranial magnetic stimulation (TMS) to causally interfere with their functioning during confidence generation. Human subjects from both sexes performed a perceptual decision-making task and provided confidence ratings. We found a clear dissociation between the two areas: DLPFC TMS lowered confidence ratings, whereas aPFC TMS increased metacognitive ability but only for the second half of the experimental blocks. These results support a functional architecture where DLPFC reads out the strength of the sensory evidence and relays it to aPFC, which makes the confidence judgement by potentially incorporating additional, non-perceptual information. Indeed, simulations from a model that incorporates these putative DLPFC and aPFC functions reproduced our behavioral results. These findings establish DLPFC and aPFC as distinct nodes in a metacognitive network and suggest specific contributions from each of these regions to confidence generation.\n\nSignificance\n\nThe prefrontal cortex (PFC) is known to be critical for metacognition. Two of its sub-regions - dorsolateral PFC (DLPFC) and anterior PFC (aPFC) - have specifically been implicated in confidence generation. However, it is unclear if these regions have distinct functions related to the underlying metacognitive computation. Using a causal intervention with transcranial magnetic stimulation (TMS), we demonstrate that DLPFC and aPFC have dissociable contributions: targeting DLPFC decreased average confidence ratings, while targeting aPFC specifically affected metacognitive scores. Based on these results, we postulated specific functions for DLPFC and aPFC in metacognitive computation and corroborated them using a computational model that reproduced our results. Our causal results reveal the existence of a specialized modular organization in PFC for confidence generation.

animal behavior and cognition↗

bioRxiv2018

idtracker.ai: Tracking all individuals in large collectives of unmarked animals

Our understanding of collective animal behavior is limited by our ability to track each of the individuals. We describe an algorithm and software, idtracker.ai, that extracts from video all trajectories with correct identities at a high accuracy for collectives of up to 100 individuals. It uses two deep networks, one detecting when animals touch or cross and an-other one for animal identification, trained adaptively to conditions and difficulty of the video.

animal behavior and cognition↗

bioRxiv2018

Multisensory expectations shape olfactory input to the brain

The mammalian brain interprets sensory input based on prior multisensory knowledge of the external world, but it is unknown how this knowledge influences neural processing in individual sensory modalities. We found that GABAergic periglomerular interneuron populations in the olfactory bulb endogenously respond not only to odors but also to visual, auditory, and somatosensory stimuli in waking (but not anesthetized) mice. When these stimuli predict future odors, they evoke enhanced interneuron activity during the time odor normally occurs. When expectations are violated by omitting an expected \"warning tone\" before an odor, odor presentation evokes a burst of interneuron activity. The resulting GABA release presynaptically suppresses neurotransmitter release from the axon terminals of olfactory sensory neurons, the cells that transduce odor in the nasal epithelium and communicate this information to the brain. Expectations, even those evoked by cues in other sensory modalities, can thus affect the very first neurons in the olfactory system.

animal behavior and cognition↗

bioRxiv2018

Motor Responses Influence Perceptual Awareness Judgements

Perception and action are tightly related, but what is the relation between perceptual awareness and action? In this study we tested the hypothesis that motor response influences perceptual awareness judgements. We design a procedure in which participants were asked to decide whether Gabor grating was oriented towards the left or the right. Presentation of the stimuli was immediately followed by a cue requiring motor response that was irrelevant to the task but could be the same, opposite or neutral to the correct response to the Gabor patch. After responding to the cue participants were asked to rate their stimulus awareness using Perceptual Awareness Scale and then to report their discrimination decision.\n\nThe results showed that participants reported a higher level of stimulus awareness after carrying out responses that were either congruent or incongruent with a response required by a stimulus, compared to the neutral condition. The results suggest that directional motor response (congruent or incongruent with correct response to the stimulus) provides information about the decision process and its outcome increasing reported awareness of a stimulus.

animal behavior and cognition↗

bioRxiv2018

A re-examination of responding on ratio and regulated-probability interval schedules

The higher response rates observed on ratio than on matched interval reward schedules has been attributed to the differential reinforcement of longer inter-response times (IRTs) on the interval contingency. Some data, however, seem to contradict this hypothesis, showing that the difference is still observed when the role of IRT reinforcement is neutralized by using a regulated-probability interval schedule (RPI). Given the mixed evidence for these predictions, we re-examined this hypothesis by training three groups of rats to lever press under ratio, interval and RPI schedules across two phases while matching reward rates within triads. At the end of the first phase, the master ratio and RPI groups responded at similar rates. In the second phase, an interval group yoked to the same master ratio group of the first phase responded at a lower rate than the RPI group. Post-hoc analysis showed comparable reward rates for master and yoked schedules. The experienced response-outcome rate correlations were likewise similar, and approached zero as training progressed. We discuss these results in terms of dual-system theories of instrumental conditioning.

animal behavior and cognition↗

bioRxiv2018

Structured priors in human forecasting

Forecasting is an increasingly important part of our daily lives. Many studies on how people produce forecasts frame their behavior as prone to systematic errors. Based on recent evidence on how people learn about functions, we propose that participants forecasts are not irrational but rather driven by structured priors, i.e. situationally induced expectations of structure derived from experience with the real world. To test this, we extract participants priors over various contexts using a free-form forecasting paradigm. Instead of exhibiting systematic biases, our results show that participants priors match well with structure found in real-world data. Moreover, given the same data set, structured priors induce predictably different posterior forecasts depending on the evoked situational context.

animal behavior and cognition↗

bioRxiv2018

When to care and when to kill: termites shape their collective response based on stage of infection

Termites defend their colonies from disease using an array of social behaviours, including allogrooming, cannibalism, and burial. We tested how groups of eastern subterranean termites (Reticulitermes flavipes) deploy these behaviours when presented with a nestmate at different stages of infection with the entomopathogenic fungus Metarhizium anisopliae. As expected, the termites groomed pathogen-exposed individuals significantly more than mock-treated controls; however, grooming levels were significantly higher after spore germination than before. Cannibalism became prevalent only after exposed termites became visibly ill, and burial was rarely observed. These results demonstrate that termites employ different strategies depending on the stage of infection that they encounter. Grooming intensity is linked not only to pathogen presence, but also to germination status, and, given the temporal correlation between cannibalism and visible signs of illness, the host may play a role in triggering its own sacrifice.

animal behavior and cognition↗

bioRxiv2018

The genetic basis of the human-cannabis relationship

Cannabis can elicit various reactions in different consumers. In order to shed light on the mechanisms underlying the human-cannabis relationship, we begin to investigate the genetic basis of this differential response. The web-based platform OpenSNP was used to collect selfreported genetic and phenotypic data. Participants either reported a positively or negative affinity to cannabis. A total of 26 individuals were retained, 10 of which indicated several negative responses and the remaining 16 indicating strong affinity for Cannabis. A total of 325895 single nucleotide polymorphisms (SNPs) were retained. The software TASSEL 5 was used to run a genome-wide association study (GWAS), with a generalized liner model (GLM) and1000 permutations. The analysis yielded a set of 45 SNPs that were significantly associated with the reported affinity to cannabis, including one strong outlier found in the MYO16 gene. A diagnostic process is proposed by which individuals can be assessed for their affinity to cannabis. We believe this type of tool may be helpful in alleviating some of the stigma associated with cannabis use in individuals sensitive to THC and other cannabis constituents such as myrcene, which may potentiate negative responses.

animal behavior and cognition↗

bioRxiv2018

Counteracting estimation bias and social influence to improve the wisdom of crowds

Aggregating multiple non-expert opinions into a collective estimate can improve accuracy across many contexts. However, two sources of error can diminish collective wisdom: individual estimation biases and information sharing between individuals. Here we measure individual biases and social influence rules in multiple experiments involving hundreds of individuals performing a classic numerosity estimation task. We first investigate how existing aggregation methods, such as calculating the arithmetic mean or the median, are influenced by these sources of error. We show that the mean tends to overestimate, and the median underestimate, the true value for a wide range of numerosities. Quantifying estimation bias, and mapping individual bias to collective bias, allows us to develop and validate three new aggregation measures that effectively counter sources of collective estimation error. In addition, we present results from a further experiment that quantifies the social influence rules that individuals employ when incorporating personal estimates with social information. We show that the corrected mean is remarkably robust to social influence, retaining high accuracy in the presence or absence of social influence, across numerosities, and across different methods for averaging social information. Utilizing knowledge of estimation biases and social influence rules may therefore be an inexpensive and general strategy to improve the wisdom of crowds.

animal behavior and cognition↗

bioRxiv2018

Effect of visual cues in addition to moderate auditory cues on temporal coordination: A comparative study in humans and chimpanzees

Our previous studies reported that chimpanzees share an ability to produce spontaneous temporal coordination with humans (Yu & Tomonaga, 2015; 2016). However, it remains unclear how visual cues of an interacting partners movement influence on the emergence of tempo convergence. The current study conducted a comparative study in humans and chimpanzees under the same experimental setup as that used in Yu & Tomonaga (2016). Three conditions, including baseline, paired-invisible and paired-visible, were prepared. In the baseline condition, the participants produced the repetitive tapping movement alone. In contrast, in the other two paired conditions, the participants in a pair produced the tapping movement concurrently while facing a conspecific partner. However, in the paired-invisible condition, a visual barrier was placed in between the participants to control visual cues of an interacting partners movement. Moderate auditory cues, corresponding to each participants tapping movement, were presented throughout the conditions. Results showed that there are significant changes on the tapping tempo between baseline and the paired-invisible condition, whereas there are little changes between paired-invisible and paired-visible condition in both species. The current stepwise analysis across three conditions demonstrates that auditory cues were more influential than additive visual cues of an interacting partners movement on the tempo convergence in humans and chimpanzees.

animal behavior and cognition↗

bioRxiv2018

Monkeys are Curious about Counterfactual Outcomes

While many non-human animals show basic exploratory behaviors, it remains unclear whether any animals possess human-like curiosity. We propose that human-like curiosity satisfies three formal criteria: (1) willingness to pay (or to sacrifice reward) to obtain information, (2) that the information provides no instrumental or strategic benefit (and the subject understands this), and (3) the amount the subject is willing to pay scales with the amount of information available. Although previous work, including our own, demonstrates that some animals will sacrifice juice rewards for information, that information normally predicts upcoming rewards and their ostensible curiosity may therefore be a byproduct of reinforcement processes. Here we get around this potential confound by showing that macaques sacrifice juice to obtain information about counterfactual outcomes (outcomes that could have occurred had the subject chosen differently). Moreover, willingness-to-pay scales with the information (Shannon entropy) offered by the counterfactual option. These results demonstrate human-like curiosity in non-human animals according to our strict criteria, which circumvent several confounds associated with less stringent criteria.

animal behavior and cognition↗