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Rescuing impaired hippocampal-cortical interactions and spatial reorientation learning and memory during sleep in a mouse model of Alzheimer's disease using hippocampal 40 Hz stimulation

Summary/AbstractIn preclinical Alzheimers disease (AD), spatial learning and memory is impaired. We reported similar impairments in 3xTg-AD mice on a virtual maze (VM) spatial-reorientation-task that requires using landmarks to navigate. Hippocampal (HPC)-cortical dysfunction during sleep (important for memory consolidation) is a potential mechanism for memory impairments in AD. We previously found deficits in HPC-cortical coordination during sleep coinciding with VM impairments the next day. Some forms of 40 Hz stimulation seem to clear AD pathology in mice, and improve functional connectivity in AD patients. Thus, we implanted a recording array targeting parietal cortex (PC) and HPC to assess HPC-PC coordination, and an optical fiber targeting HPC for 40 Hz or sham optogenetic stimulation in 3xTg/PVcre mice. We assessed PC delta waves (DW) and HPC sharp wave ripples (SWRs). In sham mice, SWR-DW cross-correlations were reduced, similar to 3xTg-AD mice. In 40 Hz mice, this phase-locking was rescued, as was performance on the VM. However, rescued HPC-PC coupling no longer predicted performance as in NonTg animals. Instead, DWs and SWRs independently predicted performance in 40 Hz mice. Thus, 40 Hz stimulation of HPC rescued functional interactions in the HPC-PC network, and rescued impairments in spatial navigation, but did not rescue the correlation between HPC-PC coordination during sleep and learning and memory. Together this pattern of results could inform AD treatment timing by suggesting that despite applying 40 Hz stimulation before significant tau and amyloid aggregation, pathophysiological processes led to brain changes that were not fully reversed even though cognition was recovered. Significance StatementOne of the earliest symptoms of Alzheimers disease (AD) is getting lost in space or experiencing deficits in spatial navigation, which involve navigation computations as well as learning and memory. We investigated cross brain region interactions supporting memory formation as a potential causative factor of impaired spatial learning and memory in AD. To assess this relationship between AD pathophysiology, brain changes, and behavioral alterations, we used a targeted approach for clearing amyloid beta and tau to rescue functional interactions in the brain. This research strongly connects brain activity patterns during sleep to tau and amyloid accumulation, and will aid in understanding the mechanisms underlying cognitive dysfunction in AD. Furthermore, the results offer insight for improving early identification and treatment strategies.

animal behavior and cognition↗

Early onset memory deficit of WMI rats compared to their nearly isogenic WLIs is reversed by enriched environment in females

We tested the hypothesis that environmental enrichment (EE) can attenuate early-onset cognitive decline in a stress-hyperresponsive rat strain. The novel genetic model, the Wistar Kyoto More Immobile (WMI) inbred rat strain demonstrates increased stress reactivity and enhanced depression-like behavior compared to its nearly isogenic control, the Wistar Kyoto Less Immobile strain (WLI). Middle-aged (12 months) WMI females exhibited diminished fear, and spatial memory in the contextual fear conditioning and Morris Water Maze paradigms, respectively, compared to young animals (6 months) of both strains and to middle-aged WLIs. Middle-aged WMI males showed a lesser age-induced deficit. EE from six to 12 months of age reversed these memory deficits in middle-aged WMI females and attenuated them in WMI males. Plasma levels of estradiol followed the same pattern as memory in WMI females following EE. RNA sequencing from female hippocampi revealed significant strain, age, and enrichment-induced differentially expressed genes. Among these, solute carrier family 35, member A4 (Slc35a4) and potassium inwardly rectifying channel, subfamily J, member 2 (Kcnj2) were confirmed to show hippocampal expression changes parallel to that of memory in the WMI. These genes have critical roles in the integrated stress response, cellular metabolism, and the effects of stress on neurovascular coupling, respectively. Pathway analyses revealed the involvement of oxidative phosphorylation and mitochondrial dysfunction in the hippocampal processes of aging and EE-induced reversal. These findings underscore the critical involvement of molecular stress responses in early-onset memory decline and suggest potential therapeutic targets for age-related cognitive impairment. HighlightsO_LIHeightened innate stress response and depression leads to early onset memory decline C_LIO_LIEnriched environment reverses memory decline of middle-aged females C_LIO_LIEnriched environment also reverses declining estrogen levels of middle-aged females C_LIO_LIMitochondrial dysfunction may underly mid-life cognitive and molecular changes C_LI

animal behavior and cognition↗

Young domestic chicks spontaneously represent the absence of objects

Absence is a notion that is usually captured by language-related concepts like zero or negation. Whether non-linguistic creatures encode similar thoughts is an open question, as everyday behavior marked by absence (of food, of social partners) can be explained solely by expecting presence somewhere else. We investigated 8-day-old chicks looking behavior in response to events violating expectations about the presence or absence of an object. We found different behavioral responses to violations of presence and absence, suggesting distinct underlying mechanisms. Importantly, chicks displayed an avian signature of novelty detection to violations of absence, namely a sex-dependent left-eye-bias. Follow-up experiments excluded accounts that would explain this bias by perceptual mismatch or by representing the object at different locations. These results suggest that the ability to spontaneously form thoughts about the absence of objects likely belongs to the initial cognitive repertoire of vertebrate species.

animal behavior and cognition↗

Effects of D1 agonist on working memory and cognitive flexibility in a zebrafish model of aging

Healthy aging is associated with a decline in memory and executive function, which have both been linked with aberrant dopaminergic signalling. We examined the relationship between cognitive performance and dopamine function of young and aging zebrafish (Danio rerio). We revealed age-related decreases in working memory and cognitive flexibility in the Free-Movement Pattern (FMP) Y-maze. An increase in drd5 gene expression in aging adults coincided with a decrease in cognitive performance. Treatment with a D1/D5 receptor agonist (SKF-38393, 35 M) 30 minutes prior to behavioural assessment resulted in improved working memory in aging zebrafish, but no effect in younger adults. However, an overdosing effect caused by agonist treatment resulted in downregulation of dat expression in 6-month old, treated zebrafish. The translational relevance of these findings was tested in humans by analysing exploratory behaviour in young-adult, 18-35-year olds, and aged adults, 70+ year olds, in a virtual FMP Y-maze. Our findings revealed similar age-related decline in working memory. Thus, strongly supporting zebrafish as a translational model of aging and cognitive decline.

animal behavior and cognition↗

Ecology dictates the value of memory for foraging bees

"Ecological intelligence" hypotheses posit that animal learning and memory evolves to meet the demands posed by foraging, and together with social intelligence and cognitive buffer hypotheses, provide a key framework for understanding cognitive evolution. However, identifying the critical environments where cognitive investment reaps significant benefits has proved challenging. Here, we capitalise upon seasonal variation in forage availability for a social insect model (Bombus terrestris) to establish how the benefits of short-term memory vary with resource availability. Through analysis of over 1700 foraging trips carried out over two years, we show that short-term memory predicts foraging efficiency - a key determinant of colony fitness - in plentiful spring foraging conditions, but that this relationship is reversed during the summer floral dearth. Our results suggest that selection for enhanced cognitive abilities is unlikely to be limited to harsh environments where food is hard to find or extract, highlighting instead that the complexity of rich and plentiful environments could be a broad driver in the evolution of certain cognitive traits.

animal behavior and cognition↗

Superstitious learning of abstract order from random reinforcement

Survival depends on identifying learnable features of the environment that predict reward, and avoiding others that are random and unlearnable. However, humans and other animals often infer spurious associations among unrelated events, raising the question of how well they can distinguish learnable patterns from unlearnable events. Here, we tasked monkeys with discovering the serial order of two pictorial sets: a "learnable" set in which the stimuli were implicitly ordered and monkeys were rewarded for choosing the higher-rank stimulus and an "unlearnable" set in which stimuli were unordered and feedback was random regardless of the choice. We replicated prior results that monkeys reliably learned the implicit order of the learnable set. Surprisingly, the monkeys behaved as though some ordering also existed in the unlearnable set, showing consistent choice preference that transferred to novel untrained pairs in this set, even under a preference-discouraging reward schedule that gave rewards more frequently to the stimulus that was selected less often. In simulations, a model-free RL algorithm (Q-learning) displayed a degree of consistent ordering among the unlearnable set but, unlike the monkeys, failed to do so under the preference, discouraging reward schedule. Our results suggest that monkeys infer abstract structures from objectively random events using heuristics that extend beyond stimulus-outcome conditional learning to more cognitive model-based learning mechanisms.

animal behavior and cognition↗

Emergent regulation of ant foraging frequency through a computationally inexpensive forager movement rule

1Ant colonies regulate foraging in response to their collective hunger, yet the mechanism behind this distributed regulation remains unclear. Previously, by imaging food flow within ant colonies we showed that the frequency of foraging events declines linearly with colony satiation ([1]). Our analysis implied that as a forager distributes food in the nest, two factors affect her decision to exit for another foraging trip: her current food load and its rate of change. Sensing these variables can be attributed to the foragers individual cognitive ability. Here, new analyses of the foragers trajectories within the nest imply a different way to achieve the observed regulation. Instead of an explicit decision to exit, foragers merely tend toward the depth of the nest when their food load is high and toward the nest exit when it is low. Thus, the colony shapes the foragers trajectory by controlling her unloading rate, while she senses only her current food load. Using an agent-based model and mathematical analysis, we show that this simple mechanism robustly yields emergent regulation of foraging frequency. These findings demonstrate how the embedding of individuals in physical space can reduce their cognitive demands without compromising their computational role in the group.

animal behavior and cognition↗

Four Individually Identified Paired Dopamine Neurons Signal Taste Punishment in Larval Drosophila

Dopaminergic neurons (DANs) carry out multiple tasks in the brain, including the transmission of information related to rewards and punishments across various animal species. They are responsible for evaluating sensory input, storing resulting associations as memory, and continuously updating them based on their relevance and reliability. Accurate comprehension of the dopaminergic systems operation necessitates an understanding of the specific functions mediated by individual DANs. To this end, our research employs Drosophila larvae, which possess approximately 12,000 neurons in their brains, of which only around 1% (approximately 120) are DANs. The presynaptic projections to the mushroom body (MB) - a brain region pivotal for associative olfactory learning in insects - are limited to only eight larval dopaminergic neurons. These DANs are further subdivided into two clusters: the primary protocerebral anterior medial cluster (pPAM) comprises four cells, and the dorsolateral 1 cluster (DL1) comprises the remaining four cells. Our findings confirm previous research that demonstrates that the pPAM DANs innervating the MBs medial lobe encode for a gustatory sugar reward signal. Furthermore, we have identified four DANs in the DL1 cluster - DAN-c1, DAN-d1, DAN-f1, and DAN-g1 - each of which innervates distinct compartments of the MB peduncle, lateral appendix, and vertical lobe. Optogenetic activation of DAN-f1 and DAN-g1 alone suffices to substitute for punishment. Furthermore, optogenetic inhibition, calcium imaging results and electron microscopy-based reconstruction of all sensory input circuits to the four DL1 DANs demonstrate that each DAN encodes a different aspect of punishment, with DAN-g1 being of central importance for the salt dependent teaching signal. To summarize, our investigation has revealed the existence of a cellular division of labor among larval DANs concerning the transmission of dopaminergic reward (pPAM cluster) and punishment signals (DL1 cluster). Individual DANs in each cluster encode for distinct but partially overlapping aspects of the teaching signal. The striking resemblance in the organizing principle of larval DANs with that of its adult counterpart and the mammalian basal ganglion suggests that there may be a limited number of efficient neural circuit solutions available to address more complex cognitive challenges in nature.

animal behavior and cognition↗

Learning performance and GABAergic pathway link to deformed wing virus in the mushroom bodies of naturally infected honey bees

Viral infections can be detrimental to the foraging ability of the Western honey bee Apis mellifera. These include the deformed wing virus (DWV), which is the most common honey bee virus and has been proposed as a possible cause of learning and memory impairment. However, evidence for this phenomenon so far has come from artificially infected bees, while less is known about the implications of natural infections with the virus. Using the proboscis extension reflex (PER), we uncovered no significant association between a simple associative learning task and natural DWV loads. However, when assessed through a reversal associative learning assay, bees with higher DWV loads performed better in the reversal learning phase. DWV is able to replicate in the honey bee mushroom bodies, where the GABAergic signalling pathway has an antagonistic effect on associative learning but is crucial for reversal learning. Hence, we assessed the pattern of expression of several GABA-related genes in bees with different learning responses. Intriguingly, mushroom body expression of selected genes was positively correlated with DWV load, but only for bees with good reversal learning performance. We hypothesize that DWV might improve olfactory learning performance by enhancing the GABAergic inhibition of responses to unrewarded stimuli, which is consistent with the behavioural patterns that we observed. Our results suggest that previously reported DWV-driven learning deficits might be exclusive to acute, artificial infections and do not occur in naturally infected bees, stressing the importance of investigating more ecologically relevant scenarios when assessing host-parasite systems. Summary statementThis study describes a virus-associated increase in learning in honey bees and proposes a mechanism based on GABA to explain the interplay between infection and cognition in the insect brain.

animal behavior and cognition↗

Digit-Tracking Reveals Curiosity-Driven Visual Attention in Macaque Monkeys

We used digit-tracking, a touch-based method for assessing visual attention, to investigate spontaneous exploration in macaque monkeys. By engaging with degraded images on a touch-sensitive display, monkeys could uncover high-resolution portions through finger movements, allowing for natural and unrestricted interaction. Monkeys received juice rewards after touching a predetermined number of pixels, but no specific regions were targeted. Attention maps were generated from their interactions, along with data from human digit-tracking and monkey eye-tracking experiments. We applied a saliency model and a Convolutional Neural Network (CNN) model to predict the empirical explorations. The correlation between model prediction maps and empirical attention maps indicated that monkeys focused non-randomly on information-rich regions, with the CNN model providing the most accurate predictions. These findings suggest that exploration was driven by intrinsic curiosity, beyond the extrinsic rewards for interaction. Digit-tracking offers a minimally invasive, portable alternative to eye-tracking, expanding research opportunities in visual cognition within ecologically valid settings.

animal behavior and cognition↗

Spring Fatigue is a Cultural Phenomenon rather than a Seasonal Syndrome

Although not as prominent as in other animals, also humans experience seasonal variations in for example sleep duration and circadian processes. These variations are likely primarily driven by changes in photoperiod length. Anecdotally, a relevant number of people report experiencing fatigue and low energy levels particularly during spring - at least in Germany, Switzerland, and Austria. Thus, this phenomenon is commonly referred to as "spring fatigue". However, scientific evidence for such a seasonal syndrome is largely missing. We thus investigated temporal variations in fatigue, daytime sleepiness, insomnia symptoms, and sleep quality through an online survey including repeated (i.e., every six weeks) assessments of the same individuals over the course of one year. We hypothesised that fatigue and daytime sleepiness would be higher during shorter photoperiods. We further expected lower sleep quality and more severe insomnia symptoms under shorter photoperiods. Additionally, we explored variations with photoperiod change, across months, and seasons. Hypotheses were tested using Bayesian linear mixed-effects models. The study and analyses were pre-registered. Between April 2024 and September 2025, 418 adults (80% women) completed at least two assessments. Nearly half of participants (47 %) reported experiencing spring fatigue. However, repeated assessments across one year showed no evidence for seasonal or monthly variations in fatigue, sleepiness, insomnia symptoms, or sleep quality. Fatigue during day-to-day activities decreased with longer photoperiods but was independent of photoperiod change. Overall, the results provide evidence against spring fatigue as a genuine seasonal phenomenon. The discrepancy between high self-reports of the phenomenon and stable longitudinal patterns suggests that spring fatigue may reflect cultural labelling and result from cognitive-perceptual biases rather than reflecting a genuine seasonal syndrome.

animal behavior and cognition↗

Effects of Short-Term Breathwork on Respiration and Cognition

Respiration is a unique physiological process that can operate automatically but can also be deliberately used to modulate the bodily state. Importantly, respiration is deeply intertwined with neural processes, influencing processes from arousal and attention to executive control. Although structured respiration (breathing practice) has been exploited for centuries, the immediate consequences of short periods of structured respiration for sensation and cognition remain poorly understood. The present study examined how brief, one-minute episodes of structured respiration affect respiration and performance in a subsequent sensory-cognitive task. Across two experiments, participants engaged in structured breathing practices manipulating either respiratory frequency (slow breathing vs. fast breathing) or the inhalation-exhalation ratio (short inspiration-long expiration; long inspiration-short expiration) prior to performing a visual emotion discrimination task. Immediately after breathing practice, participants respiration deviated from their baseline: each technique resulted in specific deviations of respiratory frequency, inhalation-exhalation ratio, or the occurrence of atypical respiratory cycles, suggesting technique-specific returns to regular respiration. During the subsequent emotion response accuracy or reaction times did not differ between breathing practices. However, we observed transient improvements in reaction times immediately following all practices, suggesting a brief facilitation of attentional or sensorimotor responsiveness following conscious breathing. Our findings indicate that even brief, consciously controlled respiration can transiently influence cognitive performance, highlighting the role of voluntary respiratory modulation in shaping brain function and behavior.

animal behavior and cognition↗

Remembrance of Inferences Past

Bayesian models of cognition assume that people compute probability distributions over hypotheses. However, the required computations are frequently intractable or prohibitively expensive. Since people often encounter many closely related distributions, selective reuse of computations (amortized inference) is a computationally efficient use of the brains limited resources. We present three experiments that provide evidence for amortization in human probabilistic reasoning. When sequentially answering two related queries about natural scenes, participants responses to the second query systematically depend on the structure of the first query. This influence is sensitive to the content of the queries, only appearing when the queries are related. Using a cognitive load manipulation, we find evidence that people amortize summary statistics of previous inferences, rather than storing the entire distribution. These findings support the view that the brain trades off accuracy and computational cost, to make efficient use of its limited cognitive resources to approximate probabilistic inference.

animal behavior and cognition↗

Temporal processing of facial expressions of mental states

Faces provide not only cues to an individuals identity, age, gender and ethnicity, but also insight into their mental states. The ability to identify the mental states of others is known as Theory of Mind. Here we present results from a study aimed at extending our understanding of differences in the temporal dynamics of the recognition of expressions beyond the basic emotions at short presentation times ranging from 12.5 to 100 ms. We measured the effect of variations in presentation time on identification accuracy for 36 different facial expressions of mental states based on the Reading the Mind in the Eyes test (Baron-Cohen et al., 2001) and compared these results to those for corresponding stimuli from the McGill Face database, a new set of images depicting mental states portrayed by professional actors. Our results show that subjects are able to identify facial expressions of complex mental states at very brief presentation times. The kind of cognition involved in the correct identification of facial expressions of complex mental states at very short presentation times suggests a fast, automatic Type-1 cognition.

animal behavior and cognition↗

Modeling the dynamics of social exchange in groups with reinforcement learning and Theory of Mind

Accurately attributing belief to others is a milestone of social cognition and serves as an indicator of intact cognitive functioning. However, tracking all others beliefs in complex social interactions is often inefficient or even impossible. We propose that in such cases, attributing ones own belief to others (i.e., egocentric belief attribution) may serve as a functional approximation, enabling individuals to interact with others successfully. In this study, we employed computational modeling with behavioral measures to investigate this approach in social exchange in a novel group decision-making task across three experiments. We found that, beyond the well-documented reciprocity, participants exhibited consistent alternating behavior, characterized by the switching between potential recipients. This alternation was not driven by fairness concerns but reflected a strategic balance between maintaining stable partnerships and exploring alternatives. Crucially, a reinforcement learning model incorporating egocentric belief attribution (eToM) consistently outperformed all alternative models. These findings highlight that egocentric belief attribution is not a cognitive deficit, but a core mechanism supporting adaptive decision-making in complex social environments.

animal behavior and cognition↗

Dissecting disgust and fear in chimpanzees: From facilitation to disruption of cognitive processes

Disgust and fear are defensive emotions that evolved to address different types of threat. Disgust reduces pathogen exposure through avoidance, whereas fear promotes vigilance and escape from predators. While cognitive mechanisms of fear have been extensively studied, those underlying disgust remain less understood, particularly in nonhuman animals. We examined how cues of disease and predation risk influence cognitive processes in captive chimpanzees (Pan troglodytes). In three touchscreen experiments, subjects performed a number ordering task while exposed to disgust-related images (carcasses, rotten food, disease-associated invertebrates), pathogen-related odors (cadaverine, butyric acid) or fear-related images (snakes). Task performance was assessed via accuracy (proportion of correct trials), reactivity (latency to touch the first numeral), and efficiency (latency to complete trials). We found that disgust cues - particularly those related to body decomposition and food spoilage - modulated task performance in distinct temporal patterns. Carcass images reduced accuracy relative to invertebrate images and slowed performance compared to snake images, while butyric acid - and to a lower extent cadaverine - initially facilitated but later disrupted efficiency upon re-exposure. In contrast, snake images enhanced performance by reducing latencies. To test whether these effects reflected differences in visual attention, we conducted a fourth eye-tracking experiment with new carcass and snake images. Both types of stimuli captured and held attention, partly echoing human data showing sustained attention to snakes but typically not to disgust images. Overall, our results reveal distinct cognitive signatures of disgust and fear in chimpanzees, offering comparative insight into the evolution of defensive emotions. Significance statementDisgust and fear are fundamental emotions that evolved to protect organisms from distinct kinds of threats - disease and predation - but their effects on cognition have rarely been compared, especially in nonhuman animals. In this study, we examined how chimpanzees respond to pathogen-and predator-related cues using touchscreen and eye-tracking experiments. We found that pathogen cues influenced cognitive performance in complex, time-dependent ways, sometimes enhancing and later disrupting it, while predator cues consistently improved performance. Both types of stimuli captured and held attention, although sustained attention to pathogen cues was unexpected. These findings reveal distinct emotional and cognitive signatures of disgust and fear, shedding light on the evolutionary roots of how emotions shape behavior and attention.

animal behavior and cognition↗

Animal Emotions and Consciousness: Researchers' Perceptions, Biases, and Prospects for Future Progress

Do animals have emotions? Scientists and philosophers have long struggled with this question, with debates ranging from whether animals experience an "internal world" to whether we are capable of studying it. Recently, theoretical, and methodological advances have rekindled this debate, yet, it is unclear where the scientific consensus on these topics lies today. To address this gap, we administered a survey of professional animal behavior researchers to assess perceptions regarding (1) the taxonomic distribution of emotions and consciousness in non-human animals, (2) respondents confidence in this assessment, and (3) attitudes towards potential for progress and possible pitfalls when addressing these questions. In general, animal behavior researchers (n=100) ascribed emotionality and consciousness to a broad swath of the animal taxa, including non-human primates, other mammals, birds, and cephalopods, with varying degrees of confidence. There was a strong positive relationship between how likely a respondent was to attribute emotions to a given taxa and their confidence in that assessment, with respondents assuming an absence of emotions and consciousness when they were unsure. In addition, respondents assessments were shaped by several traits (e.g., advanced cognitive abilities, consciousness) that they also admitted were not necessary for an animal to experience emotions. Ultimately, a large majority of researchers were optimistic that tools either currently exist or will exist in the future to rigorously address these questions (>85%) and that animal behavior, as a field, should do more to encourage emotions research (71%). We discuss implications of our findings for publication bias, ethical considerations, and identify an emergent consensus for the need of a functional definition of emotions to facilitate future work. Significance StatementEmotions and consciousness are fundamental components of human experience--these phenomena are central to our behavior, relationships, and sense of meaning. Whether these experiences are shared by non-human animals has long been a subject of philosophical and scientific debate. In this paper we describe, for the first time, results from a survey of animal behavior researchers regarding their perceptions of these questions and the ability of science to answer them. Researchers ascribe emotions and consciousness to many taxa, and their likelihood of doing was strongly predicted by phylogeny and researchers confidence in their answers. We hope these results spur additional interdisciplinary collaboration to rigorously pursue these questions and create a baseline for future comparisons to track scientific attitudes over time. O_QD"I have chosen bats instead of wasps or flounders because if one travels too far down the phylogenetic tree, people gradually shed their faith that there is experience there at all"--Thomas Nagel C_QD

animal behavior and cognition↗

Phenotypic architecture of sociality and its associated genetic polymorphisms in zebrafish

Sociality is often seen as a single phenotypic trait, but it relies on motivational and cognitive components implemented by specific causal mechanisms. Hence, these components may have evolved independently, or may have been linked by phenotypic correlations driven by a shared selective pressure for increased social competence. Furthermore, these components may be domain-specific or of general domain across social and non-social contexts. Here we have characterized the phenotypic architecture of sociality in zebrafish, which has been increasingly used as a model organism in social neuroscience. For this purpose, we have behaviorally phenotyped zebrafish from different wild type lines in four tests: social tendency, social and non-social recognition, and open-field test. Our results indicate that: (1) sociality has two main components that are independent from each other (social tendency and social recognition), hence not supporting the occurrence of a sociality syndrome; (2) both social traits are phenotypically linked to non-social traits (non-social exploration and non-social memory, respectively), forming two general behavioral modules, general inspection and general recognition, and suggesting that sociality traits have been co-opted from general-domain motivational and cognitive traits. Moreover, the study of the association between genetic polymorphisms (i.e. single nucleotide polymorphisms, SNPs) and each behavioral module further supports this view, since several SNPs from a list of candidate "social" genes, are statistically associated with the general inspection (motivational), but not with a general recognition (cognitive), behavioral module. The SNPs associated with general inspection are widespread across different chromosomes and include neurotransmitters, neuromodulators, and synaptic plasticity genes, suggesting that this behavioral module is regulated by multiple genes, each of them with small effects. Together, these results support the occurrence of general domain motivational and cognitive behavioral modules in zebrafish, which have been co-opted for the social domain. Author summarySocial living has been considered one of the major transitions in evolution and it has been considered to act as a major selective force shaping the evolution of brain and behavior in animals. Sociality relies on two basic behavioral mechanisms: (1) the willingness to approach and be near others (aka social tendency); and (2) the ability to distinguish between others (aka social recognition) in order to adjust the behavior expressed during social interactions according to the identity of the interactant. There is an ongoing debate on to what extent these social abilities have specifically evolved in response to social living and are domain specific, or if they were selected as a broad response to cognitive demands and are of general domain. Here, we used zebrafish to test the domain-specific vs. general domain hypotheses and to assess the association of social tendency and social recognition with a set of candidate "social" genes (i.e. genes that have been linked to social behavior in other studies with different vertebrate species). We found that both social traits are not correlated to each other and are of general domain, and that only social tendency is associated with candidate "social" genes, suggesting that social tendency and social recognition are independent behavioral modules that rely on separate genetic architectures and that can evolve separately.

animal behavior and cognition↗