Complex Social Behavior Research Articles

Oxytocin receptor controls distinct components of pair bonding and development in prairie voles.

Oxytocin receptor (Oxtr) signaling influences complex social behaviors in diverse species, including social monogamy in prairie voles. How Oxtr regulates specific components of social attachment behaviors and the neural mechanisms mediating them remains unknown. Here, we examine prairie voles lacking Oxtr and demonstrate that pair bonding comprises distinct behavioral modules: the preference for a bonded partner, and the rejection of novel potential mates. Our longitudinal study of social attachment shows that Oxtr sex-specifically influences early interactions between novel partners facilitating the formation of partner preference. Additionally, Oxtr suppresses promiscuity towards novel potential mates following pair bonding, contributing to rejection. Oxtr function regulates coordinated patterns of gene expression in regions implicated in attachment behaviors and regulates the expression of oxytocin in the paraventricular nucleus of the hypothalamus, a principal source of oxytocin. Thus, Oxtr controls genetically separable components of pair bonding behaviors and coordinates development of the neural substrates of attachment.

Activation of arginine vasopressin receptor 1a reduces inhibitory synaptic currents at reciprocal synapses in the mouse accessory olfactory bulb.

Central arginine vasopressin (AVP) facilitates social recognition and modulates many complex social behaviors in mammals that, in many cases, recognize each other based on olfactory and/or pheromonal signals. AVP neurons are present in the accessory olfactory bulb (AOB), which is the first relay in the vomeronasal system and has been demonstrated to be a critical site for mating-induced mate recognition (olfactory memory) in female mice. The transmission of information from the AOB to higher centers is controlled by the dendrodendritic recurrent inhibition, i.e., inhibitory postsynaptic currents (IPSCs) generated in mitral cells by recurrent dendrodendritic inhibitory inputs from granule cells. These reports suggest that AVP might play an important role in regulating dendrodendritic inhibition in the AOB. To test this hypothesis, we examined the effects of extracellularly applied AVP on synaptic responses measured from mitral and granule cells in slice preparations from 23--36-day-old Balb/c mice. To evoke dendrodendritic inhibition in a mitral cell, depolarizing voltages of -70 to 0 mV (10 ms duration) were applied to a mitral cell using a conventional whole-cell configuration. We found that AVP significantly reduced the IPSCs. The suppressive effects of AVP on the IPSCs was diminished by an antagonist for vasopressin receptor 1a (V1aR) (Manning compound), but not by an antagonist for vasopressin receptor 1b (SSR149415). An agonist for V1aRs [(Phe2)OVT] mimicked the action of AVP on IPSCs. Additionally, AVP significantly suppressed voltage-activated currents in granule cells without affecting the magnitude of the response of mitral cells to gamma-aminobutyric acid (GABA). The present results suggest that V1aRs play a role in reciprocal transmission between mitral cells and granule cells in the mouse AOB by reducing GABAergic transmission through a presynaptic mechanism in granule cells.

MiniXL: An open-source, large field-of-view epifluorescence miniature microscope for mice capable of single-cell resolution and multi-brain region imaging.

Capturing the intricate dynamics of neural activity in freely behaving animals is essential for understanding the neural mechanisms underpinning specific behaviors. Miniaturized microscopy enables investigators to track population activity at cellular level, but the field of view (FOV) of these microscopes have been limited and does not allow multiple-brain region imaging. To fill this technological gap, we have developed the eXtra Large field-of-view Miniscope (MiniXL), a 3.5g lightweight miniaturized microscope with an FOV measuring 3.5 mm in diameter and an electrically adjustable working distance of 1.9 mm ± 200 μm. We demonstrated the capability of MiniXL recording the activity of large neuronal population in both subcortical area (hippocampal dorsal CA1) and deep brain regions (medial prefrontal cortex, mPFC and nucleus accumbens, NAc). The large FOV allows simultaneous imaging of multiple brain regions such as bilateral mPFCs or mPFC and NAc during complex social behavior and tracking cells across multiple sessions. As with all microscopes in the UCLA Miniscope ecosystem, the MiniXL is fully open-source and will be shared with the neuroscience community to lower the barriers for adoption of this technology.

Feminization of social play behavior depends on microglia.

Many sex differences in brain and behavior are established developmentally by the opposing processes of feminization and masculinization, which manifest following differential steroid hormone exposure in early life. The cellular mechanisms underlying masculinization are well-documented, a result of the fact that it is steroid-mediated and can be easily induced in newborn female rodents via exogenous steroid treatment. However, the study of feminization of particular brain regions has largely been relegated to being "not masculinization" given the absence of an identified initiating trigger. As a result, the mechanisms of this key developmental process remain elusive. Here we describe a novel role for microglia, the brain's innate immune cell, in the feminization of the medial amygdala and a complex social behavior, juvenile play. In the developing amygdala, microglia promote proliferation of astrocytes equally in both sexes, with no apparent effect on rates of cell division, but support cell survival selectively in females through the trophic actions of Tumor Necrosis Factor α (TNFα). We demonstrate that disrupting TNFα signaling, either by depleting microglia or inhibiting the associated signaling pathways, prevents the feminization of astrocyte density and increases juvenile play levels to that seen in males. This data, combined with our previous finding that male-like patterns of astrocyte density are sculpted by developmental microglial phagocytosis, reveals that sexual differentiation of the medial amygdala involves opposing tensions between active masculinization and active feminization, both of which require microglia but are achieved via distinct processes.

Different neural correlates of deception: Crafting high and low creative scams

Deception is a complex social behavior that manifests in various forms, including scams. To successfully deceive victims, liars have to continually devise novel scams. This ability to create novel scams represents one kind of malevolent creativity, referred to as lying. This study aimed to explore different neural substrates involved in the generation of high and low creative scams. A total of 40 participants were required to design several creative scams, and their cortical activity was recorded by functional near-infrared spectroscopy. The results revealed that the right frontopolar cortex (FPC) was significantly active in scam generation. This region associated with theory of mind may be a key region for creating novel and complex scams. Moreover, creativity-related regions were positively involved in creative scams, while morality-related areas showed negative involvement. This suggests that individuals might attempt to use malevolent creativity while simultaneously minimizing the influence of moral considerations. The right FPC exhibited increased coupling with the right precentral gyrus during the design of high-harmfulness scams, suggesting a diminished control over immoral thoughts in the generation of harmful scams. Additionally, the perception of the victim’s emotions (related to right pre-motor cortex) might diminish the quality of highly original scams. Furthermore, an efficient and cohesive neural coupling state appears to be a key factor in generating high-creativity scams. These findings suggest that the right FPC was crucial in scam creation, highlighting a neural basis for balancing malevolent creativity against moral considerations in high-creativity deception.

Long-term co-occurrence and gregariousness in the migratory common stingray using network analysis

Aggregations and social interactions play an important role in the movement ecology of many animals, including elasmobranchs. Several of these species have shown the capability of carrying out complex social behaviours, and the importance of sociality in this taxon is being realized. Although it is a growing field of study in the case of these organisms, these processes still need to be better understood, especially to support management and conservation policies. In this study, a long-term acoustic telemetry data set collected on Dasyatis pastinaca in a coastal marine protected area was analysed. A co-occurrence network analysis was done to investigate preferential associations among individuals, revealing non-random associations among them. The analysis revealed a few strong and consistent associations that were maintained across inter-migratory periods, as this species performs seasonal migrations to a nearby estuary, suggesting temporal stability of the observed associations. Moreover, individuals had similar average positions and a generally high overlap of space use in both periods, indicating some level of site fidelity to the fully protected area. Groups of up to 64% of tagged individuals were co-detected at a same receiver, particularly in the western side of the array. Despite our limited sample size, likely underestimating associations, these results show that in addition to their large-scale movement pattern, D. pastinaca is likely to also present active partner preference and spatial structure at a finer spatial scale. The nature of such results is relevant to support the protection of these species.

The Budding Neuroscience of Ant Social Behavior.

Ant physiology has been fashioned by 100 million years of social evolution. Ants perform many sophisticated social and collective behaviors yet possess nervous systems similar in schematic and scale to that of the fruit fly Drosophila melanogaster, a popular solitary model organism. Ants are thus attractive complementary subjects to investigate adaptations pertaining to complex social behaviors that are absent in flies. Despite research interest in ant behavior and the neurobiological foundations of sociality more broadly, our understanding of the ant nervous system is incomplete. Recent technical advances have enabled cutting-edge investigations of the nervous system in a fashion that is less dependent on model choice, opening the door for mechanistic social insect neuroscience. In this review, we revisit important aspects of what is known about the ant nervous system and behavior, and we look forward to how functional circuit neuroscience in ants will help us understand what distinguishes solitary animals from highly social ones.

The self-in-the-world map emerged in the primate brain as a basis for Homo sapiens abilities.

The brain in the genus Homo expanded rapidly during evolution, accelerated by a reciprocated interaction between neural, cognitive, and ecological niches (triadic niche construction, or TNC). This biologically costly expansion incubated latent cognitive capabilities that, with a quick and inexpensive rewiring of brain areas in a second phase of TNC, provided the basis for Homo sapiens specific abilities. The neural demands for perception of the human body in interaction with tools and the environment required highly integrated sensorimotor domains, inducing the parietal lobe expansion seen in humans. These newly expanded brain areas allowed connecting the sensations felt in the body to the actions in the world through the cognitive function of "projection". In this opinion article, we suggest that as a relationship of equivalence between body parts, tools and their external effects was established, mental mechanisms of self-objectification might have emerged as described previously, grounding notions of spatial organization, idealized objects, and their transformations, as well as socio-emotional states in the sensing agent through a self-in-the-world map. Therefore, human intelligence and its features such as symbolic thought, language, mentalizing, and complex technical and social behaviors could have stemmed from the explicit awareness of the causal relationship between the self and intentional modifications to the environment.

Peptides and primate personality: Central and peripheral oxytocin and vasopressin levels and social behavior in two baboon species (Papio hamadryas and Papio anubis)

The neurohormones oxytocin (OT) and arginine vasopressin (AVP) are involved in social behaviors and psychiatric conditions. However, more research on nonhuman primates with complex social behaviors is needed. We studied two closely-related primate species with divergent social and mating systems; hamadryas baboons (Papio hamadryas, n=38 individuals) and anubis baboons (Papio anubis, n=46). We measured OT in cerebrospinal fluid (CSF, n=75), plasma (n=81) and urine (n=77), and AVP in CSF (n=45), and we collected over 250 hours of focal behavioral observations. Using Bayesian multivariate models, we found no clear species difference in hormone levels; the strongest support was for hamadryas having higher CSF OT levels than anubis (posterior probability [PP] for females = 0.75, males = 0.84). Looking at nine specific behaviors, OT was associated with affiliative behaviors (approach, proximity, grooming, PP ∼ 0.85 – 1.00), albeit inconsistently across sources of measurement (CSF, plasma, and urine, which were uncorrelated with each other). Most behaviors had low repeatability (R ∼ 0 – 0.2), i.e. they did not exhibit stable between-individual differences (or “personality”), and different behaviors did not neatly coalesce into higher-order factors (or “behavioral syndromes”), which cautions against the use of aggregate behavioral measures and highlights the need to establish stable behavioral profiles when testing associations with baseline hormone levels. In sum, we found some associations between peptides and social behavior, but also many null results, OT levels from different sources were uncorrelated, and our behavioral measures did not indicate clear individual differences in sociability.

A Wireless Wearable Ecosystem for Social Network Analysis in Free-living Animals.

Studying animal social systems requires understanding variations in contact and interaction, influenced by factors like environmental conditions, resource availability, and predation risk. Traditional observational methods have limitations, but advancements in sensor technologies and data analytics provide new opportunities. We developed a wireless wearable sensor system, "Juxta," with features such as modular battery packs and a smartphone app for data collection. A pilot study on free-living prairie voles (Microtus ochrogaster), a species with complex social behavior, demonstrated Juxta's potential for studying social networks and behavior. We propose a framework for merging temporal, spatial, and event-driven data, which can help explore complex social dynamics across species and environments.

Debugging collective digging in Drosophila melanogaster using an agent-based model

Being a member of a group entails a range of possible costs and benefits; observing when and with whom groups form can help identify how these are weighted. Clustering behaviour in fruit fly (Drosophila melanogaster) third-instar larvae has been shown to provide individuals that cluster with improved foraging opportunities on otherwise inaccessible food. To isolate how environmental and genetic factors affect who clusters and when, we created an on-lattice agent-based model and systematically explored the effects of several variables, such as population density, resource distribution, and the phenotypic composition of the group. Our simple model reproduces most of the key features of larval clustering and demonstrates drastic differences in collective behaviour and fitness in response to changes in environmental variables, in ways that align with the limited empirical data available. This model can improve our understanding of this complex social behaviour and make testable predictions about the behavioural and ecological mechanisms of larval clustering.

Orco-dependent survival of odorant receptor neurons in ants.

Olfaction is essential for complex social behavior in insects. To discriminate complex social cues, ants evolved an expanded number of odorant receptor (Or) genes. Mutations in the obligate odorant co-receptor gene orco lead to the loss of ~80% of the antennal lobe glomeruli in the jumping ant Harpegnathos saltator. However, the cellular mechanism remains unclear. Here, we demonstrate massive apoptosis of odorant receptor neurons (ORNs) in the mid to late stages of pupal development, possibly due to ER stress in the absence of Orco. Further bulk and single-nucleus transcriptome analysis shows that, although most orco-expressing ORNs die in orco mutants, a small proportion of them survive: They express ionotropic receptor (Ir) genes that form IR complexes. In addition, we found that some Or genes are expressed in mechanosensory neurons and nonneuronal cells, possibly due to leaky regulation from nearby non-Or genes. Our findings provide a comprehensive overview of ORN development and Or expression in H. saltator.

Sport, neurodegenerative illness and the social determinants of health

ABSTRACT This article proposes a Social Determinants of Health framework as a counter to the prominence of bio-determinist tropes in understandings of the relationship between concussion and later life neurodegenerative conditions in athletic populations. It is argued that debates about concussion (or repetitive head impacts) causing CTE have been particularly influenced by broader social trends towards neuro-essentialism. This paradigm reduces complex social behaviour to brain matter and continues to dominate the field despite the recent diversification of evidence from autopsy-based studies of neuropathology to epidemiological studies comparing recorded causes of death among former elite athletes. In contrast, this article explores the ‘causes of causes’ of neurodegenerative conditions. It outlines the ways in which the distinct dynamics of: a) employment, b) education, income and wealth, c) health systems and services, and d) social environment and public safety relate to the specific occupational conditions of elite sport and likely negatively shape health outcomes of athletic populations. The article concludes by arguing that to more effectively address these particular health harms we must move beyond narrow, mono-causal models and evoke a cultural change that extends beyond making rule changes and adjusting psychological attitudes and behavioural norms, to redress the social structural parameters of elite sports participation. The continuation of narrower, neuro-centric and reductionist paradigms obscures the causes of the causes of neurodegenerative decline and limits the scope for change.

Tadpoles rely on mechanosensory stimuli for communication when visual capabilities are poor

The ways in which animals sense the world changes throughout development. For example, young of many species have limited visual capabilities, but still make social decisions, likely based on information gathered through other sensory modalities. Poison frog tadpoles display complex social behaviors that have been suggested to rely on vision despite a century of research indicating tadpoles have poorly-developed visual systems relative to adults. Alternatively, other sensory modalities, such as the lateral line system, are functional at hatching in frogs and may guide social decisions while other sensory systems mature. Here, we examined development of the mechanosensory lateral line and visual systems in tadpoles of the mimic poison frog (Ranitomeya imitator) that use vibrational begging displays to stimulate egg feeding from their mothers. We found that tadpoles hatch with a fully developed lateral line system. While begging behavior increases with development, ablating the lateral line system inhibited begging in pre-metamorphic tadpoles, but not in metamorphic tadpoles. We also found that the increase in begging and decrease in reliance on the lateral line co-occurs with increased retinal neural activity and gene expression associated with eye development. Using the neural tracer neurobiotin, we found that axonal innervations from the eye to the brain proliferate during metamorphosis, with few retinotectal connections in recently-hatched tadpoles. We then tested visual function in a phototaxis assay and found tadpoles prefer darker environments. The strength of this preference increased with developmental stage, but eyes were not required for this behavior, possibly indicating a role for the pineal gland. Together, these data suggest that tadpoles rely on different sensory modalities for social interactions across development and that the development of sensory systems in socially complex poison frog tadpoles is similar to that of other frog species.

Neurobehavioral Mechanisms Influencing the Association Between Generativity, the Desire to Promote Well-Being of Younger Generations, and Purpose in Life in Older Adults at Risk for Alzheimer's Disease.

Generativity, the desire and action to improve the well-being of younger generations, is associated with purpose in life among older adults. However, the neurobehavioral factors supporting the relationship between generativity and purpose in life remain unknown. This study aims to identify the functional neuroanatomy of generativity and mechanisms linking generativity with purpose in life in at-risk older adults. Fifty-eight older adults (mean age = 70.8, SD = 5.03, 45 females) with a family history of Alzheimer's disease (AD) were recruited from the PREVENT-AD cohort. Participants underwent brain imaging and completed questionnaires assessing generativity, social support, and purpose in life. Mediation models examined whether social support mediated the association between generativity and purpose in life. Seed-to-voxel analyses investigated the association between generativity and resting-state functional connectivity (rsFC) to the ventromedial prefrontal cortex (vmPFC) and ventral striatum (VS), and whether this rsFC moderated the relationship between generativity and purpose in life. Affectionate social support mediated the association between generative desire and purpose in life. Generative desire was associated with rsFC between VS and precuneus, and, vmPFC and right dorsolateral prefrontal cortex (rdlPFC). The vmPFC-rdlPFC rsFC moderated the association between generative desire and purpose in life. These findings provide insight into how the brain supports complex social behavior and, separately, purpose in life in at-risk aging. Affectionate social support may be a putative target process to enhance purpose in life in older adults. This knowledge contributes to future developments of personalized interventions that promote healthy aging.

Generating Synthetic Sperm Whale Voice Data Using StyleGAN2-ADA

The application of deep learning neural networks enables the processing of extensive volumes of data and often requires dense datasets. In certain domains, researchers encounter challenges related to the scarcity of training data, particularly in marine biology. In addition, many sounds produced by sea mammals are of interest in technical applications, e.g., underwater communication or sonar construction. Thus, generating synthetic biological sounds is an important task for understanding and studying the behavior of various animal species, especially large sea mammals, which demonstrate complex social behavior and can use hydrolocation to navigate underwater. This study is devoted to generating sperm whale vocalizations using a limited sperm whale click dataset. Our approach utilizes an augmentation technique predicated on the transformation of audio sample spectrograms, followed by the employment of the generative adversarial network StyleGAN2-ADA to generate new audio data. The results show that using the chosen augmentation method, namely mixing along the time axis, makes it possible to create fairly similar clicks of sperm whales with a maximum deviation of 2%. The generation of new clicks was reproduced on datasets using selected augmentation approaches with two neural networks: StyleGAN2-ADA and WaveGan. StyleGAN2-ADA, trained on an augmented dataset using the axis mixing approach, showed better results compared to WaveGAN.

Distinct genetic and environmental origins of hierarchical cognitive abilities in adult humans

Human cognitive abilities ranging from basic perceptions to complex social behaviors exhibit substantial variation in individual differences. These cognitive functions can be categorized into a two-order hierarchy based on the levels of cognitive processes. Second-order cognition including metacognition and mentalizing monitors and regulates first-order cognitive processes. These two-order hierarchical cognitive functions exhibit distinct abilities. However, it remains unclear whether individual differences in these cognitive abilities have distinct origins. We employ the classical twin paradigm to compare the genetic and environmental contributions to the two-order cognitive abilities in the same tasks from the same population. The results reveal that individual differences in first-order cognitive abilities were primarily influenced by genetic factors. Conversely, the second-order cognitive abilities have a stronger influence from shared environmental factors. These findings suggest that the abilities of metacognition and mentalizing in adults are profoundly shaped by their environmental experiences and less determined by their biological nature.

An Ecological and Neural Argument for Developing Pursuit-Based Cognitive Enrichment for Sea Lions in Human Care.

While general enrichment strategies for captive animals attempt to elicit variable and species-typical behaviors, approaches to cognitive enrichment have been disappointingly one-size-fits-all. In this commentary, we address the potential benefit of tailoring cognitive enrichment to the "cognitive niche" of the species, with a particular focus on a reasonably well-studied marine carnivore, the sea lion. Sea lions likely share some cognitive evolutionary pressures with primates, including complex social behavior. Their foraging ecology, however, like that of many terrestrial carnivores, is based on the rapid and behaviorally flexible pursuit of avoidant prey. Unlike terrestrial carnivores, sea lions carry out this pursuit in a truly fluid three-dimensional field, computing and executing sensorimotor transformations from any solid angle to any other. The cognitive demands of flexible prey pursuit are unlikely to be fully elicited by typical stationary puzzle box style foraging enrichment devices or screen-based interactive games. With this species, we recommend exploring more water-based movement activities generally, and complex pursuit challenges specifically.

Evolution of delayed dispersal with group size effect and population dynamics

Individuals delay natal dispersal for many reasons. There may be no place to disperse to; immediate dispersal or reproduction may be too costly; immediate dispersal may mean that the individual and their relatives miss the benefits of group living. Understanding the factors that lead to the evolution of delayed dispersal is important because delayed dispersal sets the stage for complex social groups and social behavior. Here, we study the evolution of delayed dispersal when the quality of the local environment is improved by greater numbers of individuals (e.g., safety in numbers). We assume that individuals who delay natal dispersal also expect to delay personal reproduction. In addition, we assume that improved environmental quality benefits manifest as changes to fecundity and survival. We are interested in how do the changes in these life-history features affect delayed dispersal. We use a model that ties evolution to population dynamics. We also aim to understand the relationship between levels of delayed dispersal and the probability of establishing as an independent breeder (a population-level feature) in response to changes in life-history details. Our model emphasizes kin selection and considers a sexual organism, which allows us to study parent–offspring conflict over delayed dispersal. At evolutionary equilibrium, fecundity and survival benefits of group size or quality promote higher levels of delayed dispersal over a larger set of life histories with one exception. The exception is for benefits of increased group size or quality reaped by the individuals who delay dispersal. There, the increased benefit does not change the life histories supporting delay dispersal. Next, in contrast to previous predictions, we find that a low probability of establishing in a new location is not always associated with a higher incidence of delayed dispersal. Finally, we find that increased personal benefits of delayed dispersal exacerbate the conflict between parents and their offspring. We discuss our findings in relation to previous theoretical and empirical work, especially work related to cooperative breeding.

Evolutionary novelties underlie sound production in baleen whales.

Baleen whales (mysticetes) use vocalizations to mediate their complex social and reproductive behaviours in vast, opaque marine environments1. Adapting to an obligate aquatic lifestyle demanded fundamental physiological changes to efficiently produce sound, including laryngeal specializations2-4. Whereas toothed whales (odontocetes) evolved a nasal vocal organ5, mysticetes have been thought to use the larynx for sound production1,6-8. However, there has been no direct demonstration that the mysticete larynx can phonate, or if it does, how it produces the great diversity of mysticete sounds9. Here we combine experiments on the excised larynx of three mysticete species with detailed anatomy and computational models to show that mysticetes evolved unique laryngeal structures for sound production. These structures allow some of the largest animals that ever lived to efficiently produce frequency-modulated, low-frequency calls. Furthermore, we show that this phonation mechanism is likely to be ancestral to all mysticetes and shares its fundamental physical basis with most terrestrial mammals, including humans10, birds11, and their closest relatives, odontocetes5. However, these laryngeal structures set insurmountable physiological limits to the frequency range and depth of their vocalizations, preventing them from escaping anthropogenic vessel noise12,13 and communicating at great depths14, thereby greatly reducing their active communication range.