Complex Social Behavior Research Articles

A zinc finger transcription factor enables social behaviors while controlling transposable elements and immune response in prefrontal cortex

The neurobiological origins of social behaviors are incompletely understood. Here we utilized synthetic biology approaches to reprogram the function of ZFP189, a transcription factor whose expression and function in rodent prefrontal cortex was previously demonstrated to be protective against stress-induced social deficits. We created novel synthetic ZFP189 transcription factors including ZFP189VPR, which activates the transcription of target genes and therefore exerts opposite functional control from the endogenous, transcriptionally repressive ZFP189WT. Following viral delivery of these synthetic ZFP189 transcription factors to mouse prefrontal cortex, we observe that ZFP189-mediated transcriptional control promotes mature dendritic spine morphology on transduced pyramidal neurons. Interestingly, inversion of ZFP189-mediated transcription in this brain area, achieved by viral delivery of synthetic ZFP189VPR, precipitates social behavioral deficits in terms of social interaction, motivation, and the cognition necessary for the maintenance of social hierarchy, without other observable behavioral deficits. RNA sequencing of virally manipulated prefrontal cortex tissues reveals that ZFP189 transcription factors of opposing regulatory function (ZFP189WT versus ZFP189VPR) have opposite influence on the expression of genetic transposable elements as well as genes that participate in adaptive immune functions. Collectively, this work reveals that ZFP189 function in the prefrontal cortex coordinates structural and transcriptional neuroadaptations necessary for complex social behaviors while regulating transposable element-rich regions of DNA and the expression of immune-related genes. Given the evidence for a co-evolution of social behavior and the brain immune response, we posit that ZFP189 may have evolved to augment brain transposon-associated immune function as a way of enhancing an animal’s capacity for functioning in social groups.

Female mice prenatally exposed to valproic acid exhibit complex and prolonged social behavior deficits

Autism Spectrum Disorder (ASD) is a neurodevelopmental disorder characterized mainly by deficits in social communication and stereotyped and restricted behavior and interests with a male to female bias of 4.2/1. Social behavior in ASD animal models is commonly analyzed in males, and seldomly in females, using the widely implemented three-chambers test procedure. Here, we implemented a novel procedure, the Live Mouse Tracker (LMT), combining artificial intelligence, machine learning procedures and behavioral measures. We used it on mice that were prenatally exposed to valproic acid (VPA) (450 mg/kg) at embryonic day 12.5, a widely recognized and potent ASD model that we had previously extensively characterized. We focused on female mice offspring, in which social deficits have been rarely documented when using the 3-CT procedure. We recorded several parameters related to social behavior in these mice, continuously for three days in groups of four female mice. Comparisons were made on groups of 4 female mice with the same treatment (4 saline or 4 VPA) or with different treatments (3 saline and 1 VPA). We report that VPA females show several types of social deficits, which are different in nature and magnitude in relation with time. When VPA mice were placed in the LMT alongside saline mice, their social deficits showed significant improvement as early as 1 h from the start of the experiment, lasting up to 3 days throughout the duration of the experiment. Our findings suggest that ASD may be underdiagnosed in females. They also imply that ASD-related social deficits can be ameliorated by the presence of typical individuals.

The Application and Challenge of Non-Human Primate Experimental Animals in the Field of Neuroscience

Non-human primates (NHPs) are highly valued in the field of neuroscience due to their similarity to humans in terms of brain structure and function. They exhibit complex social behaviors and cognitive abilities, and their use in research has led to significant breakthroughs in the understanding of brain development, neurodegenerative diseases, and psychiatric disorders. In recent years, the breeding and use of NHPs has expanded, making them increasingly important as experimental animals. However, with this expansion comes the need for researchers to address important biosafety and animal ethics concerns. It is critical that animal welfare is ensured and that scientific objectives are achieved while observing ethical guidelines. This paper aims to provide an overview of NHPs in neuroscience, their applications in research, and the ethical considerations that must be taken into account. It highlights the various breeding and handling practices that are employed to ensure the health and welfare of NHPs in experimental settings. Additionally, the paper summarizes the challenges associated with the use of NHPs in research and the benefits that have been realized from their use. Overall, this paper underscores the importance of recognizing the role of NHPs in neuroscience, and the responsibility that researchers have to ensure their welfare and to address ethical considerations. By doing so, researchers can continue to advance our understanding of the brain and develop new treatments for neurological and psychiatric disorders.

The uniqueness of the human brain: a review.

The purpose of this review is to highlight the most important aspects of the anatomical and functional uniqueness of the human brain. For this, a comparison is made between our brains and those of our closest ancestors (chimpanzees and bonobos) and human ancestors. During human evolution, several changes occurred in the brain, such as an absolute increase in brain size and number of cortical neurons, in addition to a greater degree of functional lateralization and anatomical asymmetry. Also, the cortical cytoarchitecture became more diversified and there was an increase in the number of intracortical networks and networks extending from the cerebral cortex to subcortical structures, with more neural networks being invested in multisensory and sensory-motor-affective-cognitive integration. These changes permitted more complex, flexible and versatile cognitive abilities and social behavior, such as shared intentionality and symbolic articulated language, which, in turn, made possible the formation of larger social groups and cumulative cultural evolution that are characteristic of our species.

Regional and cellular organization of the autism-associated protein UBE3A/E6AP and its antisense transcript in the brain of the developing rhesus monkey.

Angelman syndrome (AS) is a neurogenetic disorder caused by mutations or deletions in the maternally-inherited UBE3A allele, leading to a loss of UBE3A protein expression in neurons. The paternally-inherited UBE3A allele is epigenetically silenced in neurons during development by a noncoding transcript (UBE3A-ATS). The absence of neuronal UBE3A results in severe neurological symptoms, including speech and language impairments, intellectual disability, and seizures. While no cure exists, therapies aiming to restore UBE3A function-either by gene addition or by targeting UBE3A-ATS-are under development. Progress in developing these treatments relies heavily on inferences drawn from mouse studies about the function of UBE3A in the human brain. To aid translational efforts and to gain an understanding of UBE3A and UBE3A-ATS biology with greater relevance to human neurodevelopmental contexts, we investigated UBE3A and UBE3A-ATS expression in the developing brain of the rhesus macaque, a species that exhibits complex social behaviors, resembling aspects of human behavior to a greater degree than mice. Combining immunohistochemistry and in situ hybridization, we mapped UBE3A and UBE3A-ATS regional and cellular expression in normal prenatal, neonatal, and adolescent rhesus macaque brains. We show that key hallmarks of UBE3A biology, well-known in rodents, are also present in macaques, and suggest paternal UBE3A silencing in neurons-but not glial cells-in the macaque brain, with onset between gestational day 48 and 100. These findings support proposals that early-life, perhaps even prenatal, intervention is optimal for overcoming the maternal allele loss of UBE3A linked to AS.

Early life social complexity shapes adult neural processing in the communal spiny mouse Acomys cahirinus.

Early life social rearing has profound consequences on offspring behavior and resilience. Yet, most studies examining early life development in rodents use species whose young are born immobile and do not produce complex social behavior until later in development. Furthermore, models of rearing under increased social complexity, rather than deprivation, are needed to provide alternative insight into the development of social neural circuitry. To understand precocial offspring social development, we manipulated early life social complexity in the communal spiny mouse Acomys cahirinus and assessed long-term consequences on offspring social behavior, exploration, and neural responses to novel social stimuli. Spiny mouse pups were raised in the presence or absence of a non-kin breeding group. Upon adulthood, subjects underwent social interaction tests, an open field test, and a novel object test. Subjects were then exposed to a novel conspecific and novel group and neural responses were quantified via immunohistochemical staining in brain regions associated with social behavior. Early life social experience did not influence behavior in the test battery, but it did influence social processing. In animals exposed to non-kin during development, adult lateral septal neural responses toward a novel conspecific were weaker and hypothalamic neural responses toward a mixed-sex group were stronger. Communal species may exhibit robust behavioral resilience to the early life social environment. But the early life environment can affect how novel social information is processed in the brain during adulthood, with long-term consequences that are likely to shape their behavioral trajectory.

On the Evolutionary, Bio-Psychological Foundations of the Human-Animal Relationship

Ever since, people live in contact with nature and animals, even in relatively non-utilitarian ways. Erich Fromm and Edward Wilson termed this human universal "Biophilia". But why different species can live together in a social way, is explained by a "common social toolbox" of neural, psychological and physiologicalmechanisms, which evolved over phylogeny.Major components of this toolbox are found in the vertebrate brain, which evolved over the past 600 million years in a succession of key innovations and conservative preservation.The tegmental and diencephalic brain hosts a 450 million year old, structurally and functionally virtually unchanged "social network" which, in crosstalk with the mammalian prefrontal cortex or the analogous bird forebrain, enables complex social behaviour - within as well as between species. In addition, this toolbox features common principles of behavioural organization, including the expression and reading of emotions, as well as shared emotional, stress and calming systems. Such a common ground for social behaviour also explains the potential effectiveness of animal-assisted interventions in a wide range of pedagogic and therapeutic settings. However, positive effects aremostly revealed by experience and plausibility, whereas studies on animal- assisted activities and interventions according to biomedical scientific standards are still rare.

Social buffering of oxidative stress and cortisol in an endemic cyprinid fish

Fish exhibit complex social behaviours that can influence their stress levels and well-being. However, little is known about the link between social interactions and stress in wild fish, especially in running water environments. While many studies have explored the stress axis in fish, most have focused on specific social contexts, leaving gaps in understanding stress responses to social changes. Our study investigated collective behaviour and stress in wild Italian riffle dace (Telestes muticellus) in a controlled experimental setup simulating a natural river system. Results reveal that group-living fish have lower cortisol and oxidative stress levels in muscle tissue compared to solitary counterparts, suggesting a calming effect of conspecific presence. Additionally, we observed upregulated expression of antioxidant enzymes in group-living fish, indicating potential benefits to antioxidant defence systems. These insights shed light on the dynamic relationship between group behaviour and stress in wild fish within running water habitats and emphasise the use of multidisciplinary approaches.

Ecological Constraints and Drivers for Human Dispersals and Adaptations in the Late Pleistocene and Early Holocene Environments of the East Siberian Arctic

Starting roughly 50,000 years ago, the Arctic region of East Siberia remained continuously populated by groups of anatomically modern humans including the most uncomfortable episodes in the development of the late Quaternary environment; for some of them, human presence in the area became ephemeral. At present, archaeological fossil records allow for distinguishing three main stages in human occupation of the area: Early (~50 to ~29 ka, MIS 3), middle (~29 to ~11.7 ka, MIS 2), and late (from 11.7 to ~8 ka). For most of the time, they the populated open landscapes of the Mammoth Steppe, which declined at the onset of the Holocene. Human settlement of the Arctic was driven by various abiotic and biotic factors and thus archaeologically visible cardinal cultural and technological changes correspond to the most important paleoclimatic and habitat changes in the late Pleistocene and early Holocene. Successful peopling of the Arctic was largely facilitated by the adoption of critically important innovations such as sewing technology based on the use of the eyed bone needle and the manufacture of long shafts and pointed implements made of mammoth tusks. Mammoth exploitation is seen in mass accumulations of mammoths formed by hunting. An obvious connection between archaeological materials and such accumulations is observed in the archaeological record. In the lithic technology, the early stage is presented by archaic-looking flake industries. Starting the LGM, the wedge-core based-microblade technology known as the Beringian microblade tradition spread widely following the shrinkage of the mammoth range. At the late stage, starting at the Holocene boundary, microprismatic blade technology occurs. In all stages, the complex social behavior of the ancient Arctic settlers is revealed. The long-distance transport of products, knowledge, and genes occurs due to the introduction of the land transportation system. Initial human settlement of this region is associated with carriers of the West Eurasian genome who became replaced by the population with East Asian ancestry constantly moving North under the pressure of climate change.

5 Social perception and ability to evaluate sincerity of speech impacted by childhood hemispherectomy

Objective:Hemispherectomy (HE) is a surgical intervention to treat intractable epilepsy. It involves disconnecting or removing the right or left cerebral hemisphere, depending on the location of the pathological substrate or epileptogenic activity. HE impacts neural functions related to social cognition (Fournier et al., 2008). This study investigates the effects of childhood HE on social deception and sarcasm using the Thames Awareness of Social Inferences Task (TASIT; McDonald, Flanagan, & Rollins, 2010) to explore emotion identification and social inference appraisal as adults.Participants and Methods:Fifteen adults with hemispherectomy and 16 neurotypical controls completed the TASIT. All HE patients underwent hemispherectomy (right-HE = 10) during childhood (age of surgery = 3 months to 16 years) and had FSIQ > 70 at the time of study. HE and control groups were matched for age (HE M = 25.7, SD = 5.4; control M = 27.1, SD = 10.7) and education (HE M = 14.0, SD = 1.88; control M = 13.3, SD = 1.8). FSIQ was significantly lower in the HE group than control group (HE M= 90.8, SD = 9.4; control (M = 100.4, SD = 7.1). TASIT uses videotaped vignettes to assess aspects of social perception: emotion recognition (Part 1), social inference regarding sincerity, simple sarcasm, and paradoxical sarcasm (Part 2) and social inference regarding sincerity of speech (lie vs sarcasm) in the presence of additional text or visual cues (Part 3).Results:For Part 1, MANCOVA (covarying FSIQ) found no group difference in emotion identification. Analysis of data from Part 2 was conducted using repeated measures ANCOVA accounting for 2 groups x 3 conditions (sincere, simple sarcasm, and paradoxical sarcasm) and revealed only a significant overall group effect, F (1, 28) = 5.72, p = .024, np2 = .170. Likewise, analysis of Part 3 using repeated measures ANCOVA accounting for 2 groups x 2 cue types (visual, text) and 2 actor intentions (lie, sarcasm) revealed only a significant overall group effect, F (1,28) = 11.35, p = .002, np2 = .288, with no interaction of group by condition.Conclusions:HE patients exhibited no difficulty identifying basic emotional expressions. Performance was significantly impaired when additional social information was added to the context (i.e., detecting sarcasm or deception). HE patients begin to struggle with the complexity of new social information or how it changes the meaning of a conversation. Even simple sarcastic exchanges are difficult to interpret. When a visual or textual cue was introduced to reveal the true state of affairs, HE patients could not could integrate the information into their interpretations of the scenario. There are unique contributions of the left and right hemispheres to cognitive processes for complex social behavior, and absence of an entire hemisphere results in deficits in social language comprehension. Future research should investigate performance differences in left vs. right HE patients.

Ontogeny and social context regulate the circadian activity patterns of Lake Malawi cichlids

Activity patterns tend to be highly stereotyped and critical for executing many different behaviors including foraging, social interactions, and predator avoidance. Differences in the circadian timing of locomotor activity and rest periods can facilitate habitat partitioning and the exploitation of novel niches. As a consequence, closely related species often display highly divergent activity patterns, suggesting that shifts from diurnal to nocturnal behavior, or vice versa, are critical for survival. In Africa’s Lake Malawi alone, there are over 500 species of cichlids, which inhabit diverse environments and exhibit extensive phenotypic variation. We have previously identified a substantial range in activity patterns across adult Lake Malawi cichlid species, from strongly diurnal to strongly nocturnal. In many species, including fishes, ecological pressures differ dramatically across life-history stages, raising the possibility that activity patterns may change over ontogeny. To determine if rest-activity patterns change across life stages, we compared the locomotor patterns of six Lake Malawi cichlid species. While total rest and activity did not change between early juvenile and adult stages, rest-activity patterns did, with juveniles displaying distinct activity rhythms that are more robust than adults. One distinct difference between juveniles and adults is the emergence of complex social behavior. To determine whether social context is required for activity rhythms, we next measured locomotor behavior in group-housed adult fish. We found that when normal social interactions were allowed, locomotor activity patterns were restored, supporting the notion that social interactions promote circadian regulation of activity in adult fish. These findings reveal a previously unidentified link between developmental stage and social interactions in the circadian timing of cichlid activity.

Shaping the development of complex social behavior.

Early life experiences can have an enduring impact on the brain and behavior, with implications for stress reactivity, cognition, and social behavior. In particular, the neural systems that contribute to the expression of social behavior are altered by early life social environments. However, paradigms that have been used to alter the social environment during development have typically focused on exposure to stress, adversity, and deprivation of species-typical social stimulation. Here, we explore whether complex social environments can shape the development of complex social behavior. We describe lab-based paradigms for studying early life social complexity in rodents that are generally focused on enriching the social and sensory experiences of the neonatal and juvenile periods of development. The impact of these experiences on social behavior and neuroplasticity is highlighted. Finally, we discuss the degree to which our current approaches for studying social behavior outcomes give insight into "complex" social behavior and how social complexity can be better integrated into lab-based methodologies.

Object use in insects.

Insects are the most diverse group of organisms in the animal kingdom, and some species exhibit complex social behaviors. Although research on insect object use is still in its early stages, insects have already been shown to display rich object-use behaviors. This review focuses on patterns and behavioral flexibility in insect object-use behavior, and the role of cultural evolution in the development of object-use behaviors. Object use in insects is not widespread but has been documented in a diverse set of taxa. Some insects can use objects flexibly and display various object-use patterns. Like mammals and birds, insects use objects in diverse activities, including foraging, predator defense, courtship, and play. Intelligence, pre-existing manipulative behaviors, and anatomical structure affect innovations in object use. In addition, learning and imitation are the main mechanisms underlying the spread of object-use behaviors within populations. Given that insects are one of the major animal groups engaging in object use, studies of insect object use could provide general insights into object use in the animal kingdom.

A fossil "Social Stomach": Micro-CT imaging unearths first fossil record of ant proventriculi and comparative analysis with recent species.

Eusociality is an extreme form of social behavior found in some invertebrates, especially in ants, which allows them to thrive and dominate the environment through their cooperative and organized behavior. Their complex colony structure and social behavior is provided, among other things, by morphological adaptations, such as the unique structure and a huge variety of proventriculi relative to other insect groups. Here, we report the first discovery of proventriculus by X-ray microcomputed tomography (µCT)in the fossil ants †Oecophylla brischkei Mayr, 1868 and †Oecophylla crassinoda Wheeler, 1922. This is a remarkable fossil find, as it opens up new perspectives for research on phylogeny, the evolution of ant sociality and feeding behavior. We present a 3D model of the proventriculus in Oecophylla smaragdina (Fabricius, 1775) and a 3D model of the proventriculus in †Oe. brischkei and compare them. Fossil proventriculi are not fundamentally different in structure from the recent. Apparently, already in the late Eocene, the lifestyle and sociality of ants of the genus Oecophylla were similar to the one we are currently observing.

Genome analysis of a plasmid-bearing myxobacterim Myxococcus sp. strain MxC21 with salt-tolerant property.

Myxobacteria are widely distributed in various habitats of soil and oceanic sediment. However, it is unclear whether soil-dwelling myxobacteria tolerate a saline environment. In this study, a salt-tolerant myxobacterium Myxococcus sp. strain MxC21 was isolated from forest soil with NaCl tolerance >2% concentration. Under 1% salt-contained condition, strain MxC21 could kill and consume bacteria prey and exhibited complex social behaviors such as S-motility, biofilm, and fruiting body formation but adopted an asocial living pattern with the presence of 1.5% NaCl. To investigate the genomic basis of stress tolerance, the complete genome of MxC21 was sequenced and analyzed. Strain MxC21 consists of a circular chromosome with a total length of 9.13 Mbp and a circular plasmid of 64.3 kb. Comparative genomic analysis revealed that the genomes of strain MxC21 and M. xanthus DK1622 share high genome synteny, while no endogenous plasmid was found in DK1622. Further analysis showed that approximately 21% of its coding genes from the genome of strain MxC21 are predominantly associated with signal transduction, transcriptional regulation, and protein folding involved in diverse niche adaptation such as salt tolerance, which enables social behavior such as gliding motility, sporulation, and predation. Meantime, a high number of genes are also found to be involved in defense against oxidative stress and production of antimicrobial compounds. All of these functional genes may be responsible for the potential salt-toleration. Otherwise, strain MxC21 is the second reported myxobacteria containing indigenous plasmid, while only a small proportion of genes was specific to the circular plasmid of strain MxC21, and most of them were annotated as hypothetical proteins, which may have a direct relationship with the habitat adaptation of strain MxC21 under saline environment. This study provides an inspiration of the adaptive evolution of salt-tolerant myxobacterium and facilitates a potential application in the improvement of saline soil in future.

Neuroactive metabolites modulated by the gut microbiota in honey bees.

Honey bees have emerged as a new model to study the gut-brain axis, as they exhibit complex social behaviors and cognitive abilities, while experiments with gnotobiotic bees have revealed that their gut microbiota alters both brain and behavioral phenotypes. Furthermore, while honey bee brain functions supporting a broad range of behaviors have been intensively studied for over 50 years, the gut microbiota of bees has been experimentally characterized only recently. Here, we combined six published datasets from metabolomic analyses to provide an overview of the neuroactive metabolites whose abundance in the gut, hemolymph and brain varies in presence of the gut microbiota. Such metabolites may either be produced by gut bacteria, released from the pollen grains during their decomposition by bacteria, or produced by other organs in response to different bacterial products. We describe the current state of knowledge regarding the impact of such metabolites on brain function and behavior and provide further hypotheses to explore in this emerging field of research.

Hormonal gatekeeping via the blood-brain barrier governs caste-specific behavior in ants

Here, we reveal an unanticipated role of the blood-brain barrier (BBB) in regulating complex social behavior in ants. Using scRNA-seq, we find localization in the BBB of a key hormone-degrading enzyme called juvenile hormone esterase (Jhe), and we show that this localization governs the level of juvenile hormone (JH3) entering the brain. Manipulation of the Jhe level reprograms the brain transcriptome between ant castes. Although ant Jhe is retained and functions intracellularly within the BBB, we show that Drosophila Jhe is naturally extracellular. Heterologous expression of ant Jhe into the Drosophila BBB alters behavior in fly to mimic what is seen in ants. Most strikingly, manipulation of Jhe levels in ants reprograms complex behavior between worker castes. Our study thus uncovers a remarkable, potentially conserved role of the BBB serving as a molecular gatekeeper for a neurohormonal pathway that regulates social behavior.

Mental Health and Aggression in Indonesian Women.

Aggression is a global problem and complex social behavior. In Indonesia, some common manifestations of aggression are sexual harassment, domestic violence, and the stigmatization of other people. However, unlike men, aggression in women is still rarely studied, whereas facts find that many conditions can make women more vulnerable. There are various aspects related to biological, psychological, social, and cultural issues that can potentially provoke female aggression. Furthermore, mental health and aggression are often viewed as an automatic association and are inseparable in society, reinforcing the stigma against people with mental problems, particularly women, who tend to suffer more stigma of mental health issues than men. However, there has not yet been a study explicitly related to this relationship in the general population of women. The current study aims to examine the overall relationship between mental health and aggression in the extensive general population of Indonesian women with various mental conditions ranging from a normal mental state to severe mental health problems. This was a cross-sectional study conducted using uncontrolled quota sampling via distributing online self-report questionnaires, the modified Indonesian version instruments of the Brief Symptoms Rating Scale-5, and the Buss Aggression Scale with high internal consistency. This study among 203 women aged 19-67 in Indonesia, a multicultural nation and the fourth densest country in the world, proposes that mental health can be a predictor of aggressive behavior, with the influence of mental health on the aggression of women being 21.6% only. The finding indicates that mental health issues are not a macro contributing factor to women's aggressiveness in society and may help reduce stigma against women with mental health problems.

Molecular signature of excessive female aggression: study of stressed mice with genetic inactivation of neuronal serotonin synthesis

Aggression is a complex social behavior, critically involving brain serotonin (5-HT) function. The neurobiology of female aggression remains elusive, while the incidence of its manifestations has been increasing. Yet, animal models of female aggression are scarce. We previously proposed a paradigm of female aggression in the context of gene x environment interaction where mice with partial genetic inactivation of tryptophan hydroxylase-2 (Tph2+/− mice), a key enzyme of neuronal 5-HT synthesis, are subjected to predation stress resulting in pathological aggression. Using deep sequencing and the EBSeq method, we studied the transcriptomic signature of excessive aggression in the prefrontal cortex of female Tph2+/− mice subjected to rat exposure stress and food deprivation. Challenged mutants, but not other groups, displayed marked aggressive behaviors. We found 26 genes with altered expression in the opposite direction between stressed groups of both Tph2 genotypes. We identified several molecular markers, including Dgkh, Arfgef3, Kcnh7, Grin2a, Tenm1 and Epha6, implicated in neurodevelopmental deficits and psychiatric conditions featuring impaired cognition and emotional dysregulation. Moreover, while 17 regulons, including several relevant to neural plasticity and function, were significantly altered in stressed mutants, no alteration in regulons was detected in stressed wildtype mice. An interplay of the uncovered pathways likely mediates partial Tph2 inactivation in interaction with severe stress experience, thus resulting in excessive female aggression.

Reciprocity in Dyads and Triads: Female Rats Alter Their Prosocial Behavior According to the Social Context

Recognizing and appropriately responding to others' helpful actions are critical components of social cognition and reciprocity. This ability has been well-documented in various species where animals differentiate between experimenters who are “unwilling” versus “unable” to provide help, but it is unclear if this ability extends to rats. The present studies investigate the prosocial decision-making behavior of female rats in response to the prior actions of another rat in both triadic and dyadic social contexts. In Experiment One, an "actor" rat repeatedly pressed a lever to open a restrainer door, enabling a trapped conspecific to access food. Consistent with reciprocity, when the roles were reversed, the previously trapped conspecific helped the actor. In Experiments Two and Three, the actor rat's ability to open the door was manipulated, with some trials where the door was blocked and the actor was unable to open it and some trials where the actor was able to, but rarely opened the door. In the triadic context, the previously trapped rat then had the opportunity to help the actor, a neutral control, both, or neither (Experiment Two). In the dyadic context, the previously trapped rat could then help the actor (Experiment Three). Reciprocity was not observed in the triadic context. However, unexpectedly, relative to a neutral control conspecific, rats showed a stronger preference for the less helpful actor compared to the helpful or unable actor. In contrast, in the dyadic context, rats did show reciprocity and displayed a higher propensity to help the helpful or unable actor compared to the less helpful actor. These findings shed light on rats' complex social behavior and highlight the context-dependent nature of their helping behavior.