The spatial and temporal structure of neural activity across the fly brain.

What are the spatial and temporal scales of brainwide neuronal activity? We used swept, confocally-aligned planar excitation (SCAPE) microscopy to image all cells in a large volume of the brain of adult Drosophila with high spatiotemporal resolution while flies engaged in a variety of spontaneous behaviors. This revealed neural representations of behavior on multiple spatial and temporal scales. The activity of most neurons correlated (or anticorrelated) with running and flailing over timescales that ranged from seconds to a minute. Grooming elicited a weaker global response. Significant residual activity not directly correlated with behavior was high dimensional and reflected the activity of small clusters of spatially organized neurons that may correspond to genetically defined cell types. These clusters participate in the global dynamics, indicating that neural activity reflects a combination of local and broadly distributed components. This suggests that microcircuits with highly specified functions are provided with knowledge of the larger context in which they operate.

Trichotillomania: a perspective synthesised from neuroscience and lived experience.

Trichotillomania, or hair-pulling disorder, is one of a family of disorders called body-focused repetitive behaviours (BFRBs), which also include disordered skin-picking (dermotillomania) and nail-biting (onychophagia). The disorders affect 1%-2% of the population, cause high levels of distress and have high levels of comorbidity with other psychiatric diagnoses. The key facts and figures are briefly reviewed and some important points are further explored: (1) BFRBs are associated with psychological distress, but are distinct from other diagnoses, (2) The pathological behaviours mirror excessive self-grooming behaviours in other species, and may relate to immune-system mediated feedback loops, and (3) The resulting behaviours are stigmatised and cause intense shame and isolation for those who suffer, which might in itself maintain the feedback loop. These observations lead to the hypothesis that the core disorder is one of pathological grooming, which may have a basis in an immune response, with shame being both a consequence and a maintainer of the disorder. The major barrier to testing the hypotheses and potential interventions remains the stigma that keeps these disorders, and those who suffer from them, in the shadows.

The emerging complexity of molecular pathways implicated in mouse self-grooming behavior.

Rodent self-grooming is an important complex behavior, and its deficits are translationally relevant to a wide range of neuropsychiatric disorders. Here, we analyzed a comprehensive dataset of 227 genes whose mutations are known to evoke aberrant self-grooming in mice. Using these genes, we constructed the network of their established protein-protein interactions (PPI), yielding several distinct molecular clusters related to postsynaptic density, the Wnt signaling, transcription factors, neuronal cell cycle, NOS neurotransmission, microtubule regulation, neuronal differentiation/trafficking, neurodevelopment and mitochondrial function. Utilizing further bioinformatics analyses, we also identified novel central ('hub') proteins within these clusters, whose genes may also be implicated in aberrant self-grooming and other repetitive behaviors in general. Untangling complex molecular pathways of this important behavior using in silico approaches contributes to our understanding of related neurological disorders, and may suggest novel potential targets for their pharmacological or gene therapy.

Behavioural, demographic and fitness consequences of social instability in cooperatively breeding dwarf mongoose groups.

Social instability frequently arises in group-living species, but the potential costs have rarely been investigated in free-living cooperative breeders, especially across different timeframes. Using natural observations, body mass measurements and life-history data from dwarf mongooses (Helogale parvula), we determined the short- and long-term consequences of a change in one of the dominant breeding pairs. We found that a new breeder led to alterations in both collective and individual behaviours (i.e. increases in communal scent-marking, engagement in intergroup interactions, sentinel activity and within-group grooming), as well as reduced body mass gain, further demographic changes and decreased reproductive success (i.e. fewer pups surviving to adulthood). The effects were particularly apparent when it was the female breeder who changed; new female breeders were younger than more experienced counterparts. Our findings support the idea that stability and cooperation are strongly linked and provide potential reasons for previously documented health and fitness benefits of social stability.

Impact of dominance rank specification in dyadic interaction models.

Dominance rank is a vital descriptor of social dynamics in animal societies and regularly used in studies to explain observed interaction patterns. However, researchers can choose between different indices and standardizations, and can specify dyadic rank relations differently when studying interaction distributions. These researcher degrees of freedom potentially introduce biases into studies and reduce replicability. Here, I demonstrate the impact of researcher choices by comparing the performance of different combinations of rank index, standardization, and model specification when explaining dyadic interaction patterns in sooty mangabeys (Cercocebus atys atys). I show that while no combination consistently performed best across interaction types (aggression, grooming, proximity, supplants), model specifications allowing for nonlinear patterns performed better than other models on average. Choices made in pre-processing and model building impacted model performance and subsequent interpretation of results. Researchers could end up describing social systems differently based on the same data. These results highlight the impact of researcher choices in the processing of behavioural data and potential limitations when using indirect species comparisons in animal behaviour research. To increase repeatability, researchers could make the impact of their processing choices more transparent and report results using a variety of indices and model specifications.

Real-Time Recognition and Detection of Bactrocera minax (Diptera: Trypetidae) Grooming Behavior Using Body Region Localization and Improved C3D Network.

Pest management has long been a critical aspect of crop protection. Insect behavior is of great research value as an important indicator for assessing insect characteristics. Currently, insect behavior research is increasingly based on the quantification of behavior. Traditional manual observation and analysis methods can no longer meet the requirements of data volume and observation time. In this paper, we propose a method based on region localization combined with an improved 3D convolutional neural network for six grooming behaviors of Bactrocera minax: head grooming, foreleg grooming, fore-mid leg grooming, mid-hind leg grooming, hind leg grooming, and wing grooming. The overall recognition accuracy reached 93.46%. We compared the results obtained from the detection model with manual observations; the average difference was about 12%. This shows that the model reached a level close to manual observation. Additionally, recognition time using this method is only one-third of that required for manual observation, making it suitable for real-time detection needs. Experimental data demonstrate that this method effectively eliminates the interference caused by the walking behavior of Bactrocera minax, enabling efficient and automated detection of grooming behavior. Consequently, it offers a convenient means of studying pest characteristics in the field of crop protection.

Opportunistic availability of an infant and social relationship to a mother influence grooming before infant handling in Japanese macaques.

Biological market theory (BMT) predicts that the balance between supply and demand determines the economic value of a "commodity," which consequently determines the amount of "services" that an individual needs to provide to obtain the commodity. In infant handling among primates, the existing literature suggests that handlers need to groom a mother to obtain access to its infant, particularly when the value of the infant is high (e.g., when the number of infants is low). However, grooming by handlers may not be a prerequisite for the occurrence of infant handling, because handlers can handle an infant that is separated from its mother. Based on 3 years of behavioral observations of wild Japanese macaques (Macaca fuscata), we examined the process by which infant handling occurs and the role of grooming in infant handling. We found that infant handling occurred more frequently when the mother and infant were separated than when they were in contact. Grooming rarely occurred before infant handling. The subsequent occurrence of infant handling was not predicted by either the occurrence or duration of grooming toward mothers by non-mother individuals. Grooming by handlers was also more likely to occur when an infant was in contact with its mother and when an infant's mother was dominant to the handlers. Contrary to BMT, the number of infants in a group did not affect grooming by handlers. These results indicate that the handlers' decision to groom depended on the opportunistic availability of an infant and the social relationship between the infant's mother and themselves. We conclude that grooming was not always necessary for infant handling.

EFFECTS OF MYCOPLASMA GALLISEPTICUM INFECTION ON PREENING BEHAVIORS AND FEATHER QUALITY IN HOUSE FINCHES (HAEMORHOUS MEXICANUS).

Infections can have far-reaching sublethal effects on wildlife, including reduced maintenance of external structures. For many wildlife taxa, daily maintenance of external structures (termed preening in birds) is critical to fitness, but few studies have examined how infections alter such maintenance. Mycoplasma gallisepticum is a common pathogen in free-living House Finches (Haemorhous mexicanus), where it causes mycoplasmal conjunctivitis. Despite documented behavioral changes associated with M. gallisepticum infections in finches, no studies have examined how preening behavior may change with infection and how potential differences in preening may affect feather quality. To test this, we experimentally inoculated captive House Finches with M. gallisepticum or a control treatment, and we collected behavioral and feather quality data to detect potential changes in feather maintenance due to infection. We found that finches infected with M. gallisepticum preened significantly less often, and within the infected treatment, birds with the highest conjunctivitis severity preened the least often. However, there was no difference in the quality scores for secondary flight feathers collected from control versus infected birds. We also assayed feather water retention and found that the degree of water retention correlated with our feather quality scores, such that feathers with poor scores retained more water. However, as with quality scores, feather water retention did not differ with infection; this may be due to the controlled environment that the birds experienced while in captivity. Our data suggest that, in addition to sickness behaviors previously observed in finches, M. gallisepticum infection decreases other behaviors critical to survival, such as preening. While the consequences of reduced preening on feather maintenance were not apparent in captive conditions, further work is needed to determine whether House Finches in the wild that are infected with M. gallisepticum experience a fitness cost, such as increases in ectoparasite loads, due to this reduced feather maintenance.

A groom with a view.

Mapping mouse grooming episodes to neural activity shows that striatal cells deep in the brain collectively represent key aspects of self-grooming.

DOES PREENING BEHAVIOR REDUCE THE PREVALENCE OF AVIAN FEATHER LICE (PHTHIRAPTERA: ISCHNOCERA)?

Animals defend themselves against parasites in many ways. Defenses, such as physiological immune responses, are capable of clearing some infections. External parasites that do not feed on blood, however, are not controlled by the physiological immune system. Instead, ectoparasites like feather-feeding lice (Phthiraptera: Ischnocera) are primarily controlled by behavioral defenses such as preening. Here we test the hypothesis that birds able to preen are capable of clearing infestations of feather lice. We experimentally manipulated preening ability in a captive population of rock pigeons (Columba livia) that were infested with identical numbers of feather lice (Columbicola columbae or Campanulotes compar or both). We then monitored the feather louse infestations for 42 wk. Birds with impaired preening remained infested throughout the experiment; in contrast, the prevalence of lice on birds that could preen normally decreased by 50%. These data indicate that it is indeed possible for birds to clear themselves of feather lice, and perhaps other ectoparasites, by preening. We note, however, that captive birds spend more time preening than wild birds, and that they are less likely to be reinfested than wild birds. Thus, additional studies are necessary to determine under what circumstances wild birds can clear themselves of ectoparasites by preening.

Genetic variance and indirect genetic effects for affiliative social behavior in a wild primate.

Affiliative social behaviors are linked to fitness components in multiple species. However, the role of genetic variance in shaping such behaviors remains largely unknown, limiting our understanding of how affiliative behaviors can respond to natural selection. Here, we employed the "animal model" to estimate environmental and genetic sources of variance and covariance in grooming behavior in the well-studied Amboseli wild baboon population. We found that the tendency for a female baboon to groom others ("grooming given") is heritable (h2 = 0.22 ± 0.048), and that several environmental variables-including dominance rank and the availability of kin as grooming partners-contribute to variance in this grooming behavior. We also detected small but measurable variance due to the indirect genetic effect of partner identity on the amount of grooming given within dyadic grooming partnerships. The indirect and direct genetic effects for grooming given were positively correlated (r = 0.74 ± 0.09). Our results provide insight into the evolvability of affiliative behavior in wild animals, including the possibility for correlations between direct and indirect genetic effects to accelerate the response to selection. As such they provide novel information about the genetic architecture of social behavior in nature, with important implications for the evolution of cooperation and reciprocity.

Behavioral responses of solicitors after failure to receive grooming in Macaca fuscata.

Grooming is one of the most common cooperative behaviors among several animal species. However, the tactics used to cope with uncooperative partners in grooming interactions remain unclear. Japanese macaques (Macaca fuscata) solicit grooming from partners through postural behaviors, but may not necessarily receive grooming. This study investigated the behavior of female Japanese macaques after they solicited but did not receive grooming. We predicted that unsuccessful solicitors would engage in grooming interactions with uncooperative partners if they were affiliated. If they were not affiliated, the solicitors would not do so and may seek grooming interactions with other grooming partners. We used a focal-animal sampling method, targeting 17 females at Katsuyama, Okayama Prefecture, Japan. We recognized affiliative relationships by measuring close spatial association. After unsuccessful solicitation, females tended to scratch themselves, suggesting that solicitors may experience anxiety or distress when they do not receive grooming. They also tended to be proximate with affiliated partners after solicitation, regardless of whether the solicitors received grooming from their partners. In contrast, when solicitors failed to receive grooming from unaffiliated partners, their subsequent proximity was lower than when they were groomed. Moreover, unsuccessful solicitors were likely to engage in grooming interactions with affiliated partners who were uncooperative (receivers of unsuccessful solicitations). However, they were less likely to engage in grooming interactions with unaffiliated partners and instead engaged in grooming interactions with other nearby partners. These findings indicate that female Japanese macaques decide whether to engage in grooming interactions with uncooperative partners who have not groomed solicitors based on affiliative relationships and the availability of other grooming partners. It is probable that, when the cost of searching for a grooming partner is low, female Japanese macaques are likely to switch partners, potentially leading to an increase in the benefits obtained from grooming interactions.

Multi-group analysis of grooming network position in a highly social primate.

Individual variation in complex social behavioral traits, like primate grooming, can be influenced by the characteristics of the individual and those of its social group. To better grasp this complexity, social network analysis can be used to quantify direct and indirect grooming relationships. However, multi-group social network studies remain rare, despite their importance to disentangle individual from group-level trait effects on grooming strategies. We applied social network analysis to grooming data of 22 groups of zoo-housed bonobos and investigated the impact of three individual (sex, age, and rearing-history) and two group-level traits (group size and sex ratio) on five social network measures (out-strength, in-strength, disparity, affinity, and eigenvector centrality). Our results showed age-effects on all investigated measures: for females, all measures except for affinity showed quadratic relationships with age, while in males, the effects of age were more variable depending on the network measure. Bonobos with atypical rearing histories showed lower out-strength and eigenvector centrality, while in-strength was only impacted by rearing history in males. Group size showed a negative association with disparity and eigenvector centrality, while sex ratio did not influence any of the investigated measures. Standardization for group size did not impact the effects of sex and age, indicating the robustness of these findings. Our study provides comprehensive insights into the complexity of grooming behavior in zoo-housed bonobos, and underlines the importance of multi-group analyses for the generalizability of social network analysis results for species as a whole.

Consistency of limb preference across unimanual feeding, bipedal locomotion, and social grooming in golden snub-nosed monkeys (Rhinopithecus roxellana).

The golden snub-nosed monkey (Rhinopithecus roxellana) is a typical arboreal group-living Old World primate. While limb preference has been extensively studied in this species, limb preference consistency has not yet been explored. Here, based on 26 R. roxellana adults, we investigated whether individuals exhibit consistent motor biases in manual- (e.g., unimanual feeding and social grooming) and foot-related (e.g., bipedal locomotion) tasks and whether limb preference consistency is influenced by increased social interactions during social grooming. Results showed no consistency in the direction or strength of limb preference among tasks, except for lateral strength in handedness for unimanual feeding and footedness in the initiation of locomotion. Population-level foot preference was only found among right-handers. Marked lateral bias was found in unimanual feeding, indicating that it may be a sensitive behavioural measure for assessing manual preference, especially for provisioned populations. This study not only improves our understanding of the relationship between hand and foot preference in R. roxellana but also reveals potential differential hemispheric regulation of limb preference and the influence of increased social interaction on handedness consistency.

Grooming Time Predicts Survival: American Kestrels, Falco sparverius, on a Subtropical Island.

AbstractAnimals have evolved a variety of adaptations to care for their body surfaces, such as grooming behavior, which keeps the integument clean, parasite-free, and properly arranged. Despite extensive research on the grooming of mammals, birds, and arthropods, the survival value of grooming has never been directly measured in natural populations. We monitored grooming and survival in a population of marked American kestrels (Falco sparverius) on San Salvador Island, Bahamas. We found a strong association between time spent grooming and survival over a 2-year period. The quadratic relationship we show is consistent with stabilizing natural selection on grooming time. To our knowledge, this is the first evidence for a correlation between grooming time and survival in a natural population. Grooming time may predict the survival of many animal taxa, but additional studies are needed to determine the shape and strength of the relationship among birds, mammals, and arthropods.

Disruption of Astrocyte-Dependent Dopamine Control in the Developing Medial Prefrontal Cortex Leads to Excessive Grooming in Mice.

BACKGROUND: Astrocytes control synaptic activity by modulating perisynaptic concentrations of ions and neurotransmitters including dopamine (DA) and, as such, could be involved in the modulating aspects of mammalian behavior. METHODS: We produced a conditional deletion of the vesicular monoamine transporter 2 (VMAT2) specifically in astrocytes (aVMTA2cKO mice) and studied the effects of the lack of VMAT2 in prefrontal cortex (PFC) astrocytes on the regulation of DA levels, PFC circuit functions, and behavioral processes. RESULTS: We found a significant reduction of medial PFC (mPFC) DA levels and excessive grooming and compulsive repetitive behaviors in aVMAT2cKO mice. The mice also developed a synaptic pathology, expressed through increased relative AMPA versus NMDA receptor currents in synapses of the dorsal striatum receiving inputs from the mPFC. Importantly, behavioral and synaptic phenotypes were rescued by re-expression of mPFC VMAT2 and L-DOPA treatment, showing that the deficits were driven by mPFC astrocytes that are critically involved in developmental DA homeostasis. By analyzing human tissue samples, we found that VMAT2 is expressed in human PFC astrocytes, corroborating the potential translational relevance of our observations in mice. CONCLUSIONS: Our study shows that impairment of the astrocytic control of DA in the mPFC leads to symptoms resembling obsessive-compulsive spectrum disorders such as trichotillomania and has a profound impact on circuit function and behaviors.

Show me your best side: Lateralization of social and resting behaviors in feral horses.

Growing evidence shows a variety of sensorial and motor asymmetries in social and non-social interactions in various species, indicating a lateralized processing of information by the brain. Using digital video cameras on tripods and drones, this study investigated lateralization in frequency and duration of social behavior patterns, in affiliative, agonistic, and resting contexts, in a feral population of horses (Equus ferus caballus) in Northern Portugal, consisting of 37 individuals organized in eight harem groups. Affiliative interactions (including grooming) were more often performed, and lasted longer, when recipients were positioned to the right side. In recumbent resting (animals lying down) episodes on the left side lasted longer. Our results of an affiliative behavior having a right side tendency, provide partial support to the valence-specific hypothesis of Ahern and Schwartz (1979) - left hemisphere dominance for positive affect, affiliative behaviors. Longer recumbent resting episodes on the left side may be due to synchronization. However, in both instances it is discussed how lateralization may be context dependent. Investigating the position asymmetries of social behaviors in feral equids will contribute to a better understanding of differential lateralization and hemispheric specialization from the ecological and evolutionary perspectives.

Chimpanzee communities differ in their inter- and intrasexual social relationships.

Male and female human social bonding strategies are culturally shaped, in addition to being genetically rooted. Investigating nonhuman primate bonding strategies across sex groups allows researchers to assess whether, as with humans, they are shaped by the social environment or whether they are genetically predisposed. Studies of wild chimpanzees show that in some communities males have strong bonds with other males, whereas in others, females form particularly strong intrasex bonds, potentially indicative of cultural differences across populations. However, excluding genetic or ecological explanations when comparing different wild populations is difficult. Here, we applied social network analysis to examine male and female social bonds in two neighbouring semiwild chimpanzee groups of comparable ecological conditions and subspecies compositions, but that differ in demographic makeup. Results showed differences in bonding strategies across the two groups. While female-female party co-residence patterns were significantly stronger in Group 1 (which had an even distribution of males and females) than in Group 2 (which had a higher proportion of females than males), there were no such differences for male-male or male-female associations. Conversely, female-female grooming bonds were stronger in Group 2 than in Group 1. We also found that, in line with captive studies but contrasting research with wild chimpanzees, maternal kinship strongly predicted proximity and grooming patterns across the groups. Our findings suggest that, as with humans, male and female chimpanzee social bonds are influenced by the specific social group they live in, rather than predisposed sex-based bonding strategies.

Pathogen-associated grooming.

A fungal surface protein elicits grooming in flies.

Pathogen evasion of social immunity.

Treating sick group members is a hallmark of collective disease defence in vertebrates and invertebrates alike. Despite substantial effects on pathogen fitness and epidemiology, it is still largely unknown how pathogens react to the selection pressure imposed by care intervention. Using social insects and pathogenic fungi, we here performed a serial passage experiment in the presence or absence of colony members, which provide social immunity by grooming off infectious spores from exposed individuals. We found specific effects on pathogen diversity, virulence and transmission. Under selection of social immunity, pathogens invested into higher spore production, but spores were less virulent. Notably, they also elicited a lower grooming response in colony members, compared with spores from the individual host selection lines. Chemical spore analysis suggested that the spores from social selection lines escaped the caregivers' detection by containing lower levels of ergosterol, a key fungal membrane component. Experimental application of chemically pure ergosterol indeed induced sanitary grooming, supporting its role as a microbe-associated cue triggering host social immunity against fungal pathogens. By reducing this detection cue, pathogens were able to evade the otherwise very effective collective disease defences of their social hosts.