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Behavioral differences can be observed between species or populations (variation) or between individuals in a genetically similar population (variability). Here, we investigate genetic differences as a possible source of variation and variability in Drosophila grooming. Grooming confers survival and social benefits. Grooming features of five Drosophila species exposed to a dust irritant were analyzed. Aspects of grooming behavior, such as anterior to posterior progression, were conserved between and within species. However, significant differences in activity levels, proportion of time spent in different cleaning movements, and grooming syntax were identified between species. All species tested showed individual variability in the order and duration of action sequences. Genetic diversity was not found to correlate with grooming variability within a species: melanogaster flies bred to increase or decrease genetic heterogeneity exhibited similar variability in grooming syntax. Individual flies observed on consecutive days also showed grooming sequence variability. Standardization of sensory input using optogenetics reduced but did not eliminate this variability. In aggregate, these data suggest that sequence variability may be a conserved feature of grooming behavior itself. These results also demonstrate that large genetic differences result in distinguishable grooming phenotypes (variation), but that genetic heterogeneity within a population does not necessarily correspond to an increase in the range of grooming behavior (variability).
The brain coordinates the movements that constitute behavior, but how descending neurons convey the myriad of commands required to activate the motor neurons of the limbs in the right order and combinations to produce those movements is not well understood. For anterior grooming behavior in the fly, we show that its component head sweeps and leg rubs can be initiated separately, or as a set, by different descending neurons. Head sweeps and leg rubs are mutually exclusive movements of the front legs that normally alternate, and we show that circuits in the ventral nerve cord as well as in the brain can resolve competing commands. Finally, the left and right legs must work together to remove debris. The coordination for leg rubs can be achieved by unilateral activation of a single descending neuron, while a similar manipulation of a different descending neuron decouples the legs to produce single-sided head sweeps. Taken together, these results demonstrate that distinct descending neurons orchestrate the complex alternation between the movements that make up anterior grooming.
Self-grooming plays an essential role in hygiene maintenance, thermoregulation, and stress response. However, the neural populations involved in self-grooming remain largely unknown. The paraventricular hypothalamic nucleus (PVH) has been implicated in the regulation of self-grooming. Arginine vasopressin-producing neurons are among the major neuronal populations in the PVH (PVHAVP), which play important roles in water homeostasis, blood pressure regulation, feeding, and stress response. Here, we report the critical role of PVHAVP neurons in the induction of self-grooming. Optogenetic activation of PVHAVP neurons immediately induced self-grooming in freely moving mice. Chemogenetic activation of these neurons also increased time spent self-grooming. In contrast, their chemogenetic inhibition significantly reduced naturally occurring self-grooming, suggesting that PVHAVP-induced grooming has physiological relevance. Notably, optogenetic activation of PVHAVP neurons triggered self-grooming over other adaptive behaviors, such as voracious feeding induced by fasting and social interaction with female mice. Thus, our study proposes the novel role of PVHAVP neurons in regulating self-grooming behavior and, consequently, hygiene maintenance and stress response. Furthermore, uncontrolled activation of these neurons may be potentially relevant to diseases characterized by compulsive behaviors and impaired social interaction, such as autism, obsessive-compulsive disorder, and anorexia nervosa.
Animals perform many stereotyped movements, but how nervous systems are organized for controlling specific movements remains unclear. Here we use anatomical, optogenetic, behavioral, and physiological techniques to identify a circuit in Drosophila melanogaster that can elicit stereotyped leg movements that groom the antennae. Mechanosensory chordotonal neurons detect displacements of the antennae and excite three different classes of functionally connected interneurons, which include two classes of brain interneurons and different parallel descending neurons. This multilayered circuit is organized such that neurons within each layer are sufficient to specifically elicit antennal grooming. However, we find differences in the durations of antennal grooming elicited by neurons in the different layers, suggesting that the circuit is organized to both command antennal grooming and control its duration. As similar features underlie stimulus-induced movements in other animals, we infer the possibility of a common circuit organization for movement control that can be dissected in Drosophila.
Grooming is a common behavior for animals to care for their fur, maintain hygiene, and regulate body temperature. Since various factors, including stressors and genetic mutations, affect grooming quantitatively and qualitatively, the assessment of grooming is important to understand the status of experimental animals. However, current grooming detection methods are time-consuming, laborious, and require specialized equipment. In addition, they generally cannot discriminate grooming microstructures such as face washing and body licking. In this study, we aimed to develop an automated grooming detection method that can distinguish facial grooming from body grooming by image analysis using artificial intelligence. Mouse behavior was recorded using a standard hand camera. We carefully observed videos and labeled each time point as facial grooming, body grooming, and not grooming. We constructed a three-dimensional convolutional neural network (3D-CNN) and trained it using the labeled images. Since the output of the trained 3D-CNN included unlikely short grooming bouts and interruptions, we set posterior filters to remove them. The performance of the trained 3D-CNN and filters was evaluated using a first-look dataset that was not used for training. The sensitivity of facial and body grooming detection reached 81.3% and 91.9%, respectively. The positive predictive rates of facial and body grooming detection were 83.5% and 88.5%, respectively. The number of grooming bouts predicted by our method was highly correlated with human observations (face: r = 0.93, body: r = 0.98). These results highlight that our method has sufficient ability to distinguish facial grooming and body grooming in mice.
The striatum comprises multiple subdivisions and neural circuits that differentially control motor output. The islands of Calleja (IC) contain clusters of densely packed granule cells situated in the ventral striatum, predominantly in the olfactory tubercle (OT). Characterized by expression of the D3 dopamine receptor, the IC are evolutionally conserved, but have undefined functions. Here, we show that optogenetic activation of OT D3 neurons robustly initiates self-grooming in mice while suppressing other ongoing behaviors. Conversely, optogenetic inhibition of these neurons halts ongoing grooming, and genetic ablation reduces spontaneous grooming. Furthermore, OT D3 neurons show increased activity before and during grooming and influence local striatal output via synaptic connections with neighboring OT neurons (primarily spiny projection neurons), whose firing rates display grooming-related modulation. Our study uncovers a new role of the ventral striatum's IC in regulating motor output and has important implications for the neural control of grooming.
Grooming behaviour is the most common innate behaviour in animals. In rodents, it consists of sequences of movements organized in four phases, executed symmetrically on both sides of the animal and creating a syntactic chain of behavioural events. The grooming syntax can be altered by stress and novelty, as well as by several mutations and brain lesions. Grooming behaviour is known to be affected by alterations of the dopamine system, including dopamine receptor modulation, dopamine alteration in genetically modified animals, and after brain lesion. While a lot is known about the initiation and syntactic modifications of this refined sequence of movements, effects of unilateral lesion of dopamine neurons are unclear particularly regarding the symmetry of syntactic chains. In the present work we studied grooming in mice unilaterally lesioned in the medial forebrain bundle by 6-hydroxydopamine. We found a reduction in completion of grooming bouts, associated with reduction in number of transitions between grooming phases. The data also revealed the development of asymmetry in grooming behaviour, with reduced tendency to groom the contralateral side to the lesion. Symmetry was recovered following treatment with L-DOPA. Thus, the present work shows that unilateral lesion of dopamine neurons reduces self-grooming behaviour by affecting duration and numbers of events. It produces premature discontinuation of grooming chains but the sequence syntax remains correct. This deficient grooming could be considered as an intrinsic symptom of Parkinson's disease in animal models and could present some similarities with abnormalities of motor movement sequencing seen in patients. Our study also suggests grooming analysis as an additional method to screen parkinsonism in animal models.
Prolonged exposure to negative stressors could be harmful if a subject cannot respond appropriately. Strategies evolved to respond to stress, including repetitive displacement behaviours, are important in maintaining behavioural homoeostasis. In rodents, self-grooming is a frequently observed repetitive behaviour believed to contribute to post-stress de-arousal with adaptive value. Here we identified a rat limbic di-synaptic circuit that regulates stress-induced self-grooming with positive affective valence. This circuit links hippocampal ventral subiculum to ventral lateral septum (LSv) and then lateral hypothalamus tuberal nucleus. Optogenetic activation of this circuit triggers delayed but robust excessive grooming with patterns closely resembling those evoked by emotional stress. Consistently, the neural activity of LSv reaches a peak before emotional stress-induced grooming while inhibition of this circuit significantly suppresses grooming triggered by emotional stress. Our results uncover a previously unknown limbic circuitry involved in regulating stress-induced self-grooming and pinpoint a critical role of LSv in this ethologically important behaviour.
Emerging evidence suggest that appetite-regulating peptides modulate social behaviors. We here investigate whether the anorexigenic peptide neuromedin U (NMU) modulates sexual behavior in male mice. However, instead of modulating sexual behaviors, NMU administered into the third ventricle increased self-grooming behavior. In addition, NMU-treatment increased self-grooming behavior when exposed to other mice or olfactory social-cues, but not when exposed to non-social environments. As the neuropeptide oxytocin is released during social investigation and exogenous oxytocin induces self-grooming, its role in NMU-induced self-grooming behavior was investigated. In line with our hypothesis, the oxytocin receptor antagonist inhibited NMU-induced self-grooming behavior in mice exposed to olfactory social-cues. Moreover, dopamine in the mesocorticolimbic system is known to be a key regulator of self-grooming behavior. In line with this, we proved that infusion of NMU into nucleus accumbens increased self-grooming behavior in mice confronted with an olfactory social-cue and that this behavior was inhibited by antagonism of dopamine D2, but not D1/D5, receptors. Moreover repeated NMU treatment enhanced ex vivo dopamine levels and decreased the expression of dopamine D2 receptors in nucleus accumbens in socially housed mice. On the other hand, the olfactory stimuli-dependent NMU-induced self-grooming was not affected by a corticotrophin-releasing hormone antagonist, and NMU-treatment did not influence repetitive behaviors in the marble burying test. In conclusion, our results suggest that NMU treatment and, social cues - potentially triggering oxytocin release - together induce excessive grooming behavior in male mice. The mesolimbic dopamine system, including accumbal dopamine D2 receptors, was identified as a crucial downstream mechanism.
In many behaviors such walking and swimming, animals need to coordinate their left and right limbs. In Drosophila, wing grooming can be induced by activation of sensory organs called campaniform sensilla. Flies usually clean one wing at a time, coordinating their left and right hind legs to sweep the dorsal and ventral surfaces of the wing. Here, we identify a pair of interneurons located in the ventral nerve cord that we name wing projection neurons 1 (wPN1) whose optogenetic activation induces wing grooming. Inhibition of wPN1 activity reduces wing grooming. They receive synaptic input from ipsilateral wing campaniform sensilla and wing mechanosensory bristle neurons, and they extend axonal arbors to the hind leg neuropils. Although they project contralaterally, their activation induces ipsilateral wing grooming. Anatomical and behavioral data support a role for wPN1 as command neurons coordinating both hind legs to work together to clean the stimulated wing.
Pollen feeding behaviors Heliconius and Laparus (Lepidoptera: Nymphalidae) represent a key innovation that has shaped other life history traits of these neotropical butterflies. Although all flower visiting Lepidoptera regularly come in contact with pollen, only Heliconius and Laparus butterflies actively collect pollen with the proboscis and subsequently take up nutrients from the pollen grains. This study focused on the behavior of pollen processing and compared the movement patterns with proboscis grooming behavior in various nymphalid butterflies using video analysis. The proboscis movements of pollen processing behavior consisted of a lengthy series of repeated coiling and uncoiling movements in a loosely coiled proboscis position combined with up and down movements and the release of saliva. The proboscis-grooming behavior was triggered by contamination of the proboscis in both pollen feeding and non-pollen feeding nymphalid butterflies. Proboscis grooming movements included interrupted series of coiling and uncoiling movements, characteristic sideways movements, proboscis lifting, and occasionally full extension of the proboscis. Discharge of saliva was more pronounced in pollen feeding species than in non-pollen feeding butterfly species. We conclude that the pollen processing behavior of Heliconius and Laparus is a modified proboscis grooming behavior that originally served to clean the proboscis after contamination with particles.
Flies groom in response to competing mechanosensory cues in an anterior to posterior order using specific legs. From behavior screens, we identified a pair of cholinergic command-like neurons, Mago-no-Te (MGT), whose optogenetic activation elicits thoracic grooming by hind legs. Thoracic grooming is typically composed of body sweeps and leg rubs in alternation, but clonal analysis coupled with amputation experiments revealed that MGT activation only commands the body sweeps: initiation of leg rubbing requires contact between leg and thorax. With new electron microscopy (EM) connectome data for the ventral nerve cord (VNC), we uncovered a circuit-based explanation for why stimulation of posterior thoracic mechanosensory bristles initiates cleaning by the hind legs. Our previous work showed that flies weigh mechanosensory inputs across the body to select which part to groom, but we did not know why the thorax was always cleaned last. Here, the connectome for the VNC enabled us to identify a pair of GABAergic inhibitory neurons, UMGT1, that receive diverse sensory inputs and synapse onto both MGT and components of its downstream pre-motor circuits. Optogenetic activation of UMGT1 suppresses thoracic cleaning, representing a mechanism by which mechanosensory stimuli on other body parts could take precedence in the grooming hierarchy. We also mapped the pre-motor circuit downstream of MGT, including inhibitory feedback connections that may enable rhythmicity and coordination of limb movement during thoracic grooming.
Spontaneous grooming behavior is a component of insect fitness. We quantified spontaneous grooming behavior in 201 sequenced lines of the Drosophila melanogaster Genetic Reference Panel and observed significant genetic variation in spontaneous grooming, with broad-sense heritabilities of 0.25 and 0.24 in females and males, respectively. Although grooming behavior is highly correlated between males and females, we observed significant sex by genotype interactions, indicating that the genetic basis of spontaneous grooming is partially distinct in the two sexes. We performed genome-wide association analyses of grooming behavior, and mapped 107 molecular polymorphisms associated with spontaneous grooming behavior, of which 73 were in or near 70 genes and 34 were over 1 kilobase from the nearest gene. The candidate genes were associated with a wide variety of gene ontology terms, and several of the candidate genes were significantly enriched in a genetic interaction network. We performed functional assessments of 29 candidate genes using RNA interference, and found that 11 affected spontaneous grooming behavior. The genes associated with natural variation in Drosophila grooming are involved with glutamate metabolism (Gdh) and transport (Eaat); interact genetically with (CCKLR-17D1) or are in the same gene family as (PGRP-LA) genes previously implicated in grooming behavior; are involved in the development of the nervous system and other tissues; or regulate the Notch and Epidermal growth factor receptor signaling pathways. Several DGRP lines exhibited extreme grooming behavior. Excessive grooming behavior can serve as a model for repetitive behaviors diagnostic of several human neuropsychiatric diseases.
The main features of grooming behavior are amazingly similar among arthropods and land vertebrates and serve the same needs. A particular pattern of cleaning movements in cockroaches shows cephalo-caudal progression. Grooming sequences become longer after adaptation to the new setting. Novelty related changes in grooming are recognized as a form of displacement behavior. Statistical analysis of behavior revealed that antennal grooming in American cockroach, Periplaneta americana L., was significantly enhanced in the presence of odor.
Self-grooming is a complex behavior with important biological functions and pathological relevance. How the brain coordinates with the spinal cord to generate the repetitive movements of self-grooming remains largely unknown. Here, we report that in the caudal part of the spinal trigeminal nucleus (Sp5C), neurons that express Cerebellin-2 (Cbln2+) form a neural circuit to the cervical spinal cord to maintain repetitive orofacial self-grooming. Inactivation of Cbln2+ Sp5C neurons blocked both sensory-evoked and stress-induced repetitive orofacial self-grooming. Activation of these neurons triggered short-latency repetitive forelimb movements that resembled orofacial self-grooming. The Cbln2+ Sp5C neurons were monosynaptically innervated by both somatosensory neurons in the trigeminal ganglion and paraventricular hypothalamic neurons. Among the divergent projections of Cbln2+ Sp5C neurons, a descending pathway that innervated motor neurons and interneurons in the cervical spinal cord was necessary and sufficient for repetitive orofacial self-grooming. These data reveal a brain-to-spinal sensorimotor loop for repetitive self-grooming in mice.
Animals integrate information from different sensory modalities, body parts, and time points to inform behavioral choice, but the relevant sensory comparisons and the underlying neural circuits are still largely unknown. We use the grooming behavior of Drosophila melanogaster as a model to investigate the sensory comparisons that govern a motor sequence. Flies perform grooming movements spontaneously, but when covered with dust, they clean their bodies following an anterior-to-posterior sequence. After investigating different sensory modalities that could detect dust, we focus on mechanosensory bristle neurons, whose optogenetic activation induces a similar sequence. Computational modeling predicts that higher sensory input strength to the head will cause anterior grooming to occur first. We test this prediction using an optogenetic competition assay whereby two targeted light beams independently activate mechanosensory bristle neurons on different body parts. We find that the initial choice of grooming movement is determined by the ratio of sensory inputs to different body parts. In dust-covered flies, sensory inputs change as a result of successful cleaning movements. Simulations from our model suggest that this change results in sequence progression. One possibility is that flies perform frequent comparisons between anterior and posterior sensory inputs, and the changing ratios drive different behavior choices. Alternatively, flies may track the temporal change in sensory input to a given body part to measure cleaning effectiveness. The first hypothesis is supported by our optogenetic competition experiments: iterative spatial comparisons of sensory inputs between body parts is essential for organizing grooming movements in sequence.
Deprivation of maternal care has been associated with higher pain sensitivity in offspring. In the present study, we hypothesized that the maternal licking/grooming behavior was an important factor for the development of the pain regulatory system. To test this hypothesis, we used male F2 offspring of early-weaned (EW) F1 mother mice that exhibit lower frequency of licking/grooming behavior. The formalin test revealed that F2 offspring of EW F1 dams showed significantly higher pain behavior than F2 offspring of normally-weaned (NW) F1 dams. We found that the mRNA levels of transient receptor potential vanilloid 1 (TRPV1), a nociceptor, were higher in the lumbosacral dorsal root ganglion (DRG) of F2 offspring of EW F1 dams than those of F2 offspring of NW F1 dams, suggesting that the higher pain sensitivity may be attributed to low licking/grooming, which may result in developmental changes in nociceptive neurons. In the DRG, mRNA levels of Mas-related G-protein coupled receptor B4 (MrgprB4), a marker of sensory neurons that detect gentle stroking, was also up-regulated in the F2 offspring of EW F1 dams. Considering that gentle touch alleviates pain, Mrgprb4 up-regulation may reflect a compensatory change. The present findings indicate important implications of maternal licking/grooming behavior in the development of the pain regulatory system.
Sleep restriction is a common feature of modern lifestyle and its effects can be extended to pregnancy. Several neurobehavioural consequences of sleep restriction during pregnancy have been reported, among which stand out perinatal depression and maternal fatigue, however, its effects over mother-infant relationship warrant further investigation. Thus, this study was aimed to evaluate the effects of sleep restriction during pregnancy over maternal behaviour and maternal aggression through animal models.
Self-grooming is a stereotyped behavior displayed by nearly all animals. Among other established functions, self-grooming is implicated in social communication. However, whether self-grooming specifically influences behaviors of nearby individuals has not been directly tested, partly because of the technical challenge of inducing self-grooming in a reliable and temporally controllable manner. We recently found that optogenetic activation of dopamine D3 receptor expressing neurons in the ventral striatal islands of Calleja robustly induces orofacial grooming in mice. Using this optogenetic manipulation, here we demonstrate that observer mice exhibit social preference for mice that groom more regardless of biological sex. Moreover, grooming-induced social attraction depends on volatile chemosensory cues broadcasted from grooming mice. Collectively, our study establishes self-grooming as a means of promoting social attraction among mice via volatile cues, suggesting an additional benefit for animals to allocate a significant amount of time to this behavior.
Self-grooming in rodents is stereotypically sequenced and naturally occurs after arousal, novelty, or stress. Grooming expression and syntax resulting from stressful and appetitive conditions were assessed in male Long Evans rats treated daily with 10mg/kg of phencyclidine (PCP) for 15 days. Approximately 20 h after the 1st, the 8th, and/or the 15th injection, grooming was induced with water sprays, a loud sound, or smearing food. Behaviors expressed during the seconds or minutes that followed induction were videotaped and codified. Results showed that subchronic treatment with PCP amplified the grooming response in all stressful and appetitive conditions, but provoked a disorganization of grooming sequences only under the stressful, water condition. Thus, PCP enhanced grooming expression indiscriminately. However, this behavior had to serve both hygienic and stress managing purposes in order for chain sequencing to become disorganized as a consequence of drug treatment. These results suggest that the detailed examination of grooming expression and organization is an appropriate tool to measure stress-induced behavioral sensitization and motor functions in animal models of neuropsychiatric disorders such as schizophrenia.
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