Perception of fight outcome is needed to activate socially driven changes in brain transcriptome
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ABSTRACT:
ORGANISM(S): Danio rerio
PROVIDER: GSE56549 | GEO | 2014/04/10
SECONDARY ACCESSION(S): PRJNA243902
REPOSITORIES: GEO
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Project description:Group living animals must be able to express different behavior profiles depending on their social status. This implies that the same genotype may translate into different behavioral phenotypes through socially driven differential gene expression. Here we show for the first time that what triggers the switch between status-specific neurogenomic states is not the objective structure of the social interaction but rather the subjectsM-bM-^@M-^Y perception of its outcome. For this purpose we had male zebrafish fight either a real opponent or their own image on a mirror. Massive changes in the brain transcriptome were observed in real opponent fighters, which experience either a victory or a defeat. In contrast, mirror fighters, which had no information on fight outcome despite expressing aggressive behavior, failed to activate a neurogenomic response. These results indicate that, even in cognitively simple organisms such as zebrafish, neurogenomic responses underlying changes in social status rely on cognitive appraisal. Brain samples from zebrafish, Danio rerio were collected after experimental manipulations generated 4 phenotypes regarding social experience: mirror fighters (M), winners of a real opponent fight (W), losers of a real opponent fight (L); and socially isolated fish (I). After 30 minutes of experimental manipulation animals were anesthetized with a lethal dose of MS-222 (1000-1500 mg/l) and decapitated. Brains were rapidly collected, homogenized and RNA extracted following standard methods of RNeasy Lipid Tissue Mini Kit, Qiagen. RNA was then treated with DNase (RNase-free DNase set, Qiagen) to remove possible contaminations with genomic DNA and concentration and purity was estimated by spectrophotometric absorbance in a NanoDrop ND-1000 UV-Vis Spectrophotometer (Nano-Drop Technologies).
2014-04-10 | E-GEOD-56549 | biostudies-arrayexpress
Project description:Social plasticity is a pervasive feature of animal behavior. Animals adjust the expression of their social behavior to the daily changes in social life and to transitions between life-history stages, and the ability to change in these ways impacts their Darwinian fitness. This behavioral plasticity may be achieved either by rewiring or by biochemically switching nodes of the neural network underlying the social behavior in response to perceived social information. Independent of the proximate mechanisms, at the neuromolecular level social plasticity relies on the regulation of gene expression, such that different neurogenomic states emerge in response to different social stimuli and the switches between states are orchestrated by signaling pathways that interface the social environment and the genotype. Here, we test this hypothesis by characterizing the changes in the brain profile of gene expression in response to social odors in the Mozambique Tilapia, Oreochromis mossambicus. This species has a rich repertoire of social behaviors during which both visual and chemical information are conveyed to conspecifics. Specifically, dominant males increase their urination frequency during agonist encounters and during courtship to convey chemical information reflecting their dominance status. We recorded electro-olfactograms to test the extent to which the olfactory epithelium can discriminate between olfactory information from dominant and subordinate males as well as from pre- and post-spawning females. We then performed a genome-scale gene expression analysis of the olfactory bulb and the olfactory cortex homolog in order to identify the neuromolecular systems involved in processing these social stimuli. Our results show that different olfactory stimuli from conspecificsM-bM-^@M-^Y have a major impact in the brain transcriptome, with different chemical social cues eliciting specific patterns of gene expression in the brain. These results confirm the role of rapid changes in gene expression in the brain as a genomic mechanism underlying behavioural plasticity and reinforce the idea of an extensive transcriptional plasticity of cichlid genomes, especially in response to rapid changes in their social environment. Brain samples from 40 African cichlid males, Oreochromis mossambicus were collected after stimulation with different social olfactory stimuli. Samples were collected from 2 brain areas: BO and Dp after males were exposed to dominant (DOM) and subordinate (SUB) male urine and pre- (PRE) and post-ovulatory (POST) female scent. In OB 5 replicates were collected from males exposed to DOM and 6 to the other stimuli. For Dp 5 replicates were collected from males exposed to DOM and POST, 4 to SUB and 6 to PRE.
2014-02-01 | E-GEOD-54468 | biostudies-arrayexpress
Project description:Social plasticity is a pervasive feature of animal behavior. Animals adjust the expression of their social behavior to the daily changes in social life and to transitions between life-history stages, and the ability to change in these ways impacts their Darwinian fitness. This behavioral plasticity may be achieved either by rewiring or by biochemically switching nodes of the neural network underlying the social behavior in response to perceived social information. Independent of the proximate mechanisms, at the neuromolecular level social plasticity relies on the regulation of gene expression, such that different neurogenomic states emerge in response to different social stimuli and the switches between states are orchestrated by signaling pathways that interface the social environment and the genotype. Here, we test this hypothesis by characterizing the changes in the brain profile of gene expression in response to social odors in the Mozambique Tilapia, Oreochromis mossambicus. This species has a rich repertoire of social behaviors during which both visual and chemical information are conveyed to conspecifics. Specifically, dominant males increase their urination frequency during agonist encounters and during courtship to convey chemical information reflecting their dominance status. We recorded electro-olfactograms to test the extent to which the olfactory epithelium can discriminate between olfactory information from dominant and subordinate males as well as from pre- and post-spawning females. We then performed a genome-scale gene expression analysis of the olfactory bulb and the olfactory cortex homolog in order to identify the neuromolecular systems involved in processing these social stimuli. Our results show that different olfactory stimuli from conspecifics’ have a major impact in the brain transcriptome, with different chemical social cues eliciting specific patterns of gene expression in the brain. These results confirm the role of rapid changes in gene expression in the brain as a genomic mechanism underlying behavioural plasticity and reinforce the idea of an extensive transcriptional plasticity of cichlid genomes, especially in response to rapid changes in their social environment.
2014-02-01 | GSE54468 | GEO
Project description:Motherhood is characterized by dramatic changes in brain and behavior, but less is known about fatherhood. Here we report that male sticklebacks – a small fish in which fathers provide care – experience dramatic changes in neurogenomic state as they become fathers. Some genes are unique to different stages of paternal care, some genes are shared across stages, and some genes are added to the previously acquired neurogenomic state. Comparative genomic analysis suggests that some of these neurogenomic dynamics resemble changes associated with pregnancy and reproduction in mammalian mothers. Moreover, gene regulatory analysis identified transcription factors that are regulated in opposite directions in response to a territorial challenge versus during paternal care. Altogether these results show that some of the molecular mechanisms of parental care might be deeply conserved and might not be sex-specific, and suggest that tradeoffs between opposing social behaviors are managed at the gene regulatory level.
2019-09-15 | GSE134508 | GEO
Project description:Experimental evidence suggests that environmental stress conditions can alter the expression of BDNF and the levels of this neurotrophin influence the behavioural response in mammalian models. Recently it has been demonstrated that the exposure to 34° C for 21 days alters the brain proteome and behaviour in zebrafish. The aim of this work was to investigate the role of BDNF in the nervous system of adult zebrafish under control and heat treatment conditions. For this purpose, wild type (WT), heterozygous BDNF+/- (HT) and knock out BDNF-/- (KO) zebrafish were kept for 21 days at 26° C or 34° C and then euthanized for brain analysis or subjected to behavioural tests (Y-maze test, novel tank test, light and dark test, social preference test, mirror biting test) used for assessing behavioural aspects such as boldness, anxiety, social preference, aggressivity, interest for the novel environment and exploration. RTqPCR analysis showed the reduction of gene expression of BDNF and its receptors after heat treatment. Moreover, proteomic analysis and behavioural tests showed genotype- and temperature-dependent effects on brain proteome and behaviour of zebrafish.
2022-06-09 | PXD030733 | Pride
Project description:Background Appropriate social interactions influence animal fitness by impacting several processes, such as mating, territory defense, and offspring care. Many studies shedding light on the neurobiological underpinnings of social behavior have focused on nonapeptides (vasopressin, oxytocin, and homologues) and on sexual or parent-offspring interactions. Furthermore, animals have been studied under artificial laboratory conditions, where the consequences of behavioral responses may not be as critical as when expressed under natural environments, therefore obscuring certain physiological responses. We used automated recording of social interactions of wild house mice outside of the breeding season to detect individuals at both tails of a distribution of egocentric network sizes (characterized by number of different partners encountered per day). We then used RNA-seq to perform an unbiased assessment of neural differences in gene expression in the prefrontal cortex, the hippocampus and the hypothalamus between these mice with naturally occurring extreme differences in social network size. Results We found that the neurogenomic pathways associated with having extreme social network sizes differed between the sexes. In females, hundreds of genes were differentially expressed between animals with small and large social network sizes, whereas in males very few were. In males, X-chromosome inactivation pathways in the prefrontal cortex were the ones that better differentiated animals with small from those with large social network sizes animals. In females, animals with small network size showed up-regulation of dopaminergic production and transport pathways in the hypothalamus. Additionally, in females, extracellular matrix deposition on hippocampal neurons was higher in individuals with small relative to large social network size. Conclusions Studying neural substrates of natural variation in social behavior in traditional model organisms in their habitat can open new targets of research for understanding variation in social behavior in other taxa.
2020-07-06 | GSE148075 | GEO
Project description:We studied behavioral, brain transcriptomic and epigenetic responses of honey bees to social challenge. Bees were exposed to two intruders at different intervals. The initial exposure caused two behavioral effects at the individual level: an increase in the intensity of aggression toward a second intruder at 30 and 60 minutes, and an increased probability of responding aggressively toward a second intruder that persisted for two hours. The shorter-lived response was associated with one pattern of gene expression in the mushroom bodies, highlighted by genes related to cytoskeleton remodeling. The longer-lived response was associated with a different pattern; highlighted by genes related to hormones, stress response and transcription factors. Histone profiling revealed few changes in chromatin accessibility in response to social challenge; most differentially expressed genes were “ready” to be activated. These results demonstrate how biological embedding of a social challenge involves changes in the neurogenomic state to influence future behavior.
2017-03-29 | GSE85877 | GEO
Project description:We studied behavioral, brain transcriptomic and epigenetic responses of honey bees to social challenge. Bees were exposed to two intruders at different intervals. The initial exposure caused two behavioral effects at the individual level: an increase in the intensity of aggression toward a second intruder at 30 and 60 minutes, and an increased probability of responding aggressively toward a second intruder that persisted for two hours. The shorter-lived response was associated with one pattern of gene expression in the mushroom bodies, highlighted by genes related to cytoskeleton remodeling. The longer-lived response was associated with a different pattern; highlighted by genes related to hormones, stress response and transcription factors. Histone profiling revealed few changes in chromatin accessibility in response to social challenge; most differentially expressed genes were “ready” to be activated. These results demonstrate how biological embedding of a social challenge involves changes in the neurogenomic state to influence future behavior.
2017-03-29 | GSE85876 | GEO
Project description:Human infants exhibit innate social behaviors at birth, yet little is understood about the embryonic development of sociality. We screened 1120 known drugs and found that embryonic inhibition of topoisomerase IIα (Top2a) resulted in lasting social deficits in zebrafish. In mice, prenatal Top2 inhibition caused behavioral defects related to core symptoms of autism, including impairments in social interaction and communication. Mutation of Top2a in zebrafish caused downregulation of a set of genes highly enriched for genes associated with autism in humans. Both the Top2a-regulated and autism-associated gene sets possess binding sites for polycomb repressive complex 2 (PRC2), a regulatory complex responsible for H3K27 trimethylation. Moreover, both gene sets are highly enriched for H3K27me3. Inhibition of PRC2 component Ezh2 rescued social deficits caused by Top2 inhibition. Therefore, Top2a is a key component of an evolutionarily conserved pathway that promotes the development of social behavior through PRC2 and H3K27me3.
2021-09-20 | GSE181730 | GEO
Project description:Stress is a major influence on mental health status; the ways that individuals respond to or copes with stressors determine whether they are negatively affected in the future. Stress responses are established by an interplay between genetics, environment, and life experiences. Psychosocial stress is particularly impactful during adolescence, a critical period for the development of mood disorders. In this study we compared two established, selectively-bred Sprague Dawley rat lines, the “internalizing” bred Low Responder (bLR) line versus the “externalizing” bred High Responder (bHR) line, to investigate how genetic temperament and adolescent environment impact future responses to social interactions and psychosocial stress, and how these determinants of stress response interact. Animals were exposed to social and environmental enrichment in adolescence prior to experiencing social defeat and were then assessed for social interaction and anxiety-like behavior. Adolescent enrichment caused bLR rats to display less social avoidance, more social interaction, less submission during defeat, and resilience to the prolonged effects of social stress on corticosterone, while enrichment caused bHR animals to show greater aggression during defeat and during a neutral social encounter, and decreased anxiety-like behavior. To gain insight into the development of social resilience in the anxious phenotype bLRs, RNA-seq was conducted on the hippocampus and nucleus accumbens, two brain regions that mediate stress regulation and social behavior. Gene sets previously associated with stress, social behavior, aggression and exploratory activity were enriched with differential expression in both regions, with a particularly large effect on gene sets that regulate social behaviors. These findings provide further evidence that adolescent enrichment can serve as an inoculating experience against future stressors. The ability to induce social resilience in a usually anxious line of animals by manipulating their environment has translational implications, as it underscores the feasibility of intervention strategies targeted at genetically vulnerable adolescent populations.
2024-05-01 | GSE237890 | GEO