Early Life Experience Shapes Male Behavior and Social Networks in Drosophila

Bentzur, Assa; Ben-Shaanan, Shir; Benichou, Jennifer I. C.; Costi, Eliezer; Levi, Mali; Ilany, Amiyaal; Shohat-Ophir, Galit

doi:10.1016/j.cub.2020.10.060

Cited by 38 publications

(89 citation statements)

References 103 publications

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“…Similarly, Obp69a expression decreases as a result of male flies being housed in groups [115]. We found that Obp69a expression was increased following alcohol exposure (Data S5), which is consistent with our observation that one day of intermittent ethanol-odor treatment decreases social behavior, mimicking previously demonstrated isolation phenotypes [37]. An upregulation of OBPs suggests a molecular signature through which alcohol can alter memory formation.…”

Section: Alcohol Alters Gene Expression Associated With Sensory Responsesupporting

confidence: 90%

“…Drosophila have similar responses to alcohol compared to humans; they actively seek alcohol, become intoxicated, and develop tolerance [29,[32][33][34]. Recent advancements in computer-vision and machine learning has recently revealed complex interactions between flies that are noticeably modified by changes in the environment [35][36][37][38][39][40]. Drosophila therefore serves as a powerful model to understand how alcohol simultaneously alters social behavior and corresponding gene expression.…”

Section: Introductionmentioning

confidence: 99%

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Neuromolecular and behavioral effects of ethanol deprivation inDrosophila

D'Silva

McCullar

Conard

et al. 2021

Preprint

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Alcohol use disorder (AUD) is characterized by loss of control in limiting alcohol intake. This may involve intermittent periods of abstinence followed by alcohol seeking and, consequently, relapse. However, little is understood of the molecular mechanisms underlying the impact of alcohol deprivation on behavior. Using a new Drosophila melanogaster repeated intermittent alcohol exposure model, we sought to identify how ethanol deprivation alters spontaneous behavior, determine the associated neural structures, and reveal correlated changes in brain gene expression. We found that repeated intermittent ethanol-odor exposures followed by ethanol-deprivation dynamically induces behaviors associated with a negative affect state. Although behavioral states broadly mapped to many brain regions, persistent changes in social behaviors mapped to the mushroom body and surrounding neuropil. This occurred concurrently with changes in expression of genes associated with sensory responses, neural plasticity, and immunity. Like social behaviors, immune response genes were upregulated following three-day repeated intermittent ethanol-odor exposures and persisted with one or two days of ethanol-deprivation, suggesting an enduring change in molecular function. Our study provides a framework for identifying how ethanol deprivation alters behavior with correlated underlying circuit and molecular changes.

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Section: Alcohol Alters Gene Expression Associated With Sensory Responsesupporting

confidence: 90%

Section: Introductionmentioning

confidence: 99%

Neuromolecular and behavioral effects of ethanol deprivation inDrosophila

D'Silva

McCullar

Conard

et al. 2021

Preprint

View full text Add to dashboard Cite

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“…In addition to the increased motivation to court, we also documented increased frequencies of male-male social interactions, including increased levels of song and chase behaviors, which are normally absent in socially experienced male flies that are housed in groups (Bentzur et al, 2021). This manifestation, together with the increased walking velocity and lack of social clustering behavior observed in groups of Ubc7 KO flies, resemble the behavioral properties of male flies exposed to social isolation, a condition that is known to promote aggression (Wang et al, 2008;Liu et al, 2011).…”

Section: Discussionmentioning

confidence: 86%

“…Therefore, we hypothesized that reducing ADAR expression in NPFR neurons would affect the proteomic profile and could result in behavioral phenotypes. To test this, we downregulated the expression of dADAR in NPFR neurons (NPFR > UAS-dicer, UAS-dADAR RNAi) and analyzed behavior in groups of 10 flies, using the "FlyBowl" system, a suite of tracking and behavior analysis software that score plethora of locomotion and social behaviors (Robie et al, 2012;Bentzur et al, 2021). We used the tracking data obtained to generate a comprehensive behavioral representation for experimental flies and genetic controls that included kinetic features and eight complex behaviors.…”

Section: Manipulation Of the Proteome Profile In Npfr Neurons Affectsmentioning

confidence: 99%

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Transcriptome Analysis of NPFR Neurons Reveals a Connection Between Proteome Diversity and Social Behavior

Ryvkin

Bentzur

Shmueli

et al. 2021

Front. Behav. Neurosci.

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Social behaviors are mediated by the activity of highly complex neuronal networks, the function of which is shaped by their transcriptomic and proteomic content. Contemporary advances in neurogenetics, genomics, and tools for automated behavior analysis make it possible to functionally connect the transcriptome profile of candidate neurons to their role in regulating behavior. In this study we used Drosophila melanogaster to explore the molecular signature of neurons expressing receptor for neuropeptide F (NPF), the fly homolog of neuropeptide Y (NPY). By comparing the transcription profile of NPFR neurons to those of nine other populations of neurons, we discovered that NPFR neurons exhibit a unique transcriptome, enriched with receptors for various neuropeptides and neuromodulators, as well as with genes known to regulate behavioral processes, such as learning and memory. By manipulating RNA editing and protein ubiquitination programs specifically in NPFR neurons, we demonstrate that the proper expression of their unique transcriptome and proteome is required to suppress male courtship and certain features of social group interaction. Our results highlight the importance of transcriptome and proteome diversity in the regulation of complex behaviors and pave the path for future dissection of the spatiotemporal regulation of genes within highly complex tissues, such as the brain.

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Cross species review of the physiological role of d-serine in translationally relevant behaviors

Arizanovska,

Emodogo,

Lally

et al. 2023

Amino Acids

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Bridging the gap between preclinical models of neurological and psychiatric disorders with their human manifestations is necessary to understand their underlying mechanisms, identify biomarkers, and develop novel therapeutics. Cognitive and social impairments underlie multiple neuropsychiatric and neurological disorders and are often comorbid with sleep disturbances, which can exacerbate poor outcomes. Importantly, many symptoms are conserved between vertebrates and invertebrates, although they may have subtle differences. Therefore, it is essential to determine the molecular mechanisms underlying these behaviors across different species and their translatability to humans. Genome-wide association studies have indicated an association between glutamatergic gene variants and both the risk and frequency of psychiatric disorders such as schizophrenia, bipolar disorder, and autism spectrum disorder. For example, changes in glutamatergic neurotransmission, such as glutamate receptor subtype N-methyl-d-aspartate receptor (NMDAR) hypofunction, have been shown to contribute to the pathophysiology of schizophrenia. Furthermore, in neurological disorders, such as traumatic brain injury and Alzheimer’s disease, hyperactivation of NMDARs leads to synaptic damage. In addition to glutamate binding, NMDARs require the binding of a co-agonist d-serine or glycine to the GluN1 subunit to open. d-serine, which is racemized from l-serine by the neuronal enzyme serine racemase (SRR), and both SRR and d-serine are enriched in cortico-limbic brain regions. d-serine is critical for complex behaviors, such as cognition and social behavior, where dysregulation of its synthesis and release has been implicated in many pathological conditions. In this review, we explore the role of d-serine in behaviors that are translationally relevant to multiple psychiatric and neurological disorders in different models across species.

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Early Life Experience Shapes Male Behavior and Social Networks in Drosophila

Cited by 38 publications

References 103 publications

Neuromolecular and behavioral effects of ethanol deprivation inDrosophila

Neuromolecular and behavioral effects of ethanol deprivation inDrosophila

Transcriptome Analysis of NPFR Neurons Reveals a Connection Between Proteome Diversity and Social Behavior

Cross species review of the physiological role of d-serine in translationally relevant behaviors

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