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Drosophila melanogaster grooming possesses syntax with distinct rules at different temporal scales.

ABSTRACT: Mathematical modeling of behavioral sequences yields insight into the rules and mechanisms underlying sequence generation. Grooming in Drosophila melanogaster is characterized by repeated execution of distinct, stereotyped actions in variable order. Experiments demonstrate that, following stimulation by an irritant, grooming progresses gradually from an early phase dominated by anterior cleaning to a later phase with increased walking and posterior cleaning. We also observe that, at an intermediate temporal scale, there is a strong relationship between the amount of time spent performing body-directed grooming actions and leg-directed actions. We then develop a series of data-driven Markov models that isolate and identify the behavioral features governing transitions between individual grooming bouts. We identify action order as the primary driver of probabilistic, but non-random, syntax structure, as has previously been identified. Subsequent models incorporate grooming bout duration, which also contributes significantly to sequence structure. Our results show that, surprisingly, the syntactic rules underlying probabilistic grooming transitions possess action duration-dependent structure, suggesting that sensory input-independent mechanisms guide grooming behavior at short time scales. Finally, the inclusion of a simple rule that modifies grooming transition probabilities over time yields a generative model that recapitulates the key features of observed grooming sequences at several time scales. These discoveries suggest that sensory input guides action selection by modulating internally generated dynamics. Additionally, the discovery of these principles governing grooming in D. melanogaster demonstrates the utility of incorporating temporal information when characterizing the syntax of behavioral sequences.

SUBMITTER: Mueller JM

PROVIDER: S-EPMC6594582 | biostudies-literature | 2019 Jun

REPOSITORIES: biostudies-literature

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Drosophila melanogaster grooming possesses syntax with distinct rules at different temporal scales.

Mueller Joshua M JM Ravbar Primoz P Simpson Julie H JH Carlson Jean M JM

PLoS computational biology 20190626 6

Mathematical modeling of behavioral sequences yields insight into the rules and mechanisms underlying sequence generation. Grooming in Drosophila melanogaster is characterized by repeated execution of distinct, stereotyped actions in variable order. Experiments demonstrate that, following stimulation by an irritant, grooming progresses gradually from an early phase dominated by anterior cleaning to a later phase with increased walking and posterior cleaning. We also observe that, at an intermedi ...[more]

PMID: 31242178

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Project description:The excitatory amino acid transporter EAAT3 plays an important role in the neuronal uptake of glutamate regulating the activation of glutamate receptors. Polymorphisms in the gene-encoding EAAT3 have been associated with obsessive-compulsive disorder (OCD), although the mechanisms underlying this relationship are still unknown. We recently reported that mice with increased EAAT3 expression in forebrain neurons (EAAT3 g lo /CMKII) display behavioral and synaptic features relevant to OCD, including increased grooming, higher anxiety-like behavior and altered cortico-striatal synaptic function. The dopamine neurotransmitter system is implicated in ritualistic behaviors. Indeed, dopaminergic neurons express EAAT3, and mice lacking EAAT3 exhibit decreased dopamine release and decreased expression of the dopamine D1 receptor. Moreover, EAAT3 plays a role on the effect of the psychostimulant amphetamine. As such, we sought to determine if the OCD-like behavior in EAAT3 g lo /CMKII mice is accompanied by altered nigro-striatal dopaminergic transmission. The aim of this study was to analyze dopamine transmission both in basal conditions and after an acute challenge of amphetamine, using behavioral, neurochemical, molecular, and cellular approaches. We found that in basal conditions, EAAT3 g lo /CMKII mice performed more grooming events and that they remained in phase 1 of the grooming chain syntax compared with control littermates. Administration of amphetamine increased the number of grooming events in control mice, while EAAT3 g lo /CMKII mice remain unaffected. Interestingly, the grooming syntax of amphetamine-control mice resembled that of EAAT3 g lo /CMKII mice in basal conditions. Using in vivo microdialysis, we found decreased basal dopamine levels in EAAT3 g lo /CMKII compared with control mice. Unexpectedly, we found that after acute amphetamine, EAAT3 g lo /CMKII mice had a higher release of dopamine compared with that of control mice, suggesting that EAAT3 overexpression leads to increased dopamine releasability. To determine postsynaptic effect of EAAT3 overexpression over dopamine transmission, we performed Western blot analysis of dopaminergic proteins and found that EAAT3 g lo /CMKII mice have higher expression of D2 receptors, suggesting a higher inhibition of the indirect striatal pathway. Together, the data indicate that EAAT3 overexpression impacts on dopamine transmission, making dopamine neurons more sensitive to the effect of amphetamine and leading to a disbalance between the direct and indirect striatal pathways that favors the performance of repetitive behaviors.

Dataset Information

Drosophila melanogaster grooming possesses syntax with distinct rules at different temporal scales.

Publications

Drosophila melanogaster grooming possesses syntax with distinct rules at different temporal scales.

Similar Datasets

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