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A signaling network for patterning of neuronal connectivity in the Drosophila brain.

ABSTRACT: The precise number and pattern of axonal connections generated during brain development regulates animal behavior. Therefore, understanding how developmental signals interact to regulate axonal extension and retraction to achieve precise neuronal connectivity is a fundamental goal of neurobiology. We investigated this question in the developing adult brain of Drosophila and find that it is regulated by crosstalk between Wnt, fibroblast growth factor (FGF) receptor, and Jun N-terminal kinase (JNK) signaling, but independent of neuronal activity. The Rac1 GTPase integrates a Wnt-Frizzled-Disheveled axon-stabilizing signal and a Branchless (FGF)-Breathless (FGF receptor) axon-retracting signal to modulate JNK activity. JNK activity is necessary and sufficient for axon extension, whereas the antagonistic Wnt and FGF signals act to balance the extension and retraction required for the generation of the precise wiring pattern.

SUBMITTER: Srahna M

PROVIDER: S-EPMC1592317 | biostudies-literature | 2006 Oct

REPOSITORIES: biostudies-literature

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A signaling network for patterning of neuronal connectivity in the Drosophila brain.

Srahna Mohammed M Leyssen Maarten M Choi Ching Man CM Fradkin Lee G LG Noordermeer Jasprina N JN Hassan Bassem A BA

PLoS biology 20061001 11

The precise number and pattern of axonal connections generated during brain development regulates animal behavior. Therefore, understanding how developmental signals interact to regulate axonal extension and retraction to achieve precise neuronal connectivity is a fundamental goal of neurobiology. We investigated this question in the developing adult brain of Drosophila and find that it is regulated by crosstalk between Wnt, fibroblast growth factor (FGF) receptor, and Jun N-terminal kinase (JNK ...[more]

PMID: 17032066

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Project description:Abstract We present a functionally relevant, quantitative characterization of the neural circuitry of Drosophila melanogaster at the mesoscopic level of neuron types as classified exclusively based on potential network connectivity. Starting from a large neuron-to-neuron brain-wide connectome of the fruit fly, we use stochastic block modeling and spectral graph clustering to group neurons together into a common “cell class” if they connect to neurons of other classes according to the same probability distributions. We then characterize the connectivity-based cell classes with standard neuronal biomarkers, including neurotransmitters, developmental birthtimes, morphological features, spatial embedding, and functional anatomy. Mutual information indicates that connectivity-based classification reveals aspects of neurons that are not adequately captured by traditional classification schemes. Next, using graph theoretic and random walk analyses to identify neuron classes as hubs, sources, or destinations, we detect pathways and patterns of directional connectivity that potentially underpin specific functional interactions in the Drosophila brain. We uncover a core of highly interconnected dopaminergic cell classes functioning as the backbone communication pathway for multisensory integration. Additional predicted pathways pertain to the facilitation of circadian rhythmic activity, spatial orientation, fight-or-flight response, and olfactory learning. Our analysis provides experimentally testable hypotheses critically deconstructing complex brain function from organized connectomic architecture. Author Summary The potential synaptic circuitry of a neural system constitutes the fundamental architectural underpinning of its in vivo dynamics, plasticity, and functions. The fruit fly neural circuit presented here captures the latent stochastic patterns of network connectivity and provides a fundamental parts list for reverse engineering brain computation. Mapping the interactions among connectivity-based neuronal classes to development, morphology, physiology, and transcriptomics result in testable hypotheses on the relationship between whole-brain neural architecture and behavior.

Dataset Information

A signaling network for patterning of neuronal connectivity in the Drosophila brain.

Publications

A signaling network for patterning of neuronal connectivity in the Drosophila brain.

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