Journal Article

A multilevel multimodal circuit enhances action selection in Drosophila

Mensh, Brett D., Branson, Kristin M., Ohyama, Tomoko, Rivera-Alba, Marta, Fetter, Richard D., Simpson, Julie H., Zlatic, Marta, Truman, James W., Cardona, Albert, Schneider-Mizell, Casey M., Aleman, Javier Valdes, Franconville, Romain

2015

Overview

Natural events present multiple types of sensory cues, each detected by a specialized sensory modality. Combining information from several modalities is essential for the selection of appropriate actions. Key to understanding multimodal computations is determining the structural patterns of multimodal convergence and how these patterns contribute to behaviour. Modalities could converge early, late or at multiple levels in the sensory processing hierarchy. Here we show that combining mechanosensory and nociceptive cues synergistically enhances the selection of the fastest mode of escape locomotion in Drosophila larvae. In an electron microscopy volume that spans the entire insect nervous system, we reconstructed the multisensory circuit supporting the synergy, spanning multiple levels of the sensory processing hierarchy. The wiring diagram revealed a complex multilevel multimodal convergence architecture. Using behavioural and physiological studies, we identified functionally connected circuit nodes that trigger the fastest locomotor mode, and others that facilitate it, and we provide evidence that multiple levels of multimodal integration contribute to escape mode selection. We propose that the multilevel multimodal convergence architecture may be a general feature of multisensory circuits enabling complex input–output functions and selective tuning to ecologically relevant combinations of cues. Combining neural manipulation in freely behaving animals, physiological studies and electron microscopy reconstruction in the Drosophila larva identifies a complex multilsensory circuit involved in the selection of larval escape modes that exhibits a multilevel multimodal convergence architecture. A multisensory circuit in Drosophila larvae When making decisions, animals must integrate diverse sensory stimuli but whether multi-modal sensory information is combined early or late during information processing is largely unknown. Using neural manipulation in freely behaving animals, combined with physiological studies and electron microscopy reconstruction, Marta Zlatic and colleagues have tracked all 138 neurons — among many thousands — that allow the Drosophila larva to escape mechanical or nociceptive stimuli. They map full functional connectivity at single-synapse resolution. The resulting connectome reveals a complex multilevel convergence architecture in which the two signalling pathways converge and interact at every stage, from sensory neurons to interneurons and motor neurons, which increases both the sensitivity of the system and the richness of its input–output functions. The availability of this multisensory circuit in a genetically tractable model system provides a resource for investigating multiple brain and nerve cord pathway interactions.

• Publisher: Nature Publishing Group UK,Nature Publishing Group
• Subject: 631/378/2629/1409 / Animal behavior / Animals / Central Nervous System - cytology / Central Nervous System - physiology / Cues / Drosophila melanogaster - cytology / Drosophila melanogaster - growth & development / Drosophila melanogaster - physiology / Female / Humanities and Social Sciences / Insects / Interneurons - metabolism / Larva - cytology / Larva - physiology / Larvae / Locomotion / Motor Neurons - metabolism / multidisciplinary / Nervous system / Neural Pathways - physiology / Neurons / Science / Sensory perception / Sensory Receptor Cells - metabolism / Signal Transduction / Studies / Synapses - metabolism