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4 Janelia Publications

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    02/26/24 | Nested neural circuits generate distinct acoustic signals during Drosophila courtship
    Joshua L. Lillvis , Kaiyu Wang , Hiroshi M. Shiozaki , Min Xu , David L. Stern , Barry J. Dickson
    Current Biology. 2024 Feb 26;34(4):808-24. doi: 10.1016/j.cub.2024.01.015

    Many motor control systems generate multiple movements using a common set of muscles. How are premotor circuits able to flexibly generate diverse movement patterns? Here, we characterize the neuronal circuits that drive the distinct courtship songs of Drosophila melanogaster. Male flies vibrate their wings towards females to produce two different song modes – pulse and sine song – which signal species identity and male quality. Using cell-type specific genetic reagents and the connectome, we provide a cellular and synaptic map of the circuits in the male ventral nerve cord that generate these songs and examine how activating or inhibiting each cell type within these circuits affects the song. Our data reveal that the song circuit is organized into two nested feed-forward pathways, with extensive reciprocal and feed-back connections. The larger network produces pulse song, the more complex and ancestral song form. A subset of this network produces sine song, the simpler and more recent form. Such nested organization may be a common feature of motor control circuits in which evolution has layered increasing flexibility on to a basic movement pattern.

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    09/07/23 | Combinatorial circuit dynamics orchestrate flexible motor patterns in Drosophila.
    Hiroshi M. Shiozaki , Kaiyu Wang , Joshua L. Lillvis , Min Xu , Barry J. Dickson , David L. Stern
    bioRxiv. 2023 Sep 07:. doi: 10.1101/2022.12.14.520499

    Motor systems flexibly implement diverse motor programs to pattern behavioral sequences, yet their neural underpinnings remain unclear. Here, we investigated the neural circuit mechanisms of flexible courtship behavior in Drosophila. Courting males alternately produce two types of courtship song. By recording calcium signals in the ventral nerve cord (VNC) in behaving flies, we found that different songs are produced by activating overlapping neural populations with distinct motor functions in a combinatorial manner. Recordings from the brain suggest that song is driven by two descending pathways – one defines when to sing and the other specifies what song to sing. Connectomic analysis reveals that these “when” and “what” descending pathways provide structured input to VNC neurons with different motor functions. These results suggest that dynamic changes in the activation patterns of descending pathways drive different combinations of motor modules, thereby flexibly switching between different motor actions.

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    06/01/23 | Single-cell type analysis of wing premotor circuits in the ventral nerve cord of Drosophila melanogaster
    Erica Ehrhardt , Samuel C Whitehead , Shigehiro Namiki , Ryo Minegishi , Igor Siwanowicz , Kai Feng , Hideo Otsuna , FlyLight Project Team , Geoffrey W Meissner , David Stern , Jim Truman , David Shepherd , Michael H. Dickinson , Kei Ito , Barry J Dickson , Itai Cohen , Gwyneth M Card , Wyatt Korff
    bioRxiv. 2023 Jun 01:. doi: 10.1101/2023.05.31.542897

    To perform most behaviors, animals must send commands from higher-order processing centers in the brain to premotor circuits that reside in ganglia distinct from the brain, such as the mammalian spinal cord or insect ventral nerve cord. How these circuits are functionally organized to generate the great diversity of animal behavior remains unclear. An important first step in unraveling the organization of premotor circuits is to identify their constituent cell types and create tools to monitor and manipulate these with high specificity to assess their function. This is possible in the tractable ventral nerve cord of the fly. To generate such a toolkit, we used a combinatorial genetic technique (split-GAL4) to create 195 sparse driver lines targeting 198 individual cell types in the ventral nerve cord. These included wing and haltere motoneurons, modulatory neurons, and interneurons. Using a combination of behavioral, developmental, and anatomical analyses, we systematically characterized the cell types targeted in our collection. Taken together, the resources and results presented here form a powerful toolkit for future investigations of neural circuits and connectivity of premotor circuits while linking them to behavioral outputs.

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    12/15/22 | Neural coding of distinct motor patterns during Drosophila courtship song
    Hiroshi M. Shiozaki , Kaiyu Wang , Joshua L. Lillvis , Min Xu , Barry J. Dickson , David L. Stern
    bioRxiv. 2022 Dec 15:. doi: 10.1101/2022.12.14.520499

    Animals flexibly switch between different actions by changing neural activity patterns for motor control. Courting Drosophila melanogaster males produce two different acoustic signals, pulse and sine song, each of which can be promoted by artificial activation of distinct neurons. However, how the activity of these neurons implements flexible song production is unknown. Here, we developed an assay to record neuronal calcium signals in the ventral nerve cord, which contains the song motor circuit, in singing flies. We found that sine-promoting neurons, but not pulse-promoting neurons, show strong activation during sine song. In contrast, both pulse- and sine-promoting neurons are active during pulse song. Furthermore, population calcium imaging in the song circuit suggests that sine song involves activation of a subset of neurons that are also active during pulse song. Thus, differential activation of overlapping, rather than distinct, neural populations underlies flexible motor actions during acoustic communication in D. melanogaster.

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