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A Drosophila computational brain model reveals sensorimotor processing

Author

Listed:
  • Philip K. Shiu

    (University of California
    Eon Systems)

  • Gabriella R. Sterne

    (University of California
    Department of Biomedical Genetics)

  • Nico Spiller

    (Max Planck Florida Institute for Neuroscience)

  • Romain Franconville

    (HHMI Janelia Research Campus)

  • Andrea Sandoval

    (University of California)

  • Joie Zhou

    (University of California)

  • Neha Simha

    (University of California)

  • Chan Hyuk Kang

    (Sungkyunkwan University)

  • Seongbong Yu

    (Sungkyunkwan University)

  • Jinseop S. Kim

    (Sungkyunkwan University)

  • Sven Dorkenwald

    (Princeton University
    Princeton University)

  • Arie Matsliah

    (Princeton University)

  • Philipp Schlegel

    (University of Cambridge
    MRC Laboratory of Molecular Biology)

  • Szi-chieh Yu

    (Princeton University)

  • Claire E. McKellar

    (Princeton University)

  • Amy Sterling

    (Princeton University)

  • Marta Costa

    (University of Cambridge)

  • Katharina Eichler

    (Princeton University)

  • Alexander Shakeel Bates

    (MRC Laboratory of Molecular Biology
    The University of Oxford
    Harvard Medical School)

  • Nils Eckstein

    (HHMI Janelia Research Campus)

  • Jan Funke

    (HHMI Janelia Research Campus)

  • Gregory S. X. E. Jefferis

    (University of Cambridge
    MRC Laboratory of Molecular Biology)

  • Mala Murthy

    (Princeton University)

  • Salil S. Bidaye

    (Max Planck Florida Institute for Neuroscience)

  • Stefanie Hampel

    (University of Puerto Rico-Medical Sciences Campus)

  • Andrew M. Seeds

    (University of Puerto Rico-Medical Sciences Campus)

  • Kristin Scott

    (University of California)

Abstract

The recent assembly of the adult Drosophila melanogaster central brain connectome, containing more than 125,000 neurons and 50 million synaptic connections, provides a template for examining sensory processing throughout the brain1,2. Here we create a leaky integrate-and-fire computational model of the entire Drosophila brain, on the basis of neural connectivity and neurotransmitter identity3, to study circuit properties of feeding and grooming behaviours. We show that activation of sugar-sensing or water-sensing gustatory neurons in the computational model accurately predicts neurons that respond to tastes and are required for feeding initiation4. In addition, using the model to activate neurons in the feeding region of the Drosophila brain predicts those that elicit motor neuron firing5—a testable hypothesis that we validate by optogenetic activation and behavioural studies. Activating different classes of gustatory neurons in the model makes accurate predictions of how several taste modalities interact, providing circuit-level insight into aversive and appetitive taste processing. Additionally, we applied this model to mechanosensory circuits and found that computational activation of mechanosensory neurons predicts activation of a small set of neurons comprising the antennal grooming circuit, and accurately describes the circuit response upon activation of different mechanosensory subtypes6–10. Our results demonstrate that modelling brain circuits using only synapse-level connectivity and predicted neurotransmitter identity generates experimentally testable hypotheses and can describe complete sensorimotor transformations.

Suggested Citation

  • Philip K. Shiu & Gabriella R. Sterne & Nico Spiller & Romain Franconville & Andrea Sandoval & Joie Zhou & Neha Simha & Chan Hyuk Kang & Seongbong Yu & Jinseop S. Kim & Sven Dorkenwald & Arie Matsliah , 2024. "A Drosophila computational brain model reveals sensorimotor processing," Nature, Nature, vol. 634(8032), pages 210-219, October.
  • Handle: RePEc:nat:nature:v:634:y:2024:i:8032:d:10.1038_s41586-024-07763-9
    DOI: 10.1038/s41586-024-07763-9
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