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The spatial and temporal structure of neural activity across the fly brain

Author

Listed:
  • Evan S. Schaffer

    (Columbia University)

  • Neeli Mishra

    (Columbia University)

  • Matthew R. Whiteway

    (Columbia University
    Columbia University)

  • Wenze Li

    (Columbia University
    Columbia University)

  • Michelle B. Vancura

    (Columbia University)

  • Jason Freedman

    (Columbia University)

  • Kripa B. Patel

    (Columbia University
    Columbia University)

  • Venkatakaushik Voleti

    (Columbia University
    Columbia University)

  • Liam Paninski

    (Columbia University
    Columbia University)

  • Elizabeth M. C. Hillman

    (Columbia University
    Columbia University
    Columbia University)

  • L. F. Abbott

    (Columbia University
    Columbia University)

  • Richard Axel

    (Columbia University
    Columbia University
    Columbia University)

Abstract

What are the spatial and temporal scales of brainwide neuronal activity? We used swept, confocally-aligned planar excitation (SCAPE) microscopy to image all cells in a large volume of the brain of adult Drosophila with high spatiotemporal resolution while flies engaged in a variety of spontaneous behaviors. This revealed neural representations of behavior on multiple spatial and temporal scales. The activity of most neurons correlated (or anticorrelated) with running and flailing over timescales that ranged from seconds to a minute. Grooming elicited a weaker global response. Significant residual activity not directly correlated with behavior was high dimensional and reflected the activity of small clusters of spatially organized neurons that may correspond to genetically defined cell types. These clusters participate in the global dynamics, indicating that neural activity reflects a combination of local and broadly distributed components. This suggests that microcircuits with highly specified functions are provided with knowledge of the larger context in which they operate.

Suggested Citation

  • Evan S. Schaffer & Neeli Mishra & Matthew R. Whiteway & Wenze Li & Michelle B. Vancura & Jason Freedman & Kripa B. Patel & Venkatakaushik Voleti & Liam Paninski & Elizabeth M. C. Hillman & L. F. Abbot, 2023. "The spatial and temporal structure of neural activity across the fly brain," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41261-2
    DOI: 10.1038/s41467-023-41261-2
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    References listed on IDEAS

    as
    1. João C. Marques & Meng Li & Diane Schaak & Drew N. Robson & Jennifer M. Li, 2020. "Internal state dynamics shape brainwide activity and foraging behaviour," Nature, Nature, vol. 577(7789), pages 239-243, January.
    2. David M. Schneider & Anders Nelson & Richard Mooney, 2014. "A synaptic and circuit basis for corollary discharge in the auditory cortex," Nature, Nature, vol. 513(7517), pages 189-194, September.
    3. Fei Wang & Kaiyu Wang & Nora Forknall & Christopher Patrick & Tansy Yang & Ruchi Parekh & Davi Bock & Barry J. Dickson, 2020. "Neural circuitry linking mating and egg laying in Drosophila females," Nature, Nature, vol. 579(7797), pages 101-105, March.
    4. Tom Hindmarsh Sten & Rufei Li & Adriane Otopalik & Vanessa Ruta, 2021. "Sexual arousal gates visual processing during Drosophila courtship," Nature, Nature, vol. 595(7868), pages 549-553, July.
    5. Nicholas A. Steinmetz & Peter Zatka-Haas & Matteo Carandini & Kenneth D. Harris, 2019. "Distributed coding of choice, action and engagement across the mouse brain," Nature, Nature, vol. 576(7786), pages 266-273, December.
    6. William C. Lemon & Stefan R. Pulver & Burkhard Höckendorf & Katie McDole & Kristin Branson & Jeremy Freeman & Philipp J. Keller, 2015. "Whole-central nervous system functional imaging in larval Drosophila," Nature Communications, Nature, vol. 6(1), pages 1-16, November.
    7. Sophie Aimon & Takeo Katsuki & Tongqiu Jia & Logan Grosenick & Michael Broxton & Karl Deisseroth & Terrence J Sejnowski & Ralph J Greenspan, 2019. "Fast near-whole–brain imaging in adult Drosophila during responses to stimuli and behavior," PLOS Biology, Public Library of Science, vol. 17(2), pages 1-31, February.
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