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Multiplex translaminar imaging in the spinal cord of behaving mice

Author

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  • Pavel Shekhtmeyster

    (The Salk Institute for Biological Studies
    University of California, San Diego)

  • Erin M. Carey

    (The Salk Institute for Biological Studies)

  • Daniela Duarte

    (The Salk Institute for Biological Studies)

  • Alexander Ngo

    (The Salk Institute for Biological Studies)

  • Grace Gao

    (The Salk Institute for Biological Studies)

  • Nicholas A. Nelson

    (The Salk Institute for Biological Studies
    University of California, San Diego)

  • Charles L. Clark

    (The Salk Institute for Biological Studies)

  • Axel Nimmerjahn

    (The Salk Institute for Biological Studies)

Abstract

While the spinal cord is known to play critical roles in sensorimotor processing, including pain-related signaling, corresponding activity patterns in genetically defined cell types across spinal laminae have remained challenging to investigate. Calcium imaging has enabled cellular activity measurements in behaving rodents but is currently limited to superficial regions. Here, using chronically implanted microprisms, we imaged sensory and motor-evoked activity in regions and at speeds inaccessible by other high-resolution imaging techniques. To enable translaminar imaging in freely behaving animals through implanted microprisms, we additionally developed wearable microscopes with custom-compound microlenses. This system addresses multiple challenges of previous wearable microscopes, including their limited working distance, resolution, contrast, and achromatic range. Using this system, we show that dorsal horn astrocytes in behaving mice show sensorimotor program-dependent and lamina-specific calcium excitation. Additionally, we show that tachykinin precursor 1 (Tac1)-expressing neurons exhibit translaminar activity to acute mechanical pain but not locomotion.

Suggested Citation

  • Pavel Shekhtmeyster & Erin M. Carey & Daniela Duarte & Alexander Ngo & Grace Gao & Nicholas A. Nelson & Charles L. Clark & Axel Nimmerjahn, 2023. "Multiplex translaminar imaging in the spinal cord of behaving mice," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36959-2
    DOI: 10.1038/s41467-023-36959-2
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    References listed on IDEAS

    as
    1. Anna V. Molofsky & Kevin W. Kelley & Hui-Hsin Tsai & Stephanie A. Redmond & Sandra M. Chang & Lohith Madireddy & Jonah R. Chan & Sergio E. Baranzini & Erik M. Ullian & David H. Rowitch, 2014. "Astrocyte-encoded positional cues maintain sensorimotor circuit integrity," Nature, Nature, vol. 509(7499), pages 189-194, May.
    2. Kohei J. Sekiguchi & Pavel Shekhtmeyster & Katharina Merten & Alexander Arena & Daniela Cook & Elizabeth Hoffman & Alexander Ngo & Axel Nimmerjahn, 2016. "Imaging large-scale cellular activity in spinal cord of freely behaving mice," Nature Communications, Nature, vol. 7(1), pages 1-13, September.
    3. Tianwen Huang & Shing-Hong Lin & Nathalie M. Malewicz & Yan Zhang & Ying Zhang & Martyn Goulding & Robert H. LaMotte & Qiufu Ma, 2019. "Identifying the pathways required for coping behaviours associated with sustained pain," Nature, Nature, vol. 565(7737), pages 86-90, January.
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