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A direction-selective cortico-brainstem pathway adaptively modulates innate behaviors

Author

Listed:
  • Jiashu Liu

    (University of Toronto Mississauga
    University of Toronto)

  • Yingtian He

    (University of Toronto Mississauga
    University of Toronto)

  • Andreanne Lavoie

    (University of Toronto Mississauga
    University of Toronto)

  • Guy Bouvier

    (Université Paris-Saclay, CNRS, Institut des Neurosciences Paris-Saclay)

  • Bao-hua Liu

    (University of Toronto Mississauga
    University of Toronto)

Abstract

Sensory cortices modulate innate behaviors through corticofugal projections targeting phylogenetically-old brainstem nuclei. However, the principles behind the functional connectivity of these projections remain poorly understood. Here, we show that in mice visual cortical neurons projecting to the optic-tract and dorsal-terminal nuclei (NOT-DTN) possess distinct response properties and anatomical connectivity, supporting the adaption of an essential innate eye movement, the optokinetic reflex (OKR). We find that these corticofugal neurons are enriched in specific visual areas, and they prefer temporo-nasal visual motion, matching the direction bias of downstream NOT-DTN neurons. Remarkably, continuous OKR stimulation selectively enhances the activity of these temporo-nasally biased cortical neurons, which can efficiently promote OKR plasticity. Lastly, we demonstrate that silencing downstream NOT-DTN neurons, which project specifically to the inferior olive—a key structure in oculomotor plasticity, impairs the cortical modulation of OKR and OKR plasticity. Our results unveil a direction-selective cortico-brainstem pathway that adaptively modulates innate behaviors.

Suggested Citation

  • Jiashu Liu & Yingtian He & Andreanne Lavoie & Guy Bouvier & Bao-hua Liu, 2023. "A direction-selective cortico-brainstem pathway adaptively modulates innate behaviors," Nature Communications, Nature, vol. 14(1), pages 1-23, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42910-2
    DOI: 10.1038/s41467-023-42910-2
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    References listed on IDEAS

    as
    1. Xu Han & Ben Vermaercke & Vincent Bonin, 2022. "Diversity of spatiotemporal coding reveals specialized visual processing streams in the mouse cortex," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    2. Kevin K. Sit & Michael J. Goard, 2020. "Distributed and retinotopically asymmetric processing of coherent motion in mouse visual cortex," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    3. Xiaorui R. Xiong & Feixue Liang & Brian Zingg & Xu-ying Ji & Leena A. Ibrahim & Huizhong W. Tao & Li I. Zhang, 2015. "Auditory cortex controls sound-driven innate defense behaviour through corticofugal projections to inferior colliculus," Nature Communications, Nature, vol. 6(1), pages 1-12, November.
    4. Dario L. Ringach & Patrick J. Mineault & Elaine Tring & Nicholas D. Olivas & Pablo Garcia-Junco-Clemente & Joshua T. Trachtenberg, 2016. "Spatial clustering of tuning in mouse primary visual cortex," Nature Communications, Nature, vol. 7(1), pages 1-9, November.
    5. Xu Han & Ben Vermaercke & Vincent Bonin, 2022. "Publisher Correction: Diversity of spatiotemporal coding reveals specialized visual processing streams in the mouse cortex," Nature Communications, Nature, vol. 13(1), pages 1-1, December.
    6. Aniek Schoups & Rufin Vogels & Ning Qian & Guy Orban, 2001. "Practising orientation identification improves orientation coding in V1 neurons," Nature, Nature, vol. 412(6846), pages 549-553, August.
    7. Bao-hua Liu & Andrew D. Huberman & Massimo Scanziani, 2016. "Cortico-fugal output from visual cortex promotes plasticity of innate motor behaviour," Nature, Nature, vol. 538(7625), pages 383-387, October.
    8. Seung Wook Oh & Julie A. Harris & Lydia Ng & Brent Winslow & Nicholas Cain & Stefan Mihalas & Quanxin Wang & Chris Lau & Leonard Kuan & Alex M. Henry & Marty T. Mortrud & Benjamin Ouellette & Thuc Ngh, 2014. "A mesoscale connectome of the mouse brain," Nature, Nature, vol. 508(7495), pages 207-214, April.
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