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Hierarchical organization of cortical and thalamic connectivity

Author

Listed:
  • Julie A. Harris

    (Allen Institute for Brain Science)

  • Stefan Mihalas

    (Allen Institute for Brain Science)

  • Karla E. Hirokawa

    (Allen Institute for Brain Science)

  • Jennifer D. Whitesell

    (Allen Institute for Brain Science)

  • Hannah Choi

    (Allen Institute for Brain Science
    Department of Applied Mathematics)

  • Amy Bernard

    (Allen Institute for Brain Science)

  • Phillip Bohn

    (Allen Institute for Brain Science)

  • Shiella Caldejon

    (Allen Institute for Brain Science)

  • Linzy Casal

    (Allen Institute for Brain Science)

  • Andrew Cho

    (Allen Institute for Brain Science)

  • Aaron Feiner

    (Allen Institute for Brain Science)

  • David Feng

    (Allen Institute for Brain Science)

  • Nathalie Gaudreault

    (Allen Institute for Brain Science)

  • Charles R. Gerfen

    (National Institute of Mental Health)

  • Nile Graddis

    (Allen Institute for Brain Science)

  • Peter A. Groblewski

    (Allen Institute for Brain Science)

  • Alex M. Henry

    (Allen Institute for Brain Science)

  • Anh Ho

    (Allen Institute for Brain Science)

  • Robert Howard

    (Allen Institute for Brain Science)

  • Joseph E. Knox

    (Allen Institute for Brain Science)

  • Leonard Kuan

    (Allen Institute for Brain Science)

  • Xiuli Kuang

    (Wenzhou Medical University)

  • Jerome Lecoq

    (Allen Institute for Brain Science)

  • Phil Lesnar

    (Allen Institute for Brain Science)

  • Yaoyao Li

    (Wenzhou Medical University)

  • Jennifer Luviano

    (Allen Institute for Brain Science)

  • Stephen McConoughey

    (Allen Institute for Brain Science)

  • Marty T. Mortrud

    (Allen Institute for Brain Science)

  • Maitham Naeemi

    (Allen Institute for Brain Science)

  • Lydia Ng

    (Allen Institute for Brain Science)

  • Seung Wook Oh

    (Allen Institute for Brain Science)

  • Benjamin Ouellette

    (Allen Institute for Brain Science)

  • Elise Shen

    (Allen Institute for Brain Science)

  • Staci A. Sorensen

    (Allen Institute for Brain Science)

  • Wayne Wakeman

    (Allen Institute for Brain Science)

  • Quanxin Wang

    (Allen Institute for Brain Science)

  • Yun Wang

    (Allen Institute for Brain Science)

  • Ali Williford

    (Allen Institute for Brain Science)

  • John W. Phillips

    (Allen Institute for Brain Science)

  • Allan R. Jones

    (Allen Institute for Brain Science)

  • Christof Koch

    (Allen Institute for Brain Science)

  • Hongkui Zeng

    (Allen Institute for Brain Science)

Abstract

The mammalian cortex is a laminar structure containing many areas and cell types that are densely interconnected in complex ways, and for which generalizable principles of organization remain mostly unknown. Here we describe a major expansion of the Allen Mouse Brain Connectivity Atlas resource1, involving around a thousand new tracer experiments in the cortex and its main satellite structure, the thalamus. We used Cre driver lines (mice expressing Cre recombinase) to comprehensively and selectively label brain-wide connections by layer and class of projection neuron. Through observations of axon termination patterns, we have derived a set of generalized anatomical rules to describe corticocortical, thalamocortical and corticothalamic projections. We have built a model to assign connection patterns between areas as either feedforward or feedback, and generated testable predictions of hierarchical positions for individual cortical and thalamic areas and for cortical network modules. Our results show that cell-class-specific connections are organized in a shallow hierarchy within the mouse corticothalamic network.

Suggested Citation

  • Julie A. Harris & Stefan Mihalas & Karla E. Hirokawa & Jennifer D. Whitesell & Hannah Choi & Amy Bernard & Phillip Bohn & Shiella Caldejon & Linzy Casal & Andrew Cho & Aaron Feiner & David Feng & Nath, 2019. "Hierarchical organization of cortical and thalamic connectivity," Nature, Nature, vol. 575(7781), pages 195-202, November.
  • Handle: RePEc:nat:nature:v:575:y:2019:i:7781:d:10.1038_s41586-019-1716-z
    DOI: 10.1038/s41586-019-1716-z
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    Cited by:

    1. Yongcheng Jin & Ellina Mikhailova & Ming Lei & Sally A. Cowley & Tianyi Sun & Xingyun Yang & Yujia Zhang & Kaili Liu & Daniel Catarino da Silva & Luana Campos Soares & Sara Bandiera & Francis G. Szele, 2023. "Integration of 3D-printed cerebral cortical tissue into an ex vivo lesioned brain slice," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    2. Li Yuan & Xiaoyin Chen & Huiqing Zhan & Gilbert L. Henry & Anthony M. Zador, 2024. "Massive multiplexing of spatially resolved single neuron projections with axonal BARseq," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    3. Wen-Hao Zhang & Si Wu & Krešimir Josić & Brent Doiron, 2023. "Sampling-based Bayesian inference in recurrent circuits of stochastic spiking neurons," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    4. Stuart Oldham & Gareth Ball, 2023. "A phylogenetically-conserved axis of thalamocortical connectivity in the human brain," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    5. Yanjie Wang & Zhaonan Chen & Guofen Ma & Lizhao Wang & Yanmei Liu & Meiling Qin & Xiang Fei & Yifan Wu & Min Xu & Siyu Zhang, 2023. "A frontal transcallosal inhibition loop mediates interhemispheric balance in visuospatial processing," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    6. Daniel G. Taub & Qiufen Jiang & Francesca Pietrafesa & Junfeng Su & Aloe Carroll & Caitlin Greene & Michael R. Blanchard & Aakanksha Jain & Mahmoud El-Rifai & Alexis Callen & Katherine Yager & Clara C, 2024. "The secondary somatosensory cortex gates mechanical and heat sensitivity," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    7. Adam R. Pines & Bart Larsen & Zaixu Cui & Valerie J. Sydnor & Maxwell A. Bertolero & Azeez Adebimpe & Aaron F. Alexander-Bloch & Christos Davatzikos & Damien A. Fair & Ruben C. Gur & Raquel E. Gur & H, 2022. "Dissociable multi-scale patterns of development in personalized brain networks," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    8. Jun Ma & John J. O’Malley & Malaz Kreiker & Yan Leng & Isbah Khan & Morgan Kindel & Mario A. Penzo, 2024. "Convergent direct and indirect cortical streams shape avoidance decisions in mice via the midline thalamus," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    9. Siva Venkadesh & Anthony Santarelli & Tyler Boesen & Hong-Wei Dong & Giorgio A. Ascoli, 2023. "Combinatorial quantification of distinct neural projections from retrograde tracing," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    10. Yuwen Chen & Haoyu Yang & Yan Luo & Yijun Niu & Muzhou Yu & Shanjun Deng & Xuanhao Wang & Handi Deng & Haichao Chen & Lixia Gao & Xinjian Li & Pingyong Xu & Fudong Xue & Jing Miao & Song-Hai Shi & Yi , 2024. "Photoacoustic Tomography with Temporal Encoding Reconstruction (PATTERN) for cross-modal individual analysis of the whole brain," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    11. Yao Fei & Qihang Wu & Shijie Zhao & Kun Song & Junwei Han & Cirong Liu, 2024. "Diverse and asymmetric patterns of single-neuron projectome in regulating interhemispheric connectivity," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    12. Disheng Tang & Joel Zylberberg & Xiaoxuan Jia & Hannah Choi, 2024. "Stimulus type shapes the topology of cellular functional networks in mouse visual cortex," Nature Communications, Nature, vol. 15(1), pages 1-17, December.

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