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Survey of spiking in the mouse visual system reveals functional hierarchy

Author

Listed:
  • Joshua H. Siegle

    (Allen Institute for Brain Science)

  • Xiaoxuan Jia

    (Allen Institute for Brain Science)

  • Séverine Durand

    (Allen Institute for Brain Science)

  • Sam Gale

    (Allen Institute for Brain Science)

  • Corbett Bennett

    (Allen Institute for Brain Science)

  • Nile Graddis

    (Allen Institute for Brain Science)

  • Greggory Heller

    (Allen Institute for Brain Science)

  • Tamina K. Ramirez

    (Allen Institute for Brain Science)

  • Hannah Choi

    (Allen Institute for Brain Science
    University of Washington)

  • Jennifer A. Luviano

    (Allen Institute for Brain Science)

  • Peter A. Groblewski

    (Allen Institute for Brain Science)

  • Ruweida Ahmed

    (Allen Institute for Brain Science)

  • Anton Arkhipov

    (Allen Institute for Brain Science)

  • Amy Bernard

    (Allen Institute for Brain Science)

  • Yazan N. Billeh

    (Allen Institute for Brain Science)

  • Dillan Brown

    (Allen Institute for Brain Science)

  • Michael A. Buice

    (Allen Institute for Brain Science)

  • Nicolas Cain

    (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)

  • Maggie Chvilicek

    (Allen Institute for Brain Science)

  • Timothy C. Cox

    (University of Missouri-Kansas City School of Dentistry)

  • Kael Dai

    (Allen Institute for Brain Science)

  • Daniel J. Denman

    (Allen Institute for Brain Science
    The University of Colorado Denver, Anschutz Medical Campus)

  • Saskia E. J. Vries

    (Allen Institute for Brain Science)

  • Roald Dietzman

    (Allen Institute for Brain Science)

  • Luke Esposito

    (Allen Institute for Brain Science)

  • Colin Farrell

    (Allen Institute for Brain Science)

  • David Feng

    (Allen Institute for Brain Science)

  • John Galbraith

    (Allen Institute for Brain Science)

  • Marina Garrett

    (Allen Institute for Brain Science)

  • Emily C. Gelfand

    (Allen Institute for Brain Science)

  • Nicole Hancock

    (Allen Institute for Brain Science)

  • Julie A. Harris

    (Allen Institute for Brain Science)

  • Robert Howard

    (Allen Institute for Brain Science)

  • Brian Hu

    (Allen Institute for Brain Science)

  • Ross Hytnen

    (Allen Institute for Brain Science)

  • Ramakrishnan Iyer

    (Allen Institute for Brain Science)

  • Erika Jessett

    (Allen Institute for Brain Science)

  • Katelyn Johnson

    (Allen Institute for Brain Science)

  • India Kato

    (Allen Institute for Brain Science)

  • Justin Kiggins

    (Allen Institute for Brain Science)

  • Sophie Lambert

    (Allen Institute for Brain Science)

  • Jerome Lecoq

    (Allen Institute for Brain Science)

  • Peter Ledochowitsch

    (Allen Institute for Brain Science)

  • Jung Hoon Lee

    (Allen Institute for Brain Science)

  • Arielle Leon

    (Allen Institute for Brain Science)

  • Yang Li

    (Allen Institute for Brain Science)

  • Elizabeth Liang

    (Allen Institute for Brain Science)

  • Fuhui Long

    (Allen Institute for Brain Science)

  • Kyla Mace

    (Allen Institute for Brain Science)

  • Jose Melchior

    (Allen Institute for Brain Science)

  • Daniel Millman

    (Allen Institute for Brain Science)

  • Tyler Mollenkopf

    (Allen Institute for Brain Science)

  • Chelsea Nayan

    (Allen Institute for Brain Science)

  • Lydia Ng

    (Allen Institute for Brain Science)

  • Kiet Ngo

    (Allen Institute for Brain Science)

  • Thuyahn Nguyen

    (Allen Institute for Brain Science)

  • Philip R. Nicovich

    (Allen Institute for Brain Science)

  • Kat North

    (Allen Institute for Brain Science)

  • Gabriel Koch Ocker

    (Allen Institute for Brain Science)

  • Doug Ollerenshaw

    (Allen Institute for Brain Science)

  • Michael Oliver

    (Allen Institute for Brain Science)

  • Marius Pachitariu

    (Janelia Research Campus)

  • Jed Perkins

    (Allen Institute for Brain Science)

  • Melissa Reding

    (Allen Institute for Brain Science)

  • David Reid

    (Allen Institute for Brain Science)

  • Miranda Robertson

    (Allen Institute for Brain Science)

  • Kara Ronellenfitch

    (Allen Institute for Brain Science)

  • Sam Seid

    (Allen Institute for Brain Science)

  • Cliff Slaughterbeck

    (Allen Institute for Brain Science)

  • Michelle Stoecklin

    (Allen Institute for Brain Science)

  • David Sullivan

    (Allen Institute for Brain Science)

  • Ben Sutton

    (Allen Institute for Brain Science)

  • Jackie Swapp

    (Allen Institute for Brain Science)

  • Carol Thompson

    (Allen Institute for Brain Science)

  • Kristen Turner

    (Allen Institute for Brain Science)

  • Wayne Wakeman

    (Allen Institute for Brain Science)

  • Jennifer D. Whitesell

    (Allen Institute for Brain Science)

  • Derric Williams

    (Allen Institute for Brain Science)

  • Ali Williford

    (Allen Institute for Brain Science)

  • Rob Young

    (Allen Institute for Brain Science)

  • Hongkui Zeng

    (Allen Institute for Brain Science)

  • Sarah Naylor

    (Allen Institute for Brain Science)

  • John W. Phillips

    (Allen Institute for Brain Science)

  • R. Clay Reid

    (Allen Institute for Brain Science)

  • Stefan Mihalas

    (Allen Institute for Brain Science)

  • Shawn R. Olsen

    (Allen Institute for Brain Science)

  • Christof Koch

    (Allen Institute for Brain Science)

Abstract

The anatomy of the mammalian visual system, from the retina to the neocortex, is organized hierarchically1. However, direct observation of cellular-level functional interactions across this hierarchy is lacking due to the challenge of simultaneously recording activity across numerous regions. Here we describe a large, open dataset—part of the Allen Brain Observatory2—that surveys spiking from tens of thousands of units in six cortical and two thalamic regions in the brains of mice responding to a battery of visual stimuli. Using cross-correlation analysis, we reveal that the organization of inter-area functional connectivity during visual stimulation mirrors the anatomical hierarchy from the Allen Mouse Brain Connectivity Atlas3. We find that four classical hierarchical measures—response latency, receptive-field size, phase-locking to drifting gratings and response decay timescale—are all correlated with the hierarchy. Moreover, recordings obtained during a visual task reveal that the correlation between neural activity and behavioural choice also increases along the hierarchy. Our study provides a foundation for understanding coding and signal propagation across hierarchically organized cortical and thalamic visual areas.

Suggested Citation

  • Joshua H. Siegle & Xiaoxuan Jia & Séverine Durand & Sam Gale & Corbett Bennett & Nile Graddis & Greggory Heller & Tamina K. Ramirez & Hannah Choi & Jennifer A. Luviano & Peter A. Groblewski & Ruweida , 2021. "Survey of spiking in the mouse visual system reveals functional hierarchy," Nature, Nature, vol. 592(7852), pages 86-92, April.
  • Handle: RePEc:nat:nature:v:592:y:2021:i:7852:d:10.1038_s41586-020-03171-x
    DOI: 10.1038/s41586-020-03171-x
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    Citations

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    Cited by:

    1. Roxana Zeraati & Yan-Liang Shi & Nicholas A. Steinmetz & Marc A. Gieselmann & Alexander Thiele & Tirin Moore & Anna Levina & Tatiana A. Engel, 2023. "Intrinsic timescales in the visual cortex change with selective attention and reflect spatial connectivity," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    2. Rita Gil & Mafalda Valente & Noam Shemesh, 2024. "Rat superior colliculus encodes the transition between static and dynamic vision modes," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    3. Ziqi Gao & Chenran Jiang & Jiawen Zhang & Xiaosen Jiang & Lanqing Li & Peilin Zhao & Huanming Yang & Yong Huang & Jia Li, 2023. "Hierarchical graph learning for protein–protein interaction," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    4. Jérémie Sibille & Carolin Gehr & Jonathan I. Benichov & Hymavathy Balasubramanian & Kai Lun Teh & Tatiana Lupashina & Daniela Vallentin & Jens Kremkow, 2022. "High-density electrode recordings reveal strong and specific connections between retinal ganglion cells and midbrain neurons," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    5. Kotaro Ishizu & Shosuke Nishimoto & Yutaro Ueoka & Akihiro Funamizu, 2024. "Localized and global representation of prior value, sensory evidence, and choice in male mouse cerebral cortex," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    6. Edward A. B. Horrocks & Fabio R. Rodrigues & Aman B. Saleem, 2024. "Flexible neural population dynamics govern the speed and stability of sensory encoding in mouse visual cortex," Nature Communications, Nature, vol. 15(1), pages 1-23, 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. Yina Wei & Anirban Nandi & Xiaoxuan Jia & Joshua H. Siegle & Daniel Denman & Soo Yeun Lee & Anatoly Buchin & Werner Geit & Clayton P. Mosher & Shawn Olsen & Costas A. Anastassiou, 2023. "Associations between in vitro, in vivo and in silico cell classes in mouse primary visual cortex," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    9. Brandon R. Munn & Eli J. Müller & Vicente Medel & Sharon L. Naismith & Joseph T. Lizier & Robert D. Sanders & James M. Shine, 2023. "Neuronal connected burst cascades bridge macroscale adaptive signatures across arousal states," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    10. Natalie Klein & Joshua H Siegle & Tobias Teichert & Robert E Kass, 2021. "Cross-population coupling of neural activity based on Gaussian process current source densities," PLOS Computational Biology, Public Library of Science, vol. 17(11), pages 1-24, November.
    11. 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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