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Distributed coding of choice, action and engagement across the mouse brain

Author

Listed:
  • Nicholas A. Steinmetz

    (University College London
    University of Washington)

  • Peter Zatka-Haas

    (University College London)

  • Matteo Carandini

    (University College London)

  • Kenneth D. Harris

    (University College London)

Abstract

Vision, choice, action and behavioural engagement arise from neuronal activity that may be distributed across brain regions. Here we delineate the spatial distribution of neurons underlying these processes. We used Neuropixels probes1,2 to record from approximately 30,000 neurons in 42 brain regions of mice performing a visual discrimination task3. Neurons in nearly all regions responded non-specifically when the mouse initiated an action. By contrast, neurons encoding visual stimuli and upcoming choices occupied restricted regions in the neocortex, basal ganglia and midbrain. Choice signals were rare and emerged with indistinguishable timing across regions. Midbrain neurons were activated before contralateral choices and were suppressed before ipsilateral choices, whereas forebrain neurons could prefer either side. Brain-wide pre-stimulus activity predicted engagement in individual trials and in the overall task, with enhanced subcortical but suppressed neocortical activity during engagement. These results reveal organizing principles for the distribution of neurons encoding behaviourally relevant variables across the mouse brain.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:nature:v:576:y:2019:i:7786:d:10.1038_s41586-019-1787-x
    DOI: 10.1038/s41586-019-1787-x
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    Cited by:

    1. João D. Semedo & Anna I. Jasper & Amin Zandvakili & Aravind Krishna & Amir Aschner & Christian K. Machens & Adam Kohn & Byron M. Yu, 2022. "Feedforward and feedback interactions between visual cortical areas use different population activity patterns," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
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    3. Camille Mazo & Margarida Baeta & Leopoldo Petreanu, 2024. "Auditory cortex conveys non-topographic sound localization signals to visual cortex," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    4. Christopher M. Kim & Arseny Finkelstein & Carson C. Chow & Karel Svoboda & Ran Darshan, 2023. "Distributing task-related neural activity across a cortical network through task-independent connections," Nature Communications, Nature, vol. 14(1), pages 1-21, 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. Guo, Lei & Guo, Minxin & Wu, Youxi & Xu, Guizhi, 2023. "Specific neural coding of fMRI spiking neural network based on time coding," Chaos, Solitons & Fractals, Elsevier, vol. 174(C).
    7. 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.
    8. 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.
    9. 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.
    10. Aniruddha Das & Sarah Holden & Julie Borovicka & Jacob Icardi & Abigail O’Niel & Ariel Chaklai & Davina Patel & Rushik Patel & Stefanie Kaech Petrie & Jacob Raber & Hod Dana, 2023. "Large-scale recording of neuronal activity in freely-moving mice at cellular resolution," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    11. Yue Liu & Xiao-Jing Wang, 2024. "Flexible gating between subspaces in a neural network model of internally guided task switching," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    12. Kenneth W. Latimer & David J. Freedman, 2023. "Low-dimensional encoding of decisions in parietal cortex reflects long-term training history," Nature Communications, Nature, vol. 14(1), pages 1-24, December.
    13. Alyse Thomas & Weiguo Yang & Catherine Wang & Sri Laasya Tipparaju & Guang Chen & Brennan Sullivan & Kylie Swiekatowski & Mahima Tatam & Charles Gerfen & Nuo Li, 2023. "Superior colliculus bidirectionally modulates choice activity in frontal cortex," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    14. Frank Gelens & Juho Äijälä & Louis Roberts & Misako Komatsu & Cem Uran & Michael A. Jensen & Kai J. Miller & Robin A. A. Ince & Max Garagnani & Martin Vinck & Andres Canales-Johnson, 2024. "Distributed representations of prediction error signals across the cortical hierarchy are synergistic," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    15. Javier G. Orlandi & Mohammad Abdolrahmani & Ryo Aoki & Dmitry R. Lyamzin & Andrea Benucci, 2023. "Distributed context-dependent choice information in mouse posterior cortex," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    16. Xiaoyu Lu & Yunmiao Wang & Zhuohe Liu & Yueyang Gou & Dieter Jaeger & François St-Pierre, 2023. "Widefield imaging of rapid pan-cortical voltage dynamics with an indicator evolved for one-photon microscopy," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    17. Lloyd E. Russell & Mehmet Fişek & Zidan Yang & Lynn Pei Tan & Adam M. Packer & Henry W. P. Dalgleish & Selmaan N. Chettih & Christopher D. Harvey & Michael Häusser, 2024. "The influence of cortical activity on perception depends on behavioral state and sensory context," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    18. Christopher F. Angeloni & Wiktor Młynarski & Eugenio Piasini & Aaron M. Williams & Katherine C. Wood & Linda Garami & Ann M. Hermundstad & Maria N. Geffen, 2023. "Dynamics of cortical contrast adaptation predict perception of signals in noise," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    19. 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.
    20. Drew C. Schreiner & Christian Cazares & Rafael Renteria & Christina M. Gremel, 2022. "Information normally considered task-irrelevant drives decision-making and affects premotor circuit recruitment," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    21. Gal Atlan & Noa Matosevich & Noa Peretz-Rivlin & Idit Marsh-Yvgi & Noam Zelinger & Eden Chen & Timna Kleinman & Noa Bleistein & Efrat Sheinbach & Maya Groysman & Yuval Nir & Ami Citri, 2024. "Claustrum neurons projecting to the anterior cingulate restrict engagement during sleep and behavior," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    22. Masashi Hasegawa & Ziyan Huang & Ricardo Paricio-Montesinos & Jan Gründemann, 2024. "Network state changes in sensory thalamus represent learned outcomes," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    23. Pierre-Marie Gardères & Sébastien Gal & Charly Rousseau & Alexandre Mamane & Dan Alin Ganea & Florent Haiss, 2024. "Coexistence of state, choice, and sensory integration coding in barrel cortex LII/III," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    24. Matthijs N. Oude Lohuis & Jean L. Pie & Pietro Marchesi & Jorrit S. Montijn & Christiaan P. J. Kock & Cyriel M. A. Pennartz & Umberto Olcese, 2022. "Multisensory task demands temporally extend the causal requirement for visual cortex in perception," Nature Communications, Nature, vol. 13(1), pages 1-19, December.

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