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A distributed and efficient population code of mixed selectivity neurons for flexible navigation decisions

Author

Listed:
  • Shinichiro Kira

    (Harvard Medical School)

  • Houman Safaai

    (Harvard Medical School
    Istituto Italiano di Tecnologia)

  • Ari S. Morcos

    (Harvard Medical School)

  • Stefano Panzeri

    (Istituto Italiano di Tecnologia
    University Medical Center Hamburg-Eppendorf (UKE))

  • Christopher D. Harvey

    (Harvard Medical School)

Abstract

Decision-making requires flexibility to rapidly switch one’s actions in response to sensory stimuli depending on information stored in memory. We identified cortical areas and neural activity patterns underlying this flexibility during virtual navigation, where mice switched navigation toward or away from a visual cue depending on its match to a remembered cue. Optogenetics screening identified V1, posterior parietal cortex (PPC), and retrosplenial cortex (RSC) as necessary for accurate decisions. Calcium imaging revealed neurons that can mediate rapid navigation switches by encoding a mixture of a current and remembered visual cue. These mixed selectivity neurons emerged through task learning and predicted the mouse’s choices by forming efficient population codes before correct, but not incorrect, choices. They were distributed across posterior cortex, even V1, and were densest in RSC and sparsest in PPC. We propose flexibility in navigation decisions arises from neurons that mix visual and memory information within a visual-parietal-retrosplenial network.

Suggested Citation

  • Shinichiro Kira & Houman Safaai & Ari S. Morcos & Stefano Panzeri & Christopher D. Harvey, 2023. "A distributed and efficient population code of mixed selectivity neurons for flexible navigation decisions," Nature Communications, Nature, vol. 14(1), pages 1-28, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37804-2
    DOI: 10.1038/s41467-023-37804-2
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    as
    1. Caroline A. Runyan & Eugenio Piasini & Stefano Panzeri & Christopher D. Harvey, 2017. "Distinct timescales of population coding across cortex," Nature, Nature, vol. 548(7665), pages 92-96, August.
    2. Valerio Mante & David Sussillo & Krishna V. Shenoy & William T. Newsome, 2013. "Context-dependent computation by recurrent dynamics in prefrontal cortex," Nature, Nature, vol. 503(7474), pages 78-84, November.
    3. Tianming Yang & Michael N. Shadlen, 2007. "Probabilistic reasoning by neurons," Nature, Nature, vol. 447(7148), pages 1075-1080, June.
    4. Noah L. Pettit & Ee-Lynn Yap & Michael E. Greenberg & Christopher D. Harvey, 2022. "Fos ensembles encode and shape stable spatial maps in the hippocampus," Nature, Nature, vol. 609(7926), pages 327-334, September.
    5. Jonathan W. Pillow & Jonathon Shlens & Liam Paninski & Alexander Sher & Alan M. Litke & E. J. Chichilnisky & Eero P. Simoncelli, 2008. "Spatio-temporal correlations and visual signalling in a complete neuronal population," Nature, Nature, vol. 454(7207), pages 995-999, August.
    6. Timothy D. Hanks & Charles D. Kopec & Bingni W. Brunton & Chunyu A. Duan & Jeffrey C. Erlich & Carlos D. Brody, 2015. "Distinct relationships of parietal and prefrontal cortices to evidence accumulation," Nature, Nature, vol. 520(7546), pages 220-223, April.
    7. Christopher D. Harvey & Forrest Collman & Daniel A. Dombeck & David W. Tank, 2009. "Intracellular dynamics of hippocampal place cells during virtual navigation," Nature, Nature, vol. 461(7266), pages 941-946, October.
    8. Simon Peron & Ravi Pancholi & Bettina Voelcker & Jason D. Wittenbach & H. Freyja Ólafsdóttir & Jeremy Freeman & Karel Svoboda, 2020. "Recurrent interactions in local cortical circuits," Nature, Nature, vol. 579(7798), pages 256-259, March.
    9. Aman B. Saleem & E. Mika Diamanti & Julien Fournier & Kenneth D. Harris & Matteo Carandini, 2018. "Coherent encoding of subjective spatial position in visual cortex and hippocampus," Nature, Nature, vol. 562(7725), pages 124-127, October.
    10. Athena Akrami & Charles D. Kopec & Mathew E. Diamond & Carlos D. Brody, 2018. "Posterior parietal cortex represents sensory history and mediates its effects on behaviour," Nature, Nature, vol. 554(7692), pages 368-372, February.
    11. David J. Freedman & John A. Assad, 2006. "Experience-dependent representation of visual categories in parietal cortex," Nature, Nature, vol. 443(7107), pages 85-88, September.
    12. Johannes Friedrich & Pengcheng Zhou & Liam Paninski, 2017. "Fast online deconvolution of calcium imaging data," PLOS Computational Biology, Public Library of Science, vol. 13(3), pages 1-26, March.
    13. Cristina Domnisoru & Amina A. Kinkhabwala & David W. Tank, 2013. "Correction: Corrigendum: Membrane potential dynamics of grid cells," Nature, Nature, vol. 504(7480), pages 470-470, December.
    14. Friedman, Jerome H. & Hastie, Trevor & Tibshirani, Rob, 2010. "Regularization Paths for Generalized Linear Models via Coordinate Descent," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 33(i01).
    15. Mattia Rigotti & Omri Barak & Melissa R. Warden & Xiao-Jing Wang & Nathaniel D. Daw & Earl K. Miller & Stefano Fusi, 2013. "The importance of mixed selectivity in complex cognitive tasks," Nature, Nature, vol. 497(7451), pages 585-590, May.
    16. Qianli Yang & Edgar Walker & R. James Cotton & Andreas S. Tolias & Xaq Pitkow, 2021. "Revealing nonlinear neural decoding by analyzing choices," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    17. Cristina Domnisoru & Amina A. Kinkhabwala & David W. Tank, 2013. "Membrane potential dynamics of grid cells," Nature, Nature, vol. 495(7440), pages 199-204, March.
    18. Sandra Reinert & Mark Hübener & Tobias Bonhoeffer & Pieter M. Goltstein, 2021. "Mouse prefrontal cortex represents learned rules for categorization," Nature, Nature, vol. 593(7859), pages 411-417, May.
    19. Abhishek Banerjee & Giuseppe Parente & Jasper Teutsch & Christopher Lewis & Fabian F. Voigt & Fritjof Helmchen, 2020. "Value-guided remapping of sensory cortex by lateral orbitofrontal cortex," Nature, Nature, vol. 585(7824), pages 245-250, September.
    20. Ralf D. Wimmer & L. Ian Schmitt & Thomas J. Davidson & Miho Nakajima & Karl Deisseroth & Michael M. Halassa, 2015. "Thalamic control of sensory selection in divided attention," Nature, Nature, vol. 526(7575), pages 705-709, October.
    21. Christopher D. Harvey & Philip Coen & David W. Tank, 2012. "Choice-specific sequences in parietal cortex during a virtual-navigation decision task," Nature, Nature, vol. 484(7392), pages 62-68, April.
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