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Noise correlations in neural ensemble activity limit the accuracy of hippocampal spatial representations

Author

Listed:
  • Omer Hazon

    (Stanford University)

  • Victor H. Minces

    (University California San Diego)

  • David P. Tomàs

    (Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS))

  • Surya Ganguli

    (Stanford University)

  • Mark J. Schnitzer

    (Stanford University)

  • Pablo E. Jercog

    (Stanford University
    Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS))

Abstract

Neurons in the CA1 area of the mouse hippocampus encode the position of the animal in an environment. However, given the variability in individual neurons responses, the accuracy of this code is still poorly understood. It was proposed that downstream areas could achieve high spatial accuracy by integrating the activity of thousands of neurons, but theoretical studies point to shared fluctuations in the firing rate as a potential limitation. Using high-throughput calcium imaging in freely moving mice, we demonstrated the limiting factors in the accuracy of the CA1 spatial code. We found that noise correlations in the hippocampus bound the estimation error of spatial coding to ~10 cm (the size of a mouse). Maximal accuracy was obtained using approximately [300–1400] neurons, depending on the animal. These findings reveal intrinsic limits in the brain’s representations of space and suggest that single neurons downstream of the hippocampus can extract maximal spatial information from several hundred inputs.

Suggested Citation

  • Omer Hazon & Victor H. Minces & David P. Tomàs & Surya Ganguli & Mark J. Schnitzer & Pablo E. Jercog, 2022. "Noise correlations in neural ensemble activity limit the accuracy of hippocampal spatial representations," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-31254-y
    DOI: 10.1038/s41467-022-31254-y
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    References listed on IDEAS

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    1. Ryan C Williamson & Benjamin R Cowley & Ashok Litwin-Kumar & Brent Doiron & Adam Kohn & Matthew A Smith & Byron M Yu, 2016. "Scaling Properties of Dimensionality Reduction for Neural Populations and Network Models," PLOS Computational Biology, Public Library of Science, vol. 12(12), pages 1-27, December.
    2. MohammadMehdi Kafashan & Anna W. Jaffe & Selmaan N. Chettih & Ramon Nogueira & Iñigo Arandia-Romero & Christopher D. Harvey & Rubén Moreno-Bote & Jan Drugowitsch, 2021. "Scaling of sensory information in large neural populations shows signatures of information-limiting correlations," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    3. Johan Wessberg & Christopher R. Stambaugh & Jerald D. Kralik & Pamela D. Beck & Mark Laubach & John K. Chapin & Jung Kim & S. James Biggs & Mandayam A. Srinivasan & Miguel A. L. Nicolelis, 2000. "Real-time prediction of hand trajectory by ensembles of cortical neurons in primates," Nature, Nature, vol. 408(6810), pages 361-365, November.
    4. Kenneth D. Harris & Jozsef Csicsvari & Hajime Hirase & George Dragoi & György Buzsáki, 2003. "Organization of cell assemblies in the hippocampus," Nature, Nature, vol. 424(6948), pages 552-556, July.
    5. P. E. Jercog & Y. Ahmadian & C. Woodruff & R. Deb-Sen & L. F. Abbott & E. R. Kandel, 2019. "Heading direction with respect to a reference point modulates place-cell activity," Nature Communications, Nature, vol. 10(1), pages 1-8, December.
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    Cited by:

    1. Diego B. Piza & Benjamin W. Corrigan & Roberto A. Gulli & Sonia Carmo & A. Claudio Cuello & Lyle Muller & Julio Martinez-Trujillo, 2024. "Primacy of vision shapes behavioral strategies and neural substrates of spatial navigation in marmoset hippocampus," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    2. Vincent Douchamps & Matteo Volo & Alessandro Torcini & Demian Battaglia & Romain Goutagny, 2024. "Gamma oscillatory complexity conveys behavioral information in hippocampal networks," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    3. M. Agustina Frechou & Sunaina S. Martin & Kelsey D. McDermott & Evan A. Huaman & Şölen Gökhan & Wolfgang A. Tomé & Ruben Coen-Cagli & J. Tiago Gonçalves, 2024. "Adult neurogenesis improves spatial information encoding in the mouse hippocampus," Nature Communications, Nature, vol. 15(1), pages 1-14, December.

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