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A distributed neural code in the dentate gyrus and in CA1

Fabio Stefanini, Mazen A. Kheirbek, Lyudmila Kushnir, Jessica C. Jimenez, Joshua H. Jennings, Garret D. Stuber, René Hen, Stefano Fusi
doi: https://doi.org/10.1101/292953
Fabio Stefanini
1Center for Theoretical Neuroscience, College of Physicians and Surgeons, Columbia University
2Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University
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Mazen A. Kheirbek
3Department of Psychiatry, University of California, San Francisco, San Francisco, CA, USA
4Neuroscience Graduate Program, University of California, San Francisco, San Francisco, CA, USA
5Weill Institute for Neurosciences, University of California, San Francisco, San Francisco, CA, USA
6Kavli Institute for Fundamental Neuroscience, University of California, San Francisco, San Francisco, CA, USA
7Center for Integrative Neuroscience, University of California, San Francisco, San Francisco, CA, USA
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Lyudmila Kushnir
8GNT - LNC, Department d’ètudes cognitives, École Normale Supérieure, INSERM, PSL Research University, 75005, Paris, France
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Jessica C. Jimenez
13Departments of Neuroscience, Psychiatry & Pharmacology, Columbia University, New York, NY, USA
14Division of Integrative Neuroscience, Department of Psychiatry, New York State Psychiatric Institute, New York, NY, USA
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Joshua H. Jennings
9Department of Bioengineering, Stanford University, Stanford, CA, 94305, USA
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Garret D. Stuber
10Department of Psychiatry, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA
11Neuroscience Center, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA
12Department of Cell Biology and Physiology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA
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René Hen
13Departments of Neuroscience, Psychiatry & Pharmacology, Columbia University, New York, NY, USA
14Division of Integrative Neuroscience, Department of Psychiatry, New York State Psychiatric Institute, New York, NY, USA
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  • For correspondence: rh95@cumc.columbia.edu sf2237@columbia.edu
Stefano Fusi
1Center for Theoretical Neuroscience, College of Physicians and Surgeons, Columbia University
2Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University
15Kavli Institute for Brain Sciences, Columbia University
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  • For correspondence: rh95@cumc.columbia.edu sf2237@columbia.edu
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ABSTRACT

The tuning properties of neurons in a given brain region have been traditionally viewed as the under-pinnings of computation in neural circuits. However, at the higher levels of processing, specialization is often elusive, instead a mix of sensory, cognitive and behavioural quantities drive neural activity. In such networks, ensembles of neurons, rather than single units with easily interpretable tuning properties, encode behaviourally relevant variables. Here we show that this is the case also in the dentate gyrus and CA1 subregions of the hippocampus. Using calcium imaging in freely moving mice, we decoded the instantaneous position, direction of motion and speed from the activity of hundreds of cells in the hippocampus of mice freely exploring an arena. For the vast majority of neurons in both regions, their response properties were not predictive of their importance for encoding position. Furthermore, we could decode position from populations of cells that were important for decoding direction of motion and vice versa, showing that these quantities are encoded by largely overlapping ensembles as in distributed neural code. Finally, we found that correlated activities had an impact on decoding performance in CA1 but not in dentate gyrus, suggesting different enconding strategies for these areas. Our analysis indicates that classical methods of analysis based on single cell response properties might be insufficient to accurately characterize the neural computation in a given area. In contrast, population analysis may help highlight previously overlooked properties of hippocampal circuits.

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Posted February 28, 2019.
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A distributed neural code in the dentate gyrus and in CA1
Fabio Stefanini, Mazen A. Kheirbek, Lyudmila Kushnir, Jessica C. Jimenez, Joshua H. Jennings, Garret D. Stuber, René Hen, Stefano Fusi
bioRxiv 292953; doi: https://doi.org/10.1101/292953
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A distributed neural code in the dentate gyrus and in CA1
Fabio Stefanini, Mazen A. Kheirbek, Lyudmila Kushnir, Jessica C. Jimenez, Joshua H. Jennings, Garret D. Stuber, René Hen, Stefano Fusi
bioRxiv 292953; doi: https://doi.org/10.1101/292953

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