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The dendritic spatial code: branch-specific place tuning and its experience-dependent decoupling

Shannon K. Rashid, Victor Pedrosa, Martial A. Dufour, Jason J. Moore, Spyridon Chavlis, Rodrigo G. Delatorre, Panayiota Poirazi, Claudia Clopath, Jayeeta Basu
doi: https://doi.org/10.1101/2020.01.24.916643
Shannon K. Rashid
New York University Neuroscience Institute, New York University, New York, NY 10016, USADepartment of Neuroscience and Physiology, New York University School of Medicine, New York, NY 10016, USA
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Victor Pedrosa
Department of Bioengineering, Imperial College London, London, SW7 2AZ, UKCAPES Foundation, Ministry of Education of Brazil, Brasilia, 70040-020, Brazil
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Martial A. Dufour
New York University Neuroscience Institute, New York University, New York, NY 10016, USADepartment of Neuroscience and Physiology, New York University School of Medicine, New York, NY 10016, USA
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Jason J. Moore
New York University Neuroscience Institute, New York University, New York, NY 10016, USADepartment of Neuroscience and Physiology, New York University School of Medicine, New York, NY 10016, USA
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Spyridon Chavlis
Institute of Molecular Biology and Biotechnology (IMBB), Foundation for Research and Technology-Hellas (FORTH), Heraklion, Crete, Greece
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Rodrigo G. Delatorre
New York University Neuroscience Institute, New York University, New York, NY 10016, USADepartment of Neuroscience and Physiology, New York University School of Medicine, New York, NY 10016, USA
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Panayiota Poirazi
Institute of Molecular Biology and Biotechnology (IMBB), Foundation for Research and Technology-Hellas (FORTH), Heraklion, Crete, Greece
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Claudia Clopath
Department of Bioengineering, Imperial College London, London, SW7 2AZ, UK
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Jayeeta Basu
New York University Neuroscience Institute, New York University, New York, NY 10016, USADepartment of Neuroscience and Physiology, New York University School of Medicine, New York, NY 10016, USACenter for Neural Science, New York University, New York, NY 10003, USADepartment of Psychiatry, New York University School of Medicine, New York, NY 10016, USA
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  • For correspondence: jayeeta.basu@nyulangone.org
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Abstract

Dendrites of pyramidal neurons integrate different sensory inputs, and non-linear dendritic computations drive feature selective tuning and plasticity. Yet little is known about how dendrites themselves represent the environment, the degree to which they are coupled to their soma, and how that coupling is sculpted with experience. In order to answer these questions, we developed a novel preparation in which we image soma and connected dendrites in a single plane across days using in vivo two-photon microscopy. Using this preparation, we monitored spatially tuned activity in area CA3 of the hippocampus in head-fixed mice running on a linear track. We identified “place dendrites”, which can stably and precisely represent both familiar and novel spatial environments. Dendrites could display place tuning independent of their connected soma and even their sister dendritic branches, the first evidence for branch-specific tuning in the hippocampus. In a familiar environment, spatially tuned somata were more decoupled from their dendrites as compared to non-tuned somata. This relationship was absent in a novel environment, suggesting an experience dependent selective gating of dendritic spatial inputs. We then built a data-driven multicompartment computational model that could capture the experimentally observed correlations. Our model predicts that place cells exhibiting branch-specific tuning have more flexible place fields, while neurons with homogenous or co-tuned dendritic branches have higher place field stability. These findings demonstrate that spatial representation is organized in a branch-specific manner within dendrites of hippocampal pyramidal cells. Further, spatial inputs from dendrites to soma are selectively and dynamically gated in an experience-dependent manner, endowing both flexibility and stability to the cognitive map of space.

One sentence summary Hippocampal pyramidal cells show branch-specific tuning for different place fields, and their coupling to their soma changes with experience of an environment.

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Posted January 24, 2020.
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The dendritic spatial code: branch-specific place tuning and its experience-dependent decoupling
Shannon K. Rashid, Victor Pedrosa, Martial A. Dufour, Jason J. Moore, Spyridon Chavlis, Rodrigo G. Delatorre, Panayiota Poirazi, Claudia Clopath, Jayeeta Basu
bioRxiv 2020.01.24.916643; doi: https://doi.org/10.1101/2020.01.24.916643
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The dendritic spatial code: branch-specific place tuning and its experience-dependent decoupling
Shannon K. Rashid, Victor Pedrosa, Martial A. Dufour, Jason J. Moore, Spyridon Chavlis, Rodrigo G. Delatorre, Panayiota Poirazi, Claudia Clopath, Jayeeta Basu
bioRxiv 2020.01.24.916643; doi: https://doi.org/10.1101/2020.01.24.916643

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