Calcium Imaging Reveals Fast Tuning Dynamics of Hippocampal Place Cells and CA1 Population Activity during Free Exploration Task in Mice

Hippocampal place cells are a well-known object in neuroscience, but their place field formation in the first moments of navigating in a novel environment remains an ill-defined process. To address these dynamics, we performed in vivo imaging of neuronal activity in the CA1 field of the mouse hippoc...

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Main Authors: Vladimir P. Sotskov, Nikita A. Pospelov, Viktor V. Plusnin, Konstantin V. Anokhin
Format: Article
Language:English
Published: MDPI AG 2022-01-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/23/2/638
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author Vladimir P. Sotskov
Nikita A. Pospelov
Viktor V. Plusnin
Konstantin V. Anokhin
author_facet Vladimir P. Sotskov
Nikita A. Pospelov
Viktor V. Plusnin
Konstantin V. Anokhin
author_sort Vladimir P. Sotskov
collection DOAJ
description Hippocampal place cells are a well-known object in neuroscience, but their place field formation in the first moments of navigating in a novel environment remains an ill-defined process. To address these dynamics, we performed in vivo imaging of neuronal activity in the CA1 field of the mouse hippocampus using genetically encoded green calcium indicators, including the novel NCaMP7 and FGCaMP7, designed specifically for in vivo calcium imaging. Mice were injected with a viral vector encoding calcium sensor, head-mounted with an NVista HD miniscope, and allowed to explore a completely novel environment (circular track surrounded by visual cues) without any reinforcement stimuli, in order to avoid potential interference from reward-related behavior. First, we calculated the average time required for each CA1 cell to acquire its place field. We found that 25% of CA1 place fields were formed at the first arrival in the corresponding place, while the average tuning latency for all place fields in a novel environment equaled 247 s. After 24 h, when the environment was familiar to the animals, place fields formed faster, independent of retention of cognitive maps during this session. No cumulation of selectivity score was observed between these two sessions. Using dimensionality reduction, we demonstrated that the population activity of rapidly tuned CA1 place cells allowed the reconstruction of the geometry of the navigated circular maze; the distribution of reconstruction error between the mice was consistent with the distribution of the average place field selectivity score in them. Our data thus show that neuronal activity recorded with genetically encoded calcium sensors revealed fast behavior-dependent plasticity in the mouse hippocampus, resulting in the rapid formation of place fields and population activity that allowed the reconstruction of the geometry of the navigated maze.
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spelling doaj.art-32da002e528c47a588129db4b3ccd4e12023-11-23T14:01:47ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672022-01-0123263810.3390/ijms23020638Calcium Imaging Reveals Fast Tuning Dynamics of Hippocampal Place Cells and CA1 Population Activity during Free Exploration Task in MiceVladimir P. Sotskov0Nikita A. Pospelov1Viktor V. Plusnin2Konstantin V. Anokhin3Institute for Advanced Brain Studies, Lomonosov Moscow State University, 119991 Moscow, RussiaInstitute for Advanced Brain Studies, Lomonosov Moscow State University, 119991 Moscow, RussiaNational Research Center “Kurchatov Institute”, 123098 Moscow, RussiaInstitute for Advanced Brain Studies, Lomonosov Moscow State University, 119991 Moscow, RussiaHippocampal place cells are a well-known object in neuroscience, but their place field formation in the first moments of navigating in a novel environment remains an ill-defined process. To address these dynamics, we performed in vivo imaging of neuronal activity in the CA1 field of the mouse hippocampus using genetically encoded green calcium indicators, including the novel NCaMP7 and FGCaMP7, designed specifically for in vivo calcium imaging. Mice were injected with a viral vector encoding calcium sensor, head-mounted with an NVista HD miniscope, and allowed to explore a completely novel environment (circular track surrounded by visual cues) without any reinforcement stimuli, in order to avoid potential interference from reward-related behavior. First, we calculated the average time required for each CA1 cell to acquire its place field. We found that 25% of CA1 place fields were formed at the first arrival in the corresponding place, while the average tuning latency for all place fields in a novel environment equaled 247 s. After 24 h, when the environment was familiar to the animals, place fields formed faster, independent of retention of cognitive maps during this session. No cumulation of selectivity score was observed between these two sessions. Using dimensionality reduction, we demonstrated that the population activity of rapidly tuned CA1 place cells allowed the reconstruction of the geometry of the navigated circular maze; the distribution of reconstruction error between the mice was consistent with the distribution of the average place field selectivity score in them. Our data thus show that neuronal activity recorded with genetically encoded calcium sensors revealed fast behavior-dependent plasticity in the mouse hippocampus, resulting in the rapid formation of place fields and population activity that allowed the reconstruction of the geometry of the navigated maze.https://www.mdpi.com/1422-0067/23/2/638Ca2+ indicatorscalcium in vivo imagingplace cellsplace fieldscognitive maps
spellingShingle Vladimir P. Sotskov
Nikita A. Pospelov
Viktor V. Plusnin
Konstantin V. Anokhin
Calcium Imaging Reveals Fast Tuning Dynamics of Hippocampal Place Cells and CA1 Population Activity during Free Exploration Task in Mice
International Journal of Molecular Sciences
Ca2+ indicators
calcium in vivo imaging
place cells
place fields
cognitive maps
title Calcium Imaging Reveals Fast Tuning Dynamics of Hippocampal Place Cells and CA1 Population Activity during Free Exploration Task in Mice
title_full Calcium Imaging Reveals Fast Tuning Dynamics of Hippocampal Place Cells and CA1 Population Activity during Free Exploration Task in Mice
title_fullStr Calcium Imaging Reveals Fast Tuning Dynamics of Hippocampal Place Cells and CA1 Population Activity during Free Exploration Task in Mice
title_full_unstemmed Calcium Imaging Reveals Fast Tuning Dynamics of Hippocampal Place Cells and CA1 Population Activity during Free Exploration Task in Mice
title_short Calcium Imaging Reveals Fast Tuning Dynamics of Hippocampal Place Cells and CA1 Population Activity during Free Exploration Task in Mice
title_sort calcium imaging reveals fast tuning dynamics of hippocampal place cells and ca1 population activity during free exploration task in mice
topic Ca2+ indicators
calcium in vivo imaging
place cells
place fields
cognitive maps
url https://www.mdpi.com/1422-0067/23/2/638
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AT viktorvplusnin calciumimagingrevealsfasttuningdynamicsofhippocampalplacecellsandca1populationactivityduringfreeexplorationtaskinmice
AT konstantinvanokhin calciumimagingrevealsfasttuningdynamicsofhippocampalplacecellsandca1populationactivityduringfreeexplorationtaskinmice