GABAergic CA1 neurons are more stable following context changes than glutamatergic cells

Abstract The CA1 region of the hippocampus contains both glutamatergic pyramidal cells and GABAergic interneurons. Numerous reports have characterized glutamatergic CAMK2A cell activity, showing how these cells respond to environmental changes such as local cue rotation and context re-sizing. Additi...

Full description

Bibliographic Details
Main Authors: Peter J. Schuette, Juliane M. Ikebara, Sandra Maesta-Pereira, Anita Torossian, Ekayana Sethi, Alexandre H. Kihara, Jonathan C. Kao, Fernando M. C. V. Reis, Avishek Adhikari
Format: Article
Language:English
Published: Nature Portfolio 2022-06-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-022-13799-6
_version_ 1811334578668830720
author Peter J. Schuette
Juliane M. Ikebara
Sandra Maesta-Pereira
Anita Torossian
Ekayana Sethi
Alexandre H. Kihara
Jonathan C. Kao
Fernando M. C. V. Reis
Avishek Adhikari
author_facet Peter J. Schuette
Juliane M. Ikebara
Sandra Maesta-Pereira
Anita Torossian
Ekayana Sethi
Alexandre H. Kihara
Jonathan C. Kao
Fernando M. C. V. Reis
Avishek Adhikari
author_sort Peter J. Schuette
collection DOAJ
description Abstract The CA1 region of the hippocampus contains both glutamatergic pyramidal cells and GABAergic interneurons. Numerous reports have characterized glutamatergic CAMK2A cell activity, showing how these cells respond to environmental changes such as local cue rotation and context re-sizing. Additionally, the long-term stability of spatial encoding and turnover of these cells across days is also well-characterized. In contrast, these classic hippocampal experiments have never been conducted with CA1 GABAergic cells. Here, we use chronic calcium imaging of male and female mice to compare the neural activity of VGAT and CAMK2A cells during exploration of unaltered environments and also during exposure to contexts before and after rotating and changing the length of the context across multiple recording days. Intriguingly, compared to CAMK2A cells, VGAT cells showed decreased remapping induced by environmental changes, such as context rotations and contextual length resizing. However, GABAergic neurons were also less likely than glutamatergic neurons to remain active and exhibit consistent place coding across recording days. Interestingly, despite showing significant spatial remapping across days, GABAergic cells had stable speed encoding between days. Thus, compared to glutamatergic cells, spatial encoding of GABAergic cells is more stable during within-session environmental perturbations, but is less stable across days. These insights may be crucial in accurately modeling the features and constraints of hippocampal dynamics in spatial coding.
first_indexed 2024-04-13T17:10:18Z
format Article
id doaj.art-abb180db018f4399a8b1a97c0182fe28
institution Directory Open Access Journal
issn 2045-2322
language English
last_indexed 2024-04-13T17:10:18Z
publishDate 2022-06-01
publisher Nature Portfolio
record_format Article
series Scientific Reports
spelling doaj.art-abb180db018f4399a8b1a97c0182fe282022-12-22T02:38:18ZengNature PortfolioScientific Reports2045-23222022-06-0112111810.1038/s41598-022-13799-6GABAergic CA1 neurons are more stable following context changes than glutamatergic cellsPeter J. Schuette0Juliane M. Ikebara1Sandra Maesta-Pereira2Anita Torossian3Ekayana Sethi4Alexandre H. Kihara5Jonathan C. Kao6Fernando M. C. V. Reis7Avishek Adhikari8Department of Psychology, University of California, Los AngelesCentro de Matemática, Computação e Cognição, Universidade Federal do ABCDepartment of Psychology, University of California, Los AngelesDepartment of Psychology, University of California, Los AngelesDepartment of Psychology, University of California, Los AngelesCentro de Matemática, Computação e Cognição, Universidade Federal do ABCDepartment of Electrical and Computer Engineering, University of California, Los AngelesDepartment of Psychology, University of California, Los AngelesDepartment of Psychology, University of California, Los AngelesAbstract The CA1 region of the hippocampus contains both glutamatergic pyramidal cells and GABAergic interneurons. Numerous reports have characterized glutamatergic CAMK2A cell activity, showing how these cells respond to environmental changes such as local cue rotation and context re-sizing. Additionally, the long-term stability of spatial encoding and turnover of these cells across days is also well-characterized. In contrast, these classic hippocampal experiments have never been conducted with CA1 GABAergic cells. Here, we use chronic calcium imaging of male and female mice to compare the neural activity of VGAT and CAMK2A cells during exploration of unaltered environments and also during exposure to contexts before and after rotating and changing the length of the context across multiple recording days. Intriguingly, compared to CAMK2A cells, VGAT cells showed decreased remapping induced by environmental changes, such as context rotations and contextual length resizing. However, GABAergic neurons were also less likely than glutamatergic neurons to remain active and exhibit consistent place coding across recording days. Interestingly, despite showing significant spatial remapping across days, GABAergic cells had stable speed encoding between days. Thus, compared to glutamatergic cells, spatial encoding of GABAergic cells is more stable during within-session environmental perturbations, but is less stable across days. These insights may be crucial in accurately modeling the features and constraints of hippocampal dynamics in spatial coding.https://doi.org/10.1038/s41598-022-13799-6
spellingShingle Peter J. Schuette
Juliane M. Ikebara
Sandra Maesta-Pereira
Anita Torossian
Ekayana Sethi
Alexandre H. Kihara
Jonathan C. Kao
Fernando M. C. V. Reis
Avishek Adhikari
GABAergic CA1 neurons are more stable following context changes than glutamatergic cells
Scientific Reports
title GABAergic CA1 neurons are more stable following context changes than glutamatergic cells
title_full GABAergic CA1 neurons are more stable following context changes than glutamatergic cells
title_fullStr GABAergic CA1 neurons are more stable following context changes than glutamatergic cells
title_full_unstemmed GABAergic CA1 neurons are more stable following context changes than glutamatergic cells
title_short GABAergic CA1 neurons are more stable following context changes than glutamatergic cells
title_sort gabaergic ca1 neurons are more stable following context changes than glutamatergic cells
url https://doi.org/10.1038/s41598-022-13799-6
work_keys_str_mv AT peterjschuette gabaergicca1neuronsaremorestablefollowingcontextchangesthanglutamatergiccells
AT julianemikebara gabaergicca1neuronsaremorestablefollowingcontextchangesthanglutamatergiccells
AT sandramaestapereira gabaergicca1neuronsaremorestablefollowingcontextchangesthanglutamatergiccells
AT anitatorossian gabaergicca1neuronsaremorestablefollowingcontextchangesthanglutamatergiccells
AT ekayanasethi gabaergicca1neuronsaremorestablefollowingcontextchangesthanglutamatergiccells
AT alexandrehkihara gabaergicca1neuronsaremorestablefollowingcontextchangesthanglutamatergiccells
AT jonathanckao gabaergicca1neuronsaremorestablefollowingcontextchangesthanglutamatergiccells
AT fernandomcvreis gabaergicca1neuronsaremorestablefollowingcontextchangesthanglutamatergiccells
AT avishekadhikari gabaergicca1neuronsaremorestablefollowingcontextchangesthanglutamatergiccells