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Juxtacellular opto-tagging of hippocampal CA1 neurons in freely moving mice

Neural circuits are made of a vast diversity of neuronal cell types. While immense progress has been made in classifying neurons based on morphological, molecular, and functional properties, understanding how this heterogeneity contributes to brain function during natural behavior has remained large...

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Autores principales: Ding, Lingjun, Balsamo, Giuseppe, Chen, Hongbiao, Blanco-Hernandez, Eduardo, Zouridis, Ioannis S, Naumann, Robert, Preston-Ferrer, Patricia, Burgalossi, Andrea
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8791633/
https://www.ncbi.nlm.nih.gov/pubmed/35080491
http://dx.doi.org/10.7554/eLife.71720
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author Ding, Lingjun
Balsamo, Giuseppe
Chen, Hongbiao
Blanco-Hernandez, Eduardo
Zouridis, Ioannis S
Naumann, Robert
Preston-Ferrer, Patricia
Burgalossi, Andrea
author_facet Ding, Lingjun
Balsamo, Giuseppe
Chen, Hongbiao
Blanco-Hernandez, Eduardo
Zouridis, Ioannis S
Naumann, Robert
Preston-Ferrer, Patricia
Burgalossi, Andrea
author_sort Ding, Lingjun
collection PubMed
description Neural circuits are made of a vast diversity of neuronal cell types. While immense progress has been made in classifying neurons based on morphological, molecular, and functional properties, understanding how this heterogeneity contributes to brain function during natural behavior has remained largely unresolved. In the present study, we combined the juxtacellular recording and labeling technique with optogenetics in freely moving mice. This allowed us to selectively target molecularly defined cell classes for in vivo single-cell recordings and morphological analysis. We validated this strategy in the CA1 region of the mouse hippocampus by restricting Channelrhodopsin expression to Calbindin-positive neurons. Directly versus indirectly light-activated neurons could be readily distinguished based on the latencies of light-evoked spikes, with juxtacellular labeling and post hoc histological analysis providing ‘ground-truth’ validation. Using these opto-juxtacellular procedures in freely moving mice, we found that Calbindin-positive CA1 pyramidal cells were weakly spatially modulated and conveyed less spatial information than Calbindin-negative neurons – pointing to pyramidal cell identity as a key determinant for neuronal recruitment into the hippocampal spatial map. Thus, our method complements current in vivo techniques by enabling optogenetic-assisted structure–function analysis of single neurons recorded during natural, unrestrained behavior.
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spelling pubmed-87916332022-01-27 Juxtacellular opto-tagging of hippocampal CA1 neurons in freely moving mice Ding, Lingjun Balsamo, Giuseppe Chen, Hongbiao Blanco-Hernandez, Eduardo Zouridis, Ioannis S Naumann, Robert Preston-Ferrer, Patricia Burgalossi, Andrea eLife Neuroscience Neural circuits are made of a vast diversity of neuronal cell types. While immense progress has been made in classifying neurons based on morphological, molecular, and functional properties, understanding how this heterogeneity contributes to brain function during natural behavior has remained largely unresolved. In the present study, we combined the juxtacellular recording and labeling technique with optogenetics in freely moving mice. This allowed us to selectively target molecularly defined cell classes for in vivo single-cell recordings and morphological analysis. We validated this strategy in the CA1 region of the mouse hippocampus by restricting Channelrhodopsin expression to Calbindin-positive neurons. Directly versus indirectly light-activated neurons could be readily distinguished based on the latencies of light-evoked spikes, with juxtacellular labeling and post hoc histological analysis providing ‘ground-truth’ validation. Using these opto-juxtacellular procedures in freely moving mice, we found that Calbindin-positive CA1 pyramidal cells were weakly spatially modulated and conveyed less spatial information than Calbindin-negative neurons – pointing to pyramidal cell identity as a key determinant for neuronal recruitment into the hippocampal spatial map. Thus, our method complements current in vivo techniques by enabling optogenetic-assisted structure–function analysis of single neurons recorded during natural, unrestrained behavior. eLife Sciences Publications, Ltd 2022-01-26 /pmc/articles/PMC8791633/ /pubmed/35080491 http://dx.doi.org/10.7554/eLife.71720 Text en © 2022, Ding et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Ding, Lingjun
Balsamo, Giuseppe
Chen, Hongbiao
Blanco-Hernandez, Eduardo
Zouridis, Ioannis S
Naumann, Robert
Preston-Ferrer, Patricia
Burgalossi, Andrea
Juxtacellular opto-tagging of hippocampal CA1 neurons in freely moving mice
title Juxtacellular opto-tagging of hippocampal CA1 neurons in freely moving mice
title_full Juxtacellular opto-tagging of hippocampal CA1 neurons in freely moving mice
title_fullStr Juxtacellular opto-tagging of hippocampal CA1 neurons in freely moving mice
title_full_unstemmed Juxtacellular opto-tagging of hippocampal CA1 neurons in freely moving mice
title_short Juxtacellular opto-tagging of hippocampal CA1 neurons in freely moving mice
title_sort juxtacellular opto-tagging of hippocampal ca1 neurons in freely moving mice
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8791633/
https://www.ncbi.nlm.nih.gov/pubmed/35080491
http://dx.doi.org/10.7554/eLife.71720
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