Cargando…

Cell type composition and circuit organization of clonally related excitatory neurons in the juvenile mouse neocortex

Clones of excitatory neurons derived from a common progenitor have been proposed to serve as elementary information processing modules in the neocortex. To characterize the cell types and circuit diagram of clonally related excitatory neurons, we performed multi-cell patch clamp recordings and Patch...

Descripción completa

Detalles Bibliográficos
Autores principales: Cadwell, Cathryn R, Scala, Federico, Fahey, Paul G, Kobak, Dmitry, Mulherkar, Shalaka, Sinz, Fabian H, Papadopoulos, Stelios, Tan, Zheng H, Johnsson, Per, Hartmanis, Leonard, Li, Shuang, Cotton, Ronald J, Tolias, Kimberley F, Sandberg, Rickard, Berens, Philipp, Jiang, Xiaolong, Tolias, Andreas Savas
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7162653/
https://www.ncbi.nlm.nih.gov/pubmed/32134385
http://dx.doi.org/10.7554/eLife.52951
_version_ 1783523073423572992
author Cadwell, Cathryn R
Scala, Federico
Fahey, Paul G
Kobak, Dmitry
Mulherkar, Shalaka
Sinz, Fabian H
Papadopoulos, Stelios
Tan, Zheng H
Johnsson, Per
Hartmanis, Leonard
Li, Shuang
Cotton, Ronald J
Tolias, Kimberley F
Sandberg, Rickard
Berens, Philipp
Jiang, Xiaolong
Tolias, Andreas Savas
author_facet Cadwell, Cathryn R
Scala, Federico
Fahey, Paul G
Kobak, Dmitry
Mulherkar, Shalaka
Sinz, Fabian H
Papadopoulos, Stelios
Tan, Zheng H
Johnsson, Per
Hartmanis, Leonard
Li, Shuang
Cotton, Ronald J
Tolias, Kimberley F
Sandberg, Rickard
Berens, Philipp
Jiang, Xiaolong
Tolias, Andreas Savas
author_sort Cadwell, Cathryn R
collection PubMed
description Clones of excitatory neurons derived from a common progenitor have been proposed to serve as elementary information processing modules in the neocortex. To characterize the cell types and circuit diagram of clonally related excitatory neurons, we performed multi-cell patch clamp recordings and Patch-seq on neurons derived from Nestin-positive progenitors labeled by tamoxifen induction at embryonic day 10.5. The resulting clones are derived from two radial glia on average, span cortical layers 2–6, and are composed of a random sampling of transcriptomic cell types. We find an interaction between shared lineage and connection type: related neurons are more likely to be connected vertically across cortical layers, but not laterally within the same layer. These findings challenge the view that related neurons show uniformly increased connectivity and suggest that integration of vertical intra-clonal input with lateral inter-clonal input may represent a developmentally programmed connectivity motif supporting the emergence of functional circuits.
format Online
Article
Text
id pubmed-7162653
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher eLife Sciences Publications, Ltd
record_format MEDLINE/PubMed
spelling pubmed-71626532020-04-20 Cell type composition and circuit organization of clonally related excitatory neurons in the juvenile mouse neocortex Cadwell, Cathryn R Scala, Federico Fahey, Paul G Kobak, Dmitry Mulherkar, Shalaka Sinz, Fabian H Papadopoulos, Stelios Tan, Zheng H Johnsson, Per Hartmanis, Leonard Li, Shuang Cotton, Ronald J Tolias, Kimberley F Sandberg, Rickard Berens, Philipp Jiang, Xiaolong Tolias, Andreas Savas eLife Developmental Biology Clones of excitatory neurons derived from a common progenitor have been proposed to serve as elementary information processing modules in the neocortex. To characterize the cell types and circuit diagram of clonally related excitatory neurons, we performed multi-cell patch clamp recordings and Patch-seq on neurons derived from Nestin-positive progenitors labeled by tamoxifen induction at embryonic day 10.5. The resulting clones are derived from two radial glia on average, span cortical layers 2–6, and are composed of a random sampling of transcriptomic cell types. We find an interaction between shared lineage and connection type: related neurons are more likely to be connected vertically across cortical layers, but not laterally within the same layer. These findings challenge the view that related neurons show uniformly increased connectivity and suggest that integration of vertical intra-clonal input with lateral inter-clonal input may represent a developmentally programmed connectivity motif supporting the emergence of functional circuits. eLife Sciences Publications, Ltd 2020-03-05 /pmc/articles/PMC7162653/ /pubmed/32134385 http://dx.doi.org/10.7554/eLife.52951 Text en © 2020, Cadwell et al http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Developmental Biology
Cadwell, Cathryn R
Scala, Federico
Fahey, Paul G
Kobak, Dmitry
Mulherkar, Shalaka
Sinz, Fabian H
Papadopoulos, Stelios
Tan, Zheng H
Johnsson, Per
Hartmanis, Leonard
Li, Shuang
Cotton, Ronald J
Tolias, Kimberley F
Sandberg, Rickard
Berens, Philipp
Jiang, Xiaolong
Tolias, Andreas Savas
Cell type composition and circuit organization of clonally related excitatory neurons in the juvenile mouse neocortex
title Cell type composition and circuit organization of clonally related excitatory neurons in the juvenile mouse neocortex
title_full Cell type composition and circuit organization of clonally related excitatory neurons in the juvenile mouse neocortex
title_fullStr Cell type composition and circuit organization of clonally related excitatory neurons in the juvenile mouse neocortex
title_full_unstemmed Cell type composition and circuit organization of clonally related excitatory neurons in the juvenile mouse neocortex
title_short Cell type composition and circuit organization of clonally related excitatory neurons in the juvenile mouse neocortex
title_sort cell type composition and circuit organization of clonally related excitatory neurons in the juvenile mouse neocortex
topic Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7162653/
https://www.ncbi.nlm.nih.gov/pubmed/32134385
http://dx.doi.org/10.7554/eLife.52951
work_keys_str_mv AT cadwellcathrynr celltypecompositionandcircuitorganizationofclonallyrelatedexcitatoryneuronsinthejuvenilemouseneocortex
AT scalafederico celltypecompositionandcircuitorganizationofclonallyrelatedexcitatoryneuronsinthejuvenilemouseneocortex
AT faheypaulg celltypecompositionandcircuitorganizationofclonallyrelatedexcitatoryneuronsinthejuvenilemouseneocortex
AT kobakdmitry celltypecompositionandcircuitorganizationofclonallyrelatedexcitatoryneuronsinthejuvenilemouseneocortex
AT mulherkarshalaka celltypecompositionandcircuitorganizationofclonallyrelatedexcitatoryneuronsinthejuvenilemouseneocortex
AT sinzfabianh celltypecompositionandcircuitorganizationofclonallyrelatedexcitatoryneuronsinthejuvenilemouseneocortex
AT papadopoulosstelios celltypecompositionandcircuitorganizationofclonallyrelatedexcitatoryneuronsinthejuvenilemouseneocortex
AT tanzhengh celltypecompositionandcircuitorganizationofclonallyrelatedexcitatoryneuronsinthejuvenilemouseneocortex
AT johnssonper celltypecompositionandcircuitorganizationofclonallyrelatedexcitatoryneuronsinthejuvenilemouseneocortex
AT hartmanisleonard celltypecompositionandcircuitorganizationofclonallyrelatedexcitatoryneuronsinthejuvenilemouseneocortex
AT lishuang celltypecompositionandcircuitorganizationofclonallyrelatedexcitatoryneuronsinthejuvenilemouseneocortex
AT cottonronaldj celltypecompositionandcircuitorganizationofclonallyrelatedexcitatoryneuronsinthejuvenilemouseneocortex
AT toliaskimberleyf celltypecompositionandcircuitorganizationofclonallyrelatedexcitatoryneuronsinthejuvenilemouseneocortex
AT sandbergrickard celltypecompositionandcircuitorganizationofclonallyrelatedexcitatoryneuronsinthejuvenilemouseneocortex
AT berensphilipp celltypecompositionandcircuitorganizationofclonallyrelatedexcitatoryneuronsinthejuvenilemouseneocortex
AT jiangxiaolong celltypecompositionandcircuitorganizationofclonallyrelatedexcitatoryneuronsinthejuvenilemouseneocortex
AT toliasandreassavas celltypecompositionandcircuitorganizationofclonallyrelatedexcitatoryneuronsinthejuvenilemouseneocortex