A Sparse, Spatially Biased Subtype of Mature Granule Cell Dominates Recruitment in Hippocampal-Associated Behaviors

Summary: Animals can store information about experiences by activating specific neuronal populations, and subsequent reactivation of these neural ensembles can lead to recall of salient experiences. In the hippocampus, granule cells of the dentate gyrus participate in such memory engrams; however, w...

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Main Authors: Sarah R. Erwin, Weinan Sun, Monique Copeland, Sarah Lindo, Nelson Spruston, Mark S. Cembrowski
Format: Article
Language:English
Published: Elsevier 2020-04-01
Series:Cell Reports
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124720304617
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spelling doaj-06f42d084beb482280f186a9e77454cc2020-11-25T03:16:25ZengElsevierCell Reports2211-12472020-04-01314A Sparse, Spatially Biased Subtype of Mature Granule Cell Dominates Recruitment in Hippocampal-Associated BehaviorsSarah R. Erwin0Weinan Sun1Monique Copeland2Sarah Lindo3Nelson Spruston4Mark S. Cembrowski5Department of Cellular and Physiological Sciences, Life Sciences Institute, University of British Columbia, 2350 Health Sciences Boulevard, Vancouver, BC, Canada; Janelia Research Campus, Howard Hughes Medical Institute, 19700 Helix Drive, Ashburn, VA 20147, USAJanelia Research Campus, Howard Hughes Medical Institute, 19700 Helix Drive, Ashburn, VA 20147, USAJanelia Research Campus, Howard Hughes Medical Institute, 19700 Helix Drive, Ashburn, VA 20147, USAJanelia Research Campus, Howard Hughes Medical Institute, 19700 Helix Drive, Ashburn, VA 20147, USAJanelia Research Campus, Howard Hughes Medical Institute, 19700 Helix Drive, Ashburn, VA 20147, USADepartment of Cellular and Physiological Sciences, Life Sciences Institute, University of British Columbia, 2350 Health Sciences Boulevard, Vancouver, BC, Canada; Janelia Research Campus, Howard Hughes Medical Institute, 19700 Helix Drive, Ashburn, VA 20147, USA; Djavad Mowafaghian Centre for Brain Health, University of British Columbia, 2215 Wesbrook Mall, Vancouver, BC, Canada; Corresponding authorSummary: Animals can store information about experiences by activating specific neuronal populations, and subsequent reactivation of these neural ensembles can lead to recall of salient experiences. In the hippocampus, granule cells of the dentate gyrus participate in such memory engrams; however, whether there is an underlying logic to granule cell participation has not been examined. Here, we find that a range of novel experiences preferentially activates granule cells of the suprapyramidal blade relative to the infrapyramidal blade. Motivated by this, we identify a suprapyramidal-blade-enriched population of granule cells with distinct spatial, morphological, physiological, and developmental properties. Via transcriptomics, we map these traits onto a sparse and discrete granule cell subtype that is recruited at a 10-fold greater frequency than expected by subtype prevalence, constituting the majority of all recruited granule cells. Thus, in behaviors known to involve hippocampal-dependent memory formation, a rare and spatially localized subtype dominates overall granule cell recruitment. : Erwin et al. identify a sparse subtype of mature granule cell, spatially localized within the dentate gyrus, which dominates overall granule cell activity across a range of behavioral paradigms. Thus, subtype-specific heterogeneity exists and predicts cellular recruitment at the first stage of hippocampal processing. Keywords: dentate gyrus, granule cell, single-cell RNA-seq, transcriptomics, memory, cell type, hippocampushttp://www.sciencedirect.com/science/article/pii/S2211124720304617
collection DOAJ
language English
format Article
sources DOAJ
author Sarah R. Erwin
Weinan Sun
Monique Copeland
Sarah Lindo
Nelson Spruston
Mark S. Cembrowski
spellingShingle Sarah R. Erwin
Weinan Sun
Monique Copeland
Sarah Lindo
Nelson Spruston
Mark S. Cembrowski
A Sparse, Spatially Biased Subtype of Mature Granule Cell Dominates Recruitment in Hippocampal-Associated Behaviors
Cell Reports
author_facet Sarah R. Erwin
Weinan Sun
Monique Copeland
Sarah Lindo
Nelson Spruston
Mark S. Cembrowski
author_sort Sarah R. Erwin
title A Sparse, Spatially Biased Subtype of Mature Granule Cell Dominates Recruitment in Hippocampal-Associated Behaviors
title_short A Sparse, Spatially Biased Subtype of Mature Granule Cell Dominates Recruitment in Hippocampal-Associated Behaviors
title_full A Sparse, Spatially Biased Subtype of Mature Granule Cell Dominates Recruitment in Hippocampal-Associated Behaviors
title_fullStr A Sparse, Spatially Biased Subtype of Mature Granule Cell Dominates Recruitment in Hippocampal-Associated Behaviors
title_full_unstemmed A Sparse, Spatially Biased Subtype of Mature Granule Cell Dominates Recruitment in Hippocampal-Associated Behaviors
title_sort sparse, spatially biased subtype of mature granule cell dominates recruitment in hippocampal-associated behaviors
publisher Elsevier
series Cell Reports
issn 2211-1247
publishDate 2020-04-01
description Summary: Animals can store information about experiences by activating specific neuronal populations, and subsequent reactivation of these neural ensembles can lead to recall of salient experiences. In the hippocampus, granule cells of the dentate gyrus participate in such memory engrams; however, whether there is an underlying logic to granule cell participation has not been examined. Here, we find that a range of novel experiences preferentially activates granule cells of the suprapyramidal blade relative to the infrapyramidal blade. Motivated by this, we identify a suprapyramidal-blade-enriched population of granule cells with distinct spatial, morphological, physiological, and developmental properties. Via transcriptomics, we map these traits onto a sparse and discrete granule cell subtype that is recruited at a 10-fold greater frequency than expected by subtype prevalence, constituting the majority of all recruited granule cells. Thus, in behaviors known to involve hippocampal-dependent memory formation, a rare and spatially localized subtype dominates overall granule cell recruitment. : Erwin et al. identify a sparse subtype of mature granule cell, spatially localized within the dentate gyrus, which dominates overall granule cell activity across a range of behavioral paradigms. Thus, subtype-specific heterogeneity exists and predicts cellular recruitment at the first stage of hippocampal processing. Keywords: dentate gyrus, granule cell, single-cell RNA-seq, transcriptomics, memory, cell type, hippocampus
url http://www.sciencedirect.com/science/article/pii/S2211124720304617
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