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Adult-born granule cells improve stimulus encoding and discrimination in the dentate gyrus

Heterogeneity plays an important role in diversifying neural responses to support brain function. Adult neurogenesis provides the dentate gyrus with a heterogeneous population of granule cells (GCs) that were born and developed their properties at different times. Immature GCs have distinct intrinsi...

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Autores principales: Arribas, Diego M, Marin-Burgin, Antonia, Morelli, Luis G
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10476965/
https://www.ncbi.nlm.nih.gov/pubmed/37584478
http://dx.doi.org/10.7554/eLife.80250
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author Arribas, Diego M
Marin-Burgin, Antonia
Morelli, Luis G
author_facet Arribas, Diego M
Marin-Burgin, Antonia
Morelli, Luis G
author_sort Arribas, Diego M
collection PubMed
description Heterogeneity plays an important role in diversifying neural responses to support brain function. Adult neurogenesis provides the dentate gyrus with a heterogeneous population of granule cells (GCs) that were born and developed their properties at different times. Immature GCs have distinct intrinsic and synaptic properties than mature GCs and are needed for correct encoding and discrimination in spatial tasks. How immature GCs enhance the encoding of information to support these functions is not well understood. Here, we record the responses to fluctuating current injections of GCs of different ages in mouse hippocampal slices to study how they encode stimuli. Immature GCs produce unreliable responses compared to mature GCs, exhibiting imprecise spike timings across repeated stimulation. We use a statistical model to describe the stimulus-response transformation performed by GCs of different ages. We fit this model to the data and obtain parameters that capture GCs’ encoding properties. Parameter values from this fit reflect the maturational differences of the population and indicate that immature GCs perform a differential encoding of stimuli. To study how this age heterogeneity influences encoding by a population, we perform stimulus decoding using populations that contain GCs of different ages. We find that, despite their individual unreliability, immature GCs enhance the fidelity of the signal encoded by the population and improve the discrimination of similar time-dependent stimuli. Thus, the observed heterogeneity confers the population with enhanced encoding capabilities.
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spelling pubmed-104769652023-09-05 Adult-born granule cells improve stimulus encoding and discrimination in the dentate gyrus Arribas, Diego M Marin-Burgin, Antonia Morelli, Luis G eLife Computational and Systems Biology Heterogeneity plays an important role in diversifying neural responses to support brain function. Adult neurogenesis provides the dentate gyrus with a heterogeneous population of granule cells (GCs) that were born and developed their properties at different times. Immature GCs have distinct intrinsic and synaptic properties than mature GCs and are needed for correct encoding and discrimination in spatial tasks. How immature GCs enhance the encoding of information to support these functions is not well understood. Here, we record the responses to fluctuating current injections of GCs of different ages in mouse hippocampal slices to study how they encode stimuli. Immature GCs produce unreliable responses compared to mature GCs, exhibiting imprecise spike timings across repeated stimulation. We use a statistical model to describe the stimulus-response transformation performed by GCs of different ages. We fit this model to the data and obtain parameters that capture GCs’ encoding properties. Parameter values from this fit reflect the maturational differences of the population and indicate that immature GCs perform a differential encoding of stimuli. To study how this age heterogeneity influences encoding by a population, we perform stimulus decoding using populations that contain GCs of different ages. We find that, despite their individual unreliability, immature GCs enhance the fidelity of the signal encoded by the population and improve the discrimination of similar time-dependent stimuli. Thus, the observed heterogeneity confers the population with enhanced encoding capabilities. eLife Sciences Publications, Ltd 2023-08-16 /pmc/articles/PMC10476965/ /pubmed/37584478 http://dx.doi.org/10.7554/eLife.80250 Text en © 2023, Arribas 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 Computational and Systems Biology
Arribas, Diego M
Marin-Burgin, Antonia
Morelli, Luis G
Adult-born granule cells improve stimulus encoding and discrimination in the dentate gyrus
title Adult-born granule cells improve stimulus encoding and discrimination in the dentate gyrus
title_full Adult-born granule cells improve stimulus encoding and discrimination in the dentate gyrus
title_fullStr Adult-born granule cells improve stimulus encoding and discrimination in the dentate gyrus
title_full_unstemmed Adult-born granule cells improve stimulus encoding and discrimination in the dentate gyrus
title_short Adult-born granule cells improve stimulus encoding and discrimination in the dentate gyrus
title_sort adult-born granule cells improve stimulus encoding and discrimination in the dentate gyrus
topic Computational and Systems Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10476965/
https://www.ncbi.nlm.nih.gov/pubmed/37584478
http://dx.doi.org/10.7554/eLife.80250
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