Cargando…

Recurrent Excitatory Feedback From Mossy Cells Enhances Sparsity and Pattern Separation in the Dentate Gyrus via Indirect Feedback Inhibition

It is generally appreciated that storing memories of specific events in the mammalian brain, and associating features of the environment with behavioral outcomes requires fine-tuning of the strengths of connections between neurons through synaptic plasticity. It is less understood whether the organi...

Descripción completa

Detalles Bibliográficos
Autores principales: Galloni, Alessandro R., Samadzelkava, Aya, Hiremath, Kiran, Oumnov, Reuben, Milstein, Aaron D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8866186/
https://www.ncbi.nlm.nih.gov/pubmed/35221956
http://dx.doi.org/10.3389/fncom.2022.826278
_version_ 1784655783773863936
author Galloni, Alessandro R.
Samadzelkava, Aya
Hiremath, Kiran
Oumnov, Reuben
Milstein, Aaron D.
author_facet Galloni, Alessandro R.
Samadzelkava, Aya
Hiremath, Kiran
Oumnov, Reuben
Milstein, Aaron D.
author_sort Galloni, Alessandro R.
collection PubMed
description It is generally appreciated that storing memories of specific events in the mammalian brain, and associating features of the environment with behavioral outcomes requires fine-tuning of the strengths of connections between neurons through synaptic plasticity. It is less understood whether the organization of neuronal circuits comprised of multiple distinct neuronal cell types provides an architectural prior that facilitates learning and memory by generating unique patterns of neuronal activity in response to different stimuli in the environment, even before plasticity and learning occur. Here we simulated a neuronal network responding to sensory stimuli, and systematically determined the effects of specific neuronal cell types and connections on three key metrics of neuronal sensory representations: sparsity, selectivity, and discriminability. We found that when the total amount of input varied considerably across stimuli, standard feedforward and feedback inhibitory circuit motifs failed to discriminate all stimuli without sacrificing sparsity or selectivity. Interestingly, networks that included dedicated excitatory feedback interneurons based on the mossy cells of the hippocampal dentate gyrus exhibited improved pattern separation, a result that depended on the indirect recruitment of feedback inhibition. These results elucidate the roles of cellular diversity and neural circuit architecture on generating neuronal representations with properties advantageous for memory storage and recall.
format Online
Article
Text
id pubmed-8866186
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-88661862022-02-25 Recurrent Excitatory Feedback From Mossy Cells Enhances Sparsity and Pattern Separation in the Dentate Gyrus via Indirect Feedback Inhibition Galloni, Alessandro R. Samadzelkava, Aya Hiremath, Kiran Oumnov, Reuben Milstein, Aaron D. Front Comput Neurosci Neuroscience It is generally appreciated that storing memories of specific events in the mammalian brain, and associating features of the environment with behavioral outcomes requires fine-tuning of the strengths of connections between neurons through synaptic plasticity. It is less understood whether the organization of neuronal circuits comprised of multiple distinct neuronal cell types provides an architectural prior that facilitates learning and memory by generating unique patterns of neuronal activity in response to different stimuli in the environment, even before plasticity and learning occur. Here we simulated a neuronal network responding to sensory stimuli, and systematically determined the effects of specific neuronal cell types and connections on three key metrics of neuronal sensory representations: sparsity, selectivity, and discriminability. We found that when the total amount of input varied considerably across stimuli, standard feedforward and feedback inhibitory circuit motifs failed to discriminate all stimuli without sacrificing sparsity or selectivity. Interestingly, networks that included dedicated excitatory feedback interneurons based on the mossy cells of the hippocampal dentate gyrus exhibited improved pattern separation, a result that depended on the indirect recruitment of feedback inhibition. These results elucidate the roles of cellular diversity and neural circuit architecture on generating neuronal representations with properties advantageous for memory storage and recall. Frontiers Media S.A. 2022-02-10 /pmc/articles/PMC8866186/ /pubmed/35221956 http://dx.doi.org/10.3389/fncom.2022.826278 Text en Copyright © 2022 Galloni, Samadzelkava, Hiremath, Oumnov and Milstein. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Galloni, Alessandro R.
Samadzelkava, Aya
Hiremath, Kiran
Oumnov, Reuben
Milstein, Aaron D.
Recurrent Excitatory Feedback From Mossy Cells Enhances Sparsity and Pattern Separation in the Dentate Gyrus via Indirect Feedback Inhibition
title Recurrent Excitatory Feedback From Mossy Cells Enhances Sparsity and Pattern Separation in the Dentate Gyrus via Indirect Feedback Inhibition
title_full Recurrent Excitatory Feedback From Mossy Cells Enhances Sparsity and Pattern Separation in the Dentate Gyrus via Indirect Feedback Inhibition
title_fullStr Recurrent Excitatory Feedback From Mossy Cells Enhances Sparsity and Pattern Separation in the Dentate Gyrus via Indirect Feedback Inhibition
title_full_unstemmed Recurrent Excitatory Feedback From Mossy Cells Enhances Sparsity and Pattern Separation in the Dentate Gyrus via Indirect Feedback Inhibition
title_short Recurrent Excitatory Feedback From Mossy Cells Enhances Sparsity and Pattern Separation in the Dentate Gyrus via Indirect Feedback Inhibition
title_sort recurrent excitatory feedback from mossy cells enhances sparsity and pattern separation in the dentate gyrus via indirect feedback inhibition
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8866186/
https://www.ncbi.nlm.nih.gov/pubmed/35221956
http://dx.doi.org/10.3389/fncom.2022.826278
work_keys_str_mv AT gallonialessandror recurrentexcitatoryfeedbackfrommossycellsenhancessparsityandpatternseparationinthedentategyrusviaindirectfeedbackinhibition
AT samadzelkavaaya recurrentexcitatoryfeedbackfrommossycellsenhancessparsityandpatternseparationinthedentategyrusviaindirectfeedbackinhibition
AT hiremathkiran recurrentexcitatoryfeedbackfrommossycellsenhancessparsityandpatternseparationinthedentategyrusviaindirectfeedbackinhibition
AT oumnovreuben recurrentexcitatoryfeedbackfrommossycellsenhancessparsityandpatternseparationinthedentategyrusviaindirectfeedbackinhibition
AT milsteinaarond recurrentexcitatoryfeedbackfrommossycellsenhancessparsityandpatternseparationinthedentategyrusviaindirectfeedbackinhibition