Cargando…

Release probability increases towards distal dendrites boosting high-frequency signal transfer in the rodent hippocampus

Dendritic integration of synaptic inputs involves their increased electrotonic attenuation at distal dendrites, which can be counterbalanced by the increased synaptic receptor density. However, during network activity, the influence of individual synapses depends on their release fidelity, the dendr...

Descripción completa

Detalles Bibliográficos
Autores principales: Jensen, Thomas P, Kopach, Olga, Reynolds, James P, Savtchenko, Leonid P, Rusakov, Dmitri A
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7837677/
https://www.ncbi.nlm.nih.gov/pubmed/33438578
http://dx.doi.org/10.7554/eLife.62588
_version_ 1783643004777529344
author Jensen, Thomas P
Kopach, Olga
Reynolds, James P
Savtchenko, Leonid P
Rusakov, Dmitri A
author_facet Jensen, Thomas P
Kopach, Olga
Reynolds, James P
Savtchenko, Leonid P
Rusakov, Dmitri A
author_sort Jensen, Thomas P
collection PubMed
description Dendritic integration of synaptic inputs involves their increased electrotonic attenuation at distal dendrites, which can be counterbalanced by the increased synaptic receptor density. However, during network activity, the influence of individual synapses depends on their release fidelity, the dendritic distribution of which remains poorly understood. Here, we employed classical optical quantal analyses and a genetically encoded optical glutamate sensor in acute hippocampal slices of rats and mice to monitor glutamate release at CA3-CA1 synapses. We find that their release probability increases with greater distances from the soma. Similar-fidelity synapses tend to group together, whereas release probability shows no trends regarding the branch ends. Simulations with a realistic CA1 pyramidal cell hosting stochastic synapses suggest that the observed trends boost signal transfer fidelity, particularly at higher input frequencies. Because high-frequency bursting has been associated with learning, the release probability pattern we have found may play a key role in memory trace formation.
format Online
Article
Text
id pubmed-7837677
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher eLife Sciences Publications, Ltd
record_format MEDLINE/PubMed
spelling pubmed-78376772021-01-27 Release probability increases towards distal dendrites boosting high-frequency signal transfer in the rodent hippocampus Jensen, Thomas P Kopach, Olga Reynolds, James P Savtchenko, Leonid P Rusakov, Dmitri A eLife Neuroscience Dendritic integration of synaptic inputs involves their increased electrotonic attenuation at distal dendrites, which can be counterbalanced by the increased synaptic receptor density. However, during network activity, the influence of individual synapses depends on their release fidelity, the dendritic distribution of which remains poorly understood. Here, we employed classical optical quantal analyses and a genetically encoded optical glutamate sensor in acute hippocampal slices of rats and mice to monitor glutamate release at CA3-CA1 synapses. We find that their release probability increases with greater distances from the soma. Similar-fidelity synapses tend to group together, whereas release probability shows no trends regarding the branch ends. Simulations with a realistic CA1 pyramidal cell hosting stochastic synapses suggest that the observed trends boost signal transfer fidelity, particularly at higher input frequencies. Because high-frequency bursting has been associated with learning, the release probability pattern we have found may play a key role in memory trace formation. eLife Sciences Publications, Ltd 2021-01-13 /pmc/articles/PMC7837677/ /pubmed/33438578 http://dx.doi.org/10.7554/eLife.62588 Text en © 2021, Jensen 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 Neuroscience
Jensen, Thomas P
Kopach, Olga
Reynolds, James P
Savtchenko, Leonid P
Rusakov, Dmitri A
Release probability increases towards distal dendrites boosting high-frequency signal transfer in the rodent hippocampus
title Release probability increases towards distal dendrites boosting high-frequency signal transfer in the rodent hippocampus
title_full Release probability increases towards distal dendrites boosting high-frequency signal transfer in the rodent hippocampus
title_fullStr Release probability increases towards distal dendrites boosting high-frequency signal transfer in the rodent hippocampus
title_full_unstemmed Release probability increases towards distal dendrites boosting high-frequency signal transfer in the rodent hippocampus
title_short Release probability increases towards distal dendrites boosting high-frequency signal transfer in the rodent hippocampus
title_sort release probability increases towards distal dendrites boosting high-frequency signal transfer in the rodent hippocampus
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7837677/
https://www.ncbi.nlm.nih.gov/pubmed/33438578
http://dx.doi.org/10.7554/eLife.62588
work_keys_str_mv AT jensenthomasp releaseprobabilityincreasestowardsdistaldendritesboostinghighfrequencysignaltransferintherodenthippocampus
AT kopacholga releaseprobabilityincreasestowardsdistaldendritesboostinghighfrequencysignaltransferintherodenthippocampus
AT reynoldsjamesp releaseprobabilityincreasestowardsdistaldendritesboostinghighfrequencysignaltransferintherodenthippocampus
AT savtchenkoleonidp releaseprobabilityincreasestowardsdistaldendritesboostinghighfrequencysignaltransferintherodenthippocampus
AT rusakovdmitria releaseprobabilityincreasestowardsdistaldendritesboostinghighfrequencysignaltransferintherodenthippocampus