Experience-dependent shaping of hippocampal CA1 intracellular activity in novel and familiar environments

The hippocampus is critical for producing stable representations of familiar spaces. How these representations arise is poorly understood, largely because changes to hippocampal inputs have not been measured during spatial learning. Here, using intracellular recording, we monitored inputs and plasti...

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Main Authors: Jeremy D Cohen, Mark Bolstad, Albert K Lee
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2017-07-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/23040
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author Jeremy D Cohen
Mark Bolstad
Albert K Lee
author_facet Jeremy D Cohen
Mark Bolstad
Albert K Lee
author_sort Jeremy D Cohen
collection DOAJ
description The hippocampus is critical for producing stable representations of familiar spaces. How these representations arise is poorly understood, largely because changes to hippocampal inputs have not been measured during spatial learning. Here, using intracellular recording, we monitored inputs and plasticity-inducing complex spikes (CSs) in CA1 neurons while mice explored novel and familiar virtual environments. Inputs driving place field spiking increased in amplitude – often suddenly – during novel environment exploration. However, these increases were not sustained in familiar environments. Rather, the spatial tuning of inputs became increasingly similar across repeated traversals of the environment with experience – both within fields and throughout the whole environment. In novel environments, CSs were not necessary for place field formation. Our findings support a model in which initial inhomogeneities in inputs are amplified to produce robust place field activity, then plasticity refines this representation into one with less strongly modulated, but more stable, inputs for long-term storage.
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spelling doaj.art-8769b85aa32c4013812bc18d8bafed3e2022-12-22T03:52:57ZengeLife Sciences Publications LtdeLife2050-084X2017-07-01610.7554/eLife.23040Experience-dependent shaping of hippocampal CA1 intracellular activity in novel and familiar environmentsJeremy D Cohen0https://orcid.org/0000-0003-4961-222XMark Bolstad1Albert K Lee2https://orcid.org/0000-0003-4332-8332Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United StatesJanelia Research Campus, Howard Hughes Medical Institute, Ashburn, United StatesJanelia Research Campus, Howard Hughes Medical Institute, Ashburn, United StatesThe hippocampus is critical for producing stable representations of familiar spaces. How these representations arise is poorly understood, largely because changes to hippocampal inputs have not been measured during spatial learning. Here, using intracellular recording, we monitored inputs and plasticity-inducing complex spikes (CSs) in CA1 neurons while mice explored novel and familiar virtual environments. Inputs driving place field spiking increased in amplitude – often suddenly – during novel environment exploration. However, these increases were not sustained in familiar environments. Rather, the spatial tuning of inputs became increasingly similar across repeated traversals of the environment with experience – both within fields and throughout the whole environment. In novel environments, CSs were not necessary for place field formation. Our findings support a model in which initial inhomogeneities in inputs are amplified to produce robust place field activity, then plasticity refines this representation into one with less strongly modulated, but more stable, inputs for long-term storage.https://elifesciences.org/articles/23040hippocampusCA1place cellspatial memoryintracellularwhole-cell
spellingShingle Jeremy D Cohen
Mark Bolstad
Albert K Lee
Experience-dependent shaping of hippocampal CA1 intracellular activity in novel and familiar environments
eLife
hippocampus
CA1
place cell
spatial memory
intracellular
whole-cell
title Experience-dependent shaping of hippocampal CA1 intracellular activity in novel and familiar environments
title_full Experience-dependent shaping of hippocampal CA1 intracellular activity in novel and familiar environments
title_fullStr Experience-dependent shaping of hippocampal CA1 intracellular activity in novel and familiar environments
title_full_unstemmed Experience-dependent shaping of hippocampal CA1 intracellular activity in novel and familiar environments
title_short Experience-dependent shaping of hippocampal CA1 intracellular activity in novel and familiar environments
title_sort experience dependent shaping of hippocampal ca1 intracellular activity in novel and familiar environments
topic hippocampus
CA1
place cell
spatial memory
intracellular
whole-cell
url https://elifesciences.org/articles/23040
work_keys_str_mv AT jeremydcohen experiencedependentshapingofhippocampalca1intracellularactivityinnovelandfamiliarenvironments
AT markbolstad experiencedependentshapingofhippocampalca1intracellularactivityinnovelandfamiliarenvironments
AT albertklee experiencedependentshapingofhippocampalca1intracellularactivityinnovelandfamiliarenvironments