Distinct hippocampal-cortical memory representations for experiences associated with movement versus immobility

While ongoing experience proceeds continuously, memories of past experience are often recalled as episodes with defined beginnings and ends. The neural mechanisms that lead to the formation of discrete episodes from the stream of neural activity patterns representing ongoing experience are unknown....

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Main Authors: Jai Y Yu, Kenneth Kay, Daniel F Liu, Irene Grossrubatscher, Adrianna Loback, Marielena Sosa, Jason E Chung, Mattias P Karlsson, Margaret C Larkin, Loren M Frank
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2017-08-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/27621
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author Jai Y Yu
Kenneth Kay
Daniel F Liu
Irene Grossrubatscher
Adrianna Loback
Marielena Sosa
Jason E Chung
Mattias P Karlsson
Margaret C Larkin
Loren M Frank
author_facet Jai Y Yu
Kenneth Kay
Daniel F Liu
Irene Grossrubatscher
Adrianna Loback
Marielena Sosa
Jason E Chung
Mattias P Karlsson
Margaret C Larkin
Loren M Frank
author_sort Jai Y Yu
collection DOAJ
description While ongoing experience proceeds continuously, memories of past experience are often recalled as episodes with defined beginnings and ends. The neural mechanisms that lead to the formation of discrete episodes from the stream of neural activity patterns representing ongoing experience are unknown. To investigate these mechanisms, we recorded neural activity in the rat hippocampus and prefrontal cortex, structures critical for memory processes. We show that during spatial navigation, hippocampal CA1 place cells maintain a continuous spatial representation across different states of motion (movement and immobility). In contrast, during sharp-wave ripples (SWRs), when representations of experience are transiently reactivated from memory, movement- and immobility-associated activity patterns are most often reactivated separately. Concurrently, distinct hippocampal reactivations of movement- or immobility-associated representations are accompanied by distinct modulation patterns in prefrontal cortex. These findings demonstrate a continuous representation of ongoing experience can be separated into independently reactivated memory representations.
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spelling doaj.art-a28740a4b446409fb68ab204b9e97b382022-12-22T04:32:18ZengeLife Sciences Publications LtdeLife2050-084X2017-08-01610.7554/eLife.27621Distinct hippocampal-cortical memory representations for experiences associated with movement versus immobilityJai Y Yu0https://orcid.org/0000-0003-0628-2531Kenneth Kay1Daniel F Liu2Irene Grossrubatscher3Adrianna Loback4Marielena Sosa5Jason E Chung6Mattias P Karlsson7Margaret C Larkin8Loren M Frank9https://orcid.org/0000-0002-1752-5677Department of Physiology, UCSF Center for Integrative Neuroscience, University of California, San Francisco, San Francisco, United States; Howard Hughes Medical Institute, University of California, San Francisco, San Francisco, United StatesDepartment of Physiology, UCSF Center for Integrative Neuroscience, University of California, San Francisco, San Francisco, United States; Howard Hughes Medical Institute, University of California, San Francisco, San Francisco, United StatesUniversity of California, Berkeley, Berkeley, United StatesUniversity of California, Berkeley, Berkeley, United StatesPrinceton University, Princeton, United StatesDepartment of Physiology, UCSF Center for Integrative Neuroscience, University of California, San Francisco, San Francisco, United StatesDepartment of Physiology, UCSF Center for Integrative Neuroscience, University of California, San Francisco, San Francisco, United StatesDepartment of Physiology, UCSF Center for Integrative Neuroscience, University of California, San Francisco, San Francisco, United StatesDepartment of Physiology, UCSF Center for Integrative Neuroscience, University of California, San Francisco, San Francisco, United StatesDepartment of Physiology, UCSF Center for Integrative Neuroscience, University of California, San Francisco, San Francisco, United States; Howard Hughes Medical Institute, University of California, San Francisco, San Francisco, United States; Kavli Institute for Fundamental Neuroscience, University of California, San Francisco, San Francisco, United StatesWhile ongoing experience proceeds continuously, memories of past experience are often recalled as episodes with defined beginnings and ends. The neural mechanisms that lead to the formation of discrete episodes from the stream of neural activity patterns representing ongoing experience are unknown. To investigate these mechanisms, we recorded neural activity in the rat hippocampus and prefrontal cortex, structures critical for memory processes. We show that during spatial navigation, hippocampal CA1 place cells maintain a continuous spatial representation across different states of motion (movement and immobility). In contrast, during sharp-wave ripples (SWRs), when representations of experience are transiently reactivated from memory, movement- and immobility-associated activity patterns are most often reactivated separately. Concurrently, distinct hippocampal reactivations of movement- or immobility-associated representations are accompanied by distinct modulation patterns in prefrontal cortex. These findings demonstrate a continuous representation of ongoing experience can be separated into independently reactivated memory representations.https://elifesciences.org/articles/27621hippocampusprefrontal cortexsharp wave-ripplememory
spellingShingle Jai Y Yu
Kenneth Kay
Daniel F Liu
Irene Grossrubatscher
Adrianna Loback
Marielena Sosa
Jason E Chung
Mattias P Karlsson
Margaret C Larkin
Loren M Frank
Distinct hippocampal-cortical memory representations for experiences associated with movement versus immobility
eLife
hippocampus
prefrontal cortex
sharp wave-ripple
memory
title Distinct hippocampal-cortical memory representations for experiences associated with movement versus immobility
title_full Distinct hippocampal-cortical memory representations for experiences associated with movement versus immobility
title_fullStr Distinct hippocampal-cortical memory representations for experiences associated with movement versus immobility
title_full_unstemmed Distinct hippocampal-cortical memory representations for experiences associated with movement versus immobility
title_short Distinct hippocampal-cortical memory representations for experiences associated with movement versus immobility
title_sort distinct hippocampal cortical memory representations for experiences associated with movement versus immobility
topic hippocampus
prefrontal cortex
sharp wave-ripple
memory
url https://elifesciences.org/articles/27621
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