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....
Main Authors: | , , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
eLife Sciences Publications Ltd
2017-08-01
|
Series: | eLife |
Subjects: | |
Online Access: | https://elifesciences.org/articles/27621 |
_version_ | 1811181410135834624 |
---|---|
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. |
first_indexed | 2024-04-11T09:17:18Z |
format | Article |
id | doaj.art-a28740a4b446409fb68ab204b9e97b38 |
institution | Directory Open Access Journal |
issn | 2050-084X |
language | English |
last_indexed | 2024-04-11T09:17:18Z |
publishDate | 2017-08-01 |
publisher | eLife Sciences Publications Ltd |
record_format | Article |
series | eLife |
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 |
work_keys_str_mv | AT jaiyyu distincthippocampalcorticalmemoryrepresentationsforexperiencesassociatedwithmovementversusimmobility AT kennethkay distincthippocampalcorticalmemoryrepresentationsforexperiencesassociatedwithmovementversusimmobility AT danielfliu distincthippocampalcorticalmemoryrepresentationsforexperiencesassociatedwithmovementversusimmobility AT irenegrossrubatscher distincthippocampalcorticalmemoryrepresentationsforexperiencesassociatedwithmovementversusimmobility AT adriannaloback distincthippocampalcorticalmemoryrepresentationsforexperiencesassociatedwithmovementversusimmobility AT marielenasosa distincthippocampalcorticalmemoryrepresentationsforexperiencesassociatedwithmovementversusimmobility AT jasonechung distincthippocampalcorticalmemoryrepresentationsforexperiencesassociatedwithmovementversusimmobility AT mattiaspkarlsson distincthippocampalcorticalmemoryrepresentationsforexperiencesassociatedwithmovementversusimmobility AT margaretclarkin distincthippocampalcorticalmemoryrepresentationsforexperiencesassociatedwithmovementversusimmobility AT lorenmfrank distincthippocampalcorticalmemoryrepresentationsforexperiencesassociatedwithmovementversusimmobility |