Methodological Caveats in the Detection of Coordinated Replay between Place Cells and Grid Cells

At rest, hippocampal “place cells,” neurons with receptive fields corresponding to specific spatial locations, reactivate in a manner that reflects recently traveled trajectories. These “replay” events have been proposed as a mechanism underlying memory consolidation, or the transfer of a memory rep...

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Main Authors: John B. Trimper, Sean G. Trettel, Ernie Hwaun, Laura Lee Colgin
Format: Article
Language:English
Published: Frontiers Media S.A. 2017-08-01
Series:Frontiers in Systems Neuroscience
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fnsys.2017.00057/full
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author John B. Trimper
John B. Trimper
Sean G. Trettel
Sean G. Trettel
Sean G. Trettel
Ernie Hwaun
Ernie Hwaun
Ernie Hwaun
Laura Lee Colgin
Laura Lee Colgin
Laura Lee Colgin
author_facet John B. Trimper
John B. Trimper
Sean G. Trettel
Sean G. Trettel
Sean G. Trettel
Ernie Hwaun
Ernie Hwaun
Ernie Hwaun
Laura Lee Colgin
Laura Lee Colgin
Laura Lee Colgin
author_sort John B. Trimper
collection DOAJ
description At rest, hippocampal “place cells,” neurons with receptive fields corresponding to specific spatial locations, reactivate in a manner that reflects recently traveled trajectories. These “replay” events have been proposed as a mechanism underlying memory consolidation, or the transfer of a memory representation from the hippocampus to neocortical regions associated with the original sensory experience. Accordingly, it has been hypothesized that hippocampal replay of a particular experience should be accompanied by simultaneous reactivation of corresponding representations in the neocortex and in the entorhinal cortex, the primary interface between the hippocampus and the neocortex. Recent studies have reported that coordinated replay may occur between hippocampal place cells and medial entorhinal cortex grid cells, cells with multiple spatial receptive fields. Assessing replay in grid cells is problematic, however, as the cells exhibit regularly spaced spatial receptive fields in all environments and, therefore, coordinated replay between place cells and grid cells may be detected by chance. In the present report, we adapted analytical approaches utilized in recent studies of grid cell and place cell replay to determine the extent to which coordinated replay is spuriously detected between grid cells and place cells recorded from separate rats. For a subset of the employed analytical methods, coordinated replay was detected spuriously in a significant proportion of cases in which place cell replay events were randomly matched with grid cell firing epochs of equal duration. More rigorous replay evaluation procedures and minimum spike count requirements greatly reduced the amount of spurious findings. These results provide insights into aspects of place cell and grid cell activity during rest that contribute to false detection of coordinated replay. The results further emphasize the need for careful controls and rigorous methods when testing the hypothesis that place cells and grid cells exhibit coordinated replay.
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spelling doaj.art-abb20edf10b743c791c6a84df434d42a2022-12-22T01:45:39ZengFrontiers Media S.A.Frontiers in Systems Neuroscience1662-51372017-08-011110.3389/fnsys.2017.00057268118Methodological Caveats in the Detection of Coordinated Replay between Place Cells and Grid CellsJohn B. Trimper0John B. Trimper1Sean G. Trettel2Sean G. Trettel3Sean G. Trettel4Ernie Hwaun5Ernie Hwaun6Ernie Hwaun7Laura Lee Colgin8Laura Lee Colgin9Laura Lee Colgin10Center for Learning and Memory, University of Texas at Austin, AustinTX, United StatesDepartment of Neuroscience, University of Texas at Austin, AustinTX, United StatesCenter for Learning and Memory, University of Texas at Austin, AustinTX, United StatesDepartment of Neuroscience, University of Texas at Austin, AustinTX, United StatesInstitute for Neuroscience, University of Texas at Austin, AustinTX, United StatesCenter for Learning and Memory, University of Texas at Austin, AustinTX, United StatesDepartment of Neuroscience, University of Texas at Austin, AustinTX, United StatesInstitute for Neuroscience, University of Texas at Austin, AustinTX, United StatesCenter for Learning and Memory, University of Texas at Austin, AustinTX, United StatesDepartment of Neuroscience, University of Texas at Austin, AustinTX, United StatesInstitute for Neuroscience, University of Texas at Austin, AustinTX, United StatesAt rest, hippocampal “place cells,” neurons with receptive fields corresponding to specific spatial locations, reactivate in a manner that reflects recently traveled trajectories. These “replay” events have been proposed as a mechanism underlying memory consolidation, or the transfer of a memory representation from the hippocampus to neocortical regions associated with the original sensory experience. Accordingly, it has been hypothesized that hippocampal replay of a particular experience should be accompanied by simultaneous reactivation of corresponding representations in the neocortex and in the entorhinal cortex, the primary interface between the hippocampus and the neocortex. Recent studies have reported that coordinated replay may occur between hippocampal place cells and medial entorhinal cortex grid cells, cells with multiple spatial receptive fields. Assessing replay in grid cells is problematic, however, as the cells exhibit regularly spaced spatial receptive fields in all environments and, therefore, coordinated replay between place cells and grid cells may be detected by chance. In the present report, we adapted analytical approaches utilized in recent studies of grid cell and place cell replay to determine the extent to which coordinated replay is spuriously detected between grid cells and place cells recorded from separate rats. For a subset of the employed analytical methods, coordinated replay was detected spuriously in a significant proportion of cases in which place cell replay events were randomly matched with grid cell firing epochs of equal duration. More rigorous replay evaluation procedures and minimum spike count requirements greatly reduced the amount of spurious findings. These results provide insights into aspects of place cell and grid cell activity during rest that contribute to false detection of coordinated replay. The results further emphasize the need for careful controls and rigorous methods when testing the hypothesis that place cells and grid cells exhibit coordinated replay.http://journal.frontiersin.org/article/10.3389/fnsys.2017.00057/fullhippocampusmedial entorhinal cortexgrid cellsplace cellsreplayreactivation
spellingShingle John B. Trimper
John B. Trimper
Sean G. Trettel
Sean G. Trettel
Sean G. Trettel
Ernie Hwaun
Ernie Hwaun
Ernie Hwaun
Laura Lee Colgin
Laura Lee Colgin
Laura Lee Colgin
Methodological Caveats in the Detection of Coordinated Replay between Place Cells and Grid Cells
Frontiers in Systems Neuroscience
hippocampus
medial entorhinal cortex
grid cells
place cells
replay
reactivation
title Methodological Caveats in the Detection of Coordinated Replay between Place Cells and Grid Cells
title_full Methodological Caveats in the Detection of Coordinated Replay between Place Cells and Grid Cells
title_fullStr Methodological Caveats in the Detection of Coordinated Replay between Place Cells and Grid Cells
title_full_unstemmed Methodological Caveats in the Detection of Coordinated Replay between Place Cells and Grid Cells
title_short Methodological Caveats in the Detection of Coordinated Replay between Place Cells and Grid Cells
title_sort methodological caveats in the detection of coordinated replay between place cells and grid cells
topic hippocampus
medial entorhinal cortex
grid cells
place cells
replay
reactivation
url http://journal.frontiersin.org/article/10.3389/fnsys.2017.00057/full
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