Successful retrieval of competing spatial environments in humans involves hippocampal pattern separation mechanisms

The rodent hippocampus represents different spatial environments distinctly via changes in the pattern of “place cell” firing. It remains unclear, though, how spatial remapping in rodents relates more generally to human memory. Here participants retrieved four virtual reality environments with repea...

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Main Authors: Colin T Kyle, Jared D Stokes, Jennifer S Lieberman, Abdul S Hassan, Arne D Ekstrom
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2015-11-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/10499
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author Colin T Kyle
Jared D Stokes
Jennifer S Lieberman
Abdul S Hassan
Arne D Ekstrom
author_facet Colin T Kyle
Jared D Stokes
Jennifer S Lieberman
Abdul S Hassan
Arne D Ekstrom
author_sort Colin T Kyle
collection DOAJ
description The rodent hippocampus represents different spatial environments distinctly via changes in the pattern of “place cell” firing. It remains unclear, though, how spatial remapping in rodents relates more generally to human memory. Here participants retrieved four virtual reality environments with repeating or novel landmarks and configurations during high-resolution functional magnetic resonance imaging (fMRI). Both neural decoding performance and neural pattern similarity measures revealed environment-specific hippocampal neural codes. Conversely, an interfering spatial environment did not elicit neural codes specific to that environment, with neural activity patterns instead resembling those of competing environments, an effect linked to lower retrieval performance. We find that orthogonalized neural patterns accompany successful disambiguation of spatial environments while erroneous reinstatement of competing patterns characterized interference errors. These results provide the first evidence for environment-specific neural codes in the human hippocampus, suggesting that pattern separation/completion mechanisms play an important role in how we successfully retrieve memories.
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spelling doaj.art-eee08dba94bf480ebe33945acb6f9ec32022-12-22T03:33:26ZengeLife Sciences Publications LtdeLife2050-084X2015-11-01410.7554/eLife.10499Successful retrieval of competing spatial environments in humans involves hippocampal pattern separation mechanismsColin T Kyle0Jared D Stokes1Jennifer S Lieberman2Abdul S Hassan3Arne D Ekstrom4Center for Neuroscience, University of California, Davis, Davis, United StatesCenter for Neuroscience, University of California, Davis, Davis, United States; Department of Psychology, University of California, Davis, Davis, United StatesCenter for Neuroscience, University of California, Davis, Davis, United StatesCenter for Neuroscience, University of California, Davis, Davis, United StatesCenter for Neuroscience, University of California, Davis, Davis, United States; Department of Psychology, University of California, Davis, Davis, United StatesThe rodent hippocampus represents different spatial environments distinctly via changes in the pattern of “place cell” firing. It remains unclear, though, how spatial remapping in rodents relates more generally to human memory. Here participants retrieved four virtual reality environments with repeating or novel landmarks and configurations during high-resolution functional magnetic resonance imaging (fMRI). Both neural decoding performance and neural pattern similarity measures revealed environment-specific hippocampal neural codes. Conversely, an interfering spatial environment did not elicit neural codes specific to that environment, with neural activity patterns instead resembling those of competing environments, an effect linked to lower retrieval performance. We find that orthogonalized neural patterns accompany successful disambiguation of spatial environments while erroneous reinstatement of competing patterns characterized interference errors. These results provide the first evidence for environment-specific neural codes in the human hippocampus, suggesting that pattern separation/completion mechanisms play an important role in how we successfully retrieve memories.https://elifesciences.org/articles/10499NavigationMemoryCA3CA1MVPAfMRI
spellingShingle Colin T Kyle
Jared D Stokes
Jennifer S Lieberman
Abdul S Hassan
Arne D Ekstrom
Successful retrieval of competing spatial environments in humans involves hippocampal pattern separation mechanisms
eLife
Navigation
Memory
CA3
CA1
MVPA
fMRI
title Successful retrieval of competing spatial environments in humans involves hippocampal pattern separation mechanisms
title_full Successful retrieval of competing spatial environments in humans involves hippocampal pattern separation mechanisms
title_fullStr Successful retrieval of competing spatial environments in humans involves hippocampal pattern separation mechanisms
title_full_unstemmed Successful retrieval of competing spatial environments in humans involves hippocampal pattern separation mechanisms
title_short Successful retrieval of competing spatial environments in humans involves hippocampal pattern separation mechanisms
title_sort successful retrieval of competing spatial environments in humans involves hippocampal pattern separation mechanisms
topic Navigation
Memory
CA3
CA1
MVPA
fMRI
url https://elifesciences.org/articles/10499
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