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Adding Meaning to Memories: How Parietal Cortex Combines Semantic Content with Episodic Experience

Neuroimaging studies of human memory have consistently found that univariate responses in parietal cortex track episodic experience with stimuli (whether stimuli are 'old' or 'new'). More recently, pattern-based fMRI studies have shown that parietal cortex also carries informatio...

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Autores principales: Lee, Hongmi, Keene, Paul A., Sweigart, Sarah C., Hutchinson, J. Benjamin, Kuhl, Brice A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10513070/
https://www.ncbi.nlm.nih.gov/pubmed/37596054
http://dx.doi.org/10.1523/JNEUROSCI.1919-22.2023
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author Lee, Hongmi
Keene, Paul A.
Sweigart, Sarah C.
Hutchinson, J. Benjamin
Kuhl, Brice A.
author_facet Lee, Hongmi
Keene, Paul A.
Sweigart, Sarah C.
Hutchinson, J. Benjamin
Kuhl, Brice A.
author_sort Lee, Hongmi
collection PubMed
description Neuroimaging studies of human memory have consistently found that univariate responses in parietal cortex track episodic experience with stimuli (whether stimuli are 'old' or 'new'). More recently, pattern-based fMRI studies have shown that parietal cortex also carries information about the semantic content of remembered experiences. However, it is not well understood how memory-based and content-based signals are integrated within parietal cortex. Here, in humans (males and females), we used voxel-wise encoding models and a recognition memory task to predict the fMRI activity patterns evoked by complex natural scene images based on (1) the episodic history and (2) the semantic content of each image. Models were generated and compared across distinct subregions of parietal cortex and for occipitotemporal cortex. We show that parietal and occipitotemporal regions each encode memory and content information, but they differ in how they combine this information. Among parietal subregions, angular gyrus was characterized by robust and overlapping effects of memory and content. Moreover, subject-specific semantic tuning functions revealed that successful recognition shifted the amplitude of tuning functions in angular gyrus but did not change the selectivity of tuning. In other words, effects of memory and content were additive in angular gyrus. This pattern of data contrasted with occipitotemporal cortex where memory and content effects were interactive: memory effects were preferentially expressed by voxels tuned to the content of a remembered image. Collectively, these findings provide unique insight into how parietal cortex combines information about episodic memory and semantic content. SIGNIFICANCE STATEMENT Neuroimaging studies of human memory have identified multiple brain regions that not only carry information about “whether” a visual stimulus is successfully recognized but also “what” the content of that stimulus includes. However, a fundamental and open question concerns how the brain integrates these two types of information (memory and content). Here, using a powerful combination of fMRI analysis methods, we show that parietal cortex, particularly the angular gyrus, robustly combines memory- and content-related information, but these two forms of information are represented via additive, independent signals. In contrast, memory effects in high-level visual cortex critically depend on (and interact with) content representations. Together, these findings reveal multiple and distinct ways in which the brain combines memory- and content-related information.
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spelling pubmed-105130702023-09-22 Adding Meaning to Memories: How Parietal Cortex Combines Semantic Content with Episodic Experience Lee, Hongmi Keene, Paul A. Sweigart, Sarah C. Hutchinson, J. Benjamin Kuhl, Brice A. J Neurosci Research Articles Neuroimaging studies of human memory have consistently found that univariate responses in parietal cortex track episodic experience with stimuli (whether stimuli are 'old' or 'new'). More recently, pattern-based fMRI studies have shown that parietal cortex also carries information about the semantic content of remembered experiences. However, it is not well understood how memory-based and content-based signals are integrated within parietal cortex. Here, in humans (males and females), we used voxel-wise encoding models and a recognition memory task to predict the fMRI activity patterns evoked by complex natural scene images based on (1) the episodic history and (2) the semantic content of each image. Models were generated and compared across distinct subregions of parietal cortex and for occipitotemporal cortex. We show that parietal and occipitotemporal regions each encode memory and content information, but they differ in how they combine this information. Among parietal subregions, angular gyrus was characterized by robust and overlapping effects of memory and content. Moreover, subject-specific semantic tuning functions revealed that successful recognition shifted the amplitude of tuning functions in angular gyrus but did not change the selectivity of tuning. In other words, effects of memory and content were additive in angular gyrus. This pattern of data contrasted with occipitotemporal cortex where memory and content effects were interactive: memory effects were preferentially expressed by voxels tuned to the content of a remembered image. Collectively, these findings provide unique insight into how parietal cortex combines information about episodic memory and semantic content. SIGNIFICANCE STATEMENT Neuroimaging studies of human memory have identified multiple brain regions that not only carry information about “whether” a visual stimulus is successfully recognized but also “what” the content of that stimulus includes. However, a fundamental and open question concerns how the brain integrates these two types of information (memory and content). Here, using a powerful combination of fMRI analysis methods, we show that parietal cortex, particularly the angular gyrus, robustly combines memory- and content-related information, but these two forms of information are represented via additive, independent signals. In contrast, memory effects in high-level visual cortex critically depend on (and interact with) content representations. Together, these findings reveal multiple and distinct ways in which the brain combines memory- and content-related information. Society for Neuroscience 2023-09-20 /pmc/articles/PMC10513070/ /pubmed/37596054 http://dx.doi.org/10.1523/JNEUROSCI.1919-22.2023 Text en Copyright © 2023 Lee et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Articles
Lee, Hongmi
Keene, Paul A.
Sweigart, Sarah C.
Hutchinson, J. Benjamin
Kuhl, Brice A.
Adding Meaning to Memories: How Parietal Cortex Combines Semantic Content with Episodic Experience
title Adding Meaning to Memories: How Parietal Cortex Combines Semantic Content with Episodic Experience
title_full Adding Meaning to Memories: How Parietal Cortex Combines Semantic Content with Episodic Experience
title_fullStr Adding Meaning to Memories: How Parietal Cortex Combines Semantic Content with Episodic Experience
title_full_unstemmed Adding Meaning to Memories: How Parietal Cortex Combines Semantic Content with Episodic Experience
title_short Adding Meaning to Memories: How Parietal Cortex Combines Semantic Content with Episodic Experience
title_sort adding meaning to memories: how parietal cortex combines semantic content with episodic experience
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10513070/
https://www.ncbi.nlm.nih.gov/pubmed/37596054
http://dx.doi.org/10.1523/JNEUROSCI.1919-22.2023
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