Structure-Function Dissociations of Human Hippocampal Subfield Stiffness and Memory Performance

Peyton L Delgorio; Lucy V. Hiscox; Ana M. Daugherty; Faria Sanjana; Grace  McIlvain; Ryan T Pohlig; Matthew D. J. McGarry; Christopher  Martens; Hillary  Schwarb; Curtis L. Johnson

doi:10.1523/JNEUROSCI.0592-22.2022

Structure-Function Dissociations of Human Hippocampal Subfield Stiffness and Memory Performance

Peyton L Delgorio, Lucy V. Hiscox, Ana M. Daugherty, Faria Sanjana, Grace McIlvain, Ryan T Pohlig, Matthew D. J. McGarry, Christopher Martens , Hillary Schwarb, Curtis L. Johnson

Department of Psychology

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Abstract

Aging and neurodegenerative diseases lead to decline in thinking and memory ability. The subfields of the hippocampus (HCsf) play important roles in memory formation and recall. Imaging techniques sensitive to the underlying HCsf tissue microstructure can reveal unique structure-function associations and their vulnerability in aging and disease. The goal of this study was to use magnetic resonance elastography (MRE), a noninvasive MR imaging-based technique that can quantitatively image the viscoelastic mechanical properties of tissue, to determine the associations of HCsf stiffness with different cognitive domains across the lifespan. 88 adult participants completed the study (age: 23-81 years, M/F 36/51), in which we aimed to determine which HCsf regions most strongly correlated with different memory performance outcomes and if viscoelasticity of specific HCsf regions mediated the relationship between age and performance. Our results revealed that both interference cost on a verbal memory task and relational memory task performance were significantly related to cornu ammonis 1-2 (CA1-CA2) stiffness (p = 0.018 and p = 0.011, respectively), with CA1-CA2 stiffness significantly mediating the relationship between age and interference cost performance (p = 0.031). There were also significant associations between delayed free verbal recall performance and stiffness of both the dentate gyrus-cornu ammonis 3 (DG-CA3) (p = 0.016) and subiculum (SUB) (p = 0.032) regions. This further exemplifies the functional specialization of HCsf in declarative memory and the potential use of MRE measures as clinical biomarkers in assessing brain health in aging and disease.

Original language	English
Pages (from-to)	7957-7968
Number of pages	12
Journal	Journal of Neuroscience
Volume	42
Issue number	42
Early online date	6 Sept 2022
DOIs	https://doi.org/10.1523/JNEUROSCI.0592-22.2022
Publication status	Published - 19 Oct 2022

Funding

Received Mar. 24, 2022; revised Aug. 16, 2022; accepted Aug. 18, 2022. Author contributions: P.L.D., H.S., and C.L.J. designed research; P.L.D., L.V.H., F.S., and G.M. performed research; P.L.D., R.T.P., M.D.J.M., C.R.M., and C.L.J. contributed unpublished reagents/analytic tools; P.L.D., L.V.H., A.M.D., R.T.P., and H.S. analyzed data; P.L.D. wrote the paper. This work was supported by National Institutes of Health Grants R01-AG058853, R01-EB027577, K01-AG054731, and R03-AG065894; Delaware IDeA Network of Biomedical Research Excellence Grant P20-GM103446; Delaware Cardiovascular Center for Biomedical Research Excellence Grant P20-GM113125; and Delaware Neuroscience Center for Biomedical Research Excellence Grant P20-GM103653. The authors declare no competing financial interests. Correspondence should be addressed to Curtis L. Johnson at [email protected]. https://doi.org/10.1523/JNEUROSCI.0592-22.2022 Copyright © 2022 the authors

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title = "Structure-Function Dissociations of Human Hippocampal Subfield Stiffness and Memory Performance",

abstract = "Aging and neurodegenerative diseases lead to decline in thinking and memory ability. The subfields of the hippocampus (HCsf) play important roles in memory formation and recall. Imaging techniques sensitive to the underlying HCsf tissue microstructure can reveal unique structure-function associations and their vulnerability in aging and disease. The goal of this study was to use magnetic resonance elastography (MRE), a noninvasive MR imaging-based technique that can quantitatively image the viscoelastic mechanical properties of tissue, to determine the associations of HCsf stiffness with different cognitive domains across the lifespan. 88 adult participants completed the study (age: 23-81 years, M/F 36/51), in which we aimed to determine which HCsf regions most strongly correlated with different memory performance outcomes and if viscoelasticity of specific HCsf regions mediated the relationship between age and performance. Our results revealed that both interference cost on a verbal memory task and relational memory task performance were significantly related to cornu ammonis 1-2 (CA1-CA2) stiffness (p = 0.018 and p = 0.011, respectively), with CA1-CA2 stiffness significantly mediating the relationship between age and interference cost performance (p = 0.031). There were also significant associations between delayed free verbal recall performance and stiffness of both the dentate gyrus-cornu ammonis 3 (DG-CA3) (p = 0.016) and subiculum (SUB) (p = 0.032) regions. This further exemplifies the functional specialization of HCsf in declarative memory and the potential use of MRE measures as clinical biomarkers in assessing brain health in aging and disease.",

author = "Delgorio, {Peyton L} and Hiscox, {Lucy V.} and Daugherty, {Ana M.} and Faria Sanjana and Grace McIlvain and Pohlig, {Ryan T} and McGarry, {Matthew D. J.} and Christopher Martens and Hillary Schwarb and Johnson, {Curtis L.}",

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doi = "10.1523/JNEUROSCI.0592-22.2022",

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T1 - Structure-Function Dissociations of Human Hippocampal Subfield Stiffness and Memory Performance

AU - Delgorio, Peyton L

AU - Hiscox, Lucy V.

AU - Daugherty, Ana M.

AU - Sanjana, Faria

AU - McIlvain, Grace

AU - Pohlig, Ryan T

AU - McGarry, Matthew D. J.

AU - Martens , Christopher

AU - Schwarb, Hillary

AU - Johnson, Curtis L.

PY - 2022/10/19

Y1 - 2022/10/19

N2 - Aging and neurodegenerative diseases lead to decline in thinking and memory ability. The subfields of the hippocampus (HCsf) play important roles in memory formation and recall. Imaging techniques sensitive to the underlying HCsf tissue microstructure can reveal unique structure-function associations and their vulnerability in aging and disease. The goal of this study was to use magnetic resonance elastography (MRE), a noninvasive MR imaging-based technique that can quantitatively image the viscoelastic mechanical properties of tissue, to determine the associations of HCsf stiffness with different cognitive domains across the lifespan. 88 adult participants completed the study (age: 23-81 years, M/F 36/51), in which we aimed to determine which HCsf regions most strongly correlated with different memory performance outcomes and if viscoelasticity of specific HCsf regions mediated the relationship between age and performance. Our results revealed that both interference cost on a verbal memory task and relational memory task performance were significantly related to cornu ammonis 1-2 (CA1-CA2) stiffness (p = 0.018 and p = 0.011, respectively), with CA1-CA2 stiffness significantly mediating the relationship between age and interference cost performance (p = 0.031). There were also significant associations between delayed free verbal recall performance and stiffness of both the dentate gyrus-cornu ammonis 3 (DG-CA3) (p = 0.016) and subiculum (SUB) (p = 0.032) regions. This further exemplifies the functional specialization of HCsf in declarative memory and the potential use of MRE measures as clinical biomarkers in assessing brain health in aging and disease.

AB - Aging and neurodegenerative diseases lead to decline in thinking and memory ability. The subfields of the hippocampus (HCsf) play important roles in memory formation and recall. Imaging techniques sensitive to the underlying HCsf tissue microstructure can reveal unique structure-function associations and their vulnerability in aging and disease. The goal of this study was to use magnetic resonance elastography (MRE), a noninvasive MR imaging-based technique that can quantitatively image the viscoelastic mechanical properties of tissue, to determine the associations of HCsf stiffness with different cognitive domains across the lifespan. 88 adult participants completed the study (age: 23-81 years, M/F 36/51), in which we aimed to determine which HCsf regions most strongly correlated with different memory performance outcomes and if viscoelasticity of specific HCsf regions mediated the relationship between age and performance. Our results revealed that both interference cost on a verbal memory task and relational memory task performance were significantly related to cornu ammonis 1-2 (CA1-CA2) stiffness (p = 0.018 and p = 0.011, respectively), with CA1-CA2 stiffness significantly mediating the relationship between age and interference cost performance (p = 0.031). There were also significant associations between delayed free verbal recall performance and stiffness of both the dentate gyrus-cornu ammonis 3 (DG-CA3) (p = 0.016) and subiculum (SUB) (p = 0.032) regions. This further exemplifies the functional specialization of HCsf in declarative memory and the potential use of MRE measures as clinical biomarkers in assessing brain health in aging and disease.

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DO - 10.1523/JNEUROSCI.0592-22.2022

M3 - Article

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SP - 7957

EP - 7968

JO - Journal of Neuroscience

JF - Journal of Neuroscience

IS - 42

ER -

Structure-Function Dissociations of Human Hippocampal Subfield Stiffness and Memory Performance

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