Brain structure and function as mediators of the effects of amyloid on memory

doi:10.1212/WNL.0000000000001375

. 2015 Mar 17;84(11):1136-44.

doi: 10.1212/WNL.0000000000001375. Epub 2015 Feb 13.

Brain structure and function as mediators of the effects of amyloid on memory

Niklas Mattsson¹, Philip S Insel², Paul S Aisen², William Jagust², Scott Mackin², Michael Weiner²; Alzheimer's Disease Neuroimaging Initiative

Collaborators, Affiliations

Collaborators

Alzheimer's Disease Neuroimaging Initiative:
Michael Weiner, Paul Aisen, Michael Weiner, Paul Aisen, Ronald Petersen, Clifford R Jack Jr, William Jagust, John Q Trojanowki, Arthur W Toga, Laurel Beckett, Robert C Green, Andrew J Saykin, John Morris, Enchi Liu, Robert C Green, Tom Montine, Ronald Petersen, Paul Aisen, Anthony Gamst, Ronald G Thomas, Michael Donohue, Sarah Walter, Devon Gessert, Tamie Sather, Laurel Beckett, Danielle Harvey, Anthony Gamst, Michael Donohue, John Kornak, Clifford R Jack Jr, Anders Dale, Matthew Bernstein, Joel Felmlee, Nick Fox, Paul Thompson, Norbert Schuff, Gene Alexander, Charles DeCarli, William Jagust, Dan Bandy, Robert A Koeppe, Norm Foster, Eric M Reiman, Kewei Chen, Chet Mathis, John Morris, Nigel J Cairns, Lisa Taylor-Reinwald, J Q Trojanowki, Les Shaw, Virginia M Y Lee, Magdalena Korecka, Arthur W Toga, Karen Crawford, Scott Neu, Andrew J Saykin, Tatiana M Foroud, Steven Potkin, Li Shen, Zaven Kachaturian, Richard Frank, Peter J Snyder, Susan Molchan, Jeffrey Kaye, Joseph Quinn, Betty Lind, Sara Dolen, Lon S Schneider, Sonia Pawluczyk, Bryan M Spann, James Brewer, Helen Vanderswag, Judith L Heidebrink, Joanne L Lord, Ronald Petersen, Kris Johnson, Rachelle S Doody, Javier Villanueva-Meyer, Munir Chowdhury, Yaakov Stern, Lawrence S Honig, Karen L Bell, John C Morris, Beau Ances, Maria Carroll, Sue Leon, Mark A Mintun, Stacy Schneider, Daniel Marson, Randall Griffith, David Clark, Hillel Grossman, Effie Mitsis, Aliza Romirowsky, Leyla deToledo-Morrell, Raj C Shah, Ranjan Duara, Daniel Varon, Peggy Roberts, Marilyn Albert, Chiadi Onyike, Stephanie Kielb, Henry Rusinek, Mony J de Leon, Lidia Glodzik, Susan De Santi, P Murali Doraiswamy, Jeffrey R Petrella, R Edward Coleman, Steven E Arnold, Jason H Karlawish, David Wolk, Charles D Smith, Greg Jicha, Peter Hardy, Oscar L Lopez, Mary Ann Oakley, Donna M Simpson, Anton P Porsteinsson, Bonnie S Goldstein, Kim Martin, Kelly M Makino, M Saleem Ismail, Connie Brand, Ruth A Mulnard, Gaby Thai, Catherine Mc-Adams-Ortiz, Kyle Womack, Dana Mathews, Mary Quiceno, Ramon Diaz-Arrastia, Richard King, Myron Weiner, Kristen Martin-Cook, Michael DeVous, Allan I Levey, James J Lah, Janet S Cellar, Jeffrey M Burns, Heather S Anderson, Russell H Swerdlow, Liana Apostolova, Po H Lu, George Bartzokis, Daniel H S Silverman, Neill R Graff-Radford, Francine Parfitt, Heather Johnson, Martin R Farlow, Ann Marie Hake, Brandy R Matthews, Scott Herring, Christopher H van Dyck, Richard E Carson, Martha G MacAvoy, Howard Chertkow, Howard Bergman, Chris Hosein, Sandra Black, Bojana Stefanovic, Curtis Caldwell, Ging-Yuek Robin Hsiung, Howard Feldman, Benita Mudge, Michele Assaly, Andrew Kertesz, John Rogers, Dick Trost, Charles Bernick, Donna Munic, Diana Kerwin, Marek-Marsel Mesulam, Kristina Lipowski, Chuang-Kuo Wu, Nancy Johnson, Carl Sadowsky, Walter Martinez, Teresa Villena, Raymond Scott Turner, Kathleen Johnson, Brigid Reynolds, Reisa A Sperling, Keith A Johnson, Gad Marshall, Meghan Frey, Jerome Yesavage, Joy L Taylor, Barton Lane, Allyson Rosen, Jared Tinklenberg, Marwan Sabbagh, Christine Belden, Sandra Jacobson, Neil Kowall, Ronald Killiany, Andrew E Budson, Alexander Norbash, Patricia Lynn Johnson, Thomas O Obisesan, Saba Wolday, Salome K Bwayo, Alan Lerner, Leon Hudson, Paula Ogrocki, Evan Fletcher, Owen Carmichael, John Olichney, Charles DeCarli, Smita Kittur, Michael Borrie, T-Y Lee, Dr Rob Bartha, Sterling Johnson, Sanjay Asthana, Cynthia M Carlsson, Steven G Potkin, Adrian Preda, Dana Nguyen, Pierre Tariot, Adam Fleisher, Stephanie Reeder, Vernice Bates, Horacio Capote, Michelle Rainka, Douglas W Scharre, Maria Kataki, Earl A Zimmerman, Dzintra Celmins, Alice D Brown, Godfrey D Pearlson, Karen Blank, Karen Anderson, Andrew J Saykin, Robert B Santulli, Eben S Schwartz, Kaycee M Sink, Jeff D Williamson, Pradeep Garg, Franklin Watkins, Brian R Ott, Henry Querfurth, Geoffrey Tremont, Stephen Salloway, Paul Malloy, Stephen Correia, Howard J Rosen, Bruce L Miller, Jacobo Mintzer, Crystal Flynn Longmire, Kenneth Spicer, Elizabether Finger, Irina Rachinsky, John Rogers, Andrew Kertesz, Dick Drost, Nunzio Pomara, Raymundo Hernando, Antero Sarrael, Susan K Schultz, Laura L Boles Ponto, Hyungsub Shim, Karen Elizabeth Smith, Norman Relkin, Gloria Chaing, Lisa Raudin, Amanda Smith, Kristin Fargher, Balebail Ashok Raj

Affiliations

¹ From the Department of Veterans Affairs Medical Center (N.M., P.S.I., S.M., M.W.), Center for Imaging of Neurodegenerative Diseases, San Francisco, CA; Clinical Neurochemistry Laboratory (N.M.), Institute of Neuroscience and Physiology, the Sahlgrenska Academy at the University of Gothenburg, Mölndal, Sweden; Department of Radiology and Biomedical Imaging (N.M., P.S.I., M.W.), University of California, San Francisco; Alzheimer's Disease Cooperative Study (P.S.A.), Department of Neurosciences, University of California, San Diego, La Jolla; Helen Wills Neuroscience Institute and School of Public Health (W.J.), University of California, Berkeley; and Department of Psychiatry (S.M.), University of California, San Francisco. niklas.mattsson@neuro.gu.se.
² From the Department of Veterans Affairs Medical Center (N.M., P.S.I., S.M., M.W.), Center for Imaging of Neurodegenerative Diseases, San Francisco, CA; Clinical Neurochemistry Laboratory (N.M.), Institute of Neuroscience and Physiology, the Sahlgrenska Academy at the University of Gothenburg, Mölndal, Sweden; Department of Radiology and Biomedical Imaging (N.M., P.S.I., M.W.), University of California, San Francisco; Alzheimer's Disease Cooperative Study (P.S.A.), Department of Neurosciences, University of California, San Diego, La Jolla; Helen Wills Neuroscience Institute and School of Public Health (W.J.), University of California, Berkeley; and Department of Psychiatry (S.M.), University of California, San Francisco.

PMID: 25681451
PMCID: PMC4371407
DOI: 10.1212/WNL.0000000000001375

Brain structure and function as mediators of the effects of amyloid on memory

Niklas Mattsson et al. Neurology. 2015.

. 2015 Mar 17;84(11):1136-44.

doi: 10.1212/WNL.0000000000001375. Epub 2015 Feb 13.

Authors

Niklas Mattsson¹, Philip S Insel², Paul S Aisen², William Jagust², Scott Mackin², Michael Weiner²; Alzheimer's Disease Neuroimaging Initiative

Collaborators

Alzheimer's Disease Neuroimaging Initiative:
Michael Weiner, Paul Aisen, Michael Weiner, Paul Aisen, Ronald Petersen, Clifford R Jack Jr, William Jagust, John Q Trojanowki, Arthur W Toga, Laurel Beckett, Robert C Green, Andrew J Saykin, John Morris, Enchi Liu, Robert C Green, Tom Montine, Ronald Petersen, Paul Aisen, Anthony Gamst, Ronald G Thomas, Michael Donohue, Sarah Walter, Devon Gessert, Tamie Sather, Laurel Beckett, Danielle Harvey, Anthony Gamst, Michael Donohue, John Kornak, Clifford R Jack Jr, Anders Dale, Matthew Bernstein, Joel Felmlee, Nick Fox, Paul Thompson, Norbert Schuff, Gene Alexander, Charles DeCarli, William Jagust, Dan Bandy, Robert A Koeppe, Norm Foster, Eric M Reiman, Kewei Chen, Chet Mathis, John Morris, Nigel J Cairns, Lisa Taylor-Reinwald, J Q Trojanowki, Les Shaw, Virginia M Y Lee, Magdalena Korecka, Arthur W Toga, Karen Crawford, Scott Neu, Andrew J Saykin, Tatiana M Foroud, Steven Potkin, Li Shen, Zaven Kachaturian, Richard Frank, Peter J Snyder, Susan Molchan, Jeffrey Kaye, Joseph Quinn, Betty Lind, Sara Dolen, Lon S Schneider, Sonia Pawluczyk, Bryan M Spann, James Brewer, Helen Vanderswag, Judith L Heidebrink, Joanne L Lord, Ronald Petersen, Kris Johnson, Rachelle S Doody, Javier Villanueva-Meyer, Munir Chowdhury, Yaakov Stern, Lawrence S Honig, Karen L Bell, John C Morris, Beau Ances, Maria Carroll, Sue Leon, Mark A Mintun, Stacy Schneider, Daniel Marson, Randall Griffith, David Clark, Hillel Grossman, Effie Mitsis, Aliza Romirowsky, Leyla deToledo-Morrell, Raj C Shah, Ranjan Duara, Daniel Varon, Peggy Roberts, Marilyn Albert, Chiadi Onyike, Stephanie Kielb, Henry Rusinek, Mony J de Leon, Lidia Glodzik, Susan De Santi, P Murali Doraiswamy, Jeffrey R Petrella, R Edward Coleman, Steven E Arnold, Jason H Karlawish, David Wolk, Charles D Smith, Greg Jicha, Peter Hardy, Oscar L Lopez, Mary Ann Oakley, Donna M Simpson, Anton P Porsteinsson, Bonnie S Goldstein, Kim Martin, Kelly M Makino, M Saleem Ismail, Connie Brand, Ruth A Mulnard, Gaby Thai, Catherine Mc-Adams-Ortiz, Kyle Womack, Dana Mathews, Mary Quiceno, Ramon Diaz-Arrastia, Richard King, Myron Weiner, Kristen Martin-Cook, Michael DeVous, Allan I Levey, James J Lah, Janet S Cellar, Jeffrey M Burns, Heather S Anderson, Russell H Swerdlow, Liana Apostolova, Po H Lu, George Bartzokis, Daniel H S Silverman, Neill R Graff-Radford, Francine Parfitt, Heather Johnson, Martin R Farlow, Ann Marie Hake, Brandy R Matthews, Scott Herring, Christopher H van Dyck, Richard E Carson, Martha G MacAvoy, Howard Chertkow, Howard Bergman, Chris Hosein, Sandra Black, Bojana Stefanovic, Curtis Caldwell, Ging-Yuek Robin Hsiung, Howard Feldman, Benita Mudge, Michele Assaly, Andrew Kertesz, John Rogers, Dick Trost, Charles Bernick, Donna Munic, Diana Kerwin, Marek-Marsel Mesulam, Kristina Lipowski, Chuang-Kuo Wu, Nancy Johnson, Carl Sadowsky, Walter Martinez, Teresa Villena, Raymond Scott Turner, Kathleen Johnson, Brigid Reynolds, Reisa A Sperling, Keith A Johnson, Gad Marshall, Meghan Frey, Jerome Yesavage, Joy L Taylor, Barton Lane, Allyson Rosen, Jared Tinklenberg, Marwan Sabbagh, Christine Belden, Sandra Jacobson, Neil Kowall, Ronald Killiany, Andrew E Budson, Alexander Norbash, Patricia Lynn Johnson, Thomas O Obisesan, Saba Wolday, Salome K Bwayo, Alan Lerner, Leon Hudson, Paula Ogrocki, Evan Fletcher, Owen Carmichael, John Olichney, Charles DeCarli, Smita Kittur, Michael Borrie, T-Y Lee, Dr Rob Bartha, Sterling Johnson, Sanjay Asthana, Cynthia M Carlsson, Steven G Potkin, Adrian Preda, Dana Nguyen, Pierre Tariot, Adam Fleisher, Stephanie Reeder, Vernice Bates, Horacio Capote, Michelle Rainka, Douglas W Scharre, Maria Kataki, Earl A Zimmerman, Dzintra Celmins, Alice D Brown, Godfrey D Pearlson, Karen Blank, Karen Anderson, Andrew J Saykin, Robert B Santulli, Eben S Schwartz, Kaycee M Sink, Jeff D Williamson, Pradeep Garg, Franklin Watkins, Brian R Ott, Henry Querfurth, Geoffrey Tremont, Stephen Salloway, Paul Malloy, Stephen Correia, Howard J Rosen, Bruce L Miller, Jacobo Mintzer, Crystal Flynn Longmire, Kenneth Spicer, Elizabether Finger, Irina Rachinsky, John Rogers, Andrew Kertesz, Dick Drost, Nunzio Pomara, Raymundo Hernando, Antero Sarrael, Susan K Schultz, Laura L Boles Ponto, Hyungsub Shim, Karen Elizabeth Smith, Norman Relkin, Gloria Chaing, Lisa Raudin, Amanda Smith, Kristin Fargher, Balebail Ashok Raj

Affiliations

¹ From the Department of Veterans Affairs Medical Center (N.M., P.S.I., S.M., M.W.), Center for Imaging of Neurodegenerative Diseases, San Francisco, CA; Clinical Neurochemistry Laboratory (N.M.), Institute of Neuroscience and Physiology, the Sahlgrenska Academy at the University of Gothenburg, Mölndal, Sweden; Department of Radiology and Biomedical Imaging (N.M., P.S.I., M.W.), University of California, San Francisco; Alzheimer's Disease Cooperative Study (P.S.A.), Department of Neurosciences, University of California, San Diego, La Jolla; Helen Wills Neuroscience Institute and School of Public Health (W.J.), University of California, Berkeley; and Department of Psychiatry (S.M.), University of California, San Francisco. niklas.mattsson@neuro.gu.se.
² From the Department of Veterans Affairs Medical Center (N.M., P.S.I., S.M., M.W.), Center for Imaging of Neurodegenerative Diseases, San Francisco, CA; Clinical Neurochemistry Laboratory (N.M.), Institute of Neuroscience and Physiology, the Sahlgrenska Academy at the University of Gothenburg, Mölndal, Sweden; Department of Radiology and Biomedical Imaging (N.M., P.S.I., M.W.), University of California, San Francisco; Alzheimer's Disease Cooperative Study (P.S.A.), Department of Neurosciences, University of California, San Diego, La Jolla; Helen Wills Neuroscience Institute and School of Public Health (W.J.), University of California, Berkeley; and Department of Psychiatry (S.M.), University of California, San Francisco.

PMID: 25681451
PMCID: PMC4371407
DOI: 10.1212/WNL.0000000000001375

Abstract

Objective: The objective of this study was to test whether effects of β-amyloid (Aβ) pathology on episodic memory were mediated by metabolism and gray matter volume in the early stages of Alzheimer disease.

Methods: This was a prospective cohort study. We measured baseline Aβ (using florbetapir-PET), brain function (using fluorodeoxyglucose-PET), and brain structure (using MRI). A mediation analysis was performed to test whether statistical effects of Aβ positivity on cross-sectional and longitudinal episodic memory were mediated by hypometabolism or regional gray matter volume in cognitively healthy controls (CN, n = 280) and mild cognitive impairment (MCI, n = 463).

Results: Lower memory scores were associated with Aβ positivity (CN, mildly; MCI, strongly), smaller gray matter volumes (CN, few regions, including hippocampus; MCI, widespread), and hypometabolism. Smaller volumes and hypometabolism mediated effects of Aβ in MCI but not in CN. The strongest individual regions mediated up to approximately 25%. A combination of brain structure and function mediated up to approximately 40%. In several regions, gray matter atrophy and hypometabolism predicted episodic memory without being associated (at p < 0.05) with Aβ positivity.

Conclusions: Changes in brain structure and function appear to be, in part, downstream events from Aβ pathology, ultimately resulting in episodic memory deficits. However, Aβ pathology is also strongly related to memory deficits through mechanisms that are not quantified by these imaging measurements, and episodic memory decline is partly caused by Alzheimer disease-like brain changes independently of Aβ pathology.

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Figures

**Figure 1. Direct associations between Aβ and brain structure and function**
β Coefficients for the effect of Aβ positivity on gray matter volumes (A, B) and FDG-PET (C, D) in CN (A, C) and MCI (B, D). The error bars are 95% confidence interval generated by nonparametric bootstrap. For regions with significant mediation (95% confidence interval excluding zero), results are shown in red. For convenience, regions are ranked by effect in MCI. Volumes, FDG-PET, and memory scores are standardized (scaled and centered). Only selected key regions were included in this plot. See figure e-1 for data on all tested regions. Aβ = β-amyloid; CN = cognitively healthy control; FDG = fluorodeoxyglucose; GM = gray matter; MCI = mild cognitive impairment.

**Figure 2. Brain structure and function mediating effects of Aβ on delayed recall**
Mediation by gray matter volumes (A, B) and FDG-PET (C, D) for the effect of Aβ positivity on LM delayed recall at baseline (A, C) and over time (B, D) in mild cognitive impairment. Data are indirect effects (*c-c'*) with 95% confidence interval. Significant mediations are shown in red. The right y-axes indicate the β_ratio (the proportion of Aβ's effect that is explained by volume). For example, hippocampal atrophy explained 16% to 25% of the effect of Aβ on memory. Only selected key regions were included in this plot. See figure e-4 for data on all tested regions. Only regions with some (p < 0.1) direct association with the memory scores are included. Aβ = β-amyloid; FDG = fluorodeoxyglucose; LM = Logical Memory.

**Figure 3. Mediation of effects of Aβ on change in Logical Memory delayed recall**
Path analysis showing how hippocampal volume and angular FDG-PET mediate the effect of Aβ on longitudinal change in Logical Memory delayed recall. (A) The direct effects of Aβ on memory, (B) hippocampal volume mediating effects of Aβ on memory, (C) angular FDG-PET mediating effects of Aβ on memory, and (D) the combination of hippocampal volume and FDG-PET mediating effects of Aβ on memory. The figure includes the following standardized regression coefficients: a, the effects of Aβ on hippocampal volume or FDG-PET; b, the effects of hippocampal volume or FDG-PET on memory when adjusting for Aβ; c, the direct association between Aβ and memory (without adjusting for hippocampal volume or FDG-PET); c', the association between Aβ and memory when adjusting for hippocampal volume and/or FDG-PET; and *c-c'*, the mediated effect on memory (with % mediation). *p < 0.05. Aβ = β-amyloid; FDG = fluorodeoxyglucose; hippo = hippocampal.

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References

1. Knopman DS, Jack CR, Jr, Wiste HJ, et al. Brain injury biomarkers are not dependent on β-amyloid in normal elderly. Ann Neurol 2013;73:472–480. - PMC - PubMed
1. Mormino EC, Kluth JT, Madison CM, et al. Episodic memory loss is related to hippocampal-mediated beta-amyloid deposition in elderly subjects. Brain 2009;132:1310–1323. - PMC - PubMed
1. Han SD, Gruhl J, Beckett L, et al. Beta amyloid, tau, neuroimaging, and cognition: sequence modeling of biomarkers for Alzheimer's disease. Brain Imaging Behav 2012;6:610–620. - PMC - PubMed
1. Landau SM, Mintun MA, Joshi AD, et al. Amyloid deposition, hypometabolism, and longitudinal cognitive decline. Ann Neurol 2012;72:578–586. - PMC - PubMed
1. Joshi AD, Pontecorvo MJ, Clark CM, et al. Performance characteristics of amyloid PET with florbetapir F 18 in patients with Alzheimer's disease and cognitively normal subjects. J Nucl Med 2012;53:378–384. - PubMed

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[1] Knopman DS, Jack CR, Jr, Wiste HJ, et al. Brain injury biomarkers are not dependent on β-amyloid in normal elderly. Ann Neurol 2013;73:472–480. - PMC - PubMed

[2] Knopman DS, Jack CR, Jr, Wiste HJ, et al. Brain injury biomarkers are not dependent on β-amyloid in normal elderly. Ann Neurol 2013;73:472–480. - PMC - PubMed

[3] Mormino EC, Kluth JT, Madison CM, et al. Episodic memory loss is related to hippocampal-mediated beta-amyloid deposition in elderly subjects. Brain 2009;132:1310–1323. - PMC - PubMed

[4] Mormino EC, Kluth JT, Madison CM, et al. Episodic memory loss is related to hippocampal-mediated beta-amyloid deposition in elderly subjects. Brain 2009;132:1310–1323. - PMC - PubMed

[5] Han SD, Gruhl J, Beckett L, et al. Beta amyloid, tau, neuroimaging, and cognition: sequence modeling of biomarkers for Alzheimer's disease. Brain Imaging Behav 2012;6:610–620. - PMC - PubMed

[6] Han SD, Gruhl J, Beckett L, et al. Beta amyloid, tau, neuroimaging, and cognition: sequence modeling of biomarkers for Alzheimer's disease. Brain Imaging Behav 2012;6:610–620. - PMC - PubMed

[7] Landau SM, Mintun MA, Joshi AD, et al. Amyloid deposition, hypometabolism, and longitudinal cognitive decline. Ann Neurol 2012;72:578–586. - PMC - PubMed

[8] Landau SM, Mintun MA, Joshi AD, et al. Amyloid deposition, hypometabolism, and longitudinal cognitive decline. Ann Neurol 2012;72:578–586. - PMC - PubMed

[9] Joshi AD, Pontecorvo MJ, Clark CM, et al. Performance characteristics of amyloid PET with florbetapir F 18 in patients with Alzheimer's disease and cognitively normal subjects. J Nucl Med 2012;53:378–384. - PubMed

[10] Joshi AD, Pontecorvo MJ, Clark CM, et al. Performance characteristics of amyloid PET with florbetapir F 18 in patients with Alzheimer's disease and cognitively normal subjects. J Nucl Med 2012;53:378–384. - PubMed

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Brain structure and function as mediators of the effects of amyloid on memory

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Brain structure and function as mediators of the effects of amyloid on memory

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