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Diet, psychosocial stress, and Alzheimer’s disease-related neuroanatomy in female nonhuman primates

View ORCID ProfileBrett M. Frye, View ORCID ProfileSuzanne Craft, View ORCID ProfileThomas C. Register, View ORCID ProfileRachel N. Andrews, View ORCID ProfileSusan E. Appt, View ORCID ProfileMara Z. Vitolins, View ORCID ProfileBeth Uberseder, View ORCID ProfileMarnie G. Silverstein-Metzler, Haiying Chen, View ORCID ProfileChristopher T. Whitlow, View ORCID ProfileJeongchul Kim, Richard A. Barcus, View ORCID ProfileSamuel N. Lockhart, View ORCID ProfileSiobhan Hoscheidt, Brandon M. Say, Sarah E. Corbitt, View ORCID ProfileCarol A. Shively
doi: https://doi.org/10.1101/2020.09.25.313593
Brett M. Frye
1Department of Pathology/Comparative Medicine, Wake Forest School of Medicine
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Suzanne Craft
2Wake Forest Alzheimer’s Disease Research Center
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Thomas C. Register
1Department of Pathology/Comparative Medicine, Wake Forest School of Medicine
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Rachel N. Andrews
1Department of Pathology/Comparative Medicine, Wake Forest School of Medicine
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Susan E. Appt
1Department of Pathology/Comparative Medicine, Wake Forest School of Medicine
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Mara Z. Vitolins
3Department of Epidemiology & Prevention, Wake Forest School of Medicine
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Beth Uberseder
1Department of Pathology/Comparative Medicine, Wake Forest School of Medicine
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Marnie G. Silverstein-Metzler
1Department of Pathology/Comparative Medicine, Wake Forest School of Medicine
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Haiying Chen
4Department of Biostatistics and Data Science, Wake Forest School of Medicine
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Christopher T. Whitlow
5Department of Radiology, Wake Forest School of Medicine
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Jeongchul Kim
5Department of Radiology, Wake Forest School of Medicine
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Richard A. Barcus
5Department of Radiology, Wake Forest School of Medicine
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Samuel N. Lockhart
2Wake Forest Alzheimer’s Disease Research Center
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Siobhan Hoscheidt
6Department of Psychology, University of Arizona
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Brandon M. Say
7Department of Pathology, Stanford University School of Medicine
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Sarah E. Corbitt
8Biomedical Sciences, MS program | Integrative Physiology and Pharmacology Adult Behavioral Health
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Carol A. Shively
1Department of Pathology/Comparative Medicine, Wake Forest School of Medicine
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  • For correspondence: cshively@wakehealth.edu
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ABSTRACT

INTRODUCTION Associations between diet, psychosocial stress, and neurodegenerative disease, including Alzheimer’s disease (AD), have been reported, but causal relationships are difficult to determine in human studies.

METHODS We used structural magnetic resonance imaging in a well-validated nonhuman primate model of AD-like neuropathology to examine the longitudinal effects of diet (Mediterranean versus Western) and social subordination stress on brain anatomy, including global volumes, cortical thicknesses and volumes, and twenty individual regions of interest (ROIs).

RESULTS Western diet resulted in greater cortical thicknesses, total brain volumes and gray matter, and diminished cerebrospinal fluid and white matter volumes. Socially stressed subordinates had smaller whole brain volumes but larger ROIs relevant to AD than dominants.

DISCUSSION The observation of increased size of AD-related brain areas is consistent with similar reports of mid-life volume increases predicting increased AD risk later in life. While the biological mechanisms underlying the findings require future investigation, these observations suggest that Western diet and psychosocial stress instigate pathologic changes that increase risk of AD-associated neuropathologies, whereas Mediterranean diet may protect the brain.

RESEARCH IN CONTEXT

  1. Systematic review: The authors reviewed the literature with PubMed and Google Scholar and found a number of publications which are cited that suggest that AD pathogenesis begins well before the onset of symptoms.

  2. Interpretation: Our findings support the hypothesis that Western diet and psychosocial stress may instigate neuroinflammatory responses that increase risk of later developing AD-like neuropathologies, whereas the structural stasis in the Mediterranean diet group may represent a resilient phenotype.

  3. Future directions: The manuscript serves as a critical first step in describing risk and resilient phenotypes during middle age in a nonhuman primate model of AD-like neuropathology. This report lays the groundwork for ongoing efforts to determine whether neuroinflammatory profiles differed across diet and stress groups. Future studies should aim to understand the temporal emergence of functional disparities associated with the changes in brain structure observed here.

HIGHLIGHTS

  • Global brain volumes changed in response to Western, but not Mediterranean, diet.

  • Western diet increased cortical thickness in multiple regions relevant to AD.

  • Mediterranean diet did not alter cortical thicknesses relevant to AD.

  • Brain regions associated with AD risk differed between low and high stress monkeys.

  • Psychosocial stress may modulate the effects of diet on the brain.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted September 26, 2020.
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Diet, psychosocial stress, and Alzheimer’s disease-related neuroanatomy in female nonhuman primates
Brett M. Frye, Suzanne Craft, Thomas C. Register, Rachel N. Andrews, Susan E. Appt, Mara Z. Vitolins, Beth Uberseder, Marnie G. Silverstein-Metzler, Haiying Chen, Christopher T. Whitlow, Jeongchul Kim, Richard A. Barcus, Samuel N. Lockhart, Siobhan Hoscheidt, Brandon M. Say, Sarah E. Corbitt, Carol A. Shively
bioRxiv 2020.09.25.313593; doi: https://doi.org/10.1101/2020.09.25.313593
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Diet, psychosocial stress, and Alzheimer’s disease-related neuroanatomy in female nonhuman primates
Brett M. Frye, Suzanne Craft, Thomas C. Register, Rachel N. Andrews, Susan E. Appt, Mara Z. Vitolins, Beth Uberseder, Marnie G. Silverstein-Metzler, Haiying Chen, Christopher T. Whitlow, Jeongchul Kim, Richard A. Barcus, Samuel N. Lockhart, Siobhan Hoscheidt, Brandon M. Say, Sarah E. Corbitt, Carol A. Shively
bioRxiv 2020.09.25.313593; doi: https://doi.org/10.1101/2020.09.25.313593

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