Asymmetric thinning of the cerebral cortex across the adult lifespan is accelerated in Alzheimer’s disease

James M. Roe; Didac Vidal-Piñeiro; Øystein Sørensen; Andreas M. Brandmaier; Sandra Düzel; Hector A. Gonzalez; Rogier A. Kievit; Ethan Knights; Simone Kühn; Ulman Lindenberger; Athanasia M. Mowinckel; Lars Nyberg; Denise C. Park; Sara Pudas; Melissa M. Rundle; Kristine B. Walhovd; Anders M. Fjell; René Westerhausen; The Australian Imaging Biomarkers and Lifestyle Flagship Study of Ageing

doi:10.1038/s41467-021-21057-y

Asymmetric thinning of the cerebral cortex across the adult lifespan is accelerated in Alzheimer’s disease

James M. Roe^*, Didac Vidal-Piñeiro, Øystein Sørensen, Andreas M. Brandmaier, Sandra Düzel, Hector A. Gonzalez, Rogier A. Kievit, Ethan Knights, Simone Kühn, Ulman Lindenberger, Athanasia M. Mowinckel, Lars Nyberg, Denise C. Park, Sara Pudas, Melissa M. Rundle, Kristine B. Walhovd, Anders M. Fjell, René Westerhausen, The Australian Imaging Biomarkers and Lifestyle Flagship Study of Ageing

^*Corresponding author for this work

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Abstract

Aging and Alzheimer’s disease (AD) are associated with progressive brain disorganization. Although structural asymmetry is an organizing feature of the cerebral cortex it is unknown whether continuous age- and AD-related cortical degradation alters cortical asymmetry. Here, in multiple longitudinal adult lifespan cohorts we show that higher-order cortical regions exhibiting pronounced asymmetry at age ~20 also show progressive asymmetry-loss across the adult lifespan. Hence, accelerated thinning of the (previously) thicker homotopic hemisphere is a feature of aging. This organizational principle showed high consistency across cohorts in the Lifebrain consortium, and both the topological patterns and temporal dynamics of asymmetry-loss were markedly similar across replicating samples. Asymmetry-change was further accelerated in AD. Results suggest a system-wide dedifferentiation of the adaptive asymmetric organization of heteromodal cortex in aging and AD.

Original language	English
Article number	721
Pages (from-to)	1-11
Number of pages	11
Journal	Nature Communications
Volume	12
Issue number	1
DOIs	https://doi.org/10.1038/s41467-021-21057-y
Publication status	Published - 1 Feb 2021

Bibliographical note

Copyright the Author(s) 2021. Version archived for private and non-commercial use with the permission of the author/s and according to publisher conditions. For further rights please contact the publisher.

Correction paper can be found at Roe, J.M., Vidal-Piñeiro, D., Sørensen, Ø. et al. Author Correction: Asymmetric thinning of the cerebral cortex across the adult lifespan is accelerated in Alzheimer’s disease. Nat Commun 13, 834 (2022). https://doi.org/10.1038/s41467-022-28514-2

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Roe, J. M., Vidal-Piñeiro, D., Sørensen, Ø., Brandmaier, A. M., Düzel, S., Gonzalez, H. A., Kievit, R. A., Knights, E., Kühn, S., Lindenberger, U., Mowinckel, A. M., Nyberg, L., Park, D. C., Pudas, S., Rundle, M. M., Walhovd, K. B., Fjell, A. M., Westerhausen, R., & The Australian Imaging Biomarkers and Lifestyle Flagship Study of Ageing (2021). Asymmetric thinning of the cerebral cortex across the adult lifespan is accelerated in Alzheimer’s disease. Nature Communications, 12(1), 1-11. Article 721. https://doi.org/10.1038/s41467-021-21057-y

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abstract = "Aging and Alzheimer{\textquoteright}s disease (AD) are associated with progressive brain disorganization. Although structural asymmetry is an organizing feature of the cerebral cortex it is unknown whether continuous age- and AD-related cortical degradation alters cortical asymmetry. Here, in multiple longitudinal adult lifespan cohorts we show that higher-order cortical regions exhibiting pronounced asymmetry at age ~20 also show progressive asymmetry-loss across the adult lifespan. Hence, accelerated thinning of the (previously) thicker homotopic hemisphere is a feature of aging. This organizational principle showed high consistency across cohorts in the Lifebrain consortium, and both the topological patterns and temporal dynamics of asymmetry-loss were markedly similar across replicating samples. Asymmetry-change was further accelerated in AD. Results suggest a system-wide dedifferentiation of the adaptive asymmetric organization of heteromodal cortex in aging and AD.",

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note = "Copyright the Author(s) 2021. Version archived for private and non-commercial use with the permission of the author/s and according to publisher conditions. For further rights please contact the publisher. Correction paper can be found at Roe, J.M., Vidal-Pi{\~n}eiro, D., S{\o}rensen, {\O}. et al. Author Correction: Asymmetric thinning of the cerebral cortex across the adult lifespan is accelerated in Alzheimer{\textquoteright}s disease. Nat Commun 13, 834 (2022). https://doi.org/10.1038/s41467-022-28514-2",

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Roe, JM, Vidal-Piñeiro, D, Sørensen, Ø, Brandmaier, AM, Düzel, S, Gonzalez, HA, Kievit, RA, Knights, E, Kühn, S, Lindenberger, U, Mowinckel, AM, Nyberg, L, Park, DC, Pudas, S, Rundle, MM, Walhovd, KB, Fjell, AM, Westerhausen, R & The Australian Imaging Biomarkers and Lifestyle Flagship Study of Ageing 2021, 'Asymmetric thinning of the cerebral cortex across the adult lifespan is accelerated in Alzheimer’s disease', Nature Communications, vol. 12, no. 1, 721, pp. 1-11. https://doi.org/10.1038/s41467-021-21057-y

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AU - Brown, Belinda

AU - Sohrabi, Harmid

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N1 - Copyright the Author(s) 2021. Version archived for private and non-commercial use with the permission of the author/s and according to publisher conditions. For further rights please contact the publisher. Correction paper can be found at Roe, J.M., Vidal-Piñeiro, D., Sørensen, Ø. et al. Author Correction: Asymmetric thinning of the cerebral cortex across the adult lifespan is accelerated in Alzheimer’s disease. Nat Commun 13, 834 (2022). https://doi.org/10.1038/s41467-022-28514-2

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N2 - Aging and Alzheimer’s disease (AD) are associated with progressive brain disorganization. Although structural asymmetry is an organizing feature of the cerebral cortex it is unknown whether continuous age- and AD-related cortical degradation alters cortical asymmetry. Here, in multiple longitudinal adult lifespan cohorts we show that higher-order cortical regions exhibiting pronounced asymmetry at age ~20 also show progressive asymmetry-loss across the adult lifespan. Hence, accelerated thinning of the (previously) thicker homotopic hemisphere is a feature of aging. This organizational principle showed high consistency across cohorts in the Lifebrain consortium, and both the topological patterns and temporal dynamics of asymmetry-loss were markedly similar across replicating samples. Asymmetry-change was further accelerated in AD. Results suggest a system-wide dedifferentiation of the adaptive asymmetric organization of heteromodal cortex in aging and AD.

AB - Aging and Alzheimer’s disease (AD) are associated with progressive brain disorganization. Although structural asymmetry is an organizing feature of the cerebral cortex it is unknown whether continuous age- and AD-related cortical degradation alters cortical asymmetry. Here, in multiple longitudinal adult lifespan cohorts we show that higher-order cortical regions exhibiting pronounced asymmetry at age ~20 also show progressive asymmetry-loss across the adult lifespan. Hence, accelerated thinning of the (previously) thicker homotopic hemisphere is a feature of aging. This organizational principle showed high consistency across cohorts in the Lifebrain consortium, and both the topological patterns and temporal dynamics of asymmetry-loss were markedly similar across replicating samples. Asymmetry-change was further accelerated in AD. Results suggest a system-wide dedifferentiation of the adaptive asymmetric organization of heteromodal cortex in aging and AD.

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Asymmetric thinning of the cerebral cortex across the adult lifespan is accelerated in Alzheimer’s disease

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