High-Order Interdependencies in the Aging Brain
Abstract
Background:
Brain interdependencies can be studied from either a structural/anatomical perspective (“structural connectivity”) or by considering statistical interdependencies (“functional connectivity” [FC]). Interestingly, while structural connectivity is by definition pairwise (white-matter fibers project from one region to another), FC is not. However, most FC analyses only focus on pairwise statistics and they neglect higher order interactions. A promising tool to study high-order interdependencies is the recently proposed O-Information, which can quantify the intrinsic statistical synergy and the redundancy in groups of three or more interacting variables.
Methods:
We analyzed functional magnetic resonance imaging (fMRI) data obtained at rest from 164 healthy subjects with ages ranging in 10 to 80 years and used O-Information to investigate how high-order statistical interdependencies are affected by age.
Results:
Older participants (from 60 to 80 years old) exhibited a higher predominance of redundant dependencies compared with younger participants, an effect that seems to be pervasive as it is evident for all orders of interaction. In addition, while there is strong heterogeneity across brain regions, we found a “redundancy core” constituted by the prefrontal and motor cortices in which redundancy was evident at all the interaction orders studied.
Discussion:
High-order interdependencies in fMRI data reveal a dominant redundancy in functions such as working memory, executive, and motor functions. Our methodology can be used for a broad range of applications, and the corresponding code is freely available.
Impact statement
Past research has showcased multiple changes to the brain's structural and functional properties caused by aging. Here we expand prior work through recent advancements in multivariate information theory, which provide richer and more theoretically principled analyses than existing alternatives. We show that the brains of older participants contain more redundant information at multiple spatial scales—that is, activation in different brain regions is less diverse, compared with younger participants—and identify a “redundancy core” constituted by prefrontal and motor cortices, which might explained impaired performance in the old population in functions such as working memory and executive control.
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Published In
Article first published online: November 10, 2021
Issue published: November 2021
Keywords
PubMed: 33858199
Authors
Authors' Contributions
M.G.: study conceptualization, methodology, performed the analyses, produced the figures, and drafted the article. R.C.: study conceptualization, methodology, performed the analyses, supervised the information metrics, and drafted the article. P.A.M.M.: study conceptualization, methodology, supervised the information metrics, and drafted the article. F.E.R.: study conceptualization, methodology, supervised the information metrics, and drafted the article. P.O.: study conceptualization and methodology. I.D.: preprocessed the images. S.P.S.: recruited the participants and drafted the article. J.M.C.: study conceptualization, data curation, methodology, supervised the information metrics, and drafted the article. All the authors participated in the writing of the article and agreed on the submission of the final version.
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