Dataset Information

Macroscopic resting-state brain dynamics are best described by linear models.

ABSTRACT: It is typically assumed that large networks of neurons exhibit a large repertoire of nonlinear behaviours. Here we challenge this assumption by leveraging mathematical models derived from measurements of local field potentials via intracranial electroencephalography and of whole-brain blood-oxygen-level-dependent brain activity via functional magnetic resonance imaging. We used state-of-the-art linear and nonlinear families of models to describe spontaneous resting-state activity of 700 participants in the Human Connectome Project and 122 participants in the Restoring Active Memory project. We found that linear autoregressive models provide the best fit across both data types and three performance metrics: predictive power, computational complexity and the extent of the residual dynamics unexplained by the model. To explain this observation, we show that microscopic nonlinear dynamics can be counteracted or masked by four factors associated with macroscopic dynamics: averaging over space and over time, which are inherent to aggregated macroscopic brain activity, and observation noise and limited data samples, which stem from technological limitations. We therefore argue that easier-to-interpret linear models can faithfully describe macroscopic brain dynamics during resting-state conditions.

SUBMITTER: Nozari E

PROVIDER: S-EPMC11357987 | biostudies-literature | 2024 Jan

REPOSITORIES: biostudies-literature

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Macroscopic resting-state brain dynamics are best described by linear models.

Nozari Erfan E Bertolero Maxwell A MA Stiso Jennifer J Caciagli Lorenzo L Cornblath Eli J EJ He Xiaosong X Mahadevan Arun S AS Pappas George J GJ Bassett Dani S DS

Nature biomedical engineering 20231211 1

It is typically assumed that large networks of neurons exhibit a large repertoire of nonlinear behaviours. Here we challenge this assumption by leveraging mathematical models derived from measurements of local field potentials via intracranial electroencephalography and of whole-brain blood-oxygen-level-dependent brain activity via functional magnetic resonance imaging. We used state-of-the-art linear and nonlinear families of models to describe spontaneous resting-state activity of 700 particip ...[more]

PMID: 38082179

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Project description:Personality neuroscience aims to find associations between brain measures and personality traits. Findings to date have been severely limited by a number of factors, including small sample size and omission of out-of-sample prediction. We capitalized on the recent availability of a large database, together with the emergence of specific criteria for best practices in neuroimaging studies of individual differences. We analyzed resting-state functional magnetic resonance imaging data from 884 young healthy adults in the Human Connectome Project (HCP) database. We attempted to predict personality traits from the "Big Five", as assessed with the NEO-FFI test, using individual functional connectivity matrices. After regressing out potential confounds (such as age, sex, handedness and fluid intelligence), we used a cross-validated framework, together with test-retest replication (across two sessions of resting-state fMRI for each subject), to quantify how well the neuroimaging data could predict each of the five personality factors. We tested three different (published) denoising strategies for the fMRI data, two inter-subject alignment and brain parcellation schemes, and three different linear models for prediction. As measurement noise is known to moderate statistical relationships, we performed final prediction analyses using average connectivity across both imaging sessions (1 h of data), with the analysis pipeline that yielded the highest predictability overall. Across all results (test/retest; 3 denoising strategies; 2 alignment schemes; 3 models), Openness to experience emerged as the only reliably predicted personality factor. Using the full hour of resting-state data and the best pipeline, we could predict Openness to experience (NEOFAC_O: r=0.24, R2=0.024) almost as well as we could predict the score on a 24-item intelligence test (PMAT24_A_CR: r=0.26, R2=0.044). Other factors (Extraversion, Neuroticism, Agreeableness and Conscientiousness) yielded weaker predictions across results that were not statistically significant under permutation testing. We also derived two superordinate personality factors ("α" and "β") from a principal components analysis of the NEO-FFI factor scores, thereby reducing noise and enhancing the precision of these measures of personality. We could account for 5% of the variance in the β superordinate factor (r=0.27, R2=0.050), which loads highly on Openness to experience. We conclude with a discussion of the potential for predicting personality from neuroimaging data and make specific recommendations for the field.

Dataset Information

Macroscopic resting-state brain dynamics are best described by linear models.

Publications

Macroscopic resting-state brain dynamics are best described by linear models.

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