Functional brain networks reflect spatial and temporal autocorrelation

• Published in: Nature neuroscience Vol. 26; no. 5; pp. 867 - 878
• Main Authors: Shinn, Maxwell, Hu, Amber, Turner, Laurel, Noble, Stephanie, Preller, Katrin H., Ji, Jie Lisa, Moujaes, Flora, Achard, Sophie, Scheinost, Dustin, Constable, R. Todd, Krystal, John H., Vollenweider, Franz X., Lee, Daeyeol, Anticevic, Alan, Bullmore, Edward T., Murray, John D.
• Format: Journal Article
• Language: English
• Published: New York Nature Publishing Group US 01.05.2023; Nature Publishing Group
• Subjects: 631/1647/245/1627; 631/378/116; 631/378/2649; Aging; Animal Genetics and Genomics; Autocorrelation; Behavioral Sciences; Biological Techniques; Biomedical and Life Sciences; Biomedicine; Brain; Brain - diagnostic imaging; Brain mapping; Brain Mapping - methods; Complexity; Drugs; Experimental methods; Functional magnetic resonance imaging; Magnetic resonance imaging; Magnetic Resonance Imaging - methods; Nervous system; Network topologies; Neurobiology; Neuroimaging; Neurosciences; Smoothness; Statistics; Time Factors; Time series; Topology
• ISSN: 1097-6256; 1546-1726; 1546-1726
• DOI: 10.1038/s41593-023-01299-3

High-throughput experimental methods in neuroscience have led to an explosion of techniques for measuring complex interactions and multi-dimensional patterns. However, whether sophisticated measures of emergent phenomena can be traced back to simpler, low-dimensional statistics is largely unknown. To explore this question, we examined resting-state functional magnetic resonance imaging (rs-fMRI) data using complex topology measures from network neuroscience. Here we show that spatial and temporal autocorrelation are reliable statistics that explain numerous measures of network topology. Surrogate time series with subject-matched spatial and temporal autocorrelation capture nearly all reliable individual and regional variation in these topology measures. Network topology changes during aging are driven by spatial autocorrelation, and multiple serotonergic drugs causally induce the same topographic change in temporal autocorrelation. This reductionistic interpretation of widely used complexity measures may help link them to neurobiology. Individual variation in fMRI-derived brain networks is reproduced in a model using only the smoothness (autocorrelation) of the fMRI time series. Smoothness has implication for aging and can be causally manipulated by psychedelic serotonergic drugs.