Resting-state fractal brain connectivity is associated with impaired cognitive performance in healthy aging.

Akos Czoch, Zalan Kaposzta, Peter Mukli, Orestis Stylianou, Andras Eke, Frigyes Samuel Racz

Journal: GeroScience 2024;46(1):473-489

PMID: 37458934

Abstract

Aging affects cognitive functions even in the absence of ongoing pathologies. The neurophysiological basis of age-related cognitive decline (CD), however, is not completely understood. Alterations in both functional brain connectivity and in the fractal scaling of neuronal dynamics have been linked to aging and cognitive performance. Recently, fractal connectivity (FrC) has been proposed - combining the two concepts - for capturing long-term interactions among brain regions. FrC was shown to be influenced by increased mental workload; however, no prior studies investigated how resting-state FrC relates to cognitive performance and plausible CD in healthy aging. We recruited 19 healthy elderly (HE) and 24 young control (YC) participants, who underwent resting-state electroencephalography (EEG) measurements and comprehensive cognitive evaluation using 7 tests of the Cambridge Neurophysiological Test Automated Battery. FrC networks were reconstructed from EEG data using the recently introduced multiple-resampling cross-spectral analysis (MRCSA). Elderly individuals could be characterized with increased response latency and reduced performance in 4-4 tasks, respectively, with both reaction time and accuracy being affected in two tasks. Auto- and cross-spectral exponents - characterizing regional fractal dynamics and FrC, respectively, - were found reduced in HE when compared to YC over most of the cortex. Additionally, fractal scaling of frontoparietal connections expressed an inverse relationship with task performance in visual memory and sustained attention domains in elderly, but not in young individuals. Our results confirm that the fractal nature of brain connectivity - as captured by MRCSA - is affected in healthy aging. Furthermore, FrC appears as a sensitive neurophysiological marker of age-related CD.

© 2023. The Author(s).

Address: Department of Physiology, Semmelweis University, Budapest, Hungary.; Oklahoma Center for Geroscience and Healthy Brain Aging, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA.; Vascular Cognitive Impairment and Neurodegeneration Program, Department of Neurosurgery, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA.; International Training Program in Geroscience, Doctoral School of Basic and Translational Medicine/Department of Public Health, Semmelweis University, Budapest, Hungary.; Institute of Translational Medicine, Semmelweis University, Budapest, Hungary.; Berlin Institute of Health at Charité, University Hospital Berlin, Berlin, Germany.; Department of Neurology With Experimental Neurology, Charité-University Hospital Berlin, Corporate Member of Freie Universität Berlin and Humboldt Universität Zu Berlin, Berlin, Germany.; Department of Radiology and Biomedical Imaging, Yale University School of Medicine, New Haven, CT, USA.; Department of Physiology, Semmelweis University, Budapest, Hungary. [email protected].; Department of Neurology, Dell Medical School, The University of Texas at Austin, Austin, TX, USA. [email protected].; Mulva Clinic for the Neurosciences, Dell Medical School, The University of Texas at Austin, Austin, TX, USA. [email protected].
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