The dynamic shaping of local cortical circuitry by sex and age, and its relation to pattern comparison processing speed

• Published in: Journal of neurophysiology 2022-08, Vol.128 (2), p.395-404
• Main Authors: Christova, Peka, James, Lisa M, Georgopoulos, Apostolos P
• Format: Article
• Language: English
• Subjects: Brain; Cognition; Connectome; Female; Humans; Magnetic Resonance Imaging - methods; Male; Young Adult
• ISSN: 0022-3077; 1522-1598
• DOI: 10.1152/jn.00252.2022

Previous resting-state functional magnetic resonance imaging (fMRI) studies have shown that the strength of local neural interactions decreases with distance. Here, we extend that line of research to evaluate effects of sex and age on local cortical circuitry in six cortical areas (superior frontal, precentral, postcentral, superior parietal, inferior parietal, and lateral occipital) using data acquired from 1,054 healthy young adults who participated in the Human Connectome Project. We confirmed previous findings that the strength of zero-lag correlations between prewhitened, resting-state, blood level oxygenation-dependent (BOLD) fMRI time series decreased with distance locally and documented that the rate of decrease with distance (spatial steepness) ) was progressively lower from anterior to posterior areas, ) was greater in women, especially in anterior areas, ) increased with age, particularly for women, ) was significantly correlated with percent inhibition, and ) was positively and highly significantly correlated with pattern comparison processing speed (PCPS). A hierarchical tree clustering analysis of this dependence of PCPS on spatial steepness revealed a differential organization in processing that information between the two hemispheres, namely, a more independent vs. a more integrative processing in the left and right hemispheres, respectively. These findings document sex and age differences in dynamic local cortical interactions and provide evidence that spatial sharpening of these interactions may underlie cognitive processing speed differently organized in the two hemispheres. Sex and age significantly affect shaping of local cortical interactions that are more limited in women and older brains. The net result is an increase in local spatial steepness of interactions, leading to a reduction of overlap among local ensembles and, hence, a more efficient information processing and an increase in the number of independent local cortical "processors." Remarkably, cognitive processing speed was positively associated with local spatial steepness, in keeping with the reasoning earlier.