Functional connectivity between the caudate nucleus and the frontal lobe and its association with executive functions in children and adolescents: a resting state fMRI study

Abstract

During childhood and adolescence, the human brain becomes structurally and functionally mature, affecting the development of various executive functions (EFs). The frontal lobe plays a significant role in managing a wide range of EFs from the understanding of the neurocognitive development of executive functioning. Along with the frontal lobe, the caudate nucleus (CN) is suggested to contribute to EFs. The frontal-subcortical circuit, which is a natural pathway connecting the basal ganglia to the frontal lobe, is suggested as a strongly associated circuit with EFs. Although significant functional connectivity (FC) between the CN and frontal lobe is claimed to play an important role in EFs, there is not enough data on functional connectivity between the bilateral CN and the frontal lobe and its relationship with EFs during childhood and adolescence. We investigated the degrees of FC between the caudate and the regions of the frontal lobe and their relationship with EFs in a community sample of Korean children and adolescents. To investigate EFs associated with functional brain networks, we recruited participants aged between 6 and 17. The present study used fMRI seed-based connectivity analyses with bilateral caudate and all frontal lobe regions as our regions of interest and performed partial correlation analyses with the Stroop, Children Color Trails Test (CCTT), and Wisconsin Card Sorting Test (WSCT) to measure overall EFs. Overall, 106 children and adolescents (59 males and 47 females) with a mean age of 12.40 years participated in a resting-state functional magnetic resonance imaging(rs-fMRI) study. We found strong positive correlations between the frontal-caudate FCs and Stroop, CCTT, and WSCT scores. The effect of sex was adjusted by partial correlation analyses, which revealed significant positive corrections between fronto-caudate FC strengths and each clinical score. The novelty of our findings provides new insights into functional interactions between the CN and the frontal sub-regions, especially since there is a significant association shown with participants aged 13 years and older after adjusting for sex. In Stroop, FC between bilateral CN and the left and right opercular part of the inferior frontal gyrus, left triangular of the inferior frontal gyrus, and right rolandic operculum are shown significantly. The left medial part of the orbitofrontal cortex, the left and right superior part of the orbitofrontal cortex, and the right inferior part of the orbital frontal cortex are associated with bilateral CN in CCTT scores. Bilateral CN and bilateral dorsolateral parts of the superior frontal gyrus, middle frontal gyrus, medial part of the superior frontal gyrus, and anterior cingulate cortex are functionally connected with WSCT scores. Our findings highlight a significant correlation between caudate-frontal lobe functional connectivity and EFs with a sample of children and adolescents during the critical developmental period.