Aberrant Functional Connectivity of Sensorimotor Network and Its Relationship With Executive Dysfunction in Bipolar Disorder Type I

Abstract

BackgroundThe key pathophysiological mechanism of executive dysfunction in patients with bipolar disorder type I (BD-I) is still unclear. Previous studies have demonstrated that it may be related to the disbalance of the sensory motor network (SMN).ObjectiveThis study was designed to explore the aberrant functional connectivity (FC) of SMN in BD-I patients and its potential associations with executive dysfunction.MethodsEighteen BD-I patients and 20 healthy controls (HCs) underwent resting-state fMRI scans. The intranetwork and internetwork functional connectivities of SMN were extracted by independent component analysis (ICA). Clinical symptoms were assessed by the Bech–Rafaelsen Mania Rating Scale (BRMS) and Positive and Negative Syndrome Scale (PANSS). Executive function was measured by digit span tasks and a verbal fluency test. Finally, linear regression and correlation analyses were applied to measure the potential associations between clinical symptoms, intranetwork and internetwork functional connectivities, and executive function performance.Results(1) Patients with BD-I showed increased connectivity in the right paracentral lobule and the right postcentral gyrus within the SMN, and the increased connectivity value was positively correlated with the BRMS score (P < 0.05) but negatively correlated with digit span forward scores (P < 0.05). (2) Compared with HC, the connectivity value increased between the SMN and dorsal attention network (DAN) (P < 0.01) and between the default mode network (DMN) and DAN (P < 0.05) but decreased between the DAN and auditory network (AN) (P < 0.05) and between the SMN and DMN (P < 0.01) in patients with BD-I. (3) Digit span forward scores and education of all participants were negatively correlated with FC between SMN and DAN. Age of all subjects was positively correlated with FC between SMN and DMN.ConclusionOur findings suggest that the sensorimotor network of BD-I has abnormal functional connections within and between networks, and the abnormal FC value correlated with clinical symptoms and executive function, which provide new information for exploring the neural physiopathology of executive dysfunction in BD-I patients.

Structural and functional MRI correlates of inflammation in bipolar disorder: a systematic review

“…On the other hand, the results on somatomotor network (SMN) alterations in association with inflammation agree with accumulating functional MRI literature on disruption of this network in BD patients (Kebets et al, 2019;Martino et al, 2020;Rey et al, 2021;Tang et al, 2021). These findings associate somatomotor network FC to BD symptoms, suggesting for instance that SMN hypoconnectivity may predominate in more depressed states in association with reduced psychomotor activity, while SMN hyperconnectivity has been proposed to occur in (hypo)manic states (when psychomotor agitation is more predominant) (Martino et al, 2016;Zhu et al, 2022). Furthermore, increasing evidence points to the involvement of SMN in emotional processing in BD (Ellard et al, 2018;Kebets et al, 2019;Magioncalda et al, 2020;Ping et al, 2022;Tang et al, 2021;Wang et al, 2020;Zhu et al, 2022).…”

“…These findings associate somatomotor network FC to BD symptoms, suggesting for instance that SMN hypoconnectivity may predominate in more depressed states in association with reduced psychomotor activity, while SMN hyperconnectivity has been proposed to occur in (hypo)manic states (when psychomotor agitation is more predominant) (Martino et al, 2016;Zhu et al, 2022). Furthermore, increasing evidence points to the involvement of SMN in emotional processing in BD (Ellard et al, 2018;Kebets et al, 2019;Magioncalda et al, 2020;Ping et al, 2022;Tang et al, 2021;Wang et al, 2020;Zhu et al, 2022). While these findings remain preliminary due to the caveats discussed above, and the direction of causality of these associations has yet to be uncovered, the correlations between altered FC in these brain regions and markers of inflammation strengthen the hypothesis that a pro-inflammatory state may underlie altered brain function in BD and, speculatively, BD symptoms, given the involvement of brain circuits that have been associated with affective and somatomotor processing.…”

Altered dynamic amplitude of low-frequency fluctuation between bipolar type I and type II in the depressive state

“…Most direct comparisons of previous studies between BD I and BD II are mainly based on structural analysis, and functional methods are conducted for different subtypes individually or combined indiscriminately. BD I was observed with abnormal functional connectivity (FC) within and between networks, and the FC value is correlated with symptoms and executive function ( Zhu et al, 2021 ). Significant cerebellar dysconnectivity in BD II was reported in previous research.…”

Dynamic functional hippocampal markers of residual depressive symptoms in euthymic bipolar disorder

“…This last includes for instance the motor agitation and hyperesthesia during mania, or the somatomotor slowing and dulling associated with depressive symptoms 21 . Interestingly, increasing evidence points to the involvement of somatomotor networks (SMN) in emotional and cognitive processing, with SMN having recently become a pivotal area of brain networks research in BD [22][23][24][25][26][27][28] . Disrupted inter-network stationary functional connectivity (FC) has been shown in BD in the somatomotor network (SMN), default mode network(DMN), salience system (SN), and frontoparietal network (FPN).…”

“…Disrupted inter-network stationary functional connectivity (FC) has been shown in BD in the somatomotor network (SMN), default mode network(DMN), salience system (SN), and frontoparietal network (FPN). Most importantly, it has been suggested that abnormal stationary FC may be associated with BD symptoms 22,26,29 , for instance SMN FC was positively correlated with the Bech-Rafaelsen Mania Rating Scale in 18 BD patient 26 .…”