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Aberrant brain network topology in fronto-limbic circuitry differentiates euthymic bipolar disorder from recurrent major depressive disorder.

ABSTRACT: INTRODUCTION:Previous studies have established graph theoretical analysis of functional network connectivity (FNC) as a potential tool to detect neurobiological underpinnings of psychiatric disorders. Despite the promising outcomes in studies that examined FNC aberrancies in bipolar disorder (BD) and major depressive disorder (MDD), there is still a lack of research comparing both mood disorders, especially in a nondepressed state. In this study, we used graph theoretical network analysis to compare brain network properties of euthymic BD, euthymic MDD and healthy controls (HC) to evaluate whether these groups showed distinct features in FNC. METHODS:We collected resting-state functional magnetic resonance imaging (fMRI) data from 20 BD patients, 15 patients with recurrent MDD as well as 30 age- and gender-matched HC. Graph theoretical analyses were then applied to investigate functional brain networks on a global and regional network level. RESULTS:Global network analysis revealed a significantly higher mean global clustering coefficient in BD compared to HC. We further detected frontal, temporal and subcortical nodes in emotion regulation areas such as the limbic system and associated regions exhibiting significant differences in network integration and segregation in BD compared to MDD patients and HC. Participants with MDD and HC only differed in frontal and insular network centrality. CONCLUSION:In conclusion, our findings indicate that a significantly altered brain network topology in the limbic system might be a trait marker specific to BD. Brain network analysis in these regions may therefore be used to differentiate euthymic BD not only from HC but also from patients with MDD.

SUBMITTER: Dvorak J

PROVIDER: S-EPMC6576154 | biostudies-literature | 2019 Jun

REPOSITORIES: biostudies-literature

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Aberrant brain network topology in fronto-limbic circuitry differentiates euthymic bipolar disorder from recurrent major depressive disorder.

Dvorak Jannis J Hilke Marietheres M Trettin Marco M Wenzler Sofia S Hagen Marleen M Ghirmai Naddy N Müller Maximilian M Kraft Dominik D Reif Andreas A Oertel Viola V

Brain and behavior 20190507 6

<h4>Introduction</h4>Previous studies have established graph theoretical analysis of functional network connectivity (FNC) as a potential tool to detect neurobiological underpinnings of psychiatric disorders. Despite the promising outcomes in studies that examined FNC aberrancies in bipolar disorder (BD) and major depressive disorder (MDD), there is still a lack of research comparing both mood disorders, especially in a nondepressed state. In this study, we used graph theoretical network analysi ...[more]

PMID: 31066228

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Project description:Recent investigations have used diffusion-weighted imaging to reveal disturbances in the neurocircuitry that underlie cognitive-emotional control in bipolar disorder (BD) and in unaffected siblings or children at high genetic risk (HR). It has been difficult to quantify the mechanism by which structural changes disrupt the superimposed brain dynamics, leading to the emotional lability that is characteristic of BD. Average controllability is a concept from network control theory that extends structural connectivity data to estimate the manner in which local neuronal fluctuations spread from a node or subnetwork to alter the state of the rest of the brain. We used this theory to ask whether structural connectivity deficits previously observed in HR individuals (n?=?84, mean age 22.4), patients with BD (n?=?38, mean age 23.9), and age- and gender-matched controls (n?=?96, mean age 22.6) translate to differences in the ability of brain systems to be manipulated between states. Localized impairments in network controllability were seen in the left parahippocampal, left middle occipital, left superior frontal, right inferior frontal, and right precentral gyri in BD and HR groups. Subjects with BD had distributed deficits in a subnetwork containing the left superior and inferior frontal gyri, postcentral gyrus, and insula (p?=?0.004). HR participants had controllability deficits in a right-lateralized subnetwork involving connections between the dorsomedial and ventrolateral prefrontal cortex, the superior temporal pole, putamen, and caudate nucleus (p?=?0.008). Between-group controllability differences were attenuated after removal of topological factors by network randomization. Some previously reported differences in network connectivity were not associated with controllability-differences, likely reflecting the contribution of more complex brain network properties. These analyses highlight the potential functional consequences of altered brain networks in BD, and may guide future clinical interventions.

Project description:ObjectivesAdults with bipolar disorder (BD) display aberrant activation in fronto-limbic neural circuitry during cognitive control. However, fronto-limbic response to cognitive control, and factors destabilizing this circuitry, remain under-studied during the transition from adolescence to young adulthood in BD. Sleep patterns are disturbed in BD, undergo change in adolescence, and support brain function. Among transitional age youth, BD diagnosis and sleep (duration and variability) were tested as predictors of fronto-limbic response to a stressful cognitive control task.MethodsTwo groups of youth (13-22 years old) participated: 15 with BD type I, II or not otherwise specified (NOS) [BD; age 18.1 ± 2.7 years (mean ± standard deviation, SD); 17 female] and 25 healthy controls [CTL; age 19.4 ± 2.7 years (mean ± SD); 17 female]. Sleep was monitored with actigraphy for at least 1 week prior to an adaptive multi-source interference functional magnetic resonance imaging (fMRI) paradigm (a Stroop-like cognitive interference task). Group status and sleep duration (average and intra-individual variability) were examined as predictors of activation in response to incongruent>congruent trials within the bilateral amygdala, anterior cingulate (ACC), ventrolateral prefrontal and dorsolateral prefrontal cortical regions of interest.ResultsThe BD group displayed greater right amygdala activation than the CTL group. Average sleep duration and rostroventral ACC (rvACC) activity were negatively associated in the CTL group, but exhibited a quadratic relationship in the BD group such that short and long sleep were related to greater rvACC activation. Sleep duration variability and dorsal ACC activity were negatively associated in the BD group, and unrelated in the CTL group. Findings remained significant after controlling for age, sex, and mood symptoms.ConclusionsSubjects with BD displayed a hyper-limbic response during cognitive control, and sleep was a source of variability in ACC engagement. Stabilizing sleep may be one avenue for improving cognitive control in BD.

Project description:BackgroundFour of the most consistently replicated variants associated with mood disorder occur in genes important for synaptic function: ANK3 (rs10994336), BDNF (rs6265), CACNA1C (rs1006737), and DGKH (rs1170191).AimsThe present study examined associations between these candidates, mood disorder diagnoses, cognition, and fronto-limbic regions implicated in affect regulation.Methods and materialsParticipants included 128 individuals with bipolar disorder (33% male, Mean age = 38.5), 48 with major depressive disorder (29% male, Mean age = 40.4), and 149 healthy controls (35% male, Mean age = 36.5). Genotypes were determined by 5'-fluorogenic exonuclease assays (TaqMan®). Fronto-limbic volumes were obtained from high resolution brain images using Freesurfer. Chi-square analyses, bivariate correlations, and mediational models examined relationships between genetic variants, mood diagnoses, cognitive measures, and brain volumes.ResultsCarriers of the minor BDNF and ANK3 alleles showed nonsignificant trends toward protective association in controls relative to mood disorder patients (P = 0.047). CACNA1C minor allele carriers had larger bilateral caudate, insula, globus pallidus, frontal pole, and nucleus accumbens volumes (smallest r = 0.13, P = 0.043), and increased IQ (r = 0.18, P < 0.001). CACNA1C associations with brain volumes and IQ were independent; larger fronto-limbic volumes did not mediate increased IQ. Other candidate variants were not significantly associated with diagnoses, cognition, or fronto-limbic volumes.Discussion and conclusionsCACNA1C may be associated with biological systems altered in mood disorder. Increases in fronto-limbic volumes and cognitive ability associated with CACNA1C minor allele genotypes are congruent with findings in healthy samples and may be a marker for increased risk for neuropsychiatric phenotypes. Even larger multimodal studies are needed to quantify the magnitude and specificity of genetic-imaging-cognition-symptom relationships.

Dataset Information

Aberrant brain network topology in fronto-limbic circuitry differentiates euthymic bipolar disorder from recurrent major depressive disorder.

Publications

Aberrant brain network topology in fronto-limbic circuitry differentiates euthymic bipolar disorder from recurrent major depressive disorder.

Similar Datasets

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