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Altered connectivity of the right anterior insula drives the pain connectome changes in chronic knee osteoarthritis.

ABSTRACT: Resting-state functional connectivity (FC) has proven a powerful approach to understand the neural underpinnings of chronic pain, reporting altered connectivity in 3 main networks: the default mode network (DMN), central executive network, and the salience network (SN). The interrelation and possible mechanisms of these changes are less well understood in chronic pain. Based on emerging evidence of its role to drive switches between network states, the right anterior insula (rAI, an SN hub) may play a dominant role in network connectivity changes underpinning chronic pain. To test this hypothesis, we used seed-based resting-state FC analysis including dynamic and effective connectivity metrics in 25 people with chronic osteoarthritis (OA) pain and 19 matched healthy volunteers. Compared with controls, participants with painful knee OA presented with increased anticorrelation between the rAI (SN) and DMN regions. Also, the left dorsal prefrontal cortex (central executive network hub) showed more negative FC with the right temporal gyrus. Granger causality analysis revealed increased negative influence of the rAI on the posterior cingulate (DMN) in patients with OA in line with the observed enhanced anticorrelation. Moreover, dynamic FC was lower in the DMN of patients and thus more similar to temporal dynamics of the SN. Together, these findings evidence a widespread network disruption in patients with persistent OA pain and point toward a driving role of the rAI.

SUBMITTER: Cottam WJ

PROVIDER: S-EPMC5916486 | biostudies-literature | 2018 May

REPOSITORIES: biostudies-literature

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Altered connectivity of the right anterior insula drives the pain connectome changes in chronic knee osteoarthritis.

Cottam William J WJ Iwabuchi Sarina J SJ Drabek Marianne M MM Reckziegel Diane D Auer Dorothee P DP

Pain 20180501 5

Resting-state functional connectivity (FC) has proven a powerful approach to understand the neural underpinnings of chronic pain, reporting altered connectivity in 3 main networks: the default mode network (DMN), central executive network, and the salience network (SN). The interrelation and possible mechanisms of these changes are less well understood in chronic pain. Based on emerging evidence of its role to drive switches between network states, the right anterior insula (rAI, an SN hub) may ...[more]

PMID: 29557928

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Project description:ObjectiveDaytime cognitive impairment is an essential symptom of primary insomnia (PI). However, the underlying neural substrate remains largely unknown. Many studies have shown that the right anterior insula (rAI) as a key node of salience network (SN) plays a critical role in switching between the executive control network (ECN) and the default mode network (DMN) for better performance of cognitively demanding tasks. Aberrant effective connectivity (directional functional connectivity) of rAI with ECN or DMN may be one reason for daytime cognitive impairment in PI patients. Up to now, no effective connectivity study has been conducted on patients with PI during resting state. Our aim is to investigate the effective connectivity between the rAI and the other voxels in the whole brain in PI.Materials and methodsFifty drug-naive patients with PI and forty age- and sex-matched healthy controls were scanned using resting-state functional MRI. Seed-based Granger causality analysis was used to examine effective connectivity between the rAI, including ventral and dorsal part, and the whole brain. The effective connectivity was compared between the two groups and was correlated with clinical characteristics.ResultsCompared with controls, patients showed decreased effective connectivity from the rAI to the bilateral precuneus, the left postcentral gyrus (extending to bilateral precuneus) and the bilateral cerebellum posterior lobe, and decreased effective connectivity from the bilateral orbitofrontal cortex (OFC) to the rAI (single voxel P < 0.001, AlphaSim corrected with P < 0.01). In addition, effective connectivity from the ventral rAI to the left postcentral gyrus and from the left OFC to the ventral rAI were significantly negatively correlated with Insomnia Severity Index scores (r = -0.28/P = 0.046 and r = -0.29/P = 0.038, respectively).ConclusionThe present study is the first to reveal aberrant effective connectivity between the SN hub (rAI) and the posterior DMN hub (precuneus) as well as decision-making region (OFC) and sensori-motor region in PI. These findings suggest an aberrant salience processing system of the rAI in PI patients.

Project description:IntroductionKnee osteoarthritis is a common disease in the elderly. Patients suffer from long-term chronic pain and reduced life quality. Acupuncture has been proven to be an effective treatment for KOA. However, the neural mechanism of acupuncture is unclear, so far. Periaqueductal gray (PAG) and raphe nuclei (RPN) are essential structures associated with chronic pain in human brains. This study aims to investigate functional connectivity (FC) changes of PAG and RPN in KOA to interpret the neural mechanism of acupuncture.MethodsIn 15 patients with KOA and 15 healthy controls (HC), we acquired Visual Analog Scale (VAS) scores and resting-state fMRI images of each participant before and after acupuncture stimulation on EX-LE5 acupoint. Then, PAG and RPN were selected as seeds to perform FC analysis based on resting-state fMRI images. Finally, we compared FC patterns of PAG and RPN between patients with KOA and HC, then between pre-acupuncture and post-acupuncture. Correlations between FC values and VAS scores were calculated as well.ResultsFor PAG, FC of patients with KOA was lower in the right lingual gyrus at post-acupuncture compared with HC (p <0.001, uncorrected). For dorsal RPN, FC of patients with KOA was significantly higher in right putamen at post-acupuncture compared with HC (p <0.001, corrected with FDR), and FC changes were significant between pre-acupuncture and post-acupuncture in patients with KOA. Post-acupuncture FC values between dorsal RPN and right putamen were correlated with VAS scores. For medial RPN, FC of patients with KOA was lower in the right cerebellum at post-acupuncture compared with HC (p <0.001, uncorrected), but no significant FC changes were found between pre-acupuncture and post-acupuncture in patients with KOA. FC values between medial RPN and right cerebellum were not correlated with VAS scores at pre-acupuncture and post-acupuncture.DiscussionOur study demonstrated that acupuncture enhanced FC between dorsal RPN and the right putamen in patients with KOA, which was associated with chronic pain intensity. This result suggests that acupuncture stimulation can enhance FC between dorsal raphe and striatum, illustrating a neural mechanism that acupuncture can drive the patients' brain, with KOA, to perceive pain.

Project description:The emergence of flow is a situation of high salience because externally oriented attention on the task and access to resources for goal-directed behavior are enhanced, while internally oriented or self-related cognition is decreased. The right anterior insula has been reported as a causal out-flow hub of the salience resting-state network, orchestrating the engagement of the central executive network (CEN) and the disengagement of the default-mode network (DMN) during a functional challenge. In the present study, we employed a combined task-based activation and connectivity analysis to investigate the role of the right anterior insula during the emergence of flow. A sample of 41 healthy male subjects was confronted with a functional challenge that permitted the emergence of flow during BOLD-based functional magnetic resonance imaging. Comparing connectivity changes in the right anterior insula during the flow condition against connectivity changes associated with control conditions of boredom and overload, relatively increased couplings were observed with the left and right dorsolateral prefrontal cortex. Activation data for these regions did, however, not show the flow-typical inverted U-shaped (invU) response pattern. Relatively decreased functional couplings encompassed ventral aspects of the striatum, but neither the amygdala nor the medial prefrontal cortex (MPFC). For the ventral striatum, activation data were consistent with the flow-typical U-shaped activation pattern, which supports the notion that under the high salience of autotelic situations, the anterior insula is much less positively coupled with the ventral striatum than under boundary conditions of boredom and overload. Taken together, present functional connectivity results were in alignment with the assumed role of the right anterior insula under conditions of different salience. However, this particular region does not appear to mediate the most typical flow-associated activation patterns.

Dataset Information

Altered connectivity of the right anterior insula drives the pain connectome changes in chronic knee osteoarthritis.

Publications

Altered connectivity of the right anterior insula drives the pain connectome changes in chronic knee osteoarthritis.

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