Dataset Information

Altered neural signatures of interoception in multiple sclerosis.

ABSTRACT: Multiple sclerosis (MS) patients present several alterations related to sensing of bodily signals. However, no specific neurocognitive impairment has yet been proposed as a core deficit underlying such symptoms. We aimed to determine whether MS patients present changes in interoception-that is, the monitoring of autonomic bodily information-a process that might be related to various bodily dysfunctions. We performed two studies in 34 relapsing-remitting, early-stage MS patients and 46 controls matched for gender, age, and education. In Study 1, we evaluated the heartbeat-evoked potential (HEP), a cortical signature of interoception, via a 128-channel EEG system during a heartbeat detection task including an exteroceptive and an interoceptive condition. Then, we obtained whole-brain MRI recordings. In Study 2, participants underwent fMRI recordings during two resting-state conditions: mind wandering and interoception. In Study 1, controls exhibited greater HEP modulation during the interoceptive condition than the exteroceptive one, but no systematic differences between conditions emerged in MS patients. Patients presented atrophy in the left insula, the posterior part of the right insula, and the right anterior cingulate cortex, with abnormal associations between neurophysiological and neuroanatomical patterns. In Study 2, controls showed higher functional connectivity and degree for the interoceptive state compared with mind wandering; however, this pattern was absent in patients, who nonetheless presented greater connectivity and degree than controls during mind wandering. MS patients were characterized by atypical multimodal brain signatures of interoception. This finding opens a new agenda to examine the role of inner-signal monitoring in the body symptomatology of MS.

SUBMITTER: Salamone PC

PROVIDER: S-EPMC6866398 | biostudies-literature | 2018 Dec

REPOSITORIES: biostudies-literature

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Altered neural signatures of interoception in multiple sclerosis.

Salamone Paula C PC Esteves Sol S Sinay Vladimiro J VJ García-Cordero Indira I Abrevaya Sofía S Couto Blas B Adolfi Federico F Martorell Miguel M Petroni Agustín A Yoris Adrián A Torquati Kathya K Alifano Florencia F Legaz Agustina A Cassará Fátima P FP Bruno Diana D Kemp Andrew H AH Herrera Eduar E García Adolfo M AM Ibáñez Agustín A Sedeño Lucas L

Human brain mapping 20180804 12

Multiple sclerosis (MS) patients present several alterations related to sensing of bodily signals. However, no specific neurocognitive impairment has yet been proposed as a core deficit underlying such symptoms. We aimed to determine whether MS patients present changes in interoception-that is, the monitoring of autonomic bodily information-a process that might be related to various bodily dysfunctions. We performed two studies in 34 relapsing-remitting, early-stage MS patients and 46 controls m ...[more]

PMID: 30076770

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Project description:ObjectiveTo investigate the effects of cortical thickness on the identification accuracy of fractional amplitude of low-frequency fluctuation (fALFF) in patients with multiple sclerosis (MS).MethodsResting-state functional magnetic resonance imaging data were collected from 31 remitting MS, 20 acute MS, and 42 healthy controls (HCs). After preprocessing, we first calculated two-dimensional fALFF (2d-fALFF) maps using the DPABISurf toolkit, and 2d-fALFF per unit thickness was obtained by dividing 2d-fALFF by cortical thickness. Then, between-group comparison, clinical correlation, and classification analyses were performed in 2d-fALFF and 2d-fALFF per unit thickness maps. Finally, we also examined whether the effect of cortical thickness on 2d-fALFF maps was affected by the subfrequency band.ResultsIn contrast with 2d-fALFF, more changed regions in 2d-fALFF per unit thickness maps were detected in MS patients, such as increased region of the right inferior frontal cortex and faded regions of the right paracentral lobule, middle cingulate cortex, and right medial temporal cortex. There was a significant positive correlation between the disease duration and the 2d-fALFF values in the left early visual cortex in remitting MS patients (r = 0.517, Bonferroni-corrected, p = 0.008 × 4 < 0.05). In contrast with 2d-fALFF, we detected a positive correlation between the 2d-fALFF per unit thickness of the right ventral stream visual cortex and the modified Fatigue Impact Scale (MFIS) scores (r = 0.555, Bonferroni-corrected, p = 0.017 × 4 > 0.05). For detecting MS patients, 2d-fALFF and 2d- fALFF per unit thickness both performed remarkably well in support vector machine (SVM) analysis, especially in the remitting phase (AUC = 86, 83%). Compared with 2d-fALFF, the SVM model of 2d-fALFF per unit thickness had significantly higher classification performance in distinguishing between remitting and acute MS. More changed regions and more clinically relevant 2d-fALFF per unit thickness maps in the subfrequency band were also detected in MS patients.ConclusionBy dividing the functional value by the cortical thickness, the identification accuracy of fALFF in MS patients was detected to be potentially influenced by cortical thickness. Additionally, 2d-fALFF per unit thickness is a potential diagnostic marker that can be utilized to distinguish between acute and remitting MS patients. Notably, we observed similar variations in the subfrequency band.

Project description:One of the most prominent symptoms in multiple sclerosis is pathological fatigue, often described by sufferers as one of the most debilitating symptoms, affecting quality of life and employment. However, the mechanisms of both, physical and cognitive fatigue in multiple sclerosis remain elusive. Here, we use behavioural tasks and quantitative MRI to investigate the neural correlates of interoception (the ability to sense internal bodily signals) and metacognition (the ability of the brain to assess its own performance), in modulating cognitive fatigue. Assuming that structural damage caused by multiple sclerosis pathology might impair the neural pathways subtending interoception and/or metacognition, we considered three alternative hypotheses to explain fatigue as a consequence of, respectively: (i) reduced interoceptive accuracy, (ii) reduced interoceptive insight or (iii) reduced global metacognition. We then explored associations between these behavioural measures and white matter microstructure, assessed by diffusion and magnetisation transfer MRI. Seventy-one relapsing-remitting multiple sclerosis patients participated in this cross-sectional study (mean age 43, 62% female). Patient outcomes relevant for fatigue were measured, including disability, disease duration, depression, anxiety, sleepiness, cognitive function, disease modifying treatment and quality of life. Interoceptive and metacognitive parameters were measured using heartbeat tracking and discrimination tasks, and metacognitive visual and memory tasks. MRI was performed in 69 participants, including diffusion tensor MRI, neurite orientation dispersion and density imaging and quantitative magnetisation transfer. Associations between interoception and metacognition and the odds of high cognitive fatigue were tested by unconditional binomial logistic regression. The odds of cognitive fatigue were higher in the people with low interoceptive insight (P = 0.03), while no significant relationships were found between fatigue and other interoceptive or metacognitive parameters, suggesting a specific impairment in interoceptive metacognition, rather than interoception generally, or metacognition generally. Diffusion MRI-derived fractional anisotropy and neurite density index showed significant (P < 0.05) negative associations with cognitive fatigue in a widespread bilateral white matter network. Moreover, there was a significant (P < 0.05) interaction between cognitive fatigue and interoceptive insight, suggesting that the poorer the white matter structure, the lower the interoceptive insight, and the worse the fatigue. The results point towards metacognitive impairment confined to the interoceptive domain, in relapsing-remitting patients with cognitive fatigue. The neural basis of this impairment is supported by a widespread white matter network in which loss of neurite density plays a role.

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Altered neural signatures of interoception in multiple sclerosis.

Publications

Altered neural signatures of interoception in multiple sclerosis.

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