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. 2018 Dec;39(12):4743-4754.
doi: 10.1002/hbm.24319. Epub 2018 Aug 4.

Altered neural signatures of interoception in multiple sclerosis

Paula C Salamone  1   2 , Sol Esteves  1 , Vladimiro J Sinay  1 , Indira García-Cordero  1   2 , Sofía Abrevaya  1   2 , Blas Couto  1 , Federico Adolfi  1   2 , Miguel Martorell  1 , Agustín Petroni  1   2   3   4 , Adrián Yoris  1   2 , Kathya Torquati  1 , Florencia Alifano  1 , Agustina Legaz  1 , Fátima P Cassará  1 , Diana Bruno  1 , Andrew H Kemp  5 , Eduar Herrera  6 , Adolfo M García  1   2   7 , Agustín Ibáñez  1   2   8   9   10   11 , Lucas Sedeño  1   2
Affiliations

Altered neural signatures of interoception in multiple sclerosis

Paula C Salamone et al. Hum Brain Mapp. 2018 Dec.

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.

Keywords: body perception; functional connectivity; heartbeat detection task; heartbeat evoked potential; interoceptive processing; multiple sclerosis.

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Conflict of interest statement

The authors declare that they have no conflicts of interest related to this article.

Figures

Figure 1
Figure 1
HEP results. (a) Modulations during the IC (green) and the EC (gray). The three top panels show the results of controls in both tasks, whereas the three bottom panels show the results in patients. Results for each ROI are shown separately from left to right. Scalp topography shows the differences in amplitude (microvolts) between conditions for each group. (b) Differences between IC and EC. Scalp topography shows the differences in amplitude (microvolts) between groups. For a and b: Gray boxes show statistically significant differences (at p < .05 for a minimum extension of five consecutive points of difference, following previous reports (Garcia‐Cordero et al., 2016), and shadowed bars around potentials indicate SEM statistical details in Supporting Information Tables S4 and S6
Figure 2
Figure 2
VBM: Multiple sclerosis atrophy and brain‐behavior association. (a) Atrophy pattern of multiple sclerosis patients compared with controls. VBM was performed within key interoceptive areas (namely: the insula, the ACC, and the SSC) and a control region (superior occipital cortex) (p < .001 uncorrected). Statistical details in Supporting Information Table S7. (b) Correlations between results from the VBM group comparison and HEP subtraction. The bilateral insula and the right ACC were significantly associated with HEP subtraction results in the control sample. No association was found with the SSC for this group. On the other hand, multiple sclerosis patients presented significant correlations only between HEP subtractions and the bilateral SSC. Both groups presented no association with the superior occipital cortex. L = left; R = right. See Supporting Information Figure S4 for the scatter plots of each of these correlation analyses
Figure 3
Figure 3
Functional connectivity results. (a) Differences between conditions. While for the control sample ISt showed greater inter‐regional connectivity and greater K compared with MW, no differences were found in multiple sclerosis patients. Figure supported by Supporting Information Tables S9 and S10. (b) Between‐group differences in the mind‐wandering and interoceptive conditions. While patients presented greater inter‐regional connectivity and K than controls for MW, no differences were found during the interoceptive condition. For (a) and (b): Links indicate interregional connectivity. Circles indicate network degree (K). Colors indicate statistically significant differences (p < .05; green = interoception > mind wandering; red = MS patients > controls; black = no significant differences). ACC: anterior cingulate cortex, INS: insula, SSC: somatosensory cortex. Figure supported by Supporting Information Tables S11 and S12
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