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.

Time to Face Language: Embodied Mechanisms Underpin the Inception of Face-Related Meanings in the Human Brain

“…The reference was set to link mastoids for recordings and rereferenced off-line to the average of all electrodes. In line with reported procedures ( Salamone et al. 2018 ; Vilas et al .…”

At the Heart of Neurological Dimensionality: Cross-Nosological and Multimodal Cardiac Interoceptive Deficits

“…Thus, the juxtaposition of neurological and cardiac samples can inform which interoceptive disturbances are more crucially related to central (neural) or peripheral (autonomic) disruptions. Considering previous findings ( 9 , 10 , 13 ), behavioral and neurophysiological (HEP) abnormalities should prove more consistent between neurological and cardiac diseases than neuroanatomical or FC disruptions of relevant brain systems.…”

“…A promising target in this trend is the study of interoception, i.e., the sensing of visceral signals ( 6 ). In particular, cardiac interoception encompasses multidimensional variables, such as accuracy, learning, and awareness ( 7 ), with well-established neural signatures ( 8 ) that are affected in several neurological disorders, including Alzheimer’s disease (AD), multiple sclerosis (MS), behavioral variant frontotemporal dementia (bvFTD), and stroke (ST) ( 9 , 10 ). However, with some exceptions ( 10 ), cardiac interoceptive dimensions have not been studied transnosologically in neurological disorders.…”

“…Neurophysiologically, cardiac interoceptive processes are indexed by the heart-evoked potential (HEP) ( 19 – 24 ), a cortical marker modulated by conscious attention to heartbeats ( 10 , 13 , 20 , 25 ). Moreover, cardiac interoceptive processes ( 8 , 26 , 27 ) and dysfunctions ( 9 , 13 ) are linked to the volume and functional connectivity (FC) ( 28 ) of the bilateral insula, the anterior cingulate cortex (ACC), the middle cingulate cortex, and the somatosensory cortex. Taken together, these markers allow for comprehensive assessments of cardiac interoceptive mechanisms ( 29 ).…”

“…In ST, cardiac interoceptive accuracy deficits can emerge despite spared awareness, accompanied by reduced HEP modulations and insular damage but no FC alterations ( 10 ). In MS, a more diffuse model with abnormal body signal processing, cardiac interoceptive deficits (atypical HEP, atrophy, and FC) have been observed without behavioral impairments ( 9 ) and in association with fatigue ( 30 ). In combination, these findings suggest that markers of cardiac interoceptive attention (accuracy and HEP modulations) might be transnosologically affected across neurological conditions, whereas other signatures (cardiac interoceptive learning and awareness, structural and functional neuroimaging markers) may prove more idiosyncratically affected in them.…”