Brain connectivity abnormalities extend beyond the sensorimotor network in peripheral neuropathy

Rocca, Maria A.; Valsasina, Paola; Fazio, Raffaella; Previtali, Stefano C.; Messina, Roberta; Falini, Andrea; Comi, Giancarlo; Filippi, Massimo

doi:10.1002/hbm.22198

Cited by 17 publications

(12 citation statements)

References 49 publications

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“…Enhanced interconnection of bilateral insula especially in HNP patients may reflect a similar mechanism in these sensory limbic structures trying to maintain selfawareness and homeostasis (15). This is in accordance with a previous study reporting that patients with peripheral neuropathy, both hereditary and acquired, exhibited multiple resting state functional connectivity abnormalities involving the sensorimotor, auditory and visual networks in comparison to healthy controls (16). Analogous to our results, the authors demonstrated increased resting state bold signal in posterior cingulate cortex/precuneus and suggested these modifications might reflect an adaptive mechanism.…”

Section: Discussionsupporting

confidence: 93%

Tracking Pain in Resting State Networks in Patients with Hereditary and Diabetic Neuropathy

Sag

Has

Öztekin

et al. 2017

Arch Neuropsychiatr

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Introduction: Chronic pain is associated with maladaptive plastic changes in the brain. It is usually more prominent in acquired pathologies of nerve fibers as in diabetic neuropathy despite less severe degeneration than hereditary neuropathies. Based on clinical differences concerning pain perception, we hypothesized that functional connectivity analysis would reveal distinct patterns in resting-state networks in these groups. Methods: Ten diabetic patients with painful neuropathy (5F/5M; mean age=50.10±6.05 years), 10 patients with hereditary neuropathy (5F/5M; mean age=37.80±14.01 years), 18 age-and gender-matched healthy controls (eight for painful diabetic neuropathy and 10 for hereditary neuropathy) and seven diabetic controls without painful neuropathy were enrolled in the study. All subjects (n=45) underwent a 5-min resting-state scan in a 3T magnetic resonance scanner. The images were analyzed with seed-based functional connectivity method. The grouplevel maps of the default mode network and insula-cingulate network were identified for each group. Results: Patients with hereditary neuropathy displayed increased connectivity between left insula and left anterior cingulate cortex and inversely correlated activity between left insula and left inferior parietal lobule compared to their controls. In patients with painful diabetic neuropathy, the major findings were the increased connectivity between left anterior cingulate cortex and posterior cingulate cortex/precuneus, and the increased connectivity between medial prefrontal cortex and left medial temporal region compared to their controls. Conclusion: This study revealed that hereditary and diabetic painful neuropathy patients exhibit different patterns of functional connectivity. The clinical differences in these groups regarding the presence of neuropathic pain may relate to this difference in cortical organization.

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Section: Discussionsupporting

confidence: 93%

Tracking Pain in Resting State Networks in Patients with Hereditary and Diabetic Neuropathy

Sag

Has

Öztekin

et al. 2017

Arch Neuropsychiatr

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“…In recent years, functional connectivity (FC) analyses have provided invaluable approaches for studying the human brain in healthy ( Smith et al, 2009 , 2012 ; Yeo et al, 2011 ) and diseased groups ( Napadow et al, 2010 ; Collignon et al, 2013 ; Rocca et al, 2014 ) on the brain-network level. Among the varied functional neuroimaging techniques, resting-state fMRI (rs-fMRI) is a promising tool for mapping FC.…”

Section: Introductionmentioning

confidence: 99%

Brain Functional Connectivity Plasticity Within and Beyond the Sensorimotor Network in Lower-Limb Amputees

Zhang

Wang

et al. 2018

Front. Hum. Neurosci.

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Cerebral neuroplasticity after amputation has been elucidated by functional neuroimaging. However, little is known concerning how brain network-level functional reorganization of the sensorimotor system evolves following lower-limb amputation. We studied 32 unilateral lower-limb amputees (LLAs) and 32 matched healthy controls (HCs) using resting-state functional magnetic resonance imaging (rs-fMRI). A regions of interest (ROI)-wise connectivity analysis was performed with ROIs in eight brain regions in the sensorimotor network to investigate intra-network changes, and seed-based whole-brain functional connectivity (FC) with a seed in the contralateral primary sensorimotor cortex (S1M1) was used to study the FC reorganization between the sensorimotor region (S1M1) and other parts of the brain in the LLAs. The ROI-wise connectivity analysis showed that the LLAs had decreased FC, mainly between the subcortical nuclei and the contralateral S1M1 (p < 0.05, FDR corrected). Seed-based whole-brain FC analysis revealed that brain regions with decreased FC with the contralateral S1M1 extended beyond the sensorimotor network to the prefrontal and visual cortices (p < 0.05, FDR corrected). Moreover, correlation analysis showed that decreased FC between the subcortical and the cortical regions in the sensorimotor network progressively increased in relation to the time since amputation. These findings indicated a cascade of cortical reorganization at a more extensive network level following lower-limb amputation, and also showed promise for the development of a possible neurobiological marker of changes in FC related to motor function recovery in LLAs.

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“…An increasingly popular approach to studying long-range interactions in both healthy ( Smith et al, 2009, 2012; Yeo et al, 2011 ) and clinical populations ( Collignon et al, 2013; Napadow et al, 2010; Rocca et al, 2014 ) is by measuring resting state functional connectivity. Functional connectivity is a measure of spatiotemporal synchrony of fMRI Blood-Oxygenation-Level-Dependent (BOLD) signal between anatomically distinct brain regions ( Friston et al, 1993 ), and it represents the degree of functional de/coupling between dissociated brain areas.…”

Section: Introductionmentioning

confidence: 99%

Network-level reorganisation of functional connectivity following arm amputation

et al. 2015

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One of the most striking demonstrations of plasticity in the adult human brain follows peripheral injury, such as amputation. In the primary sensorimotor cortex, arm amputation results in massive local remapping of the missing hands' cortical territory. However, little is known about the consequences of sensorimotor deprivation on global brain organisation. Here, we used resting-state fMRI to identify large-scale reorganisation beyond the primary sensorimotor cortex in arm amputees, compared with two-handed controls. Specifically, we characterised changes in functional connectivity between the cortical territory of the missing hand in the primary sensorimotor cortex (‘missing hand cortex’) and two networks of interest: the sensorimotor network, which is typically strongly associated with the hand cortex, and the default mode network (DMN), which is normally dissociated from it. Functional connectivity values between the missing hand cortex and the sensorimotor network were reduced in amputees, and connectivity was weaker in individuals amputated for longer periods. Lower levels of functional coupling between the missing hand cortex and the sensorimotor network were also associated with emerged coupling of this cortex with the DMN. Our results demonstrate that plasticity following arm amputation is not restricted to local remapping occurring within the sensorimotor homunculus of the missing hand but rather produces a cascade of cortical reorganisation at a network-level scale. These findings may provide a new framework for understanding how local deprivation following amputation could elicit complex perceptual experiences of phantom sensations, such as phantom pain.

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Brain connectivity abnormalities extend beyond the sensorimotor network in peripheral neuropathy

Cited by 17 publications

References 49 publications

Tracking Pain in Resting State Networks in Patients with Hereditary and Diabetic Neuropathy

Tracking Pain in Resting State Networks in Patients with Hereditary and Diabetic Neuropathy

Brain Functional Connectivity Plasticity Within and Beyond the Sensorimotor Network in Lower-Limb Amputees

Network-level reorganisation of functional connectivity following arm amputation

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