Publications by authors named "Nikolaos Petsas"

41 Publications

Machine learning classifier to identify clinical and radiological features relevant to disability progression in multiple sclerosis.

J Neurol 2021 May 10. Epub 2021 May 10.

Department of Human Neurosciences, Sapienza University of Rome, Viale dell'Università, 30, 00185, Rome, Italy.

Objectives: To evaluate the accuracy of a data-driven approach, such as machine learning classification, in predicting disability progression in MS.

Methods: We analyzed structural brain images of 163 subjects diagnosed with MS acquired at two different sites. Participants were followed up for 2-6 years, with disability progression defined according to the expanded disability status scale (EDSS) increment at follow-up. T2-weighted lesion load (T2LL), thalamic and cerebellar gray matter (GM) volumes, fractional anisotropy of the normal appearing white matter were calculated at baseline and included in supervised machine learning classifiers. Age, sex, phenotype, EDSS at baseline, therapy and time to follow-up period were also included. Classes were labeled as stable or progressed disability. Participants were randomly chosen from both sites to build a sample including 50% patients showing disability progression and 50% patients being stable. One-thousand machine learning classifiers were applied to the resulting sample, and after testing for overfitting, classifier confusion matrix, relative metrics and feature importance were evaluated.

Results: At follow-up, 36% of participants showed disability progression. The classifier with the highest resulting metrics had accuracy of 0.79, area under the true positive versus false positive rates curve of 0.81, sensitivity of 0.90 and specificity of 0.71. T2LL, thalamic volume, disability at baseline and administered therapy were identified as important features in predicting disability progression. Classifiers built on radiological features had higher accuracy than those built on clinical features.

Conclusions: Disability progression in MS may be predicted via machine learning classifiers, mostly evaluating neuroradiological features.
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http://dx.doi.org/10.1007/s00415-021-10605-7DOI Listing
May 2021

A matter of atrophy: differential impact of brain and spine damage on disability worsening in multiple sclerosis.

J Neurol 2021 May 3. Epub 2021 May 3.

Department of Human Neurosciences, Sapienza University, Rome, Italy.

As atrophy represents the most relevant driver of progression in multiple sclerosis (MS), we investigated the impact of different patterns of brain and spinal cord atrophy on disability worsening in MS. We acquired clinical and MRI data from 90 patients with relapsing-remitting MS and 24 healthy controls (HC). Clinical progression at follow-up (mean 3.7 years) was defined according to the Expanded Disability Status Scale-Plus. Brain and spinal cord volumes were computed on MRI brain scans. After normalizing each participants' brain and spine volume to the mean of the HC, z-score cut-offs were applied to separate pathologically atrophic from normal brain and spine volumes (accepting a 2.5% error probability). Accordingly, MS patients were classified into four groups (Group I: no brain or spinal cord atrophy N = 40, Group II: brain atrophy/no spinal cord atrophy N = 11, Group III: no brain atrophy/ spinal cord atrophy N = 32, Group IV: both brain and spinal cord atrophy N = 7). All patients' groups showed significantly lower brain volume than HC (p < 0.0001). Group III and IV showed lower spine volume than HC (p < 0.0001 for both). Higher brain lesion load was identified in Group II (p = 0.049) and Group IV (p = 0.023) vs Group I, and in Group IV (p = 0.048) vs Group III. Spinal cord atrophy (OR = 3.75, p = 0.018) and brain + spinal cord atrophy (OR = 5.71, p = 0.046) were significant predictors of disability progression. The presence of concomitant brain and spinal cord atrophy is the strongest correlate of progression over time. Isolated spinal cord atrophy exerts a similar effect, confirming the leading role of spinal cord atrophy in the determination of motor disability.
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http://dx.doi.org/10.1007/s00415-021-10576-9DOI Listing
May 2021

Increased Within-Network Functional Connectivity May Predict NEDA Status in Fingolimod-Treated MS Patients.

Front Neurol 2021 5;12:632917. Epub 2021 Mar 5.

Department of Human Neurosciences, Sapienza University of Rome, Rome, Italy.

Only a few studies have evaluated the brain functional changes associated with disease-modifying therapies (DMTs) in multiple sclerosis (MS), though none used a composite measure of clinical and MRI outcomes to evaluate DMT-related brain functional connectivity (FC) measures predictive of short-term outcome. Therefore, we investigated the following: (1) baseline FC differences between patients who showed evidence of disease activity after a specific DMT and those who did not; (2) DMT-related effects on FC, and; (3) possible relationships between DMT-related FC changes and changes in performance. We used a previously analyzed dataset of 30 relapsing MS patients who underwent fingolimod treatment for 6 months and applied the "no evidence of disease activity" (NEDA-3) status as a clinical response indicator of treatment efficacy. Resting-state fMRI data were analyzed to obtain within- and between-network FC measures. After therapy, 14 patients achieved NEDA-3 status (hereinafter NEDA), while 16 did not (EDA). The two groups significantly differed at baseline, with the NEDA group having higher within-network FC in the anterior and posterior default mode, auditory, orbitofrontal, and right frontoparietal networks than the EDA. After therapy, NEDA showed significantly reduced within-network FC in the posterior default mode and left frontoparietal networks and increased between-network FC in the posterior default mode/orbitofrontal networks; they also showed PASAT improvement, which was correlated with greater within-network FC decrease in the posterior default mode network and with greater between-network FC increase. No significant longitudinal FC changes were found in the EDA. Taken together, these findings suggest that NEDA status after fingolimod is related to higher within-network FC at baseline and to a consistent functional reorganization after therapy.
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http://dx.doi.org/10.3389/fneur.2021.632917DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7973271PMC
March 2021

No evidence of iron deposition in essential tremor: a susceptibility-weighted imaging study.

Neurol Sci 2021 Mar 15. Epub 2021 Mar 15.

Department of Neurology, Neuromed Institute IRCCS, Via Atinense, 18, 86077, Pozzilli, IS, Italy.

Objective: To evaluate the role of iron deposition in subcortical nuclei of patients with essential tremor (ET).

Methods: Twenty-three patients with ET underwent a standardized 3T-MRI protocol. We specifically assessed iron deposition using susceptibility-weighted angiography (SWAN) images in seven specific regions of interest (ROIs): the thalamus, putamen, globus pallidus, caudate nucleus, substantia nigra, red nucleus, and dentate nucleus. Tremor in ET patients was clinically assessed using the Fahn-Tolosa-Marin Tremor Rating Scale (FTM-TRS). ET patient data were compared with data obtained from 23 Parkinson's disease (PD) patients and 14 healthy subjects (HS).

Results: No differences in iron deposition in the seven ROIs were found between ET patients and HS. Conversely, PD patients showed increased iron deposition in the substantia nigra in comparison with both ET patients and HS.

Conclusions: Our results indicate the absence of iron deposition in subcortical nuclei of ET patients, which is generally considered a marker of neurodegeneration.
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http://dx.doi.org/10.1007/s10072-021-05173-7DOI Listing
March 2021

A Comprehensive Approach to Disentangle the Effect of Cerebellar Damage on Physical Disability in Multiple Sclerosis.

Front Neurol 2020 30;11:529. Epub 2020 Jun 30.

Department of Human Neurosciences, "Sapienza" Rome University, Rome, Italy.

Cerebellar damage occurs frequently in multiple sclerosis (MS) patients, with a wide exhibition of symptoms particularly as impairments of balance and gait. Recent studies implementing new postprocessing magnetic resonance imaging (MRI) techniques showed how cerebellar subregional atrophy provides an explanation of disability in MS. The aim of this work was to evaluate the relationship between quantitative measures of physical disability, cerebellar subregional atrophy, and cerebellar peduncle disruption. Forty-nine MS patients and 32 healthy subjects as controls (HS) underwent a 3-Tesla MRI including 3D T1-weighted and diffusion tensor imaging. Patients underwent static posturography to calculate the body's center of pressure (COP) displacement, Expanded Disability Status Scale (EDSS), and 25-ft walking test (25-FWT). Cerebellar lobular volumes were automatically calculated using the Spatially Unbiased Infratentorial Toolbox. Tract-based spatial statistics (TBSS) in FSL was used to process diffusion tensor imaging (DTI) Fit-generated fractional anisotropy (FA) maps to assess structural connectivity of cerebellar peduncles. Stepwise multivariate linear regression analyses were used to explore relationships between variables. Cerebellar volumes (anterior and posterior, as well as lobular volumes from I to X) were significantly lower in patients with MS than HS ( < 0.05). FA in all cerebellar peduncles was lower in MS patients than in HS ( < 0.05). EDSS and 25-FWT showed an association with atrophy of lobule VIIIb (β = -0.37, < 0.01, and β = -0.45, < 0.001, respectively) COP measures inversely correlated with volume of lobules I-IV (β = -0.37, < 0.01, and β = -0.36, < 0.01). Lower FA in the three cerebellar peduncles of MS patients positively correlated with cerebellar lobular volumes. Our findings show how sensorimotor cerebellum atrophy and disruption of both afferent and efferent cerebellar connections contribute to physical disability in MS patients.
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http://dx.doi.org/10.3389/fneur.2020.00529DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7338682PMC
June 2020

Resting-state functional connectivity of anterior and posterior cerebellar lobes is altered in multiple sclerosis.

Mult Scler 2021 Apr 28;27(4):539-548. Epub 2020 May 28.

Department of Human Neuroscience, Sapienza University of Rome, Rome, Italy/IRCCS Neuromed, Pozzilli, Italy.

Background: Damage to the cerebellar sensorimotor and cognitive domains may underlie physical and cognitive disability.

Objective: To investigate resting-state functional connectivity (FC) of sensorimotor and cognitive cerebellum, and clinical correlates in multiple sclerosis (MS).

Methods: A total of 119 patients with MS and 42 healthy subjects underwent multimodal 3T-magnetic resonance imaging (MRI). Patients were evaluated using the Expanded Disability Status Scale and Multiple Sclerosis Functional Composite Scale. After parcellation of sensorimotor (lobules I-V + VIII) and cognitive cerebellum (lobules VI, VII, IX, X), we calculated cerebellar resting-state FC using a seed-based approach.

Results: In patients with MS, the sensorimotor cerebellum showed increased FC mainly with cerebellar, thalamic, and cortical (frontal, parietal, temporal) areas and decreased FC with insular areas; the cognitive cerebellum showed increased FC mainly with thalamic and cortical (temporal-occipital) areas, and decreased FC with frontal-insular areas. Both sensorimotor and cognitive cerebellar FC negatively correlated with disability, and positively with cognitive scores. Cerebellar structural damage only partially influenced results.

Conclusion: The two neocerebellar circuits showed altered FC with subcortical and cortical areas. The association between increased sensorimotor and cognitive cerebellar FC and low levels of physical and cognitive disability suggests that altered FC might modulate the effects of cerebellar structural damage on clinical condition.
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http://dx.doi.org/10.1177/1352458520922770DOI Listing
April 2021

Altered speech-related cortical network in frontotemporal dementia.

Brain Stimul 2020 May - Jun;13(3):765-773. Epub 2020 Feb 26.

Department of Human Neurosciences, Sapienza University of Rome, Viale Dell'Università 30, 00185, Rome, Italy; IRCCS Neuromed, Via Atinense 18, 86077, Pozzilli, IS, Italy. Electronic address:

Background: In healthy subjects (HS), transcranial magnetic stimulation (TMS) demonstrated an increase in motor-evoked potential (MEP) amplitudes during specific linguistic tasks. This finding indicates functional connections between speech-related cortical areas and the dominant primary motor cortex (M1).

Objective: To investigate M1 function with TMS and the speech-related cortical network with neuroimaging measures in frontotemporal dementia (FTD), including the non-fluent variant of primary progressive aphasia (nfv-PPA) and the behavioral variant of FTD (bv-FTD).

Methods: M1 excitability changes during specific linguistc tasks were examined using TMS in 24 patients (15 with nfv-PPA and 9 with bv-FTD) and in 18 age-matched HS. In the same patients neuroimaging was used to assess changes in specific white matter (WM) bundles and grey matter (GM) regions involved in language processing, with diffusion tensor imaging (DTI) and voxel-based morphometry (VBM).

Results: During the linguistic task, M1 excitability increased in HS, whereas in FTD patients it did not. M1 excitability changes were comparable in nfv-PPA and bv-FTD. DTI revealed decreased fractional anisotropy in the superior and inferior longitudinal and uncinate fasciculi. Moreover, VBM disclosed GM volume loss in the left frontal operculum though not in the parietal operculum or precentral gyrus. Furthermore, WM and GM changes were comparable in nfv-PPA and bv-FTD. There was no correlation between neurophysiological and neuroimaging changes in FTD. Atrophy in the left frontal operculum correlated with linguistic dysfunction, assessed by semantic and phonemic fluency tests.

Conclusion: We provide converging neurophysiological and neuroimaging evidence of abnormal speech-related cortical network activation in FTD.
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http://dx.doi.org/10.1016/j.brs.2020.02.029DOI Listing
November 2020

Multi-scale resting state functional reorganization in response to multiple sclerosis damage.

Neuroradiology 2020 Jun 18;62(6):693-704. Epub 2020 Mar 18.

Department of Human Neuroscience, Sapienza - University of Rome, Viale dell'Università 30, 00185, Rome, Italy.

Purpose: In multiple sclerosis (MS), how brain functional changes relate to clinical conditions is still a matter of debate. The aim of this study was to investigate how functional connectivity (FC) reorganization at three different scales, ranging from local to whole brain, is related to tissue damage and disability.

Methods: One-hundred-nineteen patients with MS were clinically evaluated with the Expanded Disability Status Scale and the Multiple Sclerosis Functional Composite. Patients and 42 healthy controls underwent a multimodal 3 T MRI, including resting-state functional MRI.

Results: We identified 16 resting-state networks via independent component analysis and measured within-network, between-network, and whole-brain (global efficiency and degree centrality) FC. Within-network FC was higher in patients than in controls in default mode, frontoparietal, and executive-control networks, and corresponded to low clinical impairment (default mode network versus Expanded Disability Status Scale r = - 0.31, p < 0.01; right frontoparietal network versus Paced Auditory Serial Addition Test r = 0.33, p < 0.01). All measures of between-network and whole-brain FC, except default mode network global efficiency, were lower in patients than in controls, and corresponded to high disability (i.e., basal ganglia global efficiency versus Timed 25-Foot Walk r = - 0.25, p < 0.03; default mode global efficiency versus Expanded Disability Status Scale r = - 0.44, p < 0.001). Altered measures of within-network, between-network, and whole-brain FC were combined in functional indices that were linearly related to disease duration, Paced Auditory Serial Addition Test and lesion load and non-linearly related to Expanded Disability Status Scale.

Conclusion: We suggest that the combined evaluation of functional alterations occurring at different levels, from local to whole brain, could exhaustively describe neuroplastic changes in MS, while increased within-network FC likely represents adaptive compensatory processes, decreased between-network and whole-brain FC likely represent loss of functional network integration consequent to structural disruption.
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http://dx.doi.org/10.1007/s00234-020-02393-0DOI Listing
June 2020

Loss in grey matter in a small network of brain areas underpins poor reactive inhibition in Obsessive-Compulsive Disorder patients.

Psychiatry Res Neuroimaging 2020 Feb 12;297:111044. Epub 2020 Feb 12.

IRCCS Neuromed, Pozzilli (IS), Italy; Department of Human Neuroscience, Sapienza University, Rome, Italy.

Reactive inhibition correlates with the severity of symptoms in paediatric patients with Obsessive-Compulsive Disorder (OCD) though not in those with Tourette syndrome (TS). Here we assessed whether structural alterations in both grey (GM) and white matter (WM) volumes correlate with a measure of reactive inhibition, i.e. the stop-signal reaction time (SSRT), and with clinical scale scores. Nine OCD and 11 TS uncomplicated drug-naïve paediatric patients and 12 age-matched controls underwent 3T magnetic resonance imaging scanning. Between-group differences in GM and WM volumes across the whole brain were assessed. Outside the scanner, patients performed a reaching version of the stop-signal task. Both behavioural inhibitory control and neuroimaging measures were normal in TS patients. By contrast, OCD patients exhibited a significant loss in GM volume in five areas. The GM volume of the left inferior frontal gyrus was inversely correlated with the length of the SSRT, the left mid-cingulate gyrus and the right middle frontal gyrus were inversely correlated with the severity of OCD symptoms, and the left insula and the right medial orbitofrontal gyrus were inversely correlated with both. These results indicate that cortical areas showing GM loss in OCD patients are also involved in the network subserving reactive inhibition.
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http://dx.doi.org/10.1016/j.pscychresns.2020.111044DOI Listing
February 2020

Erratum to "The Role of fMRI in the Assessment of Neuroplasticity in MS: A Systematic Review".

Neural Plast 2019 3;2019:5181649. Epub 2019 Jun 3.

Department of Human Neurosciences, Sapienza University of Rome, Rome, Italy.

[This corrects the article DOI: 10.1155/2018/3419871.].
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http://dx.doi.org/10.1155/2019/5181649DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6589227PMC
June 2019

White matter rather than gray matter damage characterizes essential tremor.

Eur Radiol 2019 Dec 28;29(12):6634-6642. Epub 2019 May 28.

IRCCS Neuromed, Pozzilli (IS), Italy.

Objectives: We investigated changes in gray matter (GM) and white matter (WM) in the whole brain, including both cortical and subcortical structures, and their relationship with tremor severity, psychiatric symptoms, and cognitive impairment in patients affected by essential tremor (ET).

Methods: We studied 19 ET patients and 15 healthy subjects (HS). All the subjects underwent a 3-T MRI study based on 3D-T1 and diffusion tensor images. For the GM analysis, cortical thickness was assessed by using the Computational Anatomy Tool, basal ganglia and thalamus volumes by using the FMRIB software library, and cerebellum lobular volumes by using the spatial unbiased atlas template. For the WM assessment, we performed a voxel-wise analysis by means of tract-based spatial statistics. Patients' tremor severity and psychiatric and cognitive disorders were evaluated by means of standard clinical scales. Neuroimaging data were correlated with clinical scores.

Results: We found significantly smaller right and left thalamic volumes in ET patients than in HS, which correlated with cognitive scores. We did not observe any significant differences either in cortical thickness or in cerebellar lobular volumes between patients and HS. WM abnormalities were detected in most hemisphere bundles, particularly in the corticospinal tract, cerebellar peduncles, and corpus callosum. The WM abnormalities significantly correlated with tremor severity, cognitive profile, and depression.

Conclusion: Our study indicates that ET is characterized by several GM and WM changes of both infra- and supratentorial brain structures. The results may help to better understand mechanisms underlying tremor severity and psychiatric and cognitive impairment in ET.

Key Points: • We performed a comprehensive evaluation of gray and white matter in the same sample of patients with essential tremor using recently developed data analysis methods. • Essential tremor is characterized by widespread gray and white matter changes in both infra- and supratentorial brain structures. The results may help to better understand motor and non-motor symptoms in patients with essential tremor.
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http://dx.doi.org/10.1007/s00330-019-06267-9DOI Listing
December 2019

Deep grey matter involvement and altered sensory gating in multiple sclerosis.

Mult Scler 2020 06 13;26(7):786-794. Epub 2019 May 13.

Department of Human Neurosciences, Sapienza University of Rome, Rome, Italy/IRCCS NEUROMED, Pozzilli, Italy.

Background: Somatosensory temporal discrimination threshold (STDT) is altered in multiple sclerosis (MS). In healthy subjects (HS), voluntary movement modulates the STDT through mechanisms of subcortical sensory gating.

Objective: With neurophysiological and magnetic resonance imaging (MRI) techniques, we investigated sensory gating and sensorimotor integration in MS.

Methods: We recruited 38 relapsing-remitting multiple sclerosis (RR-MS) patients with no-to-mild disability and 33 HS. We tested STDT at rest and during index finger abductions and recorded the movement kinematics. Participants underwent a 3T MRI protocol.

Results: Patients exhibited higher STDT values and performed slower finger movements than HS. During voluntary movement, STDT values increased in both groups, albeit to a lesser extent in patients, while the mean angular velocity of finger movements decreased in patients alone. Patients had a smaller volume of the thalamus, pallidum and caudate nucleus, and displayed higher mean diffusivity in the putamen, pallidum and thalamus. STDT correlated with thalamic volume while mean angular velocity correlated with putaminal volume. Changes in mean angular velocity during sensorimotor integration inversely correlated with mean diffusivity in the thalamus and pallidum. Changes in STDT and velocity were associated with fatigue score.

Conclusion: Altered STDT and sensorimotor integration are related to structural damage in the thalamus and basal ganglia in MS and likely to affect motor performance.
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http://dx.doi.org/10.1177/1352458519845287DOI Listing
June 2020

Functional Connectivity Changes After Initial Treatment With Fingolimod in Multiple Sclerosis.

Front Neurol 2019 22;10:153. Epub 2019 Mar 22.

Department of Radiology, IRCCS NEUROMED, Pozzilli, Italy.

On the basis of recent functional MRI studies, Multiple Sclerosis (MS) has been interpreted as a multisystem disconnection syndrome. Compared to normal subjects, MS patients show alterations in functional connectivity (FC). However, the mechanisms underlying these alterations are still debated. The aim of the study is to investigate resting state (RS) FC changes after initial treatment with fingolimod, a proven anti-inflammatory and immunomodulating agent for MS. We studied 32 right-handed relapsing-remitting MS patients (median Expanded Disability Status Scale: 2.0, mean disease duration: 8.8 years) who underwent both functional and conventional MRI with a 3 Tesla magnet. All assessments were performed 3 weeks before starting fingolimod, then, at therapy-initiation stage and at month 6. Each imaging session included scans at baseline (run1) and after (run2) a 25-min, within-session, motor-practice task, consisting of a paced right-thumb flexion. FC was assessed using a seed on the left primary motor cortex to obtain parametric maps at run1 and task-induced FC change (run2-run1). Comparison between 3-week before- and fingolimod start sessions accounted for a test-retest effect. The main outcome was the changes in both baseline and task-induced changes in FC, between initiation and 6 months. MRI contrast enhancement was detected in 14 patients at initiation and only in 3 at month 6. There was a significant improvement ( < 0.05) in cognitive function, as measured by the Paced Auditory Serial Addition Task, at month 6 compared to initiation. After accounting for test-retest effect, baseline FC significantly decreased at month 6, with respect to initiation ( < 0.05, family-wise error corrected) in bilateral occipito-parietal areas and cerebellum. A task-induced change in FC at month 6 showed a significant increment in all examined sessions, involving not only areas of the sensorimotor network, but also posterior cortical areas (cuneus and precuneus) and areas of the prefrontal and temporal cortices ( < 0.05, family-wise error corrected). Cognitive improvement at month 6 was significantly ( < 0.05) related to baseline FC reduction in posterior cortical areas. This study shows significant changes in functional connectivity, both at baseline and after the execution of a simple motor task following 6 months of fingolimod therapy.
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http://dx.doi.org/10.3389/fneur.2019.00153DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6438876PMC
March 2019

Aberrant functional connectivity in patients with Parkinson's disease and freezing of gait: a within- and between-network analysis.

Brain Imaging Behav 2020 Oct;14(5):1543-1554

Department of Human Neuroscience, Sapienza University of Rome, Viale dell'Università, 30, 00185, Rome, Italy.

Freezing of gait (FOG) is a disabling motor symptom that affects patients with Parkinson's disease (PD). MRI-based evidence suggest that multiple brain structures are involved in the occurrence of FOG. We investigated the integrity of the neuronal networks in PD patients with FOG (PD-FOG), considering both within-network resting-state functional connectivity (rsFC) and between-network rsFC. Thirty-one PD patients (15 PD-FOG and 16 PD-nFOG) and 16 healthy subjects (HS) underwent a rsfMRI study. The data was analysed by using FSL Melodic and FSLNets software to study within- and between-network rsFC. PD-FOG displayed a higher within-network rsFC that involved a greater number of resting-state networks (RSNs) than PD-nFOG. rsFC in the basal ganglia network significantly correlated with the Timed Up and Go test. Moreover, when compared with HS, PD-FOG displayed reduced rsFC between the right fronto-parietal and executive-control RSNs, which significantly correlated with FOG severity. This study demonstrates that FOG is associated with an impaired interplay and communication between the RSNs that underpin attentive and executive abilities, especially in the right hemisphere.
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http://dx.doi.org/10.1007/s11682-019-00085-9DOI Listing
October 2020

The Role of fMRI in the Assessment of Neuroplasticity in MS: A Systematic Review.

Neural Plast 2018 31;2018:3419871. Epub 2018 Dec 31.

Department of Human Neurosciences, Sapienza University of Rome, Rome, Italy.

Neuroplasticity, which is the ability of the brain to adapt to internal and external environmental changes, physiologically occurs during growth and in response to damage. The brain's response to damage is of particular interest in multiple sclerosis, a chronic disease characterized by inflammatory and neurodegenerative damage to the central nervous system. Functional MRI (fMRI) is a tool that allows functional changes related to the disease and to its evolution to be studied in vivo. Several studies have shown that abnormal brain recruitment during the execution of a task starts in the early phases of multiple sclerosis. The increased functional activation during a specific task observed has been interpreted mainly as a mechanism of adaptive plasticity designed to contrast the increase in tissue damage. More recent fMRI studies, which have focused on the activity of brain regions at rest, have yielded nonunivocal results, suggesting that changes in functional brain connections represent mechanisms of either adaptive or maladaptive plasticity. The few longitudinal studies available to date on disease evolution have also yielded discrepant results that are likely to depend on the clinical features considered and the length of the follow-up. Lastly, fMRI has been used in interventional studies to investigate plastic changes induced by pharmacological therapy or rehabilitation, though whether such changes represent a surrogate of neuroplasticity remains unclear. The aim of this paper is to systematically review the existing literature in order to provide an overall description of both the neuroplastic process itself and the evolution in the use of fMRI techniques as a means of assessing neuroplasticity. The quantitative and qualitative approach adopted here ensures an objective analysis of published, peer-reviewed research and yields an overview of up-to-date knowledge.
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http://dx.doi.org/10.1155/2018/3419871DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6332922PMC
March 2019

Abnormal Cerebellar Connectivity Patterns in Patients with Parkinson's Disease and Freezing of Gait.

Cerebellum 2019 Jun;18(3):298-308

Department of Human Neurosciences, Sapienza University of Rome, Viale dell'Università, 30, 00185, Rome, Italy.

In this study, we aimed to evaluate the importance of cerebellum in freezing of gait (FOG) pathophysiology. Due to the fundamental role of the cerebellum in posture and gait control, we examined cerebellar structural and functional connectivity (FC) in patients with PD and FOG. We recruited 15 PD with FOG (PD-FOG), 16 PD without FOG (PD-nFOG) patients, and 16 healthy subjects (HS). The FOG Questionnaire (FOG-Q) assessed FOG severity. Three tesla-MRI study included resting-state functional MRI, diffusion tensor imaging (DTI), and 3D T1-w images. We located seed regions in the cerebellar locomotor region, fastigial, and dentate nucleus to evaluate their FC. DTI parameters were obtained on the superior, middle, and inferior cerebellar peduncles. Global and lobular cerebellum volumes were also calculated. Cerebellar locomotor and fastigial FC was higher in cerebellar and posterior cortical areas in PD-FOG than in HS. FC of the cerebellar locomotor region with cerebellar areas positively correlated with FOG-Q. Dentate FC was lower in the prefrontal and parieto-occipital cortices in PD-FOG than in HS and in the brainstem, right basal ganglia, and frontal and parieto-occipital cortices than in PD-nFOG. DTI parameters in superior and middle cerebellar peduncles were altered in PD-FOG compared with PD-nFOG and significantly correlated with FOG-Q. There were no differences in cerebellar volumes between PD-FOG and either PD-nFOG or HS. Our results suggest that altered connectivity of the cerebellum contributes to the pathophysiology of FOG. FC of the cerebellar locomotor region and white matter (WM) properties of cerebellar peduncles correlate with FOG severity, supporting the hypothesis that abnormal cerebellar function underlies FOG in PD.
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http://dx.doi.org/10.1007/s12311-018-0988-4DOI Listing
June 2019

Relation between functional connectivity and disability in multiple sclerosis: a non-linear model.

J Neurol 2018 Dec 1;265(12):2881-2892. Epub 2018 Oct 1.

Department of Human Neuroscience, Sapienza University of Rome, Viale dell'Università, 30, 00185, Rome, Italy.

Objective: To characterize the relation between brain functional connectivity and disability in patients with multiple sclerosis; to investigate the existence of critical values of both disability and functional connectivity corresponding to exhaustion of functional adaptive mechanisms.

Methods: Hundred-and-nineteen patients with no-to-severe disability and 42 healthy subjects were studied via 3T resting state functional MRI. Out of 116 regions extracted from Automated Anatomical Labeling atlas, pairs of regions whose functional connectivity correlated with Expanded Disability Status Score were identified. In patients, mathematical modeling was applied to find the best models describing Expanded-Disability-Status-Score vs structural or functional measures. Functional vs structural models intersecting points were identified.

Results: Disability had direct linear relation with lesion load (r = 0.40, p < 5E-6), inverse of thalamic volume (r = 0.31 p < 1E-3) and functional connectivity in bi-frontal pairs of regions (r > 0.40, p < 0.04), while being non-linearly associated with functional connectivity in cerebello-temporal and cerebello-frontal pairs of regions (F > 1.73, p < 0.02). Structural vs functional models intersecting points corresponded to Expanded Disability Status Score of 3.0. 85% of patients scoring more than 3.0 showed functional connectivity in cerebello-temporal and cerebello-frontal pairs of regions below confidence intervals (z = [2.28-2.88] 95% CI) measured in healthy subjects.

Conclusions: Functional brain connectivity changes may represent mechanisms of adaptation to structural damage and inflammation and may be not always clinically beneficial. Functional connectivity decreases in comparison with structural measure at Expanded Disability Status Score greater than 3.0, which may be critical and indicate exhaustion of compensatory mechanisms.
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http://dx.doi.org/10.1007/s00415-018-9075-5DOI Listing
December 2018

Role of Cerebellar Dentate Functional Connectivity in Balance Deficits in Patients with Multiple Sclerosis.

Radiology 2018 04 22;287(1):267-275. Epub 2017 Dec 22.

From the Department of Neurology and Psychiatry, Sapienza University of Rome, Viale dell'Università 30, 00185 Rome, Italy (F.T., L.D.G., N.P., E.S., L.P., N.U., C.G., C.P.); Department of Neurology and Psychiatry, Sapienza University of Rome, Rome, Italy (P.P.); and IRCCS Neuromed, Pozzilli, Italy (P.P.).

Purpose To prospectively investigate, by using resting-state functional magnetic resonance (MR) imaging, cerebellar dentate nuclei (DNs) functional connectivity abnormalities in multiple sclerosis (MS) to explore their impact on balance impairment in patients with MS, considering the role of DNs and their projections in maintaining balance, posture, and muscle tone, Materials and Methods All subjects provided written informed consent, and the protocol was approved by the university institutional review board. Twenty-five patients with relapsing-remitting MS and 20 healthy control subjects underwent a 3-T resting-state functional MR imaging and static posturography. The seed-based method was applied to identify the cerebellar DNs resting-state network; first-level and high-level analyses were performed by using software tools. Results Compared with control subjects, patients had worse postural stability and altered patterns of cerebellar DNs connectivity network, with decreased connectivity in caudate nuclei and thalami and increased connectivity in the cerebellum, pons, left amygdala, and orbitofrontal cortices (cluster level, family-wise error corrected, P < .05, z threshold > 2.3). In patients, the decreased connectivity in the left caudate nucleus was related with worse balance performance (cluster level, family-wise error corrected P < .05, z threshold > 1.96) regardless of age, lesion burden, and global clinical disability. Conclusion These results reveal abnormalities of corticocerebellar circuit connectivity in patients with MS as compared with control subjects and suggest that the decreased connectivity between the DN and the left caudate nucleus could play a role in balance impairment in MS. RSNA, 2017.
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http://dx.doi.org/10.1148/radiol.2017170311DOI Listing
April 2018

Abnormal Resting-State Functional Connectivity in Progressive Supranuclear Palsy and Corticobasal Syndrome.

Front Neurol 2017 6;8:248. Epub 2017 Jun 6.

Department of Neurology and Psychiatry, Sapienza University of Rome, Rome, Italy.

Background: Pathological and MRI-based evidence suggests that multiple brain structures are likely to be involved in functional disconnection between brain areas. Few studies have investigated resting-state functional connectivity (rsFC) in progressive supranuclear palsy (PSP) and corticobasal syndrome (CBS). In this study, we investigated within- and between-network rsFC abnormalities in these two conditions.

Methods: Twenty patients with PSP, 11 patients with CBS, and 16 healthy subjects (HS) underwent a resting-state fMRI study. Resting-state networks (RSNs) were extracted to evaluate within- and between-network rsFC using the Melodic and FSLNets software packages.

Results: Increased within-network rsFC was observed in both PSP and CBS patients, with a larger number of RSNs being involved in CBS. Within-network cerebellar rsFC positively correlated with mini-mental state examination scores in patients with PSP. Compared to healthy volunteers, PSP and CBS patients exhibit reduced functional connectivity between the lateral visual and auditory RSNs, with PSP patients additionally showing lower functional connectivity between the cerebellar and insular RSNs. Moreover, rsFC between the salience and executive-control RSNs was increased in patients with CBS compared to HS.

Conclusion: This study provides evidence of functional brain reorganization in both PSP and CBS. Increased within-network rsFC could represent a higher degree of synchronization in damaged brain areas, while between-network rsFC abnormalities may mainly reflect degeneration of long-range white matter fibers.
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http://dx.doi.org/10.3389/fneur.2017.00248DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5459910PMC
June 2017

Lesion symptom map of cognitive-postural interference in multiple sclerosis.

Mult Scler 2018 04 24;24(5):653-662. Epub 2017 Mar 24.

Department of Neurology and Psychiatry, Sapienza University of Rome, Rome, Italy.

Objective: To investigate the disease-altered structure-function relationship underlying the cognitive-postural interference (CPI) phenomenon in multiple sclerosis (MS).

Methods: We measured postural sway of 96 patients and 48 sex-/age-matched healthy controls by force platform in quiet standing (single-task (ST)) while performing the Stroop test (dual-task (DT)) to estimate the dual-task cost (DTC) of balance. In patient group, binary T2 and T1 lesion masks and their corresponding lesion volumes were obtained from magnetic resonance imaging (MRI) of brain. Normalized brain volume (NBV) was also estimated by SIENAX. Correlations between DTC and lesion location were determined by voxel-based lesion symptom mapping (VLSM) analyses.

Results: Patients had greater DTC than controls ( p < 0.001). Among whole brain MRI metrics, only T1 lesion volume correlated with DTC ( r = -0.27; p < 0.01). However, VLSM analysis did not reveal any association with DTC using T1 lesion masks. By contrast, we found clusters of T2 lesions in distinct anatomical regions (anterior and superior corona radiata, bilaterally) to be correlated with DTC ( p < 0.01 false discovery rate (FDR)-corrected). A multivariable stepwise regression model confirmed findings from VLSM analysis. NBV did not contribute to fit the model.

Conclusion: Our findings suggest that the CPI phenomenon in MS can be explained by disconnection along specific areas implicated in task-switching abilities and divided attention.
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http://dx.doi.org/10.1177/1352458517701313DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5946662PMC
April 2018

Functional disconnection of thalamic and cerebellar dentate nucleus networks in progressive supranuclear palsy and corticobasal syndrome.

Parkinsonism Relat Disord 2017 06 15;39:52-57. Epub 2017 Mar 15.

Department of Neurology and Psychiatry, "Sapienza" University of Rome, Italy; IRCCS Neuromed Institute, Pozzilli (IS), Italy. Electronic address:

Aim: To assess functional rearrangement following neurodegeneration in the thalamus and dentate nucleus in patients with progressive supranuclear palsy (PSP) and corticobasal syndrome (CBS).

Methods: We recruited 19 patients with PSP, 11 with CBS and 14 healthy subjects. All the subjects underwent resting-state (rs) fMRI using a 3T system. Whole brain functional connectivity of the thalamus and dentate nucleus were calculated by means of a seed-based approach with FEAT script in FSL toolbox. Thalamic volume was calculated by means of FIRST, and the dentate area by means of Jim software.

Results: Both thalamic volume and dentate area were significantly smaller in PSP and CBS patients than in healthy subjects. No significant difference emerged in thalamic volume between PSP and CBS patients, whereas dentate area was significantly smaller in PSP than in CBS. Thalamic functional connectivity was significantly reduced in both patient groups in various cortical, subcortical and cerebellar areas. By contrast, changes in dentate nucleus functional connectivity differed in PSP and CBS: it decreased in subcortical and prefrontal cortical areas in PSP, but increased asymmetrically in the frontal cortex in CBS.

Conclusions: Evaluating the dentate nucleus size and its functional connectivity may help to differentiate patients with PSP from those with CBS.
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http://dx.doi.org/10.1016/j.parkreldis.2017.03.008DOI Listing
June 2017

Effect on Cognition of Estroprogestins Combined with Interferon Beta in Multiple Sclerosis: Analysis of Secondary Outcomes from a Randomised Controlled Trial.

CNS Drugs 2017 Feb;31(2):161-168

MS Centre Sant'Andrea Hospital, Sapienza University of Rome, Rome, Italy.

Introduction: Cognitive impairment is a disabling symptom in multiple sclerosis (MS). While its management remains challenging, beneficial effects on cognition of interferon beta (IFN-β) have been reported and a positive effect from estroprogestins has been hypothesised, suggesting that the combination of the two medications in women with MS could offer a promising treatment strategy.

Objectives: We investigated whether a combination of estroprogestins and IFN-β can improve cognition in women with MS.

Methods: Women with relapsing-remitting (RR) MS were randomly assigned (1:1:1) to receive subcutaneous IFN-β-1a (Rebif, Merck Serono, Geneva, Switzerland) 44 mcg three times a week (tiw) (group 1), subcutaneous IFN-β-1a 44 mcg tiw plus ethinyl estradiol 20 mcg and desogestrel 150 mcg (Mercilon, MSD Italia SRL, Rome, Italy) (group 2) or subcutaneous IFN-β-1a 44 mcg tiw plus ethinyl estradiol 40 mcg and desogestrel 125 mcg (Gracial, Organon Italia S.p.A., Rome, Italy) (group 3) in a randomised controlled trial, for which we report the analysis of secondary outcomes. At baseline and at 24 months, all patients underwent magnetic resonance imaging (MRI) and a comprehensive cognitive assessment, including Rao's Brief Repeatable Battery (RBRB) and questionnaires for depression, fatigue and quality of life. Failure in at least two of the RBRB tests defined 'cognitive impairment'.

Results: At baseline, there was no difference in the proportion of cognitively impaired patients. At month 24, the proportion of patients with cognitive impairment was lower in group 3 (34.8%) than in group 1 (47.6%) (p = 0.03). The risk of developing cognitive impairment over 24 months was lower in group 3 (p = 0.02). Mood and fatigue scores were comparable across the groups over time at both time points. However, at month 24, group 3 showed worsening on the sexual function subscale of the 54-item MS quality-of-life questionnaire (p = 0.03).

Conclusions: This study suggests that the combination of high-dose estroprogestins and IFN-β may have positive effects on cognition. However, the effect of this treatment on sexual function requires caution to be exercised. Protocol Number NCT00151801, registered in ClinicalTrials.gov.
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http://dx.doi.org/10.1007/s40263-016-0401-0DOI Listing
February 2017

Dentate nucleus connectivity in adult patients with multiple sclerosis: functional changes at rest and correlation with clinical features.

Mult Scler 2017 Apr 18;23(4):546-555. Epub 2016 Jul 18.

Department of Neurology and Psychiatry, Sapienza University of Rome, Rome, Italy/IRCSS Neuromed, Pozzilli (Isernia), Italy.

Background And Objective: The dentate nucleus, which is the largest of the cerebellar nuclei, plays a critical role in movement and cognition. The aim of our study was to assess any changes in dentate functional connectivity (FC) in adult relapsing remitting multiple sclerosis (RR-MS) patients and to investigate possible clinical correlates.

Materials And Methods: In all, 54 patients and 24 healthy subjects (HS) underwent multimodal magnetic resonance imaging (MRI), including diffusion tensor imaging (DTI), three-dimensional-T1-weighted and resting state (RS) functional images; they also underwent a cognitive evaluation, that is, attention and information processing speed, by means of the Paced Auditory Serial Addition Test (PASAT). Patients were also scored according to Expanded Disability Status Scale (EDSS). RS-MRI data were analysed using FMRIB Software Library (FSL) tools, with the seed-based method to identify dentate FC.

Results: When compared with HS, patients exhibited brain atrophy and widespread DTI abnormalities, as well as greater FC between the dentate nucleus and cortical areas, particularly in the frontal and parietal lobes. Within these areas, FC in patients correlated inversely with clinical impairment. Finally, FC correlated inversely with lesion load and microstructural brain damage.

Conclusion: Our findings indicate that dentate FC at rest is altered in MS patients. Whether these functional changes are induced by the disease and play a compensatory role remains to be established.
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http://dx.doi.org/10.1177/1352458516657438DOI Listing
April 2017

The effect of inflammation and its reduction on brain plasticity in multiple sclerosis: MRI evidence.

Hum Brain Mapp 2016 07 18;37(7):2431-45. Epub 2016 Mar 18.

Department of Neurology and Psychiatry, Sapienza University of Rome, Italy.

Brain plasticity is the basis for systems-level functional reorganization that promotes recovery in multiple sclerosis (MS). As inflammation interferes with plasticity, its pharmacological modulation may restore plasticity by promoting desired patterns of functional reorganization. Here, we tested the hypothesis that brain plasticity probed by a visuomotor adaptation task is impaired with MS inflammation and that pharmacological reduction of inflammation facilitates its restoration. MS patients were assessed twice before (sessions 1 and 2) and once after (session 3) the beginning of Interferon beta (IFN beta), using behavioural and structural MRI measures. During each session, 2 functional MRI runs of a visuomotor task, separated by 25-minutes of task practice, were performed. Within-session between-run change in task-related functional signal was our imaging marker of plasticity. During session 1, patients were compared with healthy controls. Comparison of patients' sessions 2 and 3 tested the effect of reduced inflammation on our imaging marker of plasticity. The proportion of patients with gadolinium-enhancing lesions reduced significantly during IFN beta. In session 1, patients demonstrated a greater between-run difference in functional MRI activity of secondary visual areas and cerebellum than controls. This abnormally large practice-induced signal change in visual areas, and in functionally connected posterior parietal and motor cortices, was reduced in patients in session 3 compared with 2. Our results suggest that MS inflammation alters short-term plasticity underlying motor practice. Reduction of inflammation with IFN beta is associated with a restoration of this plasticity, suggesting that modulation of inflammation may enhance recovery-oriented strategies that rely on patients' brain plasticity. Hum Brain Mapp 37:2431-2445, 2016. © 2016 Wiley Periodicals, Inc.
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http://dx.doi.org/10.1002/hbm.23184DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5069650PMC
July 2016

Multiple Sclerosis: Changes in Thalamic Resting-State Functional Connectivity Induced by a Home-based Cognitive Rehabilitation Program.

Radiology 2016 07 8;280(1):202-11. Epub 2016 Mar 8.

From the Department of Neurology and Psychiatry, Sapienza University of Rome, Viale dell'Università 30, 00186 Rome, Italy (L.D.G., F.T., F.D.L., N.P., L.P., C.P., P.P.); MS Center, S. Andrea Hospital, Sapienza University of Rome, Rome, Italy (L.D.G., L.P., V.B., C.P.); and IRCCS Neuromed, Pozzilli, Italy (P.P.).

Purpose To investigate thalamic connectivity changes after use of a video game-based cognitive rehabilitation program, as thalamic damage and alterations in thalamocortical functional connectivity (FC) are important factors in cognitive dysfunction in patients with multiple sclerosis (MS). Materials and Methods This prospective study was approved by the local ethical committee. Twenty-four patients with MS and cognitive impairment were randomly assigned to either an intervention or a wait-list group. Patients were evaluated with cognitive tests and 3-T resting-state functional magnetic resonance (MR) imaging at baseline and after an 8-week period. In addition, 11 healthy subjects underwent baseline resting-state functional MR imaging. Patients in the intervention group performed the video game-based cognitive rehabilitation program, while those in the wait-list group served as control subjects. Repeated measures analysis of variance was used to test efficacy of the intervention. The thalamic resting-state network was identified with a seed-based method; both first-level and high-level analyses were performed by using software tools. Results Patients showed lower baseline FC compared with healthy subjects. A significant improvement was seen in results of the Paced Auditory Serial Addition Test and the Stroop Test after 8 weeks of cognitive rehabilitation (F = 6.616, [P = .018] and F = 5.325 [P = .030], respectively). At follow-up, the intervention group had an increased FC in the cingulum, precuneus, and bilateral parietal cortex and a lower FC in the cerebellum and in left prefrontal cortex compared with the wait-list group (P < .05, family-wise error corrected); correlations were found between FC changes in these regions and cognitive improvement (P < .05, family-wise error corrected). Conclusion The results of this study show the relevance of thalamic regulation of the brain networks involved in cognition and suggest that changes in thalamic resting-state network connectivity may represent a functional substrate for cognitive improvement associated with a video game-based cognitive rehabilitation program. (©) RSNA, 2016.
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http://dx.doi.org/10.1148/radiol.2016150710DOI Listing
July 2016

Gray and white matter structural changes in corticobasal syndrome.

Neurobiol Aging 2016 Jan 19;37:82-90. Epub 2015 Oct 19.

Department of Neurology and Psychiatry, "Sapienza" University of Rome, Rome, Italy; IRCCS INM Neuromed, Pozzilli, Isernia, Italy. Electronic address:

We investigated gray matter and white matter (WM) changes in corticobasal syndrome (CBS). T1-weighted and diffusion tensor images (3T-magnet) were obtained in 11 patients and 11 healthy subjects (HS). Magnetic resonance imaging data were analyzed using FreeSurfer and Tracts Constrained by Underlying Anatomy to evaluate cortical thickness (CTh), surface area, and subcortical volumes as well as diffusion tensor image parameters along the major WM tracts. Compared with HS, the whole patient group showed decreased CTh in the prefrontal cortex, precentral gyrus, supplementary motor area, insula, and temporal pole bilaterally. When we divided patients into 2 subgroups (left: L-CBS, right: R-CBS) on the basis of the clinically more affected upper limb, the most prominent decrease in CTh occurred in the hemisphere contralateral to the more affected side. The whole patient group also had volume loss in the putamen, hippocampus, and accumbens bilaterally, in the corpus callosum and right amygdala. Finally, we found diffusion changes in several WM tracts with axial diffusivity being altered more than radial diffusivity. The upper limb motor severity negatively correlated with the contralateral CTh in the precentral and/or postcentral gyri and contralateral volumes of putamen and accumbens. The CTh asymmetry in postcentral and/or paracentral gyri also negatively correlated with disease duration. Cortical thinning, volume loss, and fiber tract degeneration in specific brain regions are important pathophysiological abnormalities in CBS.
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http://dx.doi.org/10.1016/j.neurobiolaging.2015.10.011DOI Listing
January 2016

Resting-State fMRI in MS: General Concepts and Brief Overview of Its Application.

Biomed Res Int 2015 27;2015:212693. Epub 2015 Aug 27.

Department of Neurology and Psychiatry, Sapienza University of Rome, Viale dell'Università 30, 00185 Rome, Italy ; IRCSS Neuromed, Via Atinense 18, 86077 Pozzilli, Italy.

Brain functional connectivity (FC) is defined as the coherence in the activity between cerebral areas under a task or in the resting-state (RS). By applying functional magnetic resonance imaging (fMRI), RS FC shows several patterns which define RS brain networks (RSNs) involved in specific functions, because brain function is known to depend not only on the activity within individual regions, but also on the functional interaction of different areas across the whole brain. Region-of-interest analysis and independent component analysis are the two most commonly applied methods for RS investigation. Multiple sclerosis (MS) is characterized by multiple lesions mainly affecting the white matter, determining both structural and functional disconnection between various areas of the central nervous system. The study of RS FC in MS is mainly aimed at understanding alterations in the intrinsic functional architecture of the brain and their role in disease progression and clinical impairment. In this paper, we will examine the results obtained by the application of RS fMRI in different multiple sclerosis (MS) phenotypes and the correlations of FC changes with clinical features in this pathology. The knowledge of RS FC changes may represent a substantial step forward in the MS research field, both for clinical and therapeutic purposes.
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http://dx.doi.org/10.1155/2015/212693DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4564590PMC
August 2016

The Role of fMRI to Assess Plasticity of the Motor System in MS.

Front Neurol 2015 16;6:55. Epub 2015 Mar 16.

Department of Neurology and Psychiatry, Sapienza University of Rome , Rome , Italy.

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http://dx.doi.org/10.3389/fneur.2015.00055DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4360702PMC
April 2015