Advertisement
Research Article| Volume 42, 102127, July 2020

Neuroplasticity and brain reorganization associated with positive outcomes of multidisciplinary rehabilitation in progressive multiple sclerosis: A fMRI study

      Highlights

      • Multidisciplinary rehabilitation in people with multiple sclerosis may improve their level of activity in daily activities.
      • The fMRI results revealed a significant reduction in the activity of brain areas related to task-specific networks.
      • Brain activity also increases in not specific task areas, such as medial prefrontal area that is a connectivity core network.

      Abstract

      Background

      Multiple sclerosis (MS) is characterized by a range of symptoms, including motor, sensorimotor and cognitive impairments, that limit the quality of life. A multidisciplinary rehabilitation approach in people affected by multiple sclerosis was recently reported to improve the functional abilities of MS patients in daily activities. The purpose of the study was to assess the effect of multidisciplinary rehabilitation on the whole brain of MS patients by means of functional magnetic resonance imaging (fMRI).

      Methods

      Thirty individuals affected by MS (49.9 ± 12.1 years; disease duration: 16.0 ± 8.5 years) with a medium-high severity of disease were enrolled. The fMRI examination assessed a range of action-related tasks involving passive movement, mental simulation of action and miming of action triggered by external stimuli, such as object photography. The three tasks were performed using each arm separately. The fMRI acquisitions were performed at T1 (inclusion in the study), T2 (3 months later, at the start of rehabilitation) and T3 (after 3 months of multidisciplinary rehabilitation).

      Results

      The fMRI results revealed a significant reduction in the activity of brain areas related to task-specific networks as well as the activation of cerebral regions not usually involved in task-specific related network, such as the medial prefrontal area.

      Conclusions

      The effectiveness of multidisciplinary rehabilitation on activity and participation has been established in previous studies. Our study sheds new light on the effect of such treatment on brain reorganization.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Multiple Sclerosis and Related Disorders
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Bonzano L.
        • Pedullà L.
        • Tacchino A.
        • Brichetto G.
        • Battaglia M.A.
        • Mancardi G.L.
        • Bove M.
        Upper limb motor training based on task-oriented exercises induces functional brain reorganization in patients with multiple sclerosis.
        Neuroscience. 2019; 410: 150-159
        • Büchel C.
        • Coull J.T.
        • Friston K.J.
        The predictive value of changes in effective connectivity for human learning.
        Science. 1999; 283: 1538-1541
        • Cavanna A.E.
        • Trimble M.R.
        The precuneus: a review of its functional anatomy and behavioural correlates.
        Brain. 2006; 129: 564-583
        • Calautti C.
        • Baron J.C.
        Functional neuroimaging studies of motor recovery after stroke in adults.
        Stroke. 2003; 34: 1553-1566
        • Cerasa A.
        • Gioia M.C.
        • Valentino P.
        • et al.
        Computer-assisted cognitive rehabilitation of attention deficits for multiple sclerosis: a randomized trial with fMRI correlates.
        Neurorehabil. Neural. Repair. 2013; 27: 284-295
        • Chiaravalloti N.D.
        • Wylie G.
        • Leavitt V.
        • DeLuca J.
        Increased cerebral activation after behavioral treatment for memory deficits in MS.
        J. Neurol. 2012; 259: 1337-1346
        • Compston A.
        Coles A. Multiple Sclerosis.
        Lancet. 2008; 372: 1502-1517
        • Collen F.M.
        • Wade D.T.
        • Robb G.F.
        • Bradshaw C.M.
        The rivermead mobility index: a further development of the rivermead motor assessment.
        Int. Disabil. Stud. 1991; 13: 50-54
      1. Dayan E., Cohen L.G.Neuroplasticity subserving motor skill learning Neuron. 2011; 72(3):443–454.

        • de Pasquale F.
        • Della Penna S.
        • Snyder A.Z.
        • Marzetti L.
        • Pizzella V.
        • Romani G.L.
        • Corbetta M.
        A cortical core for dynamic integration of functional networks in the resting human brain.
        Neuron. 2012; 74: 753-764
        • Ernst A.
        • Botzung A.
        • Gounot D.
        • et al.
        Induced brain plasticity after a facilitation programme for autobiographical memory in multiple sclerosis: a preliminary study.
        Mult. Scler. Int. 2012; 12
        • Falletta Caravasso C.
        • de Pasquale F.
        • Ciurli P.
        • Catani S.
        • Formisano R.
        • Sabatini U
        The default mode network connectivity predicts cognitive recovery in severe acquired brain injured patients: a longitudinal study.
        J. Neurotrauma. 2016; 33: 1247-1262
        • Filippi M.
        • Riccitelli G.
        • Mattioli F.
        • Capra R.
        • Stampatori C.
        • Pagani E.
        • Rocca M.A
        Multiple sclerosis: effects of cognitive rehabilitation on structural and functional MR imaging measures—an explorative study.
        Radiology. 2012; 262: 932-940
        • Freeman J.A.
        • Langdon D.W.
        • Hobart J.C.
        • Thompson A.J.
        Inpatient rehabilitation in multiple sclerosis Do the benefits carry over into the community?.
        Neurology. 1999; 52: 50
        • Grasso M.G.
        • Troisi E.
        • Rizzi F.
        • Morelli D.
        • Paolucci S.
        Prognostic factors in multidisciplinary rehabilitation treatment in multiple sclerosis: an outcome study.
        Multiple S=clerosis. 2005; 11: 719-724
        • Hallas J.
        • Pottegård A.
        Use of self-controlled designs in pharmacoepidemiology.
        J. Intern. Med. 2014; 275: 581-589
        • Hobart J.
        • Lamping D.
        • Fitzpatrick R.
        • Riazi A.
        • Thompson A
        The Multiple Sclerosis Impact Scale (MSIS-29): a new patient-based outcome measure.
        Brain. 2001; 124: 962-973
        • Hocking C.
        • Williams M.
        • Broad J.
        • Baskett J
        Sensitivity of Shah, Vanclay and Cooper's modified Barthel Index.
        Clin. Rehabil. 1999; 13: 141-147
        • Hsieh Y.W.
        • Wang C.H.
        • Wu S.C.
        • Chen P.C.
        • Sheu C.F.
        • Hsieh C.L
        Establishing the minimal clinically important difference of the Barthel Index in stroke patients.
        Neurorehabil. Neural Repair. 2007; 21: 233-238
        • Johansson S.
        • Ytterberg C.
        • Claesson I.M.
        • Lindberg J.
        • Hillert J.
        • Andersson M.
        • Von Koch L.
        High concurrent presence of disability in multiple sclerosis.
        J. Neurol. 2007; 254: 767-773
        • Khan F.
        • Turner-Stokes L.
        • Ng L.
        Kilpatrick T Multidisciplinary rehabilitation for adults with multiple sclerosis.
        Cochrane Database Syst. Rev. 2007; 18
        • Kurtzke J.F.
        Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS).
        Neurology. 1983; 33: 1444-1452
        • Krupp L.B.
        • La Rocca N.G.
        • Muir-Nash J.
        • Steinberg A.D.
        The fatigue severity scale. Application to patients with multiple sclerosis and systemic lupus erythematosus.
        Arch Neurol. 1989; 46: 1121-1123
        • Lee M.
        • Reddy H.
        • Johansen‐Berg H.
        • Pendlebury S.
        • Jenkinson M.
        • Smith S.
        • Matthews P.M
        The motor cortex shows adaptive functional changes to brain injury from multiple sclerosis.
        Ann. Neurol. 2000; 47: 606-613
        • Morgen K.
        • Kadom N.
        • Sawaki L.
        • Tessitore A.
        • Ohayon J.
        • McFarland H.
        • Frank J.
        • Martin R.
        • Cohen L.G
        Training-dependent plasticity in patients with multiple sclerosis.
        Brain. 2004; 127: 2506-2517
        • Nocentini U.
        • Rossini P.M.
        • Carlesimo G.A.
        • Graceffa A.
        • Grasso M.G.
        • Lupoi D.
        • Oliveri M.
        • Orlacchio A.
        • Pozzilli C.
        • Rizzato B.
        • Caltagirone C
        Patterns of Cognitive Impairment in Secondary Progressive Stable Phase of Multiple Sclerosis: correlations with MRI Findings.
        Eur. Neurol. 2001; 45: 11-18
        • Nudo R.J.
        Plasticity.
        NeuroRx. 2006; 3: 420-427
        • Penner I.K.
        • Kappos L.
        • Rausch M.
        • Opwis K.
        • Radü E.W
        Therapy-induced plasticity of cognitive functions in MS patients: insights from fMRI.
        J. Physiol. 2006; 99: 455-462
        • Péran P.
        • Démonet J.F.
        • Cardebat D.
        Paroxetine-induced modulation of cortical activity supporting language representations of action.
        Psychopharmacology. 2008; 195: 487-496
        • Péran P.
        • Démonet J.F.
        • Cherubini A.
        • Carbebat D.
        • Caltagirone C.
        • Sabatini U.
        Mental representations of action: the neural correlates of the verbal and motor components.
        Brain Res. 2010; 1328: 89-103
        • Péran P.
        • Nemmi F.
        • Méligne D.
        • Cardebat D.
        • Peppe A.
        • Rascol O.
        • Caltagirone C.
        • Demonet J.F.
        • Sabatini U.
        Effect of levodopa on both verbal and motor representations of action in Parkinson's disease: a fMRI study.
        Brain Lang. 2013; 125: 324-329
        • Péran P.
        • Catani S.
        • Falletta
        • Caravasso C.
        • Nemmi F.
        • Sabatini U.
        • Formisano R.
        Supplementary motor area activation is impaired in severe traumatic brain injury parkinsonism.
        J. Neurotrauma. 2014; 31 (1): 642-648
        • Poldrack R.A.
        Imaging Brain Plasticity: conceptual and Methodological Issues- A Theoretical Review.
        Neuroimage. 2000; 12: 1-13
        • Polman C.H.
        • Reingold S.C.
        • Banwell B.
        • Clanet M.
        • Cohen J.A.
        • Filippi M.
        • Fujihara K.
        • Havrdova E.
        • Hutchinson M.
        • Kappos L.
        • Lublin F.D.
        • Montalban X.
        • O'Connor P.
        • Sandberg-Wollheim M.
        • Thompson A.J.
        • Waubant E.
        • Weinshenker B.
        • Wolinsky J.S
        Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria.
        Ann. Neurol. 2011; 69: 292-302
        • Prosperini L.
        • Piattella M.C.
        • Giannì C.
        • Pantano P
        Functional and structural brain plasticity enhanced by motor and cognitive rehabilitation in multiple sclerosis.
        Neural Plast. 2015; 2015481574
        • Rasova K.
        • Krasensky J.
        • Havrdova E.
        • Obenberger J.
        • Seidel Z.
        • Dolezal O.
        • Zalisova M
        Is it possible to actively and purposely make use of plasticity and adaptability in the neurorehabilitation treatment of multiple sclerosis patients? A pilot project.
        Clin. Rehab. 2005; 19: 170-181
        • Rasova K.
        • Prochazkova M.
        • Tintera J.
        • Ibrahim I.
        • Zimova D.
        • Stetkarova I
        Motor programme activating therapy influences adaptive brain functions in multiple sclerosis: clinical and MRI study.
        Int. J. Rehab. Res. 2015; 38: 49-54
        • Reddy H.
        • Narayanan S.
        • Arnoutelis R.
        • Jenkinson M.
        • Antel J.
        • Matthews P.M.
        • Arnold D.L
        Evidence for adaptive functional changes in the cerebral cortex with axonal injury from multiple sclerosis.
        Brain. 2000; 123: 2314-2320
        • Rocca M.A.
        • Gavazzi C.
        • Mezzapesa D.M.
        • Falini A.
        • Colombo B.
        • Mascalchi M.
        • Filippi M
        A functional magnetic resonance imaging study of patients with secondary progressive multiple sclerosis.
        Neuroimage. 2003; 19: 1770-1777
        • Rosti-Otajärvi E.M.
        • Hämäläinen P.I
        Neuropsychological rehabilitation for multiple sclerosis.
        Cochrane Database Syst. Rev. 2011; 11
        • Sastre-Garriga J.
        • Alonso J.
        • Renom M.
        • et al.
        A functional magnetic resonance proof of concept pilot trial of cognitive rehabilitation in multiple sclerosis.
        Multiple Sclerosis. 2011; 17: 457-467
        • Seeley W.W.
        • Menon V.
        • Schatzberg A.F.
        • Keller J.
        • Glover G.H.
        • Kenna H.
        • Greicius M.D
        Dissociable intrinsic connectivity networks for salience processing and executive control.
        J. Neurosci. 2007; 27: 2349-2356
        • Solari A.
        • Filippini G.
        • Gasco P.
        • Colla L.
        • Salmaggi A.
        • La Mantia L.
        • Mendozzi L
        Physical rehabilitation has a positive effect on disability in multiple sclerosis patients.
        Neurology. 1999; 52 (-57): 57
        • Solaro C.
        • Brichetto G.
        • Casadio M.
        • Roccatagliata L.
        • Ruggiu P.
        • Mancardi G.L.
        • Sanguineti V
        Subtle upper limb impairment in asymptomatic multiple sclerosis subjects.
        Multiple Sclerosis. 2007; 13: 428-432
        • Spooren A.I.
        • Timmermans A.A.
        • Seelen H.A
        Motor training programs of arm and hand in patients with MS according to different levels of the ICF: a systematic review.
        BMC Neurol. 2012; 12: 49
        • Werring D.J.
        • Bullmore E.T.
        • Toosy A.T.
        • Miller D.H.
        • Barker G.J.
        • MacManus D.G.
        • Thompson A.J.
        Recovery from optic neuritis is associated with a change in the distribution of cerebral response to visual stimulation: a functional magnetic resonance imaging study.
        J. Neurol. Neurosurgery Psychiatry. 2000; 68: 441-449
        • Zhang S.
        • Li C.S.
        Functional connectivity mapping of the human precuneus by resting state fMRI.
        Neuroimage. 2012; 59: 3548-3562