Counteracting Fatigue in Multiple Sclerosis with Right Parietal Anodal Transcranial Direct Current Stimulation

Background Fatigue in multiple sclerosis (MS) patients appears to correlate with vigilance decrement as reflected in an increase in reaction time (RT) and errors with prolonged time-on-task. Objectives The aim of this study was to investigate whether anodal transcranial direct current stimulation (tDCS) over the right parietal or frontal cortex counteracts fatigue-associated vigilance decrement and subjective fatigue. Methods In study I, a randomized double-blind placebo-controlled study, anodal tDCS (1.5 mA) was delivered to the right parietal cortex or the right frontal cortex of 52 healthy participants during the first 20 min of a 40-min lasting visual vigilance task. Study II, also a randomized double-blind placebo-controlled study, investigated the effect of anodal tDCS (1.5 mA) over the right parietal cortex in 46 MS patients experiencing cognitive fatigue. tDCS was delivered for 20 min before patients performed a 20-min lasting visual vigilance task. Results Study I showed that right parietal stimulation, but not right frontal stimulation, counteracts the increase in RT associated with vigilance decrement. Hence, only right parietal stimulation was applied to the MS patients in study II. Stimulation had a significant effect on vigilance decrement in mildly to moderately cognitively fatigued MS patients. Vigilance testing significantly increased the feeling of fatigue independent of stimulation. Conclusion Anodal tDCS over the right parietal cortex can counteract the increase in RTs during vigilance performance, but not the increase in subjective fatigue. This finding is compatible with our model of fatigue in MS, suggesting a dissociation between the feeling and the behavioral characteristics of fatigue.

[1]  A. Kastrup,et al.  No Effect of Cooling on Cognitive Fatigue, Vigilance and Autonomic Functioning in Multiple Sclerosis , 2014 .

[2]  C. Frith,et al.  Monitoring for target objects: activation of right frontal and parietal cortices with increasing time on task , 1998, Neuropsychologia.

[3]  Christiane M. Thiel,et al.  Impact of brain networks involved in vigilance on processing irrelevant visual motion , 2011, NeuroImage.

[4]  J C Rothwell,et al.  An electrophysiological study of the mechanism of fatigue in multiple sclerosis. , 1997, Brain : a journal of neurology.

[5]  P. Eling,et al.  The Representation of Inflammatory Signals in the Brain – A Model for Subjective Fatigue in Multiple Sclerosis , 2014, Front. Neurol..

[6]  J. F. Mackworth.  PERFORMANCE DECREMENT IN VIGILANCE, THRESHOLD, AND HIGH-SPEED PERCEPTUAL MOTOR TASKS. , 1964, Canadian journal of psychology.

[7]  A. Beck,et al.  Psychometric properties of the Beck Depression Inventory: Twenty-five years of evaluation , 1988 .

[8]  N. Mackworth.  The Breakdown of Vigilance during Prolonged Visual Search 1 , 1948 .

[9]  L. Kappos,et al.  The Fatigue Scale for Motor and Cognitive Functions (FSMC): validation of a new instrument to assess multiple sclerosis-related fatigue , 2009, Multiple sclerosis.

[10]  P. Pasqualetti,et al.  Multiple sclerosis fatigue relief by bilateral somatosensory cortex neuromodulation , 2014, Journal of Neurology.

[11]  T. Ilić,et al.  Transcranial direct current stimulation , 2008, Clinical Neurophysiology.

[12]  Joel S. Warm,et al.  Vigilance Requires Hard Mental Work and Is Stressful , 2008, Hum. Factors.

[13]  W. Ammann,et al.  Reduced glucose metabolism in the frontal cortex and basal ganglia of multiple sclerosis patients with fatigue , 1997, Neurology.

[14]  Guglielmo Foffani,et al.  Prefrontal hemodynamic changes produced by anodal direct current stimulation , 2010, NeuroImage.

[15]  A. Priori,et al.  Transcranial direct current stimulation (tDCS) for fatigue in multiple sclerosis. , 2014, NeuroRehabilitation.

[16]  Walter Paulus,et al.  Transcranial direct current stimulation--update 2011. , 2011, Restorative neurology and neuroscience.

[17]  Abhishek Datta,et al.  A Feasibility Study of Bilateral Anodal Stimulation of the Prefrontal Cortex Using High-Definition Electrodes in Healthy Participants , 2015, The Yale journal of biology and medicine.

[18]  Geraint Rees,et al.  Increasing propensity to mind-wander with transcranial direct current stimulation , 2015, Proceedings of the National Academy of Sciences.

[19]  J. Lefaucheur,et al.  Fatigue in Multiple Sclerosis: Neural Correlates and the Role of Non-Invasive Brain Stimulation , 2015, Front. Cell. Neurosci..

[20]  W. N. Dember,et al.  Psychophysical Determinants of Stress in Sustained Attention , 1993, Human factors.

[21]  R. Cabeza,et al.  Imaging Cognition II: An Empirical Review of 275 PET and fMRI Studies , 2000, Journal of Cognitive Neuroscience.

[22]  A. Feinstein.  Is there a cognitive signature for multiple sclerosis-related fatigue? , 2015, Multiple sclerosis.

[23]  Daniel J Buysse,et al.  The Pittsburgh sleep quality index: A new instrument for psychiatric practice and research , 1989, Psychiatry Research.

[24]  Frank G. Hillary,et al.  Neural correlates of cognitive fatigue in multiple sclerosis using functional MRI , 2008, Journal of the Neurological Sciences.

[25]  M. Calabrese,et al.  Basal ganglia and frontal/parietal cortical atrophy is associated with fatigue in relapsing—remitting multiple sclerosis , 2010, Multiple sclerosis.

[26]  N. Larocca,et al.  The fatigue severity scale. Application to patients with multiple sclerosis and systemic lupus erythematosus. , 1989, Archives of neurology.

[27]  Alan C. Evans,et al.  Time-Related Changes in Neural Systems Underlying Attention and Arousal During the Performance of an Auditory Vigilance Task , 1997, Journal of Cognitive Neuroscience.

[28]  D. Rotstein,et al.  Multiple Sclerosis Fatigue is Associated with Reduced Psychomotor Vigilance , 2012, Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques.

[29]  Richard S. J. Frackowiak,et al.  How does transcranial DC stimulation of the primary motor cortex alter regional neuronal activity in the human brain? , 2005, The European journal of neuroscience.

[30]  Á. Pascual-Leone,et al.  Transcranial direct current stimulation , 2005, British Journal of Psychiatry.

[31]  D. Dinges,et al.  A meta-analysis of the impact of short-term sleep deprivation on cognitive variables. , 2010, Psychological bulletin.

[32]  John A. Detre,et al.  Imaging brain fatigue from sustained mental workload: An ASL perfusion study of the time-on-task effect , 2010, NeuroImage.

[33]  V. Ikonomidou,et al.  Relationship of cortical atrophy to fatigue in patients with multiple sclerosis. , 2010, Archives of neurology.

[34]  D. Dinges,et al.  Sleep Deprivation and Vigilant Attention , 2008, Annals of the New York Academy of Sciences.

[35]  Rebecca A. Grier,et al.  Fundamental dimensions of subjective state in performance settings: task engagement, distress, and worry. , 2002, Emotion.

[36]  M. Mcdermott,et al.  Cognitive fatigue during a test requiring sustained attention: a pilot study , 2003, Multiple sclerosis.

[37]  M. Loeb,et al.  The Psychology of Vigilance , 1982 .

[38]  M. Filippi,et al.  Voxelwise Assessment of the Regional Distribution of Damage in the Brains of Patients with Multiple Sclerosis and Fatigue , 2011, American Journal of Neuroradiology.

[39]  P. Eling,et al.  Is there a cognitive signature for MS-related fatigue? , 2015, Multiple sclerosis.

[40]  Jeffrey A. Cohen,et al.  Diagnostic criteria for multiple sclerosis: 2010 Revisions to the McDonald criteria , 2011, Annals of neurology.

[41]  B. Desgranges,et al.  Fatigue is associated with metabolic and density alterations of cortical and deep gray matter in Relapsing-Remitting-Multiple Sclerosis patients at the earlier stage of the disease: A PET/MR study. , 2013, Multiple sclerosis and related disorders.

[42]  P. Eling,et al.  Different cortical underpinnings for fatigue and depression in MS? , 2016, Multiple sclerosis and related disorders.

[43]  T. Ward.  Fatigue and its impact on visual vigilance in people with multiple sclerosis , 2013 .

[44]  K. Willmes,et al.  On the Functional Neuroanatomy of Intrinsic and Phasic Alertness , 2001, NeuroImage.

[45]  Thor Petersen,et al.  Regional brain atrophy in primary fatigued patients with multiple sclerosis , 2010, NeuroImage.

[46]  G. Nagels,et al.  Origin of Fatigue in Multiple Sclerosis: Review of the Literature , 2008, Neurorehabilitation and neural repair.

[47]  Joel S. Warm,et al.  Enhancing vigilance in operators with prefrontal cortex transcranial direct current stimulation (tDCS) , 2014, NeuroImage.

[48]  J. Kurtzke.  Rating neurologic impairment in multiple sclerosis , 1983, Neurology.

[49]  James L. Szalma,et al.  The Vigilance Decrement Reflects Limitations in Effortful Attention, Not Mindlessness , 2003, Hum. Factors.

[50]  M. Nitsche,et al.  Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation , 2000, The Journal of physiology.

[51]  R. Benecke,et al.  Qualitative and quantitative assessment of fatigue in multiple sclerosis (MS) , 2007, Journal of Neurology.

[52]  S. Eickhoff,et al.  Sustaining attention to simple tasks: a meta-analytic review of the neural mechanisms of vigilant attention. , 2013, Psychological bulletin.

[53]  M. Johns,et al.  Reliability and factor analysis of the Epworth Sleepiness Scale. , 1992, Sleep.

[54]  C. Frith,et al.  A fronto-parietal network for rapid visual information processing: a PET study of sustained attention and working memory , 1996, Neuropsychologia.

[55]  C. Forn,et al.  Regional Brain Atrophy and Functional Connectivity Changes Related to Fatigue in Multiple Sclerosis , 2013, PloS one.

[56]  J. Sepulcre,et al.  Fatigue in multiple sclerosis is associated with the disruption of frontal and parietal pathways , 2009, Multiple sclerosis.

[57]  U. Gschwandtner,et al.  Testbatterie zur Aufmerksamkeitsprüfung (TAP) Version 1.7 , 2003 .

[58]  M. Nitsche,et al.  Impact of transcranial direct current stimulation on fatigue in multiple sclerosis. , 2014, Restorative neurology and neuroscience.