The Neural Mechanisms of Re-Experiencing Mental Fatigue Sensation: A Magnetoencephalography Study

There have been several studies which have tried to clarify the neural mechanisms of fatigue sensation; however fatigue sensation has multiple aspects. We hypothesized that past experience related to fatigue sensation is an important factor which contributes to future formation of fatigue sensation through the transfer to memories that are located within specific brain structures. Therefore, we aimed to investigate the neural mechanisms of fatigue sensation related to memory. In the present study, we investigated the neural activity caused by re-experiencing the fatigue sensation that had been experienced during a fatigue-inducing session. Thirteen healthy volunteers participated in fatigue and non-fatigue experiments in a crossover fashion. In the fatigue experiment, they performed a 2-back test session for 40 min to induce fatigue sensation, a rest session for 15 min to recover from fatigue, and a magnetoencephalography (MEG) session in which they were asked to re-experience the state of their body with fatigue that they had experienced in the 2-back test session. In the non-fatigue experiment, the participants performed a free session for 15 min, a rest session for 15 min, and an MEG session in which they were asked to re-experience the state of their body without fatigue that they had experienced in the free session. Spatial filtering analyses of oscillatory brain activity showed that the delta band power in the left Brodmann’s area (BA) 39, alpha band power in the right pulvinar nucleus and the left BA 40, and beta band power in the left BA 40 were lower when they re-experienced the fatigue sensation than when they re-experienced the fatigue-free sensation, indicating that these brain regions are related to re-experiencing the fatigue sensation. Our findings may help clarify the neural mechanisms underlying fatigue sensation.

[1]  F. L. D. Silva,et al.  Event-related EEG/MEG synchronization and desynchronization: basic principles , 1999, Clinical Neurophysiology.

[2]  K. D. Davis,et al.  Neural correlates of prickle sensation: a percept-related fMRI study , 2002, Nature Neuroscience.

[3]  T. Harmony.  The functional significance of delta oscillations in cognitive processing , 2013, Front. Integr. Neurosci..

[4]  Masaaki Tanaka,et al.  A new hypothesis of chronic fatigue syndrome: co-conditioning theory. , 2010, Medical hypotheses.

[5]  B. Horwitz,et al.  Brain activity during transient sadness and happiness in healthy women. , 1995, The American journal of psychiatry.

[6]  A. Verbeek,et al.  Fatigue and chronic fatigue syndrome-like complaints in the general population. , 2010, European journal of public health.

[7]  Tobias Otto,et al.  Neural correlates of mental effort evaluation--involvement of structures related to self-awareness. , 2014, Social cognitive and affective neuroscience.

[8]  Sylvain Baillet,et al.  How to Detect Amygdala Activity with Magnetoencephalography using Source Imaging , 2013, Journal of visualized experiments : JoVE.

[9]  Masaaki Tanaka,et al.  Neural Correlates of Central Inhibition during Physical Fatigue , 2013, PloS one.

[10]  Edgar Erdfelder,et al.  G*Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences , 2007, Behavior research methods.

[11]  Andreas A. Ioannides,et al.  Phantom study supports claim of accurate localization from MEG data , 2007 .

[12]  E. Erdfelder,et al.  Statistical power analyses using G*Power 3.1: Tests for correlation and regression analyses , 2009, Behavior research methods.

[13]  P Wallace,et al.  Population based study of fatigue and psychological distress , 1994, BMJ.

[14]  Krish D. Singh,et al.  A new approach to neuroimaging with magnetoencephalography , 2005, Human brain mapping.

[15]  S. Taylor,et al.  The effect of graded aversive stimuli on limbic and visual activation , 2000, Neuropsychologia.

[16]  Robert T. Knight,et al.  Five-dimensional neuroimaging: Localization of the time–frequency dynamics of cortical activity , 2008, NeuroImage.

[17]  R. Lane,et al.  Neuroanatomical correlates of happiness, sadness, and disgust. , 1997, The American journal of psychiatry.

[18]  M. Phillips,et al.  Distinct neural correlates of washing, checking, and hoarding symptom dimensions in obsessive-compulsive disorder. , 2004, Archives of general psychiatry.

[19]  A. Mann,et al.  Tired, weak, or in need of rest: fatigue among general practice attenders. , 1990, BMJ.

[20]  H. Onoe,et al.  Medial Orbitofrontal Cortex Is Associated with Fatigue Sensation , 2010, Neurology research international.

[21]  F. D. Silva.  Neural mechanisms underlying brain waves: from neural membranes to networks. , 1991 .

[22]  R. Post,et al.  Regional brain activity during transient self-induced anxiety and anger in healthy adults , 1999, Biological Psychiatry.

[23]  Karl J. Friston,et al.  How Many Subjects Constitute a Study? , 1999, NeuroImage.

[24]  D. Cella,et al.  Fatigue in cancer patients compared with fatigue in the general United States population , 2002, Cancer.

[25]  P. Fox,et al.  Differential limbic–cortical correlates of sadness and anxiety in healthy subjects: implications for affective disorders , 2000, Biological Psychiatry.

[26]  G. Pfurtscheller,et al.  Event-related dynamics of cortical rhythms: frequency-specific features and functional correlates. , 2001, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[27]  Akira Ishii,et al.  The Neural Mechanisms Underlying the Decision to Rest in the Presence of Fatigue: A Magnetoencephalography Study , 2014, PloS one.

[28]  W. Singer.  Synchronization of cortical activity and its putative role in information processing and learning. , 1993, Annual review of physiology.

[29]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[30]  関原 謙介,et al.  Adaptive Spatial Filters for Electromagnetic Brain Imaging , 2008 .

[31]  S. Wessely,et al.  Development of a fatigue scale. , 1993, Journal of psychosomatic research.

[32]  Seiki Tajima,et al.  Central nervous system fatigue alters autonomic nerve activity. , 2009, Life sciences.

[33]  W. Klimesch,et al.  Theta band power in the human scalp EEG and the encoding of new information , 1996, Neuroreport.

[34]  Masaaki Tanaka,et al.  The Neural Substrates of Self-Evaluation of Mental Fatigue: A Magnetoencephalography Study , 2014, PloS one.

[35]  C. Stam.  Use of magnetoencephalography (MEG) to study functional brain networks in neurodegenerative disorders , 2010, Journal of the Neurological Sciences.

[36]  B. Mensour,et al.  Separate neural circuits for primary emotions? Brain activity during self-induced sadness and happiness in professional actors , 2003, Neuroreport.

[37]  Jan Theeuwes,et al.  OpenSesame: An open-source, graphical experiment builder for the social sciences , 2011, Behavior Research Methods.

[38]  Masaaki Tanaka,et al.  Fatigue sensation induced by the sounds associated with mental fatigue and its related neural activities: revealed by magnetoencephalography , 2013, Behavioral and Brain Functions.

[39]  Alan C. Evans,et al.  An MRI-Based Probabilistic Atlas of Neuroanatomy , 1994 .

[40]  M. George.  Seminars in Basic Neurosciences , 1995 .

[41]  Panagiotis D Bamidis,et al.  Amygdala responses to Valence and its interaction by arousal revealed by MEG. , 2014, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[42]  Y. Okada,et al.  Modeling and Detecting Deep Brain Activity with MEG & EEG , 2007, 2007 29th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[43]  O. Jensen,et al.  Frontal theta activity in humans increases with memory load in a working memory task , 2002, The European journal of neuroscience.

[44]  E. Amaro,et al.  Engagement of multifocal neural circuits during recall of autobiographical happy events. , 2008, Brazilian journal of medical and biological research = Revista brasileira de pesquisas medicas e biologicas.

[45]  Thomas H. B. FitzGerald,et al.  Thalamo-cortical cross-frequency coupling detected with MEG , 2014, Front. Hum. Neurosci..

[46]  Richard Coppola,et al.  Evoked amygdala responses to negative faces revealed by adaptive MEG beamformers , 2008, Brain Research.

[47]  M Liotti,et al.  Brain responses associated with consciousness of breathlessness (air hunger). , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[48]  M. Raichle,et al.  Integration of emotion and cognition in the lateral prefrontal cortex , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[49]  Y. Watanabe,et al.  The neural substrates of physical fatigue sensation to evaluate ourselves: A magnetoencephalography study , 2014, Neuroscience.

[50]  S. Kaasa,et al.  Fatigue in the general Norwegian population: normative data and associations. , 1998, Journal of psychosomatic research.

[51]  M. Posner,et al.  Cognitive and emotional influences in anterior cingulate cortex , 2000, Trends in Cognitive Sciences.

[52]  Karl J. Friston,et al.  Mechanisms of evoked and induced responses in MEG/EEG , 2006, NeuroImage.

[53]  T. Jodoi,et al.  Reliability and Validity of the Japanese Version of the Chalder Fatigue Scale among Youth in Japan , 2008, Psychological reports.

[54]  C. Scheiber,et al.  Implicit emotion during recollection of past events: A nonverbal fMRI study , 2006, Brain Research.

[55]  R. Dolan,et al.  Common effects of emotional valence, arousal and attention on neural activation during visual processing of pictures , 1999, Neuropsychologia.

[56]  G. Rizzolatti,et al.  Both of Us Disgusted in My Insula The Common Neural Basis of Seeing and Feeling Disgust , 2003, Neuron.

[57]  E. Denkova,et al.  Experiencing past and future personal events: Functional neuroimaging evidence on the neural bases of mental time travel , 2008, Brain and Cognition.

[58]  M. Bradley,et al.  Emotional arousal and activation of the visual cortex: an fMRI analysis. , 1998, Psychophysiology.

[59]  G. Bydder,et al.  Magnetic Resonance Scanning and Epilepsy , 1994, NATO ASI Series.

[60]  Kouzi Yamaguti,et al.  Autonomic nervous alterations associated with daily level of fatigue , 2011, Behavioral and Brain Functions.

[61]  Ferenc Bari,et al.  Capillary injury in the ischemic brain of hyperlipidemic, apolipoprotein B-100 transgenic mice. , 2009, Life sciences.

[62]  R. James R. Blair,et al.  Neural dynamics for facial threat processing as revealed by gamma band synchronization using MEG , 2007, NeuroImage.

[63]  A. Young,et al.  Neural responses to facial and vocal expressions of fear and disgust , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[64]  K. Phan,et al.  Neural correlates of internally-generated disgust via autobiographical recall: a functional magnetic resonance imaging investigation , 2004, Neuroscience Letters.

[65]  M. Brammer,et al.  The neural correlates of fatigue: an exploratory imaginal fatigue provocation study in chronic fatigue syndrome , 2008, Psychological Medicine.

[66]  G. Knyazev,et al.  Neuroscience and Biobehavioral Reviews , 2012 .

[67]  Kathryn M. McMillan,et al.  N‐back working memory paradigm: A meta‐analysis of normative functional neuroimaging studies , 2005, Human brain mapping.

[68]  G. Knyazev.  Motivation, emotion, and their inhibitory control mirrored in brain oscillations , 2007, Neuroscience & Biobehavioral Reviews.