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The neural correlates of fatigue: an exploratory imaginal fatigue provocation study in chronic fatigue syndrome

Published online by Cambridge University Press:  30 April 2008

X. Caseras*
Affiliation:
Unitat de Psicologia Mèdica, Institut de Neurociències, Universitat Autònoma de Barcelona, Catalonia, Spain Division of Psychological Medicine and Psychiatry, King's College London, Institute of Psychiatry, London, UK
D. Mataix-Cols
Affiliation:
Division of Psychological Medicine and Psychiatry, King's College London, Institute of Psychiatry, London, UK Department of Psychology, King's College London, Institute of Psychiatry, London, UK
K. A. Rimes
Affiliation:
Division of Psychological Medicine and Psychiatry, King's College London, Institute of Psychiatry, London, UK
V. Giampietro
Affiliation:
Centre for Neuroimaging Sciences, King's College London, Institute of Psychiatry, London, UK
M. Brammer
Affiliation:
Centre for Neuroimaging Sciences, King's College London, Institute of Psychiatry, London, UK
F. Zelaya
Affiliation:
Centre for Neuroimaging Sciences, King's College London, Institute of Psychiatry, London, UK
T. Chalder
Affiliation:
Division of Psychological Medicine and Psychiatry, King's College London, Institute of Psychiatry, London, UK
E. Godfrey
Affiliation:
Department of Psychology, King's College London, Institute of Psychiatry, London, UK
*
*Address for correspondence: Dr X. Caseras, PO 69, Section of Cognitive Neuropsychiatry, Institute of Psychiatry, De Crespigny Park, LondonSE5 8AF, UK. (Email: xavier.caseras@iop.kcl.ac.uk)

Abstract

Background

Fatigue is the central symptom in chronic fatigue syndrome (CFS) and yet very little is known about its neural correlates. The aim of this study was to explore the functional brain response, using functional magnetic resonance imaging (fMRI), to the imaginal experience of fatigue in CFS patients and controls.

Method

We compared the blood oxygen level dependent (BOLD) responses of 12 CFS patients and 11 healthy controls to a novel fatigue provocation procedure designed to mimic real-life situations. A non-fatiguing anxiety-provoking condition was also included to control for the non-specific effects of negative affect.

Results

During the provocation of fatigue, CFS patients reported feelings of both fatigue and anxiety and, compared to controls, they showed increased activation in the occipito-parietal cortex, posterior cingulate gyrus and parahippocampal gyrus, and decreased activation in dorsolateral and dorsomedial prefrontal cortices. The reverse pattern of findings was observed during the anxiety-provoking scenarios.

Conclusions

The results may suggest that, in CFS patients, the provocation of fatigue is associated with exaggerated emotional responses that patients may have difficulty suppressing. These findings are discussed in relation to the cognitive-behavioural model of CFS.

Type
Original Articles
Copyright
Copyright © 2008 Cambridge University Press

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References

Angst, J, Dobler-Mikola, A (1985). The Zurich Study. V. Anxiety and phobia in young adults. European Archives of Psychiatry and Neurological Sciences 235, 171178.CrossRefGoogle ScholarPubMed
Beauregard, M, Paquette, V, Levesque, J (2006). Dysfunction in the neural circuitry of emotional self-regulation in major depressive disorder. Neuroreport 17, 843846.CrossRefGoogle ScholarPubMed
Brammer, M, Bullmore, ET, Simmons, A, Williams, SCR, Grasby, PM, Howard, RJ, Woodruff, PWR, Rabe-Hesketh, S (1997). Generic brain activation mapping in functional magnetic resonance imaging: a nonparametric approach. Magnetic Resonance Imaging 15, 763770.CrossRefGoogle ScholarPubMed
Bullmore, ET, Brammer, M, Rabe-Hesketh, S, Curtis, V, Morris, R, Williams, SCR, Sharma, T, McGuire, PK (1999 a). Methods for the diagnosis and treatment of stimulus correlated motion in generic brain activation studies using fMRI. Human Brain Mapping 7, 3848.3.0.CO;2-Q>CrossRefGoogle ScholarPubMed
Bullmore, ET, Long, C, Suckling, J, Fadili, J, Calvert, GA, Zelaya, F, Carpenter, TA, Brammer, MJ (2001). Coloured noise and computational inference in neurophysiological (fMRI) time series analysis: resampling methods in time and wavelet domains. Human Brain Mapping 12, 6178.3.0.CO;2-W>CrossRefGoogle ScholarPubMed
Bullmore, ET, Suckling, J, Overmeyer, S, Rabe-Hesketh, S, Taylor, E, Brammer, MJ (1999 b). Global, voxel and cluster tests, by theory and permutation, for a difference between two groups of structural MR images of the brain. IEEE Transactions on Medical Imaging 18, 3242.CrossRefGoogle ScholarPubMed
Caseras, X, Mataix-Cols, D, Giampietro, V, Rimes, KA, Brammer, M, Zelaya, F, Chalder, T, Godfrey, EL (2006). Probing the working memory system in chronic fatigue syndrome: a functional magnetic resonance imaging study using the n-back task. Psychosomatic Medicine 68, 947955.CrossRefGoogle ScholarPubMed
Chalder, T, Berelowitz, G, Pawlikowska, T, Watts, L, Wessely, S, Wright, D, Walalce, EP (1993). Development of a fatigue scale. Journal of Psychosomatic Research 37, 147153.CrossRefGoogle ScholarPubMed
Chalder, T, Cleare, A, Wessely, S (2000). The management of stress and anxiety in chronic fatigue syndrome. In The Management of Stress and Anxiety in Medical Disorders (ed. Mostofsky, D. I. and Barlow, D. H.), pp. 160179. Alleyn and Bacon: Boston.Google Scholar
Cook, DA, O'Connor, PJ, Lange, G, Steffener, J (2007). Functional neuroimaging correlates of mental fatigue induced by cognition among chronic fatigue syndrome patients and controls. NeuroImage 36, 108122.CrossRefGoogle ScholarPubMed
Creswell, C, Chalder, T (2001). Defensive coping styles in chronic fatigue syndrome. Journal of Psychosomatic Research 51, 607610.CrossRefGoogle ScholarPubMed
Critchley, HD (2004). The human cortex responds to an interoceptive challenge. Proceedings of the National Academy of Sciences USA 101, 63336334.CrossRefGoogle Scholar
Deale, A, Chalder, T, Wessely, S (1998). Illness beliefs and outcome in chronic fatigue syndrome: is change in causal attribution necessary for clinical improvement? Journal of Psychosomatic Research 45, 7783.CrossRefGoogle Scholar
Fischler, B, Cluydts, R, De Gucht, V, Kaufman, L, DeMeirleir, K (1997). Generalised anxiety disorder in chronic fatigue syndrome. Acta Psychiatrica Scandinavica 95, 405413.CrossRefGoogle ScholarPubMed
Friman, O, Borga, M, Lundberg, P, Knutsson, H (2003). Adaptive analysis of fMRI data. NeuroImage 19, 837845.CrossRefGoogle ScholarPubMed
Fukuda, K, Straus, SE, Hickie, I, Sharpe, MC, Dobbins, JG, Komaroff, A (1994). The chronic fatigue syndrome: a comprehensive approach to its definition and study. International Chronic Fatigue Syndrome Study Group. Annals of Internal Medicine 121, 953959.CrossRefGoogle ScholarPubMed
Garret, AS, Maddock, RJ (2006). Separating subjective emotion from the perception of emotion-inducing stimuli: an fMRI study. NeuroImage 33, 263274.CrossRefGoogle Scholar
Georgiades, E, Behan, WMH, Kilduff, LP, Hadjicharalambous, M, Mackie, EE, Wilson, J, Ward, SA, Pitsiladis, YP (2003). Chronic fatigue syndrome: new evidence for a central fatigue disorder. Clinical Science 105, 213218.CrossRefGoogle ScholarPubMed
Godfrey, E, Chalder, T, Ridsdale, L, Seed, P, Ogden, J (2007). Investigating the ‘active ingredients’ of cognitive behaviour therapy and counselling for patients with chronic fatigue in primary care; developing a new process measure to assess treatment fidelity and predict outcome. British Journal of Clinical Psychology 46, 253272.CrossRefGoogle ScholarPubMed
Heim, C, Wagner, D, Maloney, E, Papanicolaou, DA, Solomon, L, Jones, JF, Unger, ER, Reeves, WC (2006). Early adverse experience and risk for chronic fatigue syndrome: results from a population-based study. Archives of General Psychiatry 63, 12581266.CrossRefGoogle ScholarPubMed
Kato, K, Sullivan, PF, Evengard, B, Pedersen, NL (2006). Premorbid predictors of chronic fatigue. Archives of General Psychiatry 63, 12671272.CrossRefGoogle ScholarPubMed
Kent-Braun, JA, Sharma, KR, Weiner, MW, Massie, B, Miller, RG (1993). Central basis of muscle fatigue in chronic fatigue syndrome. Neurology 43, 125131.CrossRefGoogle ScholarPubMed
Lange, G, Steffener, J, Cook, DB, Bly, BM, Christodoulou, C, Liu, WC, Deluca, J, Natelson, BH (2005). Objective evidence of cognitive complaints in chronic fatigue syndrome: a BOLD fMRI study of verbal working memory. NeuroImage 26, 513524.CrossRefGoogle ScholarPubMed
Mataix-Cols, D, Cowley, AJ, Hankins, M, Schneider, A, Bachofen, M, Kenwright, M, Gega, L, Cameron, R, Marks, IM (2005). Reliability and validity of the Work and Social Adjustment Scale in phobic disorders. Comprehensive Psychiatry 46, 223228.CrossRefGoogle ScholarPubMed
Mataix-Cols, D, Wooderson, S, Lawrence, N, Brammer, MJ, Speckens, A, Phillips, ML (2004). Distinct neural correlates of washing, checking, and hoarding symptom dimensions in obsessive-compulsive disorder. Archives of General Psychiatry 6, 564576.CrossRefGoogle Scholar
Mundt, JC, Marks, IM, Greist, JH, Shear, K (2002). Work and Social Adjustment Scale: a simple accurate measure of impairment in functioning. British Journal of Psychiatry 180, 461464.CrossRefGoogle Scholar
Nielsen, FA, Balslev, D, Hansen, LK (2005). Mining the posterior cingulate: segregation between memory and pain components. NeuroImage 27, 520532.CrossRefGoogle ScholarPubMed
Ochsner, KN, Bunge, SA, Gross, JJ, Gabrieli, JD (2002). Rethinking feelings: an fMRI study of the cognitive regulation of emotion. Journal of Cognitive Neuroscience 14, 12151229.CrossRefGoogle ScholarPubMed
Phan, KL, Fitzgerald, DA, Nathan, PJ, Moore, GJ, Uhde, TW, Tancer, ME (2005). Neural substrates for voluntary suppression of negative affect: a functional magnetic resonance imaging study. Biological Psychiatry 57, 210219.CrossRefGoogle ScholarPubMed
Phan, KL, Wager, T, Taylor, SF, Liberzon, I (2002). Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI. NeuroImage 16, 331348.CrossRefGoogle ScholarPubMed
Phillips, ML, Drevets, WC, Rauch, SL, Lane, R (2003). Neurobiology of emotion perception. I: Implications for major psychiatric disorders. Biological Psychiatry 54, 515528.CrossRefGoogle ScholarPubMed
Pourtois, G, Schwartz, S, Seghier, ML, Lazeyras, F, Vuilleumier, P (2006). Neural systems for orienting attention to the location of threat signals: an event-related fMRI study. NeuroImage 31, 920933.CrossRefGoogle Scholar
Sheehan, DV, Lecrubier, Y, Sheehan, KH, Amorim, P, Janavs, J, Weiller, E, Hergueta, T, Barker, R, Dunbar, GC (1998). The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. Journal of Clinical Psychiatry 59 (Suppl. 20), 2233.Google ScholarPubMed
Silver, A, Haeney, M, Vijayadurai, P, Wilks, D, Pattrick, M, Main, CJ (2002). The role of fear of physical movement and activity in chronic fatigue syndrome. Journal of Psychosomatic Research 52, 485493.CrossRefGoogle ScholarPubMed
Smith, AP, Stephan, KE, Rugg, MD, Dolan, RJ (2006). Task and content modulate amygdale-hippocampal connectivity in emotional retrieval. Neuron 49, 631638.CrossRefGoogle Scholar
St Clair Gibson, A, Baden, DA, Lambert, MI, Lambert, EV, Harley, YX, Hampson, D, Russell, VA, Noakes, TD (2003). The conscious perception of the sensation of fatigue. Sports Medicine 33, 167176.CrossRefGoogle ScholarPubMed
Talairach, J, Tournoux, P (1988). Co-planar Stereotactic Atlas of the Human Brain. Thieme: Stuttgart.Google Scholar
van der Werf, SP, Prins, JB, Vercoulen, JHMM, van der Meer, JWM, Bleijenberg, G (2000). Identifying physical activity patterns in chronic fatigue syndrome using actigraphic assessment. Journal of Psychosomatic Research 49, 373379.CrossRefGoogle ScholarPubMed
Ware, JE, Sherbourne, C (1992). The MOS 36-item short form health survey (SF-36). Medical Care 30, 473483.CrossRefGoogle ScholarPubMed
Whiteside, A, Hansen, S, Chaudhuri, A (2004). Exercise lowers pain threshold in chronic fatigue syndrome. Pain 109, 497499.CrossRefGoogle ScholarPubMed
Whiting, P, Bagna, AM, Sowden, AJ, Cornell, JE, Mulrow, CD, Ramírez, G (2001). Interventions for the treatment and management of chronic fatigue syndrome. Journal of the American Medical Association 286, 13601368.CrossRefGoogle ScholarPubMed
Zigmond, AS, Snaith, RP (1983). The Hospital Anxiety and Depression Scale. Acta Psychiatrica Scandinavica 67, 361370.CrossRefGoogle ScholarPubMed