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Neural Plasticity
Volume 2016 (2016), Article ID 6434987, 10 pages
http://dx.doi.org/10.1155/2016/6434987
Research Article

Brain Responses during the Anticipation of Dyspnea

1Department of Systems Neuroscience, University Medical Center Hamburg-Eppendorf, Martinistraße 52, 20246 Hamburg, Germany
2Department of Psychology 1, University of Würzburg, Marcusstraße 9-11, 97070 Würzburg, Germany
3Research Group Health Psychology, University of Leuven, Tiensestraat 102, 3000 Leuven, Belgium

Received 13 January 2016; Revised 6 April 2016; Accepted 15 August 2016

Academic Editor: Daniel W. Wesson

Copyright © 2016 M. Cornelia Stoeckel et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. B. Parshall, R. M. Schwartzstein, L. Adams et al., “An official American thoracic society statement: update on the mechanisms, assessment, and management of dyspnea,” American Journal of Respiratory and Critical Care Medicine, vol. 185, no. 4, pp. 435–452, 2012. View at Publisher · View at Google Scholar · View at Scopus
  2. M. A. Spruit, S. J. Singh, C. Garvey et al., “An official American Thoracic Society/European Respiratory Society statement: key concepts and advances in pulmonary rehabilitation,” American Journal of Respiratory and Critical Care Medicine, vol. 188, no. 8, pp. e13–e64, 2013. View at Publisher · View at Google Scholar · View at Scopus
  3. R. W. Lansing, R. H. Gracely, and R. B. Banzett, “The multiple dimensions of dyspnea: review and hypotheses,” Respiratory Physiology & Neurobiology, vol. 167, no. 1, pp. 53–60, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. M. Herigstad, A. Hayen, K. Wiech, and K. T. S. Pattinson, “Dyspnoea and the brain,” Respiratory Medicine, vol. 105, no. 6, pp. 809–817, 2011. View at Publisher · View at Google Scholar · View at Scopus
  5. T. Janssens, G. Verleden, S. De Peuter, I. Van Diest, and O. Van den Bergh, “Inaccurate perception of asthma symptoms: a cognitive-affective framework and implications for asthma treatment,” Clinical Psychology Review, vol. 29, no. 4, pp. 317–327, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. T. Janssens, S. De Peuter, L. Stans et al., “Dyspnea perception in COPD: association between anxiety, dyspnea-related fear, and dyspnea in a pulmonary rehabilitation program,” Chest, vol. 140, no. 3, pp. 618–625, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. R. B. Banzett, H. E. Mulnier, K. Murphy, S. D. Rosen, R. J. S. Wise, and L. Adams, “Breathlessness in humans activates insular cortex,” NeuroReport, vol. 11, no. 10, pp. 2117–2120, 2000. View at Publisher · View at Google Scholar · View at Scopus
  8. C. Peiffer, J.-B. Poline, L. Thivard, M. Aubier, and Y. Samson, “Neural substrates for the perception of acutely induced dyspnea,” American Journal of Respiratory and Critical Care Medicine, vol. 163, no. 4, pp. 951–957, 2001. View at Publisher · View at Google Scholar · View at Scopus
  9. K. C. Evans, R. B. Banzett, L. Adams, L. McKay, R. S. J. Frackowiak, and D. R. Corfield, “Bold fMRI identifies limbic, paralimbic, and cerebellar activation during air hunger,” Journal of Neurophysiology, vol. 88, no. 3, pp. 1500–1511, 2002. View at Google Scholar · View at Scopus
  10. L. C. McKay, L. Adams, R. S. J. Frackowiak, and D. R. Corfield, “A bilateral cortico-bulbar network associated with breath holding in humans, determined by functional magnetic resonance imaging,” NeuroImage, vol. 40, no. 4, pp. 1824–1832, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. A. von Leupoldt, T. Sommer, S. Kegat et al., “The unpleasantness of perceived dyspnea is processed in the anterior insula and amygdala,” American Journal of Respiratory and Critical Care Medicine, vol. 177, no. 9, pp. 1026–1032, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. A. von Leupoldt, T. Sommer, S. Kegat et al., “Dyspnea and pain share emotion-related brain network,” NeuroImage, vol. 48, no. 1, pp. 200–206, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. K. T. S. Pattinson, R. J. Governo, B. J. MacIntosh et al., “Opioids depress cortical centers responsible for the volitional control of respiration,” The Journal of Neuroscience, vol. 29, no. 25, pp. 8177–8186, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. M. Raux, L. Tyvaert, M. Ferreira et al., “Functional magnetic resonance imaging suggests automatization of the cortical response to inspiratory threshold loading in humans,” Respiratory Physiology & Neurobiology, vol. 189, no. 3, pp. 571–580, 2013. View at Publisher · View at Google Scholar · View at Scopus
  15. A. von Leupoldt and B. Dahme, “Cortical substrates for the perception of dyspnea,” Chest, vol. 128, no. 1, pp. 345–354, 2005. View at Publisher · View at Google Scholar · View at Scopus
  16. P. W. Davenport and A. Vovk, “Cortical and subcortical central neural pathways in respiratory sensations,” Respiratory Physiology & Neurobiology, vol. 167, no. 1, pp. 72–86, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. K. C. Evans, “Cortico-limbic circuitry and the airways: insights from functional neuroimaging of respiratory afferents and efferents,” Biological Psychology, vol. 84, no. 1, pp. 13–25, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. A. Von Leupoldt, P.-Y. S. Chan, R. W. Esser, and P. W. Davenport, “Emotions and neural processing of respiratory sensations investigated with respiratory-related evoked potentials,” Psychosomatic Medicine, vol. 75, no. 3, pp. 244–252, 2013. View at Publisher · View at Google Scholar · View at Scopus
  19. J. Z. Reardon, S. C. Lareau, and R. ZuWallack, “Functional status and quality of life in chronic obstructive pulmonary disease,” The American Journal of Medicine, vol. 119, no. 10, supplement 1, pp. 32–37, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. A. Hayen, M. Herigstad, and K. T. S. Pattinson, “Understanding dyspnea as a complex individual experience,” Maturitas, vol. 76, no. 1, pp. 45–50, 2013. View at Publisher · View at Google Scholar · View at Scopus
  21. M. Pappens, E. Smets, D. Vansteenwegen, O. Van Den Bergh, and I. Van Diest, “Learning to fear suffocation: a new paradigm for interoceptive fear conditioning,” Psychophysiology, vol. 49, no. 6, pp. 821–828, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. C. A. Melzig, J. M. Michalowski, K. Holtz, and A. O. Hamm, “Anticipation of interoceptive threat in highly anxiety sensitive persons,” Behaviour Research and Therapy, vol. 46, no. 10, pp. 1126–1134, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. C. A. Porro, P. Baraldi, G. Pagnoni et al., “Does anticipation of pain affect cortical nociceptive systems?” The Journal of Neuroscience, vol. 22, no. 8, pp. 3206–3214, 2002. View at Google Scholar · View at Scopus
  24. T. Koyama, J. G. McHaffie, P. J. Laurienti, and R. C. Coghill, “The subjective experience of pain: where expectations become reality,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 36, pp. 12950–12955, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. R. G. Wise, B. J. Lujan, P. Schweinhardt, G. D. Peskett, R. Rogers, and I. Tracey, “The anxiolytic effects of midazolam during anticipation to pain revealed using fMRI,” Magnetic Resonance Imaging, vol. 25, no. 6, pp. 801–810, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. M. Ploner, M. C. Lee, K. Wiech, U. Bingel, and I. Tracey, “Prestimulus functional connectivity determines pain perception in humans,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 1, pp. 355–360, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. M. Fairhurst, K. Wiech, P. Dunckley, and I. Tracey, “Anticipatory brainstem activity predicts neural processing of pain in humans,” Pain, vol. 128, no. 1-2, pp. 101–110, 2007. View at Publisher · View at Google Scholar · View at Scopus
  28. K. Wiech, C.-S. Lin, K. H. Brodersen, U. Bingel, M. Ploner, and I. Tracey, “Anterior insula integrates information about salience into perceptual decisions about pain,” The Journal of Neuroscience, vol. 30, no. 48, pp. 16324–16331, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. K. H. Brodersen, K. Wiech, E. I. Lomakina et al., “Decoding the perception of pain from fMRI using multivariate pattern analysis,” NeuroImage, vol. 63, no. 3, pp. 1162–1170, 2012. View at Publisher · View at Google Scholar · View at Scopus
  30. A. Ploghaus, I. Tracey, J. S. Gati et al., “Dissociating pain from its anticipation in the human brain,” Science, vol. 284, no. 5422, pp. 1979–1981, 1999. View at Publisher · View at Google Scholar · View at Scopus
  31. I. A. Strigo, A. N. Simmons, S. C. Matthews, A. D. Craig, and M. P. Paulus, “Association of major depressive disorder with altered functional brain response during anticipation and processing of heat pain,” Archives of General Psychiatry, vol. 65, no. 11, pp. 1275–1284, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. M. C. Stoeckel, R. W. Esser, M. Gamer, R. Kalisch, C. Büchel, and A. von Leupoldt, “Amygdala response to anticipation of dyspnea is modulated by 5-HTTLPR genotype,” Psychophysiology, vol. 52, no. 7, pp. 973–976, 2015. View at Publisher · View at Google Scholar · View at Scopus
  33. M. C. Stoeckel, R. W. Esser, M. Gamer, C. Büchel, and A. von Leupoldt, “Brain mechanisms of short-term habituation and sensitization toward dyspnea,” Frontiers in Psychology, vol. 6, article 748, 2015. View at Publisher · View at Google Scholar · View at Scopus
  34. M. R. Miller, J. Hankinson, V. Brusasco et al., “Standardisation of spirometry,” The European Respiratory Journal, vol. 26, no. 2, pp. 319–338, 2005. View at Publisher · View at Google Scholar · View at Scopus
  35. A. von Leupoldt, S. Balewski, S. Petersen et al., “Verbal descriptors of dyspnea in patients with COPD at different intensity levels of dyspnea,” Chest, vol. 132, no. 1, pp. 141–147, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. C. F. Beckmann and S. M. Smith, “Probabilistic independent component analysis for functional magnetic resonance imaging,” IEEE Transactions on Medical Imaging, vol. 23, no. 2, pp. 137–152, 2004. View at Publisher · View at Google Scholar · View at Scopus
  37. R. E. Kelly, G. S. Alexopoulos, Z. Wang et al., “Visual inspection of independent components: defining a procedure for artifact removal from fMRI data,” Journal of Neuroscience Methods, vol. 189, no. 2, pp. 233–245, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. K. J. Friston, C. Buechel, G. R. Fink, J. Morris, E. Rolls, and R. J. Dolan, “Psychophysiological and modulatory interactions in neuroimaging,” NeuroImage, vol. 6, no. 3, pp. 218–229, 1997. View at Publisher · View at Google Scholar · View at Scopus
  39. A. von Leupoldt, T. Sommer, S. Kegat et al., “Down-regulation of insular cortex responses to dyspnea and pain in asthma,” American Journal of Respiratory and Critical Care Medicine, vol. 180, no. 3, pp. 232–238, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. M. P. Paulus, T. Flagan, A. N. Simmons et al., “Subjecting elite athletes to inspiratory breathing load reveals behavioral and neural signatures of optimal performers in extreme environments,” PLoS ONE, vol. 7, no. 1, Article ID e29394, 2012. View at Publisher · View at Google Scholar · View at Scopus
  41. N. Tzourio-Mazoyer, B. Landeau, D. Papathanassiou et al., “Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain,” NeuroImage, vol. 15, no. 1, pp. 273–289, 2002. View at Publisher · View at Google Scholar · View at Scopus
  42. C. Linnman, E. A. Moulton, G. Barmettler, L. Becerra, and D. Borsook, “Neuroimaging of the periaqueductal gray: state of the field,” NeuroImage, vol. 60, no. 1, pp. 505–522, 2012. View at Publisher · View at Google Scholar · View at Scopus
  43. K. L. Mackiewicz, I. Sarinopoulos, K. L. Cleven, and J. B. Nitschke, “The effect of anticipation and the specificity of sex differences for amygdala and hippocampus function in emotional memory,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 38, pp. 14200–14205, 2006. View at Publisher · View at Google Scholar · View at Scopus
  44. J. B. Nitschke, I. Sarinopoulos, K. L. MacKiewicz, H. S. Schaefer, and R. J. Davidson, “Functional neuroanatomy of aversion and its anticipation,” NeuroImage, vol. 29, no. 1, pp. 106–116, 2006. View at Publisher · View at Google Scholar · View at Scopus
  45. G. R. Samanez-Larkin, N. G. Hollon, L. L. Carstensen, and B. Knutson, “Individual differences in insular sensitivity during loss anticipation predict avoidance learning,” Psychological Science, vol. 19, no. 4, pp. 320–323, 2008. View at Publisher · View at Google Scholar · View at Scopus
  46. K. Holtz, C. A. Pané-Farré, J. Wendt, M. Lotze, and A. O. Hamm, “Brain activation during anticipation of interoceptive threat,” NeuroImage, vol. 61, no. 4, pp. 857–865, 2012. View at Publisher · View at Google Scholar · View at Scopus
  47. W. W. Seeley, V. Menon, A. F. Schatzberg et al., “Dissociable intrinsic connectivity networks for salience processing and executive control,” The Journal of Neuroscience, vol. 27, no. 9, pp. 2349–2356, 2007. View at Publisher · View at Google Scholar · View at Scopus
  48. A. Lutz, D. R. McFarlin, D. M. Perlman, T. V. Salomons, and R. J. Davidson, “Altered anterior insula activation during anticipation and experience of painful stimuli in expert meditators,” NeuroImage, vol. 64, no. 1, pp. 538–546, 2013. View at Publisher · View at Google Scholar · View at Scopus
  49. F. Bodranghien, A. Bastian, C. Casali et al., “Consensus paper: revisiting the symptoms and signs of cerebellar syndrome,” Cerebellum, vol. 15, no. 3, pp. 369–391, 2016. View at Publisher · View at Google Scholar · View at Scopus
  50. C. J. Stoodley and J. D. Schmahmann, “Functional topography in the human cerebellum: a meta-analysis of neuroimaging studies,” NeuroImage, vol. 44, no. 2, pp. 489–501, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. E. A. Moulton, I. Elman, G. Pendse, J. Schmahmann, L. Becerra, and D. Borsook, “Aversion-related circuitry in the cerebellum: responses to noxious heat and unpleasant images,” The Journal of Neuroscience, vol. 31, no. 10, pp. 3795–3804, 2011. View at Publisher · View at Google Scholar · View at Scopus
  52. L. M. Parsons, G. Egan, M. Liotti et al., “Neuroimaging evidence implicating cerebellum in the experience of hypercapnia and hunger for air,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 4, pp. 2041–2046, 2001. View at Publisher · View at Google Scholar · View at Scopus
  53. V. G. Macefield, S. C. Gandevia, and L. A. Henderson, “Neural sites involved in the sustained increase in muscle sympathetic nerve activity induced by inspiratory capacity apnea: a fMRI study,” Journal of Applied Physiology, vol. 100, no. 1, pp. 266–273, 2006. View at Publisher · View at Google Scholar · View at Scopus
  54. A. P. Binks, K. C. Evans, J. D. Reed, S. H. Moosavi, and R. B. Banzett, “The time-course of cortico-limbic neural responses to air hunger,” Respiratory Physiology and Neurobiology, vol. 204, pp. 78–85, 2014. View at Publisher · View at Google Scholar · View at Scopus
  55. M. J. Fischer, M. Scharloo, J. Abbink et al., “Concerns about exercise are related to walk test results in pulmonary rehabilitation for patients with COPD,” International Journal of Behavioral Medicine, vol. 19, no. 1, pp. 39–47, 2012. View at Publisher · View at Google Scholar · View at Scopus
  56. M. Leeuw, M. E. J. B. Goossens, S. J. Linton, G. Crombez, K. Boersma, and J. W. S. Vlaeyen, “The fear-avoidance model of musculoskeletal pain: current state of scientific evidence,” Journal of Behavioral Medicine, vol. 30, no. 1, pp. 77–94, 2007. View at Publisher · View at Google Scholar · View at Scopus
  57. J. R. de Jong, J. W. S. Vlaeyen, M. van Eijsden, C. Loo, and P. Onghena, “Reduction of pain-related fear and increased function and participation in work-related upper extremity pain (WRUEP): effects of exposure in vivo,” Pain, vol. 153, no. 10, pp. 2109–2118, 2012. View at Publisher · View at Google Scholar · View at Scopus
  58. A. von Leupoldt and T. Janssens, “Could targeting disease specific fear and anxiety improve COPD outcomes?” Expert Review of Respiratory Medicine, vol. 10, no. 8, pp. 835–837, 2016. View at Publisher · View at Google Scholar
  59. R. W. Esser, M. C. Stoeckel, A. Kirsten et al., “Structural brain changes in patients with COPD,” Chest, vol. 149, no. 2, pp. 426–434, 2016. View at Publisher · View at Google Scholar · View at Scopus