Brain mechanisms of short-term habituation and sensitization toward dyspnea

Frontiers in Psychology

Volumn 6, Issue JUN, 2015, Pages

  Stoeckel, M Cornelia ^a   Esser, Roland W ^a   Gamer, Matthias ^a   Büchel, Christian ^a   von Leupoldt, Andreas ^a,b  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Breathlessness; Dyspnea; FMRI; Habituation; Insular cortex; Sensitization; Unpleasantness

Indexed keywords

EID: 84940495398     PISSN: None     EISSN: 16641078     Source Type: Journal    
DOI: 10.3389/fpsyg.2015.00748     Document Type: Article

References (40)

1. Bingel, U., Schoell, E., Herken, W., Büchel, C., and May, A. (2007). Habituation to painful stimulation involves the antinociceptive system. Pain 131, 21-30. doi: 10.1016/j.pain.2006.12.005.
2. 2 in ventilated humans. J. Appl. Physiol. 81, 949-956.
3. Brodersen, K. H., Wiech, K., Lomakina, E. I., Lin, C.-S., Buhmann, J. M., Bingel, U., et al. (2012). Decoding the perception of pain from fMRI using multivariate pattern analysis. Neuroimage 63, 1162-1170. doi: 10.1016/j.neuroimage.2012.08.035.
4. Carrieri-Kohlman, V., Gormley, J. M., Eiser, S., Demir-Deviren, S., Nguyen, H., Paul, S. M., et al. (2001). Dyspnea and the affective response during exercise training in obstructive pulmonary disease. Nurs. Res. 50, 136-146. doi: 10.1097/00006199-200105000-00002.
5. Davenport, P. W., and Vovk, A. (2009). Cortical and subcortical central neural pathways in respiratory sensations. Respir. Physiol. Neurobiol. 167, 72-86. doi: 10.1016/j.resp.2008.10.001.
6. Evans, K. C. (2010). Cortico-limbic circuitry and the airways: insights from functional neuroimaging of respiratory afferents and efferents. Biol. Psychol. 84, 13-25. doi: 10.1016/j.biopsycho.2010.02.005.
7. Fairhurst, M., Wiech, K., Dunckley, P., and Tracey, I. (2007). Anticipatory brainstem activity predicts neural processing of pain in humans. Pain 128, 101-110. doi: 10.1016/j.pain.2006.09.001.
8. Hayen, A., Herigstad, M., and Pattinson, K. T. S. (2013). Understanding dyspnea as a complex individual experience. Maturitas 76, 45-50. doi: 10.1016/j.maturitas.2013.06.005.
9. Hayen, A., Herigstad, M., Wiech, K., and Pattinson, K. T. S. (2015). Subjective evaluation of experimental dyspnoea-Effects of isocapnia and repeated exposure. Respir. Physiol. Neurobiol. 208, 21-28. doi: 10.1016/j.resp.2014.12.019.
10. Herigstad, M., Hayen, A., Wiech, K., and Pattinson, K. T. S. (2011). Dyspnoea and the brain. Respir. Med. 105, 809-817. doi: 10.1016/j.rmed.2010.12.022.
11. Holtz, K., Pané-Farré, C. A., Wendt, J., Lotze, M., and Hamm, A. O. (2012). Brain activation during anticipation of interoceptive threat. Neuroimage 61, 857-865. doi: 10.1016/j.neuroimage.2012.03.019.
12. Hsieh, J. C., Stone-Elander, S., and Ingvar, M. (1999). Anticipatory coping of pain expressed in the human anterior cingulate cortex: a positron emission tomography study. Neurosci. Lett. 262, 61-64. doi: 10.1016/S0304-3940(99)00060-9.
13. Janssens, T., Verleden, G., De Peuter, S., Van Diest, I., and Van den Bergh, O. (2009). Inaccurate perception of asthma symptoms: a cognitive-affective framework and implications for asthma treatment. Clin. Psychol. Rev. 29, 317-327. doi: 10.1016/j.cpr.2009.02.006.
14. Labus, J. S., Naliboff, B. D., Berman, S. M., Suyenobu, B., Vianna, E. P., Tillisch, K., et al. (2009). Brain networks underlying perceptual habituation to repeated aversive visceralstimuli in patients with iritable bowel syndrome. Neuroimage 47, 952-960. doi: 10.1016/j.neuroimage.2009.05.078.
15. Lansing, R. W., Gracely, R. H., and Banzett, R. B. (2009). The multiple dimensions of dyspnea: review and hypotheses. Respir. Physiol. Neurobiol. 167, 53-60. doi: 10.1016/j.resp.2008.07.012.
16. Laviolette, L., Laveneziana, P., and ERS Research Seminar Faculty. (2014). Dyspnoea: a multidimensional and multidisciplinary approach. Eur. Respir. J. 43, 1750-1762. doi: 10.1183/09031936.00092613.
17. Li, W., Daems, E., Van de Woestijne, K. P., Van Diest, I., Gallego, J., De Peuter, S., et al. (2006). Air hunger and ventilation in response to hypercapnia: effects of repetition and anxiety. Physiol. Behav. 88, 47-54. doi: 10.1016/j.physbeh.2006.03.001.
18. Linnman, C., Moulton, E. A., Barmettler, G., Becerra, L., and Borsook, D. (2012). Neuroimaging of the periaqueductal gray: state of the field. Neuroimage 60, 505-522. doi: 10.1016/j.neuroimage.2011.11.095.
19. Lowén, M. B. O., Mayer, E., Tillisch, K., Labus, J., Naliboff, B., Lundberg, P., et al. (2015). Deficient habituation to repeated rectal distensions in irritable bowel syndrome patients with visceral hypersensitivity. Neurogastroenterol. Motil. 27, 646-655. doi: 10.1111/nmo.12537.
20. Miller, M. R., Hankinson, J., Brusasco, V., Burgos, F., Casaburi, R., Coates, A., et al. (2005). Standardisation of spirometry. Eur. Respir. J. 26, 319-338. doi: 10.1183/09031936.05.00034805.
21. Parshall, M. B., Schwartzstein, R. M., Adams, L., Banzett, R. B., Manning, H. L., Bourbeau, J., et al. (2012). An official American Thoracic Society statement: update on the mechanisms, assessment, and management of dyspnea. Am. J. Respir. Crit. Care Med. 185, 435-452. doi: 10.1164/rccm.201111-2042ST.
22. Paulus, M. P., Flagan, T., Simmons, A. N., Gillis, K., Kotturi, S., Thom, N., et al. (2012). Subjecting elite athletes to inspiratory breathing load reveals behavioral and neural signatures of optimal performers in extreme environments. PLoS ONE 7:e29394. doi: 10.1371/journal.pone.0029394.
23. Petersen, S., Schroijen, M., Mölders, C., Zenker, S., and Van den Bergh, O. (2014). Categorical interoception: perceptual organization of sensations from inside. Psychol. Sci. 25, 1059-1066. doi: 10.1177/0956797613519110.
24. Petersen, S., van den Berg, R. A., Janssens, T., and Van den Bergh, O. (2011). Illness and symptom perception: a theoretical approach towards an integrative measurement model. Clin. Psychol. Rev. 31, 428-439. doi: 10.1016/j.cpr.2010.11.002.
25. Petrovic, P., Kalso, E., Petersson, K. M., and Ingvar, M. (2002). Placebo and opioid analgesia-imaging a shared neuronal network. Science 295, 1737-1740. doi: 10.1126/science.1067176.
26. Ploner, M., Lee, M. C., Wiech, K., Bingel, U., and Tracey, I. (2010). Prestimulus functional connectivity determines pain perception in humans. Proc. Natl. Acad. Sci. U.S.A. 1071, 355-360. doi: 10.1073/pnas.0906186106.
27. Seeley, W. W., Menon, V., Schatzberg, A. F., Keller, J., Glover, G. H., Kenna, H., et al. (2007). Dissociable intrinsic connectivity networks for salience processing and executive control. J. Neurosci. 279, 2349-2356. doi: 10.1523/JNEUROSCI.5587-06.2007.
28. Spielberger, C. D., Gorsuch, R. L., Lushene, R., Vagg, P. R., and Jacobs, G. A. (1983). Manual for the State-Trait Anxiety Inventory. Palo Alto, CA: Consulting Psychologists Press.
29. Stankewitz, A., Valet, M., Schulz, E., Wöller, A., Sprenger, T., Vogel, D., et al. (2013). Pain sensitisers exhibit grey matter changes after repetitive pain exposure: a longitudinal voxel-based morphometry study. Pain 154, 1732-1737. doi: 10.1016/j.pain.2013.05.019.
30. Tracey, I., and Mantyh, P. W. (2007). The cerebral signature for pain perception and its modulation. Neuron 55, 377-391. doi: 10.1016/j.neuron.2007.07.012.
31. Troosters, T., van der Molen, T., Polkey, M., Rabinovich, R. A., Vogiatzis, I., Weisman, I., et al. (2013). Improving physical activity in COPD: towards a new paradigm. Respir. Res. 14, 115. doi: 10.1186/1465-9921-14-115.
32. Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., et al. (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15, 273-289. doi: 10.1006/nimg.2001.0978.
33. von Leupoldt, A., and Dahme, B. (2005). Cortical substrates for the perception of dyspnea. Chest 128, 345-354. doi: 10.1378/chest.128.1.345.
34. von Leupoldt, A., Sommer, T., Kegat, S., Baumann, H. J., Klose, H., Dahme, B., et al. (2008). The unpleasantness of perceived dyspnea is processed in the anterior insula and amygdala. Am. J. Respir. Crit. Care Med. 177, 1026-1032. doi: 10.1164/rccm.200712-1821OC.
35. von Leupoldt, A., Sommer, T., Kegat, S., Eippert, F., Baumann, H. J., Klose, H., et al. (2009). Down-regulation of insular cortex responses to dyspnea and pain in asthma. Am. J. Respir. Crit. Care Med. 180, 232-238. doi: 10.1164/rccm.200902-0300OC.
36. von Leupoldt, A., Vovk, A., Bradley, M. M., Lang, P. J., and Davenport, P. W. (2011a). Habituation in neural processing and subjective perception of respiratory sensations. Psychophysiology 48, 808-812. doi: 10.1111/j.1469-8986.2010.01141.x.
37. von Leupoldt, A., Brassen, S., Baumann, H. J., Klose, H., and Büchel, C. (2011b). Structural brain changes related to disease duration in patients with asthma. PLoS ONE 6:e23739. doi: 10.1371/journal.pone.0023739.
38. Wan, L., Stans, L., Bogaerts, K., Decramer, M., and Van den Bergh, O. (2012). Sensitization in medically unexplained dyspnea: differential effects on intensity and unpleasantness. Chest 141, 989-995. doi: 10.1378/chest.11-1423.
39. Wan, L., Van Diest, I., De Peuter, S., Bogaerts, K., Oyen, N., Hombroux, N., et al. (2008). Repeated experiences of air hunger and ventilatory behavior in response to hypercapnia in the standardized rebreathing test: effects of anxiety. Biol. Psychol. 77, 223-232. doi: 10.1016/j.biopsycho.2007.10.013.
40. Wan, L., Van Diest, I., De Peuter, S., Bogaerts, K., and Van den Bergh, O. (2009). Repeated breathlessness experiences induced by hypercapnia: differential effects on intensity and unpleasantness. Chest 135, 455-461. doi: 10.1378/chest.08-1226.