Neural correlates coding stimulus level and perception of capsaicin-evoked urge-to-cough in humans

NeuroImage

Volumn 61, Issue 4, 2012, Pages 1324-1335

  Farrell, Michael J ^a   Cole, Leonie J ^a   Chiapoco, David ^a   Egan, Gary F ^a   Mazzone, Stuart B ^b  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Blood oxygen level dependent; Cortex; Cough; Functional magnetic resonance imaging; Respiratory sensation

Indexed keywords

CAPSAICIN; SODIUM CHLORIDE;

ADULT; AIRWAY; ANTERIOR INSULA; ARTICLE; BLOOD OXYGEN LEVEL DEPENDENT; BRAIN FUNCTION; BRAIN REGION; BREATHING RATE; CENTRAL OPERCULUM; CEREBELLUM; COHORT ANALYSIS; CONTROLLED STUDY; DORSAL PONS; DOSE RESPONSE; DRUG RECHALLENGE; EVOKED RESPONSE; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; INFERIOR FRONTAL GYRUS; INFERIOR PARIETAL LOBULE; INHALATION; INSULA; IRRITATIVE COUGHING; LATERAL MEDULLA; MALE; MEDULLA OBLONGATA; MIDDLE CINGULATE CORTEX; MIDDLE FRONTAL GYRUS; NORMAL HUMAN; ORBITAL CORTEX; OXYGEN BLOOD LEVEL; PARIETAL CORTEX; PERCEPTIVE DISCRIMINATION; PONS; POSTCENTRAL GYRUS; PREFRONTAL CORTEX; PREMOTOR CORTEX; PRIMARY SOMATOSENSORY CORTEX; PRIORITY JOURNAL; PUTAMEN; RESPIRATORY FUNCTION; SOMATOSENSORY CORTEX; SPATIAL DISCRIMINATION; STIMULUS RESPONSE; SUBTHALAMUS; SUPERIOR FRONTAL GYRUS; SUPPLEMENTARY MOTOR AREA; THALAMUS;

ADULT; BRAIN; BRAIN MAPPING; CAPSAICIN; COUGH; EVOKED POTENTIALS; FEMALE; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; PSYCHOPHYSIOLOGY; SENSORY SYSTEM AGENTS;

EID: 84861332560     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2012.03.030     Document Type: Article

References (62)

1. Andersson J.L. How to estimate global activity independent of changes in local activity. Neuroimage 1997, 6(4):237-244.
2. Banzett R.B., Mulnier H.E., Murphy K., Rosen S.D., Wise R.J., Adams L. Breathlessness in humans activates insular cortex. Neuroreport 2000, 11(10):2117-2120.
3. Birn R.M., Smith M.A., Jones T.B., Bandettini P.A. The respiration response function: the temporal dynamics of fMRI signal fluctuations related to changes in respiration. Neuroimage 2008, 40(2):644-654.
4. Birn R.M., Murphy K., Handwerker D.A., Bandettini P.A. fMRI in the presence of task-correlated breathing variations. Neuroimage 2009, 47(3):1092-1104.
5. Burt C.W., Schappert S.M. Ambulatory care visits to physician offices, hospital outpatient departments, and emergency departments: United States, 1999-2000. Vital Health Stat. 13 2004, 157:1-70.
6. Cervero F. Visceral nociception: peripheral and central aspects of visceral nociceptive systems. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1985, 308(1136):325-337.
7. Chikazoe J. Localizing performance of go/no-go tasks to prefrontal cortical subregions. Curr. Opin. Psychiatry 2011, 23(3):267-272.
8. Coen S.J., Gregory L.J., Yaquez L., Amaro E., Brammer M., Williams S.C., Aziz Q. Reproducibility of human brain activity evoked by esophageal stimulation using functional magnetic resonance imaging. Am. J. Physiol. Gastrointest. Liver Physiol. 2007, 293(1):G188-G197.
9. 2-stimulated breathing in man. J. Physiol. 1995, 488(Pt 1):77-84.
10. Craig A.D. How do you feel - now? The anterior insula and human awareness. Nat. Rev. Neurosci. 2009, 10(1):59-70.
11. Critchley H.D., Wiens S., Rotshtein P., Ohman A., Dolan R.J. Neural systems supporting interoceptive awareness. Nat. Neurosci. 2004, 7(2):189-195.
12. Davenport P.W. Clinical cough I: the urge-to-cough: a respiratory sensation. Handb. Exp. Pharmacol. 2009, 187:263-276.
13. Davenport P.W., Vovk A. Cortical and subcortical central neural pathways in respiratory sensations. Respir. Physiol. Neurobiol. 2009, 167(1):72-86.
14. Davenport P.W., Sapienza C.M., Bolser D.C. Psychophysical assessment of the urge-to-cough. Eur. Respir. Rev. 2002, 12:249-253.
15. Davenport P.W., Bolser D.C., Vickroy T., Berry R.B., Martin A.D., Hey J.A., Danzig M. The effect of codeine on the urge-to-cough response to inhaled capsaicin. Pulm. Pharmacol. Ther. 2007, 20(4):338-346.
16. Dicpinigaitis P.V., Rhoton W.A., Bhat R., Negassa A. Investigation of the urge-to-cough sensation in healthy volunteers. Respirology 2012, 17(2):337-341.
17. Dicpinigaitis P.V., Rauf K. The influence of gender on cough reflex sensitivity. Chest 1998, 113(5):1319-1321.
18. Dunkley P., Wise R.G., Fairhurst M., Hobden P., Qasim A., Chang L., Tracey I. A comparison of visceral and somatic pain processing in the human brainstem using functional magnetic resonance imaging. J. Neurosci. 2005, 25(32):7333-7341.
19. Ebihara S., Saito H., Kanda A., Nakajoh M., Takahashi H., Arai H., Sasaki H. Impaired efficacy of cough in patients with Parkinson's disease. Chest 2003, 124(3):1009-1015.
20. Evans K.C., Shea S.A., Saykin A.J. Functional MRI localisation of central nervous system regions associated with volitional inspiration in humans. J. Physiol. 1999, 520(Pt 2):383-392.
21. Evans K.C., Banzett R.B., Adams L., McKay L., Frackowiak R.S., Corfield D.R. BOLD fMRI identifies limbic, paralimbic, and cerebellar activation during air hunger. J. Neurophysiol. 2002, 88(3):1500-1511.
22. French C.L., Irwin R.S., Curley F.J., Krikorian C.J. Impact of chronic cough on quality of life. Arch. Intern. Med. 1998, 158(15):1657-1661.
23. Gracely R.H., Lota L., Walter D.J., Dubner A multiple random staircase method of psychophysical pain assessment. Pain 1988, 32(1):55-63.
24. Holzl R., Erasmus L.P., Moltner A. Detection, discrimination and sensation of visceral stimuli. Biol. Psychol. 1996, 42(1-2):199-214.
25. Jenkinson M., Bannister P., Brady M., Smith Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 2002, 17(2):825-841.
26. Liotti M., Brannan S., Egan G., Shade R., Madden L., Abplanalp B., Robillard R., Lancaster J., Zamarripa F.E., Fox P.T., Denton D. Brain responses associated with consciousness of breathlessness (air hunger). Proc. Natl. Acad. Sci. U.S.A. 2001, 98(4):2035-2040.
27. Lund T.E., Madsen K.H., Sidaros K., Luo W.L., Nichols T.E. Non-white noise in fMRI: does modelling have an impact?. Neuroimage 2006, 29(1):54-66.
28. Mazzone S.B., McLennan L., McGovern A.E., Egan G.F., Farrell M.J. Representation of capsaicin-evoked urge-to-cough in the human brain using functional magnetic resonance imaging. Am. J. Respir. Crit. Care Med. 2007, 176(4):327-332.
29. Mazzone S.B., McGovern A.E., Koo K., Farrell M.J. Mapping supramedullary pathways involved in cough using functional brain imaging: comparison with pain. Pulm. Pharmacol. Ther. 2009, 22(2):90-96.
30. Mazzone S.B., Cole L.J., Ando A., Egan G.F., Farrell M.J. Investigation of the neural control of cough and cough suppression in humans using functional brain imaging. J. Neurosci. 2011, 31(8):2948-2958.
31. Mazzone S.B., McGovern A.E., Cole L.J., Farrell M.J. Central nervous system control of cough: pharmacological implications. Curr. Opin. Pharmacol. 2011, 11(3):265-271.
32. McGarvey L., McKeagney P., Polley L., MacMahon J., Costello R.W. Are there clinical features of a sensitized cough reflex?. Pulm. Pharmacol. Ther. 2009, 22(2):59-64.
33. McGovern A.E., Davis-Poynter N., Farrell M.J., Mazzone S.B. Transneuronal tracing of airways-related sensory circuitry using herpes simplex virus 1, strain H129. Neuroscience 2012, 207:148-166.
34. McKay L.C., Adams L., Frackowiak R.S.J., Corfield D.R. A bilateral cortico-bulbar network associated with breath holding in humans, determined by functional magnetic resonance imaging. Neuroimage 2008, 40:1824-1832.
35. McKay L.C., Critchley H.D., Murphy K., Frackowiak R.S.J., Corfield Sub-cortical and brainstem sites associated with chemo-stimulated increases in ventilation in humans. Neuroimage 2010, 49(3):2526-2535.
36. Napadow V., Dhond R., Kennedy D., Hui K.K.S., Makris N. Automated brainstem co-registration (ABC) for MRI. Neuroimage 2006, 32:1113-1119.
37. Olausson H., Charron J., Marchand S., Villemure C., Strigo I.A., Bushnell M.C. Feelings of warmth correlate with neural activity in right anterior insular cortex. Neurosci. Lett. 2005, 389(1):1-5.
38. Oshiro Y., Quevedo A.S., McHaffie J.G., Kraft R.A., Coghill R.C. Brain mechanisms supporting spatial discrimination of pain. J. Neurosci. 2007, 27(13):3388-3394.
39. Oshiro Y., Quevedo A.S., McHaffie J.G., Kraft R.A., Coghill R.C. Brain mechanisms supporting discrimination of sensory features of pain: a new model. J. Neurosci. 2009, 29(47):14924-14931.
40. Pattinson K.T.S., Mitsis G.D., Harvey A.K., Jbabdi S., Dirckx S., Mayhew S.D., Rogers R., Tracey I., Wise R.G. Determination of the human brainstem respiratory control network and its cortical connections in vivo using functional and structural imaging. Neuroimage 2008, 44:295-306.
41. Pattinson K.T., Governo R.J., MacIntosh B.J., Russell E.C., Corfield D.R., Tracey I., Wise R.G. Opioids depress cortical centers responsible for the volitional control of respiration. J. Neurosci. 2009, 29(25):8177-8186.
42. Peiffer C., Poline J.B., Thivard L., Aubier M., Samson Y. Neural substrates for the perception of acutely induced dyspnea. Am. J. Respir. Crit. Care Med. 2001, 163(4):951-957.
43. Rainville P., Duncan G.H., Price D.D., Carrier B., Bushnell M.C. Pain affect encoded in human anterior cingulate but not somatosensory cortex. Science 1997, 277(5328):968-971.
44. Ramsay S.C., Adams L., Murphy K., Corfield D.R., Grootoonk S., Bailey D.L., Frackowiak R.S., Guz A. Regional cerebral blood flow during volitional expiration in man: a comparison with volitional inspiration. J. Physiol. 1993, 461:85-101.
45. Schappert S.M. National ambulatory medical care survey: 1991 summary. Vital Health Stat. 1993, 230:1-20.
46. Schön D., Rosenkranz M., Regelsberger J., Dahme B., Büchel C., von Leupoldt A. Reduced perception of dyspnea and pain after right insular cortex lesions. Am. J. Respir. Crit. Care Med. 2008, 178(11):1173-1179.
47. Schwarzacher S.W., Rüb U., Deller T. Neuroanatomical characteristics of the human pre-Bötzinger complex and its involvement in neurodegenerative brainstem diseases. Brain 2011, 134(Pt 1):24-35.
48. Simmonds D.J., Pekar J.J., Mostofsky S.H. Meta-analysis of Go/No-go tasks demonstrating that fMRI activation associated with response inhibition is task-dependent. Neuropsychologia 2008, 46(1):224-232.
49. Simonyan K., Saad Z.S., Loucks T.M., Poletto C.J., Ludlow C.L. Functional neuroanatomy of human voluntary cough and sniff production. Neuroimage 2007, 37(2):401-409.
50. Smina M., Salam A., Khamiees M., Gada P., Amoateng-Adjepong Y., Manthous C.A. Cough peak flows and extubation outcomes. Chest 2003, 124(1):262-268.
51. Smith S.M. Fast robust automated brain extraction. Hum. Brain Mapp. 2002, 17(3):143-155.
52. Stevens S.S. On the psychophysical law. Psychol. Rev. 1957, 64(3):153-181.
53. Strigo I.A., Bushnell M.C., Boivin M., Duncan G.H. Psychophysical analysis of visceral and cutaneous pain in human subjects. Pain 2002, 97(3):235-246.
54. Tölle T.R., Kaufmann T., Siessmeier T., Lautenbacher S., Berthele A., Munz F., Zieglgänsberger W., Willoch F., Schwaiger M., Conrad B., Bartenstein P. Region-specific encoding of sensory and affective components of pain in the human brain: a positron emission tomography correlation analysis. Ann. Neurol. 1999, 45(1):40-47.
55. Torebjork E. Nociceptor activation and pain. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1985, 308(1136):227-234.
56. Van den Bergh O., Van Diest I., Dupont L., Davenport P.W. On the psychology of cough. Lung 2012, 190(1):55-61.
57. von Leupoldt A., Dahme B. Cortical substrates for the perception of dyspnea. Chest 2005, 128(1):345-354.
58. von Leupoldt A., Sommer T., Kegat S., Baumann H.J., Klose H., Dahme B., Büchel C. Dyspnea and pain share emotion-related brain network. Neuroimage 2009, 48(1):200-206.
59. Widdicombe J., Eccles R., Fontana G. Supramedullary influences on cough. Respir. Physiol. Neurobiol. 2006, 152(3):320-328.
60. Wiech K., Lin C.S., Brodersen K.H., Bingel U., Ploner M., Tracey I. Anterior insula integrates information about salience into perceptual decisions about pain. J. Neurosci. 2010, 30(48):16324-16331.
61. Wise R.G., Ide K., Poulin M.J., Tracey I. Resting fluctuations in arterial carbon dioxide induce significant low frequency variations in bold signal. Neuroimage 2004, 21(4):1652-1664.
62. Worsley K.J., Evans A.C., Marrett S., Neelin P. A three-dimensional statistical analysis for CBF activation studies in human brain. J. Cereb. Blood Flow Metab. 1992, 12(6):900-918.