Spinal cord-midbrain functional connectivity is related to perceived pain intensity: A combined spino-cortical fMRI study

Journal of Neuroscience

Volumn 35, Issue 10, 2015, Pages 4248-4257

  Sprenger, Christian ^a   Finsterbusch, Jürgen ^a   Büchel, Christian ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

fMRI; Functional connectivity; PAG; Pain; Spinal cord

Indexed keywords

ADULT; AMYGDALOID NUCLEUS; ARTICLE; BOLD SIGNAL; BRAIN REGION; CHRONIC PAIN; CONNECTOME; CORPUS STRIATUM; DATA PROCESSING; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GRAY MATTER; HUMAN; HUMAN EXPERIMENT; HYPOTHALAMUS; IMAGE QUALITY; IMAGE RECONSTRUCTION; INSULA; MALE; MESENCEPHALON; NERVE CONDUCTION; NEUROIMAGING; NORMAL HUMAN; PAIN INTENSITY; PRIORITY JOURNAL; SIXTH CERVICAL VERTEBRA; SOMATOSENSORY CORTEX; SPINAL CORD; SPINAL CORD DORSAL HORN; THALAMUS; THERMAL STIMULATION; ADVERSE EFFECTS; BIOPHYSICS; BLOOD; BRAIN; HEAT; IMAGE PROCESSING; NERVE TRACT; NUCLEAR MAGNETIC RESONANCE IMAGING; PAIN MEASUREMENT; PAIN THRESHOLD; PHYSIOLOGY; STIMULATION; VASCULARIZATION; YOUNG ADULT;

OXYGEN;

ADULT; BIOPHYSICS; BRAIN; FEMALE; HOT TEMPERATURE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; NEURAL PATHWAYS; OXYGEN; PAIN MEASUREMENT; PAIN THRESHOLD; PHYSICAL STIMULATION; SPINAL CORD; YOUNG ADULT;

EID: 84924514456     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4897-14.2015     Document Type: Article

References (67)

1. Apkarian AV, Bushnell MC, Treede RD, Zubieta JK (2005) Human brain mechanisms of pain perception and regulation in health and disease. Eur J Pain 9:463–484.
2. Arfanakis K, Cordes D, Haughton VM, Moritz CH, Quigley MA, Meyerand ME (2000) Combining independent component analysis and correlation analysis to probe interregional connectivity in fMRI task activation datasets. Magn Reson Imaging 18:921–930.
3. Ashburner J, Friston KJ (2005) Unified segmentation. Neuroimage 26:839-851.
4. Barry RL, Smith SA, Dula AN, Gore JC (2014) Resting state functional connectivity in the human spinal cord. Elife 3:e02812.
5. Birn RM (2012) The role of physiological noise in resting-state functional connectivity. Neuroimage 62:864–870.
6. Blamire AM, Rothman DL, Nixon T (1996) Dynamic shim updating: a new approach towards optimized whole brain shimming. Magn Reson Med 36:159–165.
7. Brooks JC, Beckmann CF, Miller KL, Wise RG, Porro CA, Tracey I, Jenkinson M (2008) Physiological noise modelling for spinal functional magnetic resonance imaging studies. Neuroimage 39:680–692.
8. Brooks JC, Kong Y, Lee MC, Warnaby CE, Wanigasekera V, Jenkinson M, Tracey I (2012) Stimulus site and modality dependence of functional activity within the human spinal cord. J Neurosci 32:6231–6239.
9. Brooks JCW (2014) Physiological noise modeling and analysis for spinal cord fMRI. In: Quantitative MRI of the spinal cord, Ed 1, pp 240–257. Amsterdam: Elsevier.
10. Büchel C, Geuter S, Sprenger C, Eippert F (2014) Placebo analgesia: a predictive coding perspective. Neuron 81:1223–1239.
11. Cadotte DW, Cadotte A, Cohen-Adad J, Fleet D, Livne M, Mikulis D, Fehlings MG (2014) Resolving the anatomic variability of the human cervical spinal cord: a solution to facilitate advanced neural imaging. International Society for Magnetic Resonance in Medicine, Milan, Italy.
12. Collignon A, Maes F, Delaere D, Vandermeulen D, Suetens P, Marchal G (1995) Automated multi-modality image registration based on information theory. In: Proceedings of the XIVth International Conference on Information Processing in Medical Imaging. Computation imaging vision, Vol 3, pp. 263–274. Boston: Kluwer Academic.
13. Cooke FJ, Blamire AM, Manners DN, Styles P, Rajagopalan B (2004) Quantitative proton magnetic resonance spectroscopy of the cervical spinal cord. Magn Reson Med 51:1122–1128.
14. DaSilva AF, Becerra L, Makris N, Strassman AM, Gonzalez RG, Geatrakis N, Borsook D (2002) Somatotopic activation inthe human trigeminal pain pathway. J Neurosci 22:8183–8192.
15. Deckers RH, van Gelderen P, Ries M, Barret O, Duyn JH, Ikonomidou VN, Fukunaga M, Glover GH, de Zwart JA (2006) An adaptive filter for suppression of cardiac and respiratory noise in MRI time series data. Neuro-image 33:1072–1081.
16. Eippert F, Finsterbusch J, Bingel U, Büchel C (2009) Direct evidence for spinal cord involvement in placebo analgesia. Science 326:404.
17. Fair DA, Schlaggar BL, Cohen AL, Miezin FM, Dosenbach NU, Wenger KK, Fox MD, Snyder AZ, Raichle ME, Petersen SE (2007) A method for using blocked and event-related fMRI data to study “resting state” functional connectivity. Neuroimage 35:396–405.
18. Fields H (2004) State-dependent opioid control of pain. Nat Rev Neurosci 5:565–575.
19. Finsterbusch J, Eippert F, Büchel C (2012) Single, slice-specific z-shim gradient pulses improve T2*-weighted imaging of the spinal cord. Neuroim-age 59:2307–2315.
20. Finsterbusch J, Sprenger C, Büchel C (2013) Combined T2*-weighted measurements of the human brain and cervical spinal cord with a dynamic shim update. Neuroimage 79:153–161.
21. Friston KJ, Buechel C, Fink GR, Morris J, Rolls E, Dolan RJ (1997) Psycho-physiological and modulatory interactionsinneuroimaging. Neuroimage 6:218–229.
22. Friston KJ, Harrison L, Penny W (2003) Dynamic causal modelling. Neuro-image 19:1273–1302.
23. Geuter S, Büchel C (2013) Facilitation of pain in the human spinal cord by nocebo treatment. J Neurosci 33:13784–13790.
24. Giove F, Garreffa G, Giulietti G, Mangia S, Colonnese C, Maraviglia B (2004) Issues about the fMRI of the human spinal cord. Magn Reson Imaging 22:1505–1516.
25. Granger CW (1969) Investigating causal relations by econometric models and cross-spectral methods. Econometrica 37:424–438.
26. Heinricher MM, Tavares I, Leith JL, Lumb BM (2009) Descending control of nociception: specificity, recruitment and plasticity. Brain Res Rev 60: 214–225.
27. Kim JH, Lee CW, Chun KS, Shin WH, Bae HG, Chang JC (2012) Morpho-metric relationship between the cervicothoracic cord segments and vertebral bodies. J Korean Neurosurg Soc 52:384–390.
28. Komisaruk BR, Mosier KM, Liu WC, Criminale C, Zaborszky L, Whipple B,Kalnin A (2002) Functional localization ofbrainstem and cervical spinal cord nuclei in humans with fMRI. AJNR Am J Neuroradiol 23:609–617.
29. Kong Y, Jenkinson M, Andersson J, Tracey I, Brooks JC (2012) Assessment of physiological noise modelling methods for functional imaging of the spinal cord. Neuroimage 60:1538–1549.
30. Le Bars D (2002) The whole body receptive field of dorsal horn multirecep-tive neurones. Brain Res Brain Res Rev 40:29–44.
31. Lee MW, McPhee RW, Stringer MD (2008) An evidence-based approach to human dermatomes. Clin Anat 21:363–373.
32. Legrain V, Iannetti GD, Plaghki L, Mouraux A (2011) The pain matrix reloaded: a salience detection system for the body. Prog Neurobiol 93:111-124.
33. Maieron M, Iannetti GD, Bodurka J, Tracey I, Bandettini PA, Porro CA (2007) Functional responsesinthe human spinal cord during willed motor actions: evidence for side-and rate-dependent activity. J Neurosci 27: 4182–4190.
34. Mainero C, Zhang WT, Kumar A, Rosen BR, Sorensen AG (2007) Mapping the spinal and supraspinal pathways of dynamic mechanical allodynia in the human trigeminal system using cardiac-gated fMRI. Neuroimage 35: 1201–1210.
35. Mainero C, Boshyan J, Hadjikhani N (2011) Altered functional magnetic resonance imaging resting-state connectivity in periaqueductal gray networks in migraine. Ann Neurol 70:838–845.
36. Millan MJ (2002) Descending control of pain. Prog Neurobiol 66:355–474.
37. Moriishi J, Otani K, Tanaka K, Inoue S (1989) The intersegmental anastomoses between spinal nerve roots. Anat Rec 224:110–116.
38. Morrell G, Spielman D (1997) Dynamic shimming for multi-slice magnetic resonance imaging. Magn Reson Med 38:477–483.
39. Nash P, Wiley K, Brown J, Shinaman R, Ludlow D, Sawyer AM, Glover G, Mackey S (2013) Functional magnetic resonance imaging identifies so-matotopic organization of nociception in the human spinal cord. Pain 154:776–781.
40. Nichols TE, Holmes AP (2002) Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp 15:1–25.
41. Peyron R, Laurent B, García-Larrea L (2000) Functional imaging of brain responses to pain. A review and meta-analysis (2000). Neurophysiol Clin 30:263–288.
42. Piché M, Cohen-Adad J, Nejad MK, Perlbarg V, Xie G, Beaudoin G, Benali H, Rainville P (2009) Characterization of cardiac-related noise in fMRI of the cervical spinal cord. Magn Reson Imaging 27:300–310.
43. Poldrack RA, Mumford JA, Nichols TE (2011) Handbook of functional MRI data analysis. New York: Cambridge UP.
44. Porreca F, Ossipov MH, Gebhart GF (2002) Chronic pain and medullary descending facilitation. Trends Neurosci 25:319–325.
45. Reynolds DV (1969) Surgery in the rat during electrical analgesia induced by focal brain stimulation. Science 164:444–445.
46. Rolke R, Baron R, Maier C, Tölle TR, Treede RD, Beyer A, Binder A, Birbaumer N, Birklein F, Bötefür IC, Braune S, Flor H, Huge V, Klug R, Landwehrmeyer GB, Magerl W, Maihöfner C, Rolko C, Schaub C, Sche-rens A, et al. (2006) Quantitative sensory testing in the German Research NetworkonNeuropathic Pain (DFNS): standardized protocol and reference values. Pain 123:231–243.
47. Schoell ED, Bingel U, Eippert F, Yacubian J, Christiansen K, Andresen H, May A, Buechel C (2010) The effectofopioid receptor blockade onthe neural processing of thermal stimuli. PLoS One 5:e12344.
48. Schroth G, Klose U (1992a) Cerebrospinal fluid flow. I. Physiology of cardiac-related pulsation. Neuroradiology 35:1–9.
49. Schroth G, Klose U (1992b) Cerebrospinal fluid flow. II. Physiology of respiration-related pulsations. Neuroradiology 35:10–15.
50. Smith SM, Nichols TE (2009) Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage 44:83–98.
51. Smith SM, Miller KL, Salimi-Khorshidi G, Webster M, Beckmann CF, Nichols TE, Ramsey JD, Woolrich MW (2011) Network modelling methods for fMRI. Neuroimage 54:875–891.
52. Sprenger C, Bingel U, Büchel C (2011) Treating pain with pain: supraspinal mechanisms of endogenous analgesia elicited by heterotopic noxious conditioning stimulation. Pain 152:428–439.
53. Sprenger C, Eippert F, Finsterbusch J, Bingel U, Rose M, Büchel C (2012) Attention modulates spinal cord responses to pain. Curr Biol 22:1019-1022.
54. Stankewitz A, Voit HL, Bingel U, Peschke C, May A (2010) A new trigemino-nociceptive stimulation model for event-related fMRI. Ceph-alalgia 30:475–485.
55. Stroman PW (2005) Magnetic resonance imaging of neuronal function in the spinal cord: spinal FMRI. Clin Med Res 3:146–156.
56. Stroman PW, Wheeler-Kingshott C, Bacon M, Schwab JM, Bosma R, Brooks J, Cadotte D, Carlstedt T, Ciccarelli O, Cohen-Adad J, Curt A, Evangelou N, Fehlings MG, Filippi M, Kelley BJ, Kollias S, Mackay A, Porro CA, Smith S, Strittmatter SM, et al. (2014) The current state-of-the-art of spinal cord imaging: methods. Neuroimage 84:1070–1081.
57. Summers PE, Ferraro D, Duzzi D, Lui F, Iannetti GD, Porro CA (2010) A quantitative comparison of BOLD fMRI responses to noxious and innocuous stimuli in the human spinal cord. Neuroimage 50:1408–1415.
58. Summers PE, Brooks JCW, Cohen-Adad J (2014) Spinal cord fMRI. In: Quantitative MRI of the spinal cord (Cohen-Adad J, Wheeler-Kingshott C, eds), pp 221–239. San Diego, CA: Academic.
59. Todd AJ (2010) Neuronal circuitry for pain processing in the dorsal horn. Nat Rev Neurosci 11:823–836.
60. Tracey I, Ploghaus A, Gati JS, Clare S, Smith S, Menon RS, Matthews PM (2002) Imaging attentional modulation of pain in the periaqueductal gray in humans. J Neurosci 22:2748–2752.
61. Verma T, Cohen-Adad J (2014) Effect of respiration on the B0 field in the human spinal cord at 3T. Magn Reson Med 72:1629–1636.
62. Villanueva L, Le Bars D (1995) The activation of bulbo-spinal controls by peripheral nociceptive inputs: diffuse noxious inhibitory controls. Biol Res 28:113–125.
63. Wager TD, Atlas LY, Lindquist MA, Roy M, Woo CW, Kross E (2013) An fMRI-based neurologic signature of physical pain. N Engl J Med 368: 1388–1397.
64. Wheeler-Kingshott CA, Stroman PW, Schwab JM, Bacon M, Bosma R, Brooks J, Cadotte DW, Carlstedt T, Ciccarelli O, Cohen-Adad J, Curt A, Evangelou N, Fehlings MG, Filippi M, Kelley BJ, Kollias S, Mackay A, Porro CA, Smith S, Strittmatter SM, et al. (2014) The current state-of-the-art of spinal cord imaging: applications. Neuroimage 84:1082–1093.
65. Wiech K, Ploner M, Tracey I (2008) Neurocognitive aspects of pain perception. Trends Cogn Sci 12:306–313.
66. Willis WD Jr (2007) The somatosensory system, with emphasis on structures important for pain. Brain Res Rev 55:297–313.
67. Worsley KJ, Evans AC, Marrett S, Neelin P (1992) A three-dimensional statistical analysis for CBF activation studies in human brain. J Cereb Blood Flow Metab 12:900–918.