Neural correlates of temporal summation of second pain in the human brainstem and spinal cord

Human Brain Mapping

Volumn 36, Issue 12, 2015, Pages 5038-5050

  Bosma, Rachael L ^a   Ameli Mojarad, Elham ^a   Leung, Lawrence ^a   Pukall, Caroline ^b   Staud, Roland ^c   Stroman, Patrick W ^a,b  

^a QUEEN S UNIVERSITY   (Canada)

^b QUEEN S UNIVERSITY   (Canada)

^c UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

Brainstem; FMRI; Human; Second pain; Spinal cord; Temporal summation; Windup

Indexed keywords

ADULT; ARTICLE; BOLD SIGNAL; BRAIN ANALYSIS; BRAIN STEM RESPONSE; COMPUTED TOMOGRAPHY SCANNER; CONTROLLED STUDY; DERMATOME; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HEAT PAIN THRESHOLD; HUMAN; HUMAN EXPERIMENT; LOCUS CERULEUS; NERVE STIMULATION; NOCICEPTION; NORMAL HUMAN; PAIN; PAIN ASSESSMENT; PARABRACHIAL NUCLEUS; PERIAQUEDUCTAL GRAY MATTER; PRIORITY JOURNAL; ROSTRAL VENTROMEDIAL MEDULLA; SIXTH CERVICAL VERTEBRA; SPINAL CORD DORSAL HORN; TEMPORAL SUMMATION; TEMPORAL SUMMATION OF SECOND PAIN; THERMAL STIMULATION; WHOLE BODY MRI; ANALYSIS OF VARIANCE; BLOOD; BRAIN MAPPING; BRAIN STEM; IMAGE PROCESSING; MIDDLE AGED; NONMYELINATED NERVE; NUCLEAR MAGNETIC RESONANCE IMAGING; PAIN MEASUREMENT; PAIN THRESHOLD; PATHOLOGY; PHYSIOLOGY; QUESTIONNAIRE; REACTION TIME; SENSORY NERVE; VASCULARIZATION; YOUNG ADULT;

OXYGEN;

ADULT; AFFERENT PATHWAYS; ANALYSIS OF VARIANCE; BRAIN MAPPING; BRAIN STEM; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MIDDLE AGED; NERVE FIBERS, UNMYELINATED; OXYGEN; PAIN; PAIN MEASUREMENT; PAIN THRESHOLD; REACTION TIME; SPINAL CORD DORSAL HORN; SURVEYS AND QUESTIONNAIRES; YOUNG ADULT;

EID: 84956810580     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.22993     Document Type: Article

References (53)

1. Adriaensen H, Gybels J, Handwerker HO, Vanhees J (1984): Suppression of C-fiber discharges upon repeated heat stimulation may explain characteristics of concomitant pain sensations. Brain Res 302:203-211.
2. Anderson RJ, Craggs JG, Bialosky JE, Bishop MD, George SZ, Staud R, Robinson ME (2013): Temporal summation of second pain: Variability in responses to a fixed protocol. Eur J Pain 17:67-74.
3. Beck AT, Steer RA, Ball R, Ranieri W (1996): Comparison of Beck depression inventories-IA and -II in psychiatric outpatients. J Pers Assess 67:588-597.
4. Bosma RL, Stroman PW (2014a): Assessment of data acquisition parameters, and analysis techniques for noise reduction in spinal cord fMRI data. Magn Reson Imaging 32:473-461.
5. Bosma, RL, Stroman, PW (2014b): Spinal cord response to stepwise and block presentation of thermal stimuli: A functional MRI study. J Magn Reson Imaging 41:1318-1325.
6. 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.
7. Buhle JT, Kober H, Ochsner KN, Mende-Siedlecki P, Weber J, Hughes BL, Kross E, Atlas LY, McRae K, Wager TD (2013): Common representation of pain and negative emotion in the midbrain periaqueductal gray. Soc Cogn Affect Neurosci 8:609-616.
8. Campbell JN, LaMotte RH (1983): Latency to detection of first pain. Brain Res 266:203-208.
9. Chung JM, Kenshalo DRJ, Gerhart KD, Willis WD (1979): Excitation of primate spinothalamic neurons by cutaneous C-fiber volleys. J Neurophysiol 42:1354-1369.
10. Cohen-Adad J, Hoge RD, Leblond H, Xie G, Beaudoin G, Song AW, Krueger G, Doyon J, Benali H, Rossignol S (2009): Investigations on spinal cord fMRI of cats under ketamine. Neuroimage 44:328-339.
11. Craig AD, Andrew D (2002): Responses of spinothalamic lamina I neurons to repeated brief contact heat stimulation in the cat. J Neurophysiol 87:1902-1914.
12. Crowne DP, Marlowe D (1960): A new scale of social desirability independent of psychopathology. J Consult Psychol 24:349-354.
13. Dobek CE, Beynon ME, Bosma RL, Stroman PW (2014): Music modulation of pain perception and pain-related activity in the brain, brain stem, and spinal cord: A functional magnetic resonance imaging study. J Pain Off J Am Pain Soc 15:1057-1068.
14. Heinricher MM, Tavares I, Leith JL, Lumb BM (2009): Descending control of nociception: Specificity, recruitment and plasticity. Brain Research Reviews 60:214-225.
15. Herrero JF, Laird JM, Lopez-Garcia JA (2000): Wind-up of spinal cord neurones and pain sensation: Much ado about something? Prog Neurobiol 61:169-203.
16. Hillman P, Wall PD (1969): Inhibitory and excitatory factors influencing the receptive fields of lamina 5 spinal cord cells. Exp Brain Res 9:284-306.
17. Koltzenburg M, Handwerker HO (1994): Differential ability of human cutaneous nociceptors to signal mechanical pain and to produce vasodilatation. J Neurosci 14:1756-1765.
18. Lang J (1993): Clinical Anatomy of the Cervical Spine. New York. Thieme Medical Publishers. pp 192.
19. Lang J, Bartram CT (1982): Fila radicularia of the ventral and dorsal radices of the human spinal cord. Gegenbaurs Morphol Jahrb 128:417-462.
20. Li J, Simone DA, Larson AA (1999): Windup leads to characteristics of central sensitization. Pain 79:75-82.
21. Mendell LM (1966): Physiological properties of unmyelinated fiber projection to the spinal cord. Exp Neurol 16:316-332.
22. Mendell LM, Wall PD (1965): Responses of single dorsal cord cells to peripheral cutaneous unmyelinated fibres. Nature 206:97-99.
23. Moffitt MA, Dale BM, Duerk JL, Grill WM (2005): Functional magnetic resonance imaging of the human lumbar spinal cord. J Magn Reson Imaging, 21:527-535.
24. Myronenko A, Song XB (2009): Image registration by minimization of residual complexity. Proc Cvpr IEEE 49-56.
25. Myronenko A, Song XB (2010): Intensity-based image registration by minimizing residual complexity. IEEE Trans Med Imaging 29:1882-1891.
26. Naidich THP, Delman BN, Sorensen AG, Kollias SS, Haacke EM (2009): Internal Architecture of the Brain Stem with Key Axial Sections. Duvernoy's Atlas of the Human Brain Stem and Cerebellum. New York: Springer. pp 79-82.
27. Poline JB, Worsley KJ, Evans AC, Friston KJ (1997): Combining spatial extent and peak intensity to test for activations in functional imaging. NeuroImage 5:83-96.
28. Price DD (1972): Characteristics of second pain and flexion reflexes indicative of prolonged central summation. Exp Neurol 37:371-387.
29. Price DD, Hull CD, Buchwald NA (1971): Intracellular responses of dorsal horn cells to cutaneous and sural nerve A and C fiber stimuli. Exp Neurol 33:291.
30. Price DD, Hu JW, Dubner R, Gracely RH (1977): Peripheral suppression of first pain and central summation of second pain evoked by noxious heat pulses. Pain 3:57-68.
31. Rempe T, Wolff S, Riedel C, Baron R, Stroman PW, Jansen O, Gierthmuhlen J (2014): Spinal fMRI reveals decreased descending inhibition during secondary mechanical hyperalgesia. PLoS One 9:e112325.
32. Rempe T, Wolff S, Riedel C, Baron R, Stroman PW, Jansen O, Gierthmuhlen J (2015): Spinal and supraspinal processing of thermal stimuli: An fMRI study. J Magn Reson Imaging 41:1046-1055.
33. Robinson ME, Wise EA, Gagnon C, Fillingim RB, Price DD (2004): Influences of gender role and anxiety on sex differences in temporal summation of pain. J Pain Off J Am Pain Soc 5:77-82.
34. Spielberger CD, Gorsuch RL, Lushene R, Vagg PR, Jacobs GA (1983): Manual for the State-Trait Anxiety Inventory (STAI) (Self Evaluation Questionnaire). Palo Alto, CA: Consulting Psychologists Press.
35. Sprenger C, Eippert F, Finsterbusch J, Bingel U, Rose M, Buchel C (2012): Attention modulates spinal cord responses to pain. Curr Biol 22:1019-1022.
36. Staud R, Vierck CJ, Cannon RL, Mauderli AP, Price DD (2001): Abnormal sensitization and temporal summation of second pain (wind-up) in patients with fibromyalgia syndrome. Pain 91:165-175.
37. Staud R, Price DD, Robinson ME, Mauderli AP, Vierck CJ (2004): Maintenance of windup of second pain requires less frequent stimulation in fibromyalgia patients compared to normal controls. Pain 110:689-696.
38. Staud R, Price DD, Fillingim RB (2006): Advanced continuous-contact heat pulse design for efficient temporal summation of second pain (windup). J Pain Off J Am Pain Soc 7:575-582.
39. Staud R, Craggs JG, Robinson ME, Perlstein WM, Price DD (2007a): Brain activity related to temporal summation of C-fiber evoked pain. Pain 129:130-142.
40. Staud R, Robinson ME, Price DD (2007b): Temporal summation of second pain and its maintenance are useful for characterizing widespread central sensitization of fibromyalgia patients. J Pain Off J Am Pain Soc 8:893-901.
41. Stroman PW, Bosma RL, Tsyben A (2012): Somatotopic arrangement of thermal sensory regions in the healthy human spinal cord determined by means of spinal cord functional MRI. Magn Reson Med 68:923-931.
42. Sullivan MJL, Bishop SR, Pivik J (1995): The Pain Catastrophizing Scale: Development and validation. Psychol Assess 7:524-532.
43. Talairach J, Tournoux P. (1988) Co-planar Sterotaxic Atlas of the Human Brain. New York: Thieme Medical Publishers Inc.
44. 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.
45. Ullmann E, Pelletier Paquette JF, Thong WE, Cohen-Adad J (2014): Automatic labeling of vertebral levels using a robust template-based approach. Int J Biomed Imaging 2014:719520.
46. Valet M, Sprenger T, Boecker H, Willoch F, Rummeny E, Conrad B, Erhard P, Tolle TR (2004): Distraction modulates connectivity of the cingulo-frontal cortex and the midbrain during pain-an fMRI analysis. Pain 109:399-408.
47. Vierck CJJ, Cannon RL, Fry G, Maixner W, Whitsel BL (1997): Characteristics of temporal summation of second pain sensations elicited by brief contact of glabrous skin by a preheated thermode. J Neurophysiol 78:992-1002.
48. Wagman IH, Price DD (1969): Responses of dorsal horn cells of M. mulatta to cutaneous and sural nerve A and C fiber stimuli. J Neurophysiol 32:803-817.
49. 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, Summers P, Thompson AJ, Tracey I (2014): The current state-of-the-art of spinal cord imaging: Applications. Neuroimage 84:1082-1093.
50. Williams PL, BL, Berry MM, Collins P, Dyson M, Dussek JE, Ferguson MWJ (1995): Gray's Anatomy: The Anatomical Basis of Medicine and Surgery. New York: Churchill-Livingstone. pp 975-1011.
51. Woolf CJ, Salter MW (2000): Neuronal plasticity: Increasing the gain in pain. Science 288:1765-1769.
52. Worsley KJ, Friston KJ (1995): Analysis of fMRI time-series revisited: Again. NeuroImage 2:173-181.
53. Yu R, Gollub RL, Spaeth R, Napadow V, Wasan A, Kong J (2014): Disrupted functional connectivity of the periaqueductal gray in chronic low back pain. NeuroImage Clinical 6:100-108.