Abstract
Measures of sensory and cognitive inhibition were obtained from university students with and without a history of chronic pain. The form of sensory inhibition measured was diffuse noxious inhibitory controls (DNIC), the capacity of a painful stimulus to reduce the subjective intensity of a second stimulus delivered to a remote body site. To measure cognitive inhibition, the Stroop effect was used. Participants with a history of chronic pain showed less DNIC (i.e., less sensory inhibition) than the healthy controls, but had a smaller Stroop effect (indicating greater cognitive inhibition). The fact that chronic pain history is associated with opposite changes in these two measures casts doubt on the view that the two inhibitory processes are related. Scores on each experimental measure were equivalent in pain-history subjects with ongoing chronic pain and those whose chronic pain had resolved. This equivalence suggests that chronic pain in childhood or adolescence may have lingering effects on sensory and cognitive inhibition.
Similar content being viewed by others
References
Apkarian AV, Sosa Y, Krauss BR, Thomas PS, Fredrickson BE, Levy RE, Harden RN, Chialvo DR (2004) Chronic pain patients are impaired on an emotional decision-making task. Pain 108:129–136. https://doi.org/10.1016/j.pain.2003.12.015
Arendt-Nielsen L, Nie H, Laursen MB, Laursen BS, Madeleine P, Simonsen OH, Graven-Nielsen T (2010) Sensitization in patients with painful knee osteoarthritis. Pain 149:573–581. https://doi.org/10.1016/j.pain.2010.04.003
Augustinova M, Clarys D, Spatola N, Ferrand L (2018) Some further clarifications on age-related differences in Stroop interference. Psychon Bull Rev 25:767–774. https://doi.org/10.3758/s13423-017-1427-0
Bouwense SA, Ali UA, ten Broek RP, Issa Y, van Eijck CH, Wilder-Smith OH, van Goor H (2013) Altered central pain processing after pancreatic surgery for chronic pancreatitis. Br J Surg 100:1797–1804. https://doi.org/10.1002/bjs.9322
Bugg JM, DeLosh EL, Davalos DB, Davis HP (2007) Age differences in Stroop interference: contributions of general slowing and task-specific deficits. Aging Neuropsychol Cogn 14:155–167. https://doi.org/10.1080/138255891007065
Coggeshall RE, Lekan HA, White FA, Woolf CJ (2001) A-fiber sensory input induces neuronal cell death in the dorsal horn of the adult rat spinal cord. J Comp Neurol 435:276–282. https://doi.org/10.1002/cne.1029
de Lussanet MHE, Behrendt F, Puta C, Weiss T, Lappe M, Schulte TL, Wagner H (2012) A body-part-specific impairment in the visual recognition of actions in chronic pain patients. Pain 153:1459–1466. https://doi.org/10.1016/j.pain.2012.04.002
Edwards RR, Fillingim RB, Ness TJ (2003) Age-related differences in endogenous pain modulation: a comparison of diffuse noxious inhibitory controls in healthy older and younger adults. Pain 101:155–165. https://doi.org/10.1016/S0304-3959(02)00324-X
Garrett PH, Sarlani E, Grace EG, Greenspan JD (2013) Chronic temporomandibular disorders are not necessarily associated with a compromised endogenous analgesic system. J Orofac Pain 27:142–150. https://doi.org/10.11607/jop.943
Gerhardt A, Eich W, Treede R-D, Tesarz J (2017) Conditioned pain modulation in patients with nonspecific chronic back pain with chronic local pain, chronic widespread pain, and fibromyalgia. Pain 158:430–439. https://doi.org/10.1097/j.pain.0000000000000777
Granot M, Weissman-Fogel I, Crispel Y, Pud D, Granovsky Y, Sprecher E, Yarnitsky D (2008) Determinants of endogenous analgesia magnitude in a diffuse noxious inhibitory control (DNIC) paradigm: do conditioning stimulus painfulness, gender and personality variables matter? Pain 136:142–149. https://doi.org/10.1016/j.pain.2007.06.029
Graven-Nielsen T, Wodehouse T, Langford RM, Arendt-Nielsen L, Kidd BL (2012) Normalization of widespread hyperesthesia and facilitated spatial summation of deep-tissue pain in knee osteoarthritis patients after knee replacement. Arthritis Rheum 64:2907–2916. https://doi.org/10.1002/art.34466
Harper DE, Hollins M (2012) Is touch gating due to sensory or cognitive interference? Pain 153:1082–1090. https://doi.org/10.1016/j.pain.2012.02.011
Hollins M, Harper D, Gallagher S, Owings EW, Lim PF, Miller V, Siddiqi MQ, Maixner W (2009) Perceived intensity and unpleasantness of cutaneous and auditory stimuli: an evaluation of the generalized hypervigilance hypothesis. Pain 141:215–221. https://doi.org/10.1016/j.pain.2008.10.003
Inquimbert P, Moll M, Latremoliere A, Tong CK, Whang J, Sheehan GF, Smith BM, Korb E, Athié MCP, Babaniyi O, Ghasemlou N, Yanagawa Y, Allis CD, Hof PR, Scholz J (2018) NMDA receptor activation underlies the loss of spinal dorsal horn neurons and the transition to persistent pain after peripheral nerve injury. Cell Rep 23:2678–2689. https://doi.org/10.1016/j.celrep.2018.04.107
Julien N, Goffaux P, Arsenault P, Marchand S (2005) Widespread pain in fibromyalgia is related to a deficit of endogenous pain inhibition. Pain 114:295–302. https://doi.org/10.1016/j.pain.2004.12.032
Kass RE, Raftery AE (1995) Bayes factors. J Am Stat Assoc 90:773–795
Khasabov SG, Cain DM, Thong D, Mantyh PW, Simone DA (2001) Enhanced responses of spinal dorsal horn neurons to heat and cold stimuli following mild freeze injury to the skin. J Neurophysiol 86:986–996. https://doi.org/10.1152/jn.2001.86.2.986
King CD, Wong F, Currie T, Mauderli AP, Fillingim RB, Riley JL (2009) Deficiency in endogenous modulation of prolonged heat pain in patients with irritable bowel syndrome and temporomandibular disorder. Pain 143:172–178. https://doi.org/10.1016/j.pain.2008.12.027
Kosek E, Hansson P (1997) Modulatory influence on somatosensory perception from vibration and heterotopic noxious conditioning stimulation (HNCS) in fibromyalgia patients and healthy subjects. Pain 70:41–51. https://doi.org/10.1016/S0304-3959(96)03295-2
Kosek E, Ordeberg G (2000) Lack of pressure pain modulation by heterotopic noxious conditioning stimulation in patients with painful osteoarthritis before, but not following, surgical pain relief. Pain 88:69–78. https://doi.org/10.1016/S0304-3959(00)00310-9
Lautenbacher S, Rollman GB (1997) Possible deficiencies of pain modulation in fibromyalgia. Clin J Pain 13:189–196
Lautenbacher S, Roscher S, Strian F (2002) Inhibitory effects do not depend on the subjective experience of pain during heterotopic noxious conditioning stimulation (HNCS): a contribution to the psychophysics of pain inhibition. Eur J Pain 6:365–374. https://doi.org/10.1016/S1090-3801(02)00030-7
Le Bars D, Dickenson AH, Besson J-M (1979) Diffuse noxious inhibitory controls (DNIC). I. Effects on dorsal horn convergent neurones in the rat. Pain 6:283–304. https://doi.org/10.1016/0304-3959(79)90049-6
Lewis GN, Rice DA, McNair PJ (2012) Conditioned pain modulation in populations with chronic pain: a systematic review and meta-analysis. J Pain 13:936–944. https://doi.org/10.1016/j.jpain.2012.07.005
Marouf R, Caron S, Lussier M, Bherer L, Piché M, Rainville P (2014) Reduced pain inhibition is associated with reduced cognitive inhibition in healthy aging. Pain 155:494–502. https://doi.org/10.1016/j.pain.2013.11.011
McCracken LM (1997) "Attention" to pain in persons with chronic pain: a behavioral approach. Behav Ther 28:271–284. https://doi.org/10.1016/S0005-7894(97)80047-0
McDermid AJ, Rollman GB, McCain GA (1996) Generalized hypervigilance in fibromyalgia: evidence of perceptual amplification. Pain 66:133–144. https://doi.org/10.1016/0304-3959(96)03059-X
Miron D, Duncan GH, Bushnell MC (1989) Effects of attention on the intensity and unpleasantness of thermal pain. Pain 39:345–352. https://doi.org/10.1016/0304-3959(89)90048-1
Mullis A (2011) Chronic pain, music, and cognition. Undergraduate honors thesis. Department of Psychology, University of North Carolina at Chapel Hill, Chapel Hill
Neziri AY, Haesler S, Petersen-Felix S, Müller M, Arendt-Nielsen L, Manresa JB, Andersen OK, Curatolo M (2010) Generalized expansion of nociceptive reflex receptive fields in chronic pain patients. Pain 151:798–805. https://doi.org/10.1016/j.pain.2010.09.017
Olesen SS, Brock C, Krarup AL, Funch-Jensen P, Arendt-Nielsen L, Wilder-Smith OH, Drewes AM (2010) Descending inhibitory pain modulation is impaired in patients with chronic pancreatitis. Clin Gastroenterol Hepatol 8:724–730. https://doi.org/10.1016/j.cgh.2010.03.005
Oosterman JM, Derksen LC, van Wijck AJM, Kessels RPC, Veldhuijzen DS (2012) Executive and attentional functions in chronic pain: Does performance decrease with increasing task load? Pain Res Manag 17:159–165. https://doi.org/10.1155/2012/962786
Peng H, Gao Y, Mao X (2017) The roles of sensory function and cognitive load in age differences in inhibition: evidence from the Stroop task. Psychol Aging 32:42–50. https://doi.org/10.1037/pag0000149
Pennebaker JW (1982) The psychology of physical symptoms. Springer-Verlag, New York
Piché M, Bouin M, Arsenault M, Poitras P, Rainville P (2011) Decreased pain inhibition in irritable bowel syndrome depends on altered descending modulation and higher-order brain processes. Neurosci 195:166–175. https://doi.org/10.1016/j.neuroscience.2011.08.040
Pielsticker A, Haag G, Zaudig M, Lautenbacher S (2005) Impairment of pain inhibition in chronic tension-type headache. Pain 118:215–223. https://doi.org/10.1016/j.pain.2005.08.019
Popescu A, LeResche L, Truelove EL, Drangsholt MT (2010) Gender differences in pain modulation by diffuse noxious inhibitory controls: a systematic review. Pain 150:309–318. https://doi.org/10.1016/j.pain.2010.05.013
Price DD, Dubner R (1977) Neurons that subserve the sensory-discriminative aspects of pain. Pain 3:307–338. https://doi.org/10.1016/0304-3959(77)90063-X
Pud D, Granovsky Y, Yarnitsky D (2009) The methodology of experimentally induced diffuse noxious inhibitory control (DNIC)-like effect in humans. Pain 144:16–19. https://doi.org/10.1016/j.pain.2009.02.015
Sandrini G, Rossi P, Milanov I, Serrao M, Cecchini AP, Nappi G (2006) Abnormal modulatory influence of diffuse noxious inhibitory controls in migraine and chronic tension-type headache patients. Cephalalgia 26:782–789. https://doi.org/10.1111/j.1468-2982.2006.01130.x
Sarlani E, Greenspan JD (2003) Evidence for generalized hyperalgesia in temporomandibular disorders patients. Pain 102:221–226. https://doi.org/10.1016/S0304-3959(03)00095-2
Schmidt NB, Lerew DR, Trakowski JH (1997) Body vigilance in panic disorder: evaluating attention to bodily perturbations. J Consult Clin Psychol 65:214–220. https://doi.org/10.1037/0022-006X.65.2.214
Staud R, Robinson ME, Vierck CJ Jr, Price DD (2003) Diffuse noxious inhibitory controls (DNIC) attenuate temporal summation of second pain in normal males but not in normal females or fibromyalgia patients. Pain 101:167–174. https://doi.org/10.1016/S0304-3959(02)00325-1
Staud R, Vierck CJ, Robinson ME, Price DD (2004) Spatial summation of heat pain within and across dermatomes in fibromyalgia patients and pain-free subjects. Pain 111:342–350. https://doi.org/10.1016/j.pain.2004.07.015
Stroop JR (1935) Studies of interference in serial verbal reactions. J Exp Psychol 18:643–662
Suhr JA (2003) Neuropsychological impairment in fibromyalgia: Relation to depression, fatigue, and pain. J Psychosom Res 55:321–329. https://doi.org/10.1016/S0022-3999(02)00628-1
Sullivan MJL, Bishop SR, Pivik J (1995) The pain catastrophizing scale: development and validation. Psychol Assess 7:524–532. https://doi.org/10.1037/1040-3590.7.4.524
Treede R-D, Rief W, Barke A, Aziz Q, Bennett MI, Benoliel R, Wang SJ (2019) Chronic pain as a symptom or a disease: the IASP classification of chronic pain for the International Classification of Diseases (ICD-11). Pain 160:19–27
Turner ML, Engle RW (1989) Is working memory capacity task dependent? J Mem Lang 28:127–154
Unsworth N, Heitz RP, Schrock JC, Engle RW (2005) An automated version of the operation span task. Behav Res Methods 37:498–505. https://doi.org/10.3758/BF03192720
Van Hees J, Gybels J (1981) C nociceptor activity in human nerve during painful and non painful skin stimulation. J Neurol Neurosurg Psychiatry 44:600–607. https://doi.org/10.1136/jnnp.44.7.600
Veldhuijzen DS, Sondaal FV, Oosterman JM (2012) Intact cognitive inhibition in patients with fibromyalgia but evidence of declined processing speed. J Pain 13:507–515. https://doi.org/10.1016/j.jpain.2012.02.011
Wilder-Smith CH, Schindler D, Lovblad K, Redmond SM, Nirkko A (2004) Brain functional magnetic resonance imaging of rectal pain and activation of endogenous inhibitory mechanisms in irritable bowel syndrome patient subgroups and healthy controls. Gut 53:1595–1601. https://doi.org/10.1136/gut.2003.028514
Willer JC, Roby A, Le Bars D (1984) Psychophysical and electrophysiological approaches to the pain-relieving effects of heterotopic nociceptive stimuli. Brain 107:1095–1112. https://doi.org/10.1093/brain/107.4.1095
Yarnitsky D, Crispel Y, Eisenberg E, Granovsky Y, Ben-Nun A, Sprecher E, Best L-A, Granot M (2008) Prediction of chronic post-operative pain: pre-operative DNIC testing identifies patients at risk. Pain 138:22–28. https://doi.org/10.1016/j.pain.2007.10.033
Acknowledgements
The authors are grateful to Zack Fisher for advice on Bayesian analysis, and to Samuel Brotkin for laboratory assistance. This study was supported by a Lindquist Award from the UNC College of Arts and Sciences, and by a Dunlevie Honors Research Award to DT.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design, to preparation of materials, and to data analysis. Data Collection was carried out by CB and DT. The first draft of the manuscript was written by MH; all authors commented on drafts of the manuscript, and read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Additional information
Communicated by Melvyn A. Goodale.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Hollins, M., Bryen, C.P. & Taylor, D. Effects of chronic pain history on perceptual and cognitive inhibition. Exp Brain Res 238, 321–332 (2020). https://doi.org/10.1007/s00221-019-05715-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-019-05715-8