Abstract
In recent years the association of conditioned pain modulation (CPM) with trait fear and anxiety has become a hot topic in pain research due to the assumption that such variables may explain the low CPM efficiency in some individuals. However, empirical evidence concerning this association is still equivocal. Our study is the first to investigate the predictive power of fear and anxiety for CPM by using a well-established psycho-physiological measure of trait fear, i.e. startle potentiation, in addition to two self-report measures of pain-related trait anxiety. Forty healthy, pain-free participants (female: N = 20; age: M = 23.62 years) underwent two experimental blocks in counter-balanced order: (1) a startle paradigm with affective picture presentation and (2) a CPM procedure with hot water as conditioning stimulus (CS) and contact heat as test stimulus (TS). At the end of the experimental session, pain catastrophizing (PCS) and pain anxiety (PASS) were assessed. PCS score, PASS score and startle potentiation to threatening pictures were entered as predictors in a linear regression model with CPM magnitude as criterion. We were able to show an inhibitory CPM effect in our sample: pain ratings of the heat stimuli were significantly reduced during hot water immersion. However, CPM was neither predicted by self-report of pain-related anxiety nor by startle potentiation as psycho-physiological measure of trait fear. These results corroborate previous negative findings concerning the association between trait fear/anxiety and CPM efficiency and suggest that shifting the focus from trait to state measures might be promising.
Similar content being viewed by others
Notes
The IAPS identification numbers were as follows: Erotic pictures: 4652, 4659, 4660, 4670, 4687, 4695; Attack pictures: 1120, 1300, 1525, 6250.1, 6300, 6510; Pain-related pictures: 3010, 3180, 3261, 3350, 9253, 9410; Neutral pictures: 2200, 5120, 5534, 7002, 7031, 7150.
We translated the PCS into German, using a standard “forward–backward” procedure. Only if the resulting backward English version was very similar to the original version according to the evaluation of an English native speaker, translation accuracy was considered sufficient.
References
Baum C, Huber C, Schneider R, Lautenbacher S (2011) Prediction of experimental pain sensitivity by attention to pain-related stimuli in healthy individuals. Percept Mot Skills 112:926–946
Bingel U, Tracey I (2008) Imaging CNS modulation of pain in humans. Physiology 23:371–380
Blumenthal TD, Cuthbert BN, Filion DL, Hackley S, Lipp OV, Van Boxtel A (2005) Committee report: guidelines for human startle eyeblink electromyographic studies. Psychophysiology 42:1–15
Bolles RC, Fanselow MS (1980) A perceptual-defensive-recuperative model of fear and pain. Behav Brain Sci 3:291–301
Bouhassira D, Moisset X, Jouet P, Duboc H, Coffin B, Sabate JM (2013) Changes in the modulation of spinal pain processing are related to severity in irritable bowel syndrome. Neurogastroenterol Motil 25:623–e468
Daenen L, Nijs J, Roussel N, Wouters K, Van Loo M, Cras P (2013) Dysfunctional pain inhibition in patients with chronic whiplash-associated disorders: an experimental study. Clin Rheumatol 32:23–31
Dickenson AH, Le Bars D, Besson JM (1980) Diffuse noxious inhibitory controls (DNIC). Effects on trigeminal nucleus caudalis neurones in the rat. Brain Res 200:293–305
Dimova V, Horn C, Parthum A, Kunz M, Schöfer D, Carbon R, Griessinger N, Sittl R, Lautenbacher S (2013) Does severe acute pain provoke lasting changes in attentional and emotional mechanisms of pain-related processing? A longitudinal study. Pain 154:2737–2744
Farmer AD, Coen SJ, Kano M et al (2013) Psychophysiological responses to pain identify reproducible human clusters. Pain 154:2266–2276
Geva N, Defrin R (2013) Enhanced pain modulation among triathletes: a possible explanation for their exceptional capabilities. Pain 154:2317–2323
Geva N, Pruessner J, Defrin R (2014) Acute psychosocial stress reduces pain modulation capabilities in healthy men. Pain 155:2418–2425
Goodin BR, McGuire L, Allshouse M, Stapleton L, Haythornthwaite JA, Burns N, Mayes LA, Edwards RR (2009) Associations between catastrophizing and endogenous pain-inhibitory processes: sex differences. J Pain 10:180–190
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
Granovsky Y, Granot M, Nir RR, Yarnitsky D (2008) Objective correlate of subjective pain perception by contact heat-evoked potentials. J Pain 9:53–63
Grillon C (2008) Models and mechanisms of anxiety: evidence from startle studies. Psychopharmacology 199:421–437
Grosen K, Vase L, Pilegaard HK, Pfeiffer-Jensen M, Drewes AM (2014) Conditioned pain modulation and situational pain catastrophizing as preoperative predictors of pain following chest wall surgery: a prospective observational cohort study. PLoS ONE 9:e90185
Honigman L, Yarnitsky D, Sprecher E, Weissman-Fogel I (2013) Psychophysical testing of spatial and temporal dimensions of endogenous analgesia: conditioned pain modulation and offset analgesia. Exp Brain Res 228:493–501
Horn C, Blischke Y, Kunz M, Lautenbacher S (2012a) Does pain necessarily have an affective component? Negative evidence from blink reflex experiments. Pain Res Manag 17:15–24
Horn C, Schaller J, Lautenbacher S (2012b) Investigating the affective component of pain: no startle modulation by tonic heat pain in startle responsive individuals. Int J Psychophysiol 84:254–259
Horn-Hofmann C, Lautenbacher S (2015) Modulation of the startle reflex by heat pain: does threat play a role? Eur J Pain 19:216–224
Kunz M, Chatelle C, Lautenbacher S, Rainville P (2008) The relation between catastrophizing and facial responsiveness to pain. Pain 140:127–134
Lang PJ, Bradley MM, Cuthbert BN (1990) Emotion, attention, and the startle reflex. Psychol Rev 97:377–395
Lang PJ, Bradley MM, Cuthbert BN (1998) Emotion, motivation, and anxiety: brain mechanisms and psychophysiology. Biol Psychiatry 44:1248–1263
Lang PJ, Bradley MM, Cuthbert BN (2005) International affective picture system (IAPS): affective ratings of pictures and instruction manual (tech report A-6). University of Florida, Center for Research in Psychophysiology, Gainesville
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
Lautenbacher S, Kunz M, Burkhardt S (2008) The effects of DNIC-type inhibition on temporal summation compared to single pulse processing: does sex matter? Pain 140:429–435
Lautenbacher S, Huber C, Kunz M, Parthum A, Weber PG, Griessinger N, Sittl R (2009) Hypervigilance as predictor of postoperative acute pain: its predictive potency compared with experimental pain sensitivity, cortisol reactivity, and affective state. Clin J Pain 25:92–100
Lautenbacher S, Huber C, Schöfer D, Kunz M, Parthum A, Weber PG, Carbon R, Griessinger N, Sittl R (2010) Attentional and emotional mechanisms related to pain as predictors of chronic postoperative pain: a comparison with other psychological and physiological predictors. Pain 151:722–731
Le Bars D, Dickenson AH, Besson JM (1979a) Diffuse noxious inhibitory controls (DNIC). I. Effects on dorsal horn convergent neurones in the rat. Pain 6:283–304
Le Bars D, Dickenson AH, Besson JM (1979b) Diffuse noxious inhibitory controls (DNIC). II. Lack of effect on non-convergent neurones, supraspinal involvement and theoretical implications. Pain 6:305–327
Lee YC, Lu B, Edwards RR, Wasan AD, Nassikas NJ, Clauw DJ, Solomon DH, Karlson EW (2013) The role of sleep problems in central pain processing in rheumatoid arthritis. Arthritis Rheum 65:59–68
Leeuw M, Goossens ME, Linton SJ, Crombez G, Boersma K, Vlaeyen JW (2007) The fear-avoidance model of musculoskeletal pain: current state of scientific evidence. J Behav Med 30:77–94
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
Linton SJ, Nicholas MK, MacDonald S, Boersma K, Bergbom S, Maher C, Refshauge K (2011) The role of depression and catastrophizing in musculoskeletal pain. Eur J Pain 15:416–422
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
Martel MO, Wasan AD, Edwards RR (2013) Sex differences in the stability of conditioned pain modulation (CPM) among patients with chronic pain. Pain Med 14:1757–1768
Mauss IB, Robinson MD (2009) Measures of emotion: a review. Cogn Emot 23:209–237
McCracken LM, Zayfert C, Gross RT (1992) The Pain Anxiety Symptoms Scale: development and validation of a scale to measure fear of pain. Pain 50:67–73
Nahman-Averbuch H, Nir RR, Sprecher E, Yarnitsky D (2015) Psychological factors and conditioned pain modulation: a meta-analysis. Clin J Pain. doi:10.1097/AJP.0000000000000296
Nir RR, Yarnitsky D, Honigman L, Granot M (2012) Cognitive manipulation targeted at decreasing the conditioning pain perception reduces the efficacy of conditioned pain modulation. Pain 153:170–176
O’Neill S, Manniche C, Graven-Nielsen T, Arendt-Nielsen L (2014) Association between a composite score of pain sensitivity and clinical parameters in low-back pain. Clin J Pain 30:831–838
Pagé MG, Fuss S, Martin AL, Escobar EMR, Katz J (2010) Development and preliminary validation of the Child Pain Anxiety Symptoms Scale in a community sample. J Pediatr Psychol 35:1071–1082
Pielsticker A, Haag G, Zaudig M, Lautenbacher S (2005) Impairment of pain inhibition in chronic tension-type headache. Pain 118:215–223
Quartana PJ, Campbell CM, Edwards RR (2009) Pain catastrophizing: a critical review. Expert Rev Neurother 9:745–758
Rabey M, Poon C, Wray J, Thamajaree C, East R, Slater H (2015) Pro-nociceptive and anti-nociceptive effects of a conditioned pain modulation protocol in participants with chronic low back pain and healthy control subjects. Manual Ther 20:763–768
Rhudy JL, Meagher MW (2000) Fear and anxiety: divergent effects on human pain thresholds. Pain 84:65–75
Spielberger CD, Gorsuch RL, Lushene RE (1968) The State-trait anxiety inventory (STAI): test manual for form X. Consulting Psychologists Press, Palo Alto, CA
Sullivan MJ, Bishop SR, Pivik J (1995) The pain catastrophizing scale: development and validation. Psychol Assessment 7:524–532
Sullivan MJ, Thorn B, Haythornthwaite JA, Keefe F, Martin M, Bradley LA, Lefebvre JC (2001) Theoretical perspectives on the relation between catastrophizing and pain. Clin J Pain 17:52–64
Tang J, Gibson SJ (2005) A psychophysical evaluation of the relationship between trait anxiety, pain perception, and induced state anxiety. J Pain 6:612–619
Tsao JC, Seidman LC, Evans S, Lung KC, Zeltzer LK, Naliboff BD (2013) Conditioned pain modulation in children and adolescents: effects of sex and age. J Pain 14:558–567
Vaidyanathan U, Patrick CJ, Bernat EM (2009a) Startle reflex potentiation during aversive picture viewing as an indicator of trait fear. Psychophysiology 46:75–85
Vaidyanathan U, Patrick CJ, Cuthbert BN (2009b) Linking dimensional models of internalizing psychopathology to neurobiological systems: affect-modulated startle as an indicator of fear and distress disorders and affiliated traits. Psychol Bull 135:909–942
Villanueva L, Le Bars D (1994) The activation of bulbo-spinal controls by peripheral nociceptive inputs: diffuse noxious inhibitory controls. Biol Res 28:113–125
Villemure C, Schweinhardt P (2010) Supraspinal pain processing: distinct roles of emotion and attention. Neuroscientist 16:276–284
Vrana SR, Spence EL, Lang PJ (1988) The startle probe response: a new measure of emotion? J Abnorm Psychol 97:487–491
Walter B, Hampe D, Wild J, Vaitl D (2002) Die erfassung der angst vor schmerzen: eine modifizierte deutsche version der pain anxiety symptoms scale (PASS–D) [assessment of anxiety of pain: a modified German version of the pain and anxiety symptom scale (PASS–D)]. Schmerz 16:83
Weissman-Fogel I, Sprecher E, Pud D (2008) Effects of catastrophizing on pain perception and pain modulation. Exp Brain Res 186:79–85
Wiech K, Tracey I (2009) The influence of negative emotions on pain: behavioral effects and neural mechanisms. Neuroimage 47:987–994
Wilder-Smith OH, SchreyerT Scheffer GJ, Arendt-Nielsen L (2010) Patients with chronic pain after abdominal surgery show less preoperative endogenous pain inhibition and more postoperative hyperalgesia: a pilot study. J Pain Palliat Care Pharmacother 24:119–128
Yarnitsky D, Crispel Y, Eisenberg E, Granovsky Y, Ben-Nun A, Sprecher E, Best LA, Granot M (2008) Prediction of chronic post-operative pain: pre-operative DNIC testing identifies patients at risk. Pain 138:22–28
Yarnitsky D, Arendt-Nielsen L, Bouhassira D, Edwards RR, Fillingim RB, Granot M, Hansson P, Lautenbacher S, Wilder-Smith O Marchand S (2010) Recommendations on terminology and practice of psychophysical DNIC testing. Eur J Pain 14:339
Yarnitsky D, Granot M, Granovsky Y (2014) Pain modulation profile and pain therapy: between pro-and antinociception. Pain 155:663–665
Yarnitsky D, Bouhassira D, Drewes AM, Fillingim RB, Granot M, Hansson P, Lautenbacher S, Marchand S, Wilder-Smith O (2015) Recommendations on practice of conditioned pain modulation (CPM) testing. Eur J Pain 19:805–806
Acknowledgments
This study was supported by a research grant from the Deutsche Forschungsgemeinschaft (La 685/13-1).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
There are no conflicts of interest.
Informed consent
Informed consent was obtained from all individual participants included in the study.
Rights and permissions
About this article
Cite this article
Horn-Hofmann, C., Priebe, J.A., Schaller, J. et al. Lack of predictive power of trait fear and anxiety for conditioned pain modulation (CPM). Exp Brain Res 234, 3649–3658 (2016). https://doi.org/10.1007/s00221-016-4763-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-016-4763-9