Perceptual and motor responses directly and indirectly mediate the effects of noxious stimuli on autonomic responses.
Journal
Pain
ISSN: 1872-6623
Titre abrégé: Pain
Pays: United States
ID NLM: 7508686
Informations de publication
Date de publication:
12 2019
12 2019
Historique:
pubmed:
25
7
2019
medline:
29
8
2020
entrez:
24
7
2019
Statut:
ppublish
Résumé
Autonomic responses are an essential component of pain. They serve its adaptive function by regulating homeostasis and providing resources for protective and recuperative responses to noxious stimuli. To be adaptive and flexible, autonomic responses are not only determined by noxious stimulus characteristics, but likely also shaped by perceptual and motor responses to noxious stimuli. However, it is not fully known how noxious stimulus characteristics, perceptual responses, and motor responses interact in shaping autonomic responses. To address this question, we collected perceptual, motor, and autonomic responses to brief noxious laser stimuli of different intensities in 47 healthy human participants. Multilevel 2-path mediation analyses revealed that perceptual, but not motor responses mediated the translation of noxious stimuli into autonomic responses. Multilevel 3-path mediation analyses further specified that motor responses indirectly related to autonomic responses through their close association with perceptual responses. These findings confirm that autonomic responses are not only a reflexive reaction to noxious stimuli, but directly and indirectly shaped by perceptual and motor responses, respectively. These effects of motor and perceptual processes on autonomic responses likely allow for the integration of contextual processes into protective and regulatory autonomic responses, aiding adaptive and flexible coping with threat.
Identifiants
pubmed: 31335751
doi: 10.1097/j.pain.0000000000001661
pii: 00006396-201912000-00014
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2811-2818Références
Atlas LY, Bolger N, Lindquist MA, Wager TD. Brain mediators of predictive cue effects on perceived pain. J Neurosci 2010;30:12964–77.
Baron RM, Kenny DA. The moderator-mediator variable distinction in social psychological research: conceptual, strategic, and statistical considerations. J Pers Soc Psychol 1986;51:1173–82.
Bollen KA, Stine R. Direct and indirect effects: classical and bootstrap estimates of variability. Sociological Methodol 1990;20:115–40.
Bolles RC, Fanselow MS. A perceptual-defensive-recuperative model of fear and pain. Behav Brain Sci 1980;3:291–301.
Boucsein W. Electrodermal activity. New York: Springer, 2012.
Burton AR, Fazalbhoy A, Macefield VG. Sympathetic responses to noxious stimulation of muscle and skin. Front Neurol 2016;7:109.
Chapman CR, Bradshaw DH, Donaldson GW, Jacobson RC, Nakamura Y. Central noradrenergic mechanisms and the acute stress response during painful stimulation. J Psychopharmacol 2014;28:1135–42.
Cortelli P, Giannini G, Favoni V, Cevoli S, Pierangeli G. Nociception and autonomic nervous system. Neurol Sci 2013;34(suppl 1):S41–6.
Critchley HD. Electrodermal responses: what happens in the brain. Neuroscientist 2002;8:132–42.
Damasio A, Carvalho GB. The nature of feelings: evolutionary and neurobiological origins. Nat Rev Neurosci 2013;14:143–52.
Dawson ME, Schell AM, Filion DL. The electrodermal system. In: Cacioppo JT, Tassinary LG, Berntson GG, editors. Handbook of psychophysiology. Cambridge: Cambridge University Press, 2017. pp. 217–43.
Donaldson GW, Chapman CR, Nakamura Y, Bradshaw DH, Jacobson RC, Chapman CN. Pain and the defense response: structural equation modeling reveals a coordinated psychophysiological response to increasing painful stimulation. PAIN 2003;102:97–108.
Edelberg R. Electrical properties of the skin. In: Brown C, editor. Methods in psychophysiology. Baltimore: Williams & Wilkins, 1967. pp. 1–53.
Efron B, Tibshirani R. An introduction to the bootstrap. New York: Chapman & Hall/CRC, 1993.
Fields HL. A motivation-decision model of pain: the role of opioids. In: Flor H, Kalso E, Dostrovsky JO, editors. Proceedings of the 11th World Congress on Pain. Seattle: IASP Press, 2006. pp. 449–59.
Geuter S, Gamer M, Onat S, Büchel C. Parametric trial-by-trial prediction of pain by easily available physiological measures. PAIN 2014;155:994–1001.
Heitmann H, May ES, Tiemann L, Schmidt P, Nickel MM, Ta Dinh S, Hohn VD, Tolle TR, Ploner M. Motor responses to noxious stimuli shape pain perception in chronic pain patients. eNeuro 2018;5:ENEURO.0290-18.2018.
Karatsoreos IN, McEwen BS. Psychobiological allostasis: resistance, resilience and vulnerability. Trends Cogn Sci 2011;15:576–84.
Kenny DA, Korchmaros JD, Bolger N. Lower level mediation in multilevel models. Psychol Methods 2003;8:115–28.
Koltzenburg M, McMahon SB. The enigmatic role of the sympathetic nervous system in chronic pain. Trends Pharmacol Sci 1991;12:399–402.
Kyle BN, McNeil DW. Autonomic arousal and experimentally induced pain: a critical review of the literature. Pain Res Manag 2014;19:159–67.
LeDoux J. Rethinking the emotional brain. Neuron 2012;73:653–76.
LeDoux JE. Feelings: what are they and how does the brain make them? Daedalus 2015;144:96–111.
Loggia ML, Juneau M, Bushnell MC. Autonomic responses to heat pain: heart rate, skin conductance, and their relation to verbal ratings and stimulus intensity. PAIN 2011;152:592–8.
MacKinnon DP, Fairchild AJ, Fritz MS. Mediation analysis. Annu Rev Psychol 2007;58:593–614.
Malinen S, Vartiainen N, Hlushchuk Y, Koskinen M, Ramkumar P, Forss N, Kalso E, Hari R. Aberrant temporal and spatial brain activity during rest in patients with chronic pain. Proc Natl Acad Sci U S A 2010;107:6493–7.
May ES, Tiemann L, Schmidt P, Nickel MM, Wiedemann N, Dresel C, Sorg C, Ploner M. Behavioral responses to noxious stimuli shape the perception of pain. Sci Rep 2017;7:44083.
McEwen BS. Protective and damaging effects of stress mediators. N Engl J Med 1998;338:171–9.
Melzack R, Casey KL. Sensory, motivational, and central control determinants of pain: a new conceptual model in pain. In: Kenshalo DRJ, editor. The skin senses. Springfield: Charles C. Thomas, 1968. pp. 423–39.
Mischkowski D, Palacios-Barrios EE, Banker L, Dildine TC, Atlas LY. Pain or nociception? Subjective experience mediates the effects of acute noxious heat on autonomic responses. PAIN 2018;159:699–711.
Möltner A, Hölzl R, Strian F. Heart rate changes as an autonomic component of the pain response. PAIN 1990;43:81–9.
Mouraux A, Guerit JM, Plaghki L. Non-phase locked electroencephalogram (EEG) responses to CO2 laser skin stimulations may reflect central interactions between A-delta- and C-fibre afferent volleys. Clin Neurophysiol 2003;114:710–22.
Mouraux A, Iannetti GD, Colon E, Nozaradan S, Legrain V, Plaghki L. Nociceptive steady-state evoked potentials elicited by rapid periodic thermal stimulation of cutaneous nociceptors. J Neurosci 2011;31:6079–87.
Nickel MM, May ES, Tiemann L, Postorino M, Ta Dinh S, Ploner M. Autonomic responses to tonic pain are more closely related to stimulus intensity than to pain intensity. PAIN 2017;158:2129–36.
Sara SJ, Bouret S. Orienting and reorienting: the locus coeruleus mediates cognition through arousal. Neuron 2012;76:130–41.
Shrout PE, Bolger N. Mediation in experimental and nonexperimental studies: new procedures and recommendations. Psychol Methods 2002;7:422–45.
Stone CA, Sobel ME. The robustness of estimates of total indirect effects in covariance structure models estimated by maximum likelihood. Psychometrika 1990;55:337–52.
Sullivan MJ. Toward a biopsychomotor conceptualization of pain: implications for research and intervention. Clin J Pain 2008;24:281–90.
Tan G, Shaffer R, Lyle R, Teo I. Evidence-based practice in biofeedback and neurofeedback. 3rd ed. Wheat Ridge: Association for Applied Psychophysiology and Biofeedback, 2016.
Taylor AB, MacKinnon DP, Tein JY. Tests of the three-path mediated effect. Organ Res Methods 2008;11:241–69.
Thayer JF, Yamamoto SS, Brosschot JF. The relationship of autonomic imbalance, heart rate variability and cardiovascular disease risk factors. Int J Cardiol 2010;141:122–31.
Tiemann L, Hohn VD, Ta Dinh S, May ES, Nickel MM, Gross J, Ploner M. Distinct patterns of brain activity mediate perceptual and motor and autonomic responses to noxious stimuli. Nat Commun 2018;9:4487.
Tracey WD Jr. Nociception. Curr Biol 2017;27:R129–33.
Tracy LM, Ioannou L, Baker KS, Gibson SJ, Georgiou-Karistianis N, Giummarra MJ. Meta-analytic evidence for decreased heart rate variability in chronic pain implicating parasympathetic nervous system dysregulation. PAIN 2016;157:7–29.
Treister R, Kliger M, Zuckerman G, Goor Aryeh I, Eisenberg E. Differentiating between heat pain intensities: the combined effect of multiple autonomic parameters. PAIN 2012;153:1807–14.
Vachon-Presseau E. Effects of stress on the corticolimbic system: implications for chronic pain. Prog Neuropsychopharmacol Biol Psychiatry 2018;87(pt B):216–23.
Wager TD, Davidson ML, Hughes BL, Lindquist MA, Ochsner KN. Prefrontal-subcortical pathways mediating successful emotion regulation. Neuron 2008;59:1037–50.
Wager TD, Waugh CE, Lindquist M, Noll DC, Fredrickson BL, Taylor SF. Brain mediators of cardiovascular responses to social threat: part I: reciprocal dorsal and ventral sub-regions of the medial prefrontal cortex and heart-rate reactivity. Neuroimage 2009;47:821–35.
Wall PD. On the relation of injury to pain. John J Bonica lecture. PAIN 1979;6:253–64.
Woo CW, Roy M, Buhle JT, Wager TD. Distinct brain systems mediate the effects of nociceptive input and self-regulation on pain. PLoS Biol 2015;13:e1002036.