Highlights
- •Temporal summation of second pain (TSSP) is linked to central sensitization.
- •Affective touch (AT) decreases TSSP, while discriminative touch does not.
- •Also, higher body awareness is linked with higher pain during discriminative touch.
- •The mechanisms underpinning AT could prove useful against chronic pain.
Abstract
C-tactile (CT) fibers, responsible for the so-called “affective” touch (AT), have
drawn a fair amount of attention within the scientific community for their marked
social dimension. However, while the pain-relieving potential of discriminative touch
(DT) has been documented, proofs of the analgesic properties of AT are still scarce.
Additionally, no study has so far tested its possible pain-relieving effects on a
clinically-relevant model. Temporal summation of second pain (TSSP), otherwise referred
to as “wind-up,” relies on repetitive stimulation of C-nociceptors and it is thought
to reflect central sensitization, a process linked to many chronic pain conditions.
In the present experimental, within participants, design we induced TSSP through trains
of ascending and descending repetitive heat stimulation. Forty-two healthy participants’
pain was measured during 2 different tactile stimulations (stroking velocities AT:
10 cm/s; DT: 0.3 cm/s) or without concomitant tactile input. Since measures of pleasantness
of the tactile stimulation have been found to strongly correlate with C-tactile fibers’
firing rate, these, together with participants’ body awareness, were also taken into
account.
Our results show that AT brought about a decrease of our participants’ pain as opposed
to both DT and no touch, while DT did not produce any significant pain reduction.
Thus, only AT successfully modulated wind-up. As expected, AT was perceived as more
pleasant than DT, while a clear relationship between body awareness and pain was found
only during DT.
Targeting CT fibers could pave the way to new treatments for chronic pain conditions
whose aetiology depend on abnormal C-nociceptors’ physiology.
Perspective
This study extends previous findings on the analgesic potential of affective touch,
documenting a clear pain reduction during temporal summation of second pain (TSSP).
Since TSSP is thought to reflect central sensitization, the psychophysiological mechanisms
of affective touch could be exploited for new chronic pain treatments.
Keywords
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References
- Temporal summation of second pain: Variability in responses to a fixed protocol.Eur J Pain (United Kingdom) Eur J Pain. 2013; 17: 67-74
- Touch receptor-derived sensory information alleviates acute pain signaling and fine-tunes nociceptive reflex coordination.Neuron Cell Press;. 2017; 93: 179-193
- Pain sensitisation in osteoarthritis.Clin Exp Rheumatol Clin Experimental Rheumatol S.A.S. 2017; 35: S68-S74
- Assessment and manifestation of central sensitisation across different chronic pain conditions.Eur J Pain. 2018; 22: 216-241
- Altered central sensitization and pain modulation in the CNS in chronic joint pain.Curr Osteoporos Rep Curr Med Group LLC. 2015; 1: 225-234
- Dopamine and pain sensitivity: Neither sulpiride nor acute phenylalanine and tyrosine depletion have effects on thermal pain sensations in healthy volunteers.PLoS One. 2013; 8: e80766
- Feeling good: on the role of C fiber mediated touch in interoception.Exp. Brain Res Exp Brain Res. 2010; 207: 149-155
- Oxytocin and pain perception: From animal models to human research.Neuroscience. 2018: 149-161
Braz J, Solorzano C, Wang X, Basbaum AI: Transmitting pain and itch messages: A contemporary view of the spinal cord circuits that generate gate control. Neuron 522–536, 82, 2014
- The role of N-methyl-D-aspartate (NMDA) receptors in wind-up: A mathematical model.Math Med Biol A J IMA Oxford Acad. 1996; 13: 193-205
- Assessing body awareness and autonomic reactivity: Factor structure and psychometric properties of the Body Perception Questionnaire-Short Form (BPQ-SF).Int J Methods Psychiatr Res. 2018; 27: e1596
- Mechanisms of neuropathic pain.Neuron. 2006; 52: 77-92
- Is tactile acuity altered in people with chronic pain? A systematic review and meta-analysis.J Pain. 2014; 15: 985-1000
- Effectiveness of body awareness interventions in fibromyalgia and chronic fatigue syndrome: A systematic review and meta-analysis.J Bodyw Mov Ther Churchill Livingstone. 2015; 19: 35-56
- Effective connectivity among brain regions associated with slow temporal summation of C-fiber-evoked pain in fibromyalgia patients and healthy controls.J Pain. 2012; 13: 390-400
- Pain modulation by illusory body rotation: A new way to disclose the interaction between the vestibular system and pain processing.Eur J Pain (United Kingdom). 2020; 24: 1119-1129
- Low-threshold primary afferent drive onto GABAergic interneurons in the superficial dorsal horn of the mouse.J Neurosci. 2009; 29: 686-695
- Neurophysiologic evidence for a central sensitization in patients with fibromyalgia.Arthritis Rheum. 2003; 48: 1420-1429
Dickenson AH: Spinal cord pharmacology of pain. BJA Br J Anaesth 75:193–200, 1995"?>
- Identification of spinal circuits transmitting and gating mechanical pain.Cell Cell Press. 2014; 159: 1417-1432
- Central pain syndrome.StatPearls. 2020 (Available at:) (Accessed February 3, 2021.)
Fingleton C, Smart K, Moloney N, Fullen BM, Doody C: Pain sensitization in people with knee osteoarthritis: A systematic review and meta-analysis. OsteoarthrCartil 23, 2015, 1043–1056.
- Neglect-like symptoms in complex regional pain syndrome: Results of a self-administered survey.J Pain Symptom Manage Elsevier. 1999; 18: 213-217
- Body awareness therapy for patients with fibromyalgia and chronic pain.Disabil Rehabil Disabil Rehabil. 2005; 27: 725-728
- Evidence for distorted mental representation of the hand in osteoarthritis.Rheumatology. 2015; 54: 678-682
Gursul D, Goksan S, Hartley C, Mellado GS, Moultrie F, Hoskin A, Adams E, Hathway G, Walker S, McGlone F, Slater R: Stroking modulates noxious-evoked brain activity in human infants. CurrBiol 128, 2018, R1380–R1381.
- Low threshold unmyelinated mechanoafferents can modulate pain.BMC Neurol BioMed Central. 2017; 17: 184
- A spatiotemporal signature of cortical pain relief by tactile stimulation: An MEG study.Neuroimage. 2016; 130: 175-183
- Temporal analysis of cortical mechanisms for pain relief by tactile stimuli in humans.Cereb. Cortex. 2006 (Available at:) (Accessed February 3, 2021.)
JASP team: JASP (Version 0.12.2) [Computer software]. 2020. Available at: https://jasp-stats.org. Accessed February 3, 2021.
- Widespread pain in fibromyalgia is related to a deficit of endogenous pain inhibition.Pain. 2005; 114: 295-302
- The pathways of interoceptive awareness.Nat Neurosci NIH Public Access. 2009; 12: 1494-1496
- Affective touch and attachment style modulate pain: A laser-evoked potentials study.Philos Trans R Soc Lond B Biol Sci. 2016; 371
- Central sensitization: A generator of pain hypersensitivity by central neural plasticity.J Pain. 2009; 10: 895-926
- Altered C-tactile processing in human dynamic tactile allodynia.Pain. 2013; 154: 227-234
- Discriminative and affective touch in human experimental tactile allodynia.Neurosci Lett. 2014; 563: 75-79
- Tactile C fibers and their contributions to pleasant sensations and to tactile allodynia.Front Behav Neurosci Frontiers Media SA;. 2014; 8: 37
- Slow brushing reduces heat pain in humans.Eur J Pain. 2017; 21: 1173-1185
- Coding of pleasant touch by unmyelinated afferents in humans.Nat Neurosci. 2009; 12: 547-548
- Role of distorted body image in pain.Curr Rheumatol Rep. 2007; 9: 488-496
- A specific inhibitory pathway between substantia gelatinosa neurons receiving direct C-fiber input.J Neurosci. 2003; 23: 8752-8758
- Iannetti GDD: Touch inhibits subcortical and cortical nociceptive responses.Pain Lippincott Williams Wilkins. 2015; 156: 1936-1944
- Visual distortion of body size modulates pain perception.Psychol Sci. 2011; 22: 325-330
- Pain relief by touch: A quantitative approach.Pain. 2014; 155: 635-642
Martini M: Real, rubber or virtual: The vision of “one's own” body as a means for pain modulation. A narrative review. Conscious. Cogn. Academic Press Inc.; pp 143–512, 2016. Available at: https://pubmed.ncbi.nlm.nih.gov/27295559/. Accessed February 3, 2021.
- The body fades away: Investigating the effects of transparency of an embodied virtual body on pain threshold and body ownership.Sci Rep. 2015; 5: 13948
- What color is my arm? Changes in skin color of an embodied virtual arm modulates pain threshold.Front Hum Neurosci. 2013; 7: 438
- Decreasing pain ratings in chronic arm pain through changing a virtual body: different strategies for different pain types.J Pain. 2019; 20: 685-697
- Discriminative touch and emotional touch.Can J Exp Psychol. 2007; 61: 173-183
- Discriminative and affective touch: Sensing and feeling.Neuron Elsevier. 2014; 82: 737-755
- Body awareness: Construct and self-report measures.PLoS One. 2009; 4 (Available at:) (Accessed February 3, 2021.)
- Pain mechanisms: A new theory.Science. 1965; 150: 971-978
- Theories of pain: From specificity to gate control.J Neurophysiol. 2013; 109: 5-12
- Distorted body image in complex regional pain syndrome.Neurology. 2005; 65: 773
- Cortical interactions and integration of nociceptive and non-nociceptive somatosensory inputs in humans.Neuroscience. 2007; 150: 72-81
- Mechanical allodynia in human glabrous skin mediated by low-threshold cutaneous mechanoreceptors with unmyelinated fibres.Exp Brain Res. 2013; 231: 139-151
- Allodynia mediated by C-tactile afferents in human hairy skin.J Physiol. 2011; 589: 4065-4075
- Modulation of perception and neurophysiological correlates of brief CO2 laser stimuli in humans using concurrent large fiber stimulation.Somatosens Mot Res Somatosens Mot Res. 2003; 20: 139-147
Nijs J, Meeus M, Van Oosterwijck J, Roussel N, De Kooning M, Ickmans K, Matic M: Treatment of central sensitization in patients with “unexplained” chronic pain: What options do we have. Expert Opin. Pharmacother. Taylor & Francis; pp 1087–1098, 2011. Available at: https://www.tandfonline.com/. Accessed February 3, 2021.
- Low-threshold mechanoreceptive and nociceptive units with unmyelinated (C) fibres in the human supraorbital nerve.J Physiol. 1990; 426: 229-240
- Hyperalgesia and temporal summation of pain after heat injury in man.Pain. 1998; 74: 189-197
- On the generalised embodiment of pain: How interoceptive sensitivity modulates cutaneous pain perception.Pain. 2012; 153: 1680-1686
- Analgesic effects of multisensory illusions in osteoarthritis.Rheumatology (Oxford). 2011; 50: 2314-2315
- Characteristics of second pain and flexion reflexes indicative of prolonged central summation.Exp Neurol. 1972; 37: 371-387
- Peripheral suppression of first pain and central summation of second pain evoked by noxious heat pulses.Pain. 1977; 3: 57-68
- The N-methyl-d-aspartate receptor antagonist dextromethorphan selectively reduces temporal summation of second pain in man.Pain. 1994; 59: 165-174
- Temporal summation of heat pain in temporomandibular disorder patients.J Oral Facial Pain Headache NIH Public Access. 2009; 23: 54-64
- Differential responses of nociceptive vs. non-nociceptive spinal dorsal horn neurones to cutaneously applied vibration in the cat.Pain. 1990; 40: 311-322
- Physiological characteristics of responses of wide dynamic range spinal neurones to cutaneously applied vibration in the cat.Brain Res Elsevier. 1990; 507: 69-84
- Cutaneous C-fiber pain abnormalities of fibromyalgia patients are specifically related to temporal summation.Pain. 2008; 139: 315-323
- Brain activity associated with slow temporal summation of C-fiber evoked pain in fibromyalgia patients and healthy controls.Eur J Pain NIH Public Access. 2008; 12: 1078-1089
- Brain activity associated with slow temporal summation of C-fiber evoked pain in fibromyalgia patients and healthy controls.Eur J Pain. 2008; 12: 1078-1089
- Brain activity related to temporal summation of C-fiber evoked pain.Pain NIH Public Access. 2007; 129: 130-142
Staud R, Craggs JG, Robinson ME, Perlstein WM, Price DD: Brain activity related to temporal summation of C-fiber evoked pain.
- Advanced continuous-contact heat pulse design for efficient temporal summation of second pain (windup).J Pain. 2006; 7: 575-582
- Temporal summation of second pain and its maintenance are useful for characterizing widespread central sensitization of fibromyalgia patients.J Pain. 2007; 8: 893-901
- Abnormal sensitization and temporal summation of second pain (wind-up) in patients with fibromyalgia syndrome.Pain. 2001; 91: 165-175
- Cortical inhibition of laser pain and laser-evoked potentials by non-nociceptive somatosensory input. Acsády L, editor.Eur J Neurosci Blackwell Publishing Ltd. 2015; 42: 2407-2414
- Neuronal circuitry for pain processing in the dorsal horn.Nat Rev Neurosci Europe PMC Funders. 2010; 11: 823-836
- Sensing the body in chronic pain: A review of psychophysical studies implicating altered body representation.Neurosci Biobehav Rev. 2015; 52: 221-232
- Laser evoked potential amplitude and laser-pain rating reduction during high-frequency non-noxious somatosensory stimulation.Clin Neurophysiol. 2018; 129: 920-925
- A system of unmyelinated afferents for innocuous mechanoreception in the human skin.Brain Res. 1993; 628: 301-304
- Unmyelinated afferents constitute a second system coding tactile stimuli of the human hairy skin.J Neurophysiol. 1999; 81: 2753-2763
- Receptive field characteristics of tactile units with myelinated afferents in hairy skin of human subjects.J Physiol. 1995; 483: 783-795
- Spinal cord stimulation in chronic pain.Spine (Phila Pa 1976) Lippincott Williams and Wilkins. 2017; 42: S53-S60
- Using TENS for pain control: The state of the evidence.. Pain Manag. 2014; 4: 197-209
- Edinburgh Handedness Inventory - Short Form: A revised version based on confirmatory factor analysis.Laterality. 2014; 19: 164-177
- Painful diabetic neuropathy: Epidemiology, natural history, early diagnosis, and treatment options.Pain Med. 2008; 9: 660
- Characteristics of temporal summation of second pain sensations elicited by brief contact of glabrous kkin by a preheated thermode.J Neurophysiol. 1997; 78: 992-1002
- Cognitive modulation of pain: How do attention and emotion influence pain processing?.Pain. 2002; 95: 195-199
Walker SC, Trotter PD, Swaney WT, Marshall A, Mcglone FP: C-tactile afferents: Cutaneous mediators of oxytocin release during affiliative tactile interactions?. Neuropeptides. 64, 2017, 27–38.
- Brain activation upon selective stimulation of cutaneous C- and Aδ-fibers.Neuroimage. 2008; 41: 1372-1381
- The pain system. The neural basis of nociceptive transmission in the mammalian nervous system.Pain Headache. 1985; 8: 1-346
- Sensory Mechanisms of the Spinal Cord : Volume 1 Primary Afferent Neurons and the Spinal Dorsal Horn.Springer US, 2004
- Central sensitization: Implications for the diagnosis and treatment of pain.Pain. 2011; 152: S2-S15
- The induction and maintenance of central sensitization is dependent on N-methyl-d-aspartic acid receptor activation; implications for the treatment of post-injury pain hypersensitivity states.Pain. 1991; 44: 293-299
- Vibration reduces thermal pain in adjacent dermatomes.Pain. 1997; 69: 75-77
Article Info
Publication History
Published online: January 16, 2021
Accepted:
January 3,
2021
Received in revised form:
December 14,
2020
Received:
October 30,
2020
Footnotes
Conflicts of Interest: This research has been supported by UEL Research Capital Fund. All authors declared no potential conflict of interest with respect, authorship, and\or publication of this article.
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© 2021 by United States Association for the Study of Pain, Inc.
