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Spatial Summation of Pain in Humans Investigated Using Transcutaneous Electrical Stimulation

Published:October 19, 2014DOI:https://doi.org/10.1016/j.jpain.2014.10.001

      Highlights

      • Spatial summation exists for electrical stimuli, even at 20-cm separations.
      • Pain was greater for paired stimuli than for a single stimulus of equal intensity.
      • Pain was greater when paired stimuli were at 5-, 10-, and 20-cm separations.
      • Area- and distance-based spatial summation exists for electrical stimuli.
      • The findings suggest a proximal-distal gradient in nociceptive sensitivity.

      Abstract

      Spatial summation of pain is well accepted but surprisingly understudied. Area-based summation refers to the increase in pain evoked by increasing the area of stimulation. Distance-based summation refers to the increase in pain evoked by increasing the distance between multiple stimuli. Although transcutaneous electrical stimulation has several advantages over other experimental pain paradigms, whether or not this modality evokes spatial summation remains unknown. We aimed to answer this question in order to lay the foundation for critical studies of spatial summation. Twenty-five healthy participants received stimuli on their forearm, and the primary outcome, pain intensity, was compared across 5 spatial configurations—1 with a single stimulus and 4 paired configurations at 0-, 5-, 10-, and 20-cm separations. Importantly, the potential confounder of a proximal-distal gradient in nociceptive sensitivity was removed in this study. Pain intensity was higher in response to the paired stimuli than in response to the single stimulus (P < .001), and the paired stimuli separated by 5, 10 and 20 cm, evoked greater pain than stimuli at a separation of 0 cm (P < .001), thus confirming both area- and distance-based summation, respectively. We conclude that transcutaneous electrical stimulation is appropriate for future investigations of spatial summation.

      Perspective

      Distance-based summation is likely implicated in some clinical pain. However, current understanding for spatial summation is limited. This study demonstrates that transcutaneous electrical stimulation is safe, feasible, and valid for future investigations of spatial summation and will allow critical questions to be answered.

      Key words

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      References

        • Agostino R.
        • Cruccu G.
        • Iannetti G.
        • Romaniello A.
        • Truini A.
        • Manfredi M.
        Topographical distribution of pinprick and warmth thresholds to CO2 laser stimulation on the human skin.
        Neurosci Lett. 2000; 285: 115-118
        • Baumgärtner U.
        • Greffrath W.
        • Treede R.D.
        Contact heat and cold, mechanical, electrical and chemical stimuli to elicit small fiber-evoked potentials: Merits and limitations for basic science and clinical use.
        Clin Neurophysiol. 2010; 42: 267-280
        • Bromm B.
        • Meier W.
        The intracutaneous stimulus: A new pain model for algesimetric studies.
        Methods Find Exp Clin Pharmacol. 1984; 6: 405-410
        • Brown A.C.
        • Beeler W.J.
        • Kloka A.C.
        • Fields R.W.
        Spatial summation of pre-pain and pain in human teeth.
        Pain. 1985; 21: 1-16
        • Coghill R.C.
        • McHaffie J.G.
        • Yen Y.F.
        Neural correlates of interindividual differences in the subjective experience of pain.
        Proc Natl Acad Sci U S A. 2003; 100: 8538-8542
        • Coghill R.C.
        • Price D.D.
        • Hayes R.L.
        • Mayer D.J.
        Spatial distribution of nociceptive processing in the rat spinal cord.
        J Neurophysiol. 1991; 65: 133-140
        • Defrin R.
        • Ronat A.
        • Ravid A.
        • Peretz C.
        Spatial summation of pressure pain: Effect of body region.
        Pain. 2003; 106: 471-480
        • Defrin R.
        • Sheraizin A.
        • Malichi L.
        • Shachen O.
        Spatial summation and spatial discrimination of cold pain: Effect of spatial configuration and skin type.
        Pain. 2011; 152: 2739-2745
        • Defrin R.
        • Tsedek I.
        • Lugasi I.
        • Moriles I.
        • Urca G.
        The interactions between spatial summation and DNIC: Effect of the distance between two painful stimuli and attentional factors on pain perception.
        Pain. 2010; 151: 489-495
        • Defrin R.
        • Urca G.
        Spatial summation of heat pain: A reassessment.
        Pain. 1996; 66: 23-29
        • de Vignemont F.
        • Majid A.
        • Jola C.
        • Haggard P.
        Segmenting the body into parts: Evidence from biases in tactile perception.
        Q J Exp Psychol. 2009; 62: 500-512
        • Fernández-de-las-Peñas C.
        • Ge H.Y.
        • Alonso-Blanco C.
        • González-Iglesias J.
        • Arendt-Nielsen L.
        Referred pain areas of active myofascial trigger points in head, neck, and shoulder muscles, in chronic tension type headache.
        J Bodyw Mov Ther. 2010; 14: 391-396
        • Flach R.
        • Haggard P.
        The cutaneous rabbit revisited.
        J Exp Psychol Hum Percept Perform. 2006; 32: 717-732
        • Green B.
        Spatial summation of chemical irritation and itch produced by topical application of capsaicin.
        Percept Psychophys. 1990; 48: 12-18
        • Johansson O.
        • Wang L.
        • Hilliges M.
        • Liang Y.
        Intraepidermal nerves in the human skin: PGP 9.5 immunohistochemistry with special reference to the nerve density in skin from different body regions.
        J Peripher Nerv Syst. 1999; 4: 43-52
        • Lauria G.
        • Holland N.
        • Hauer P.
        • Cornblath D.R.
        • Griffin J.W.
        • McArthur J.C.
        Epidermal innervation: Changes with aging, topographic location, and in sensory neuropathy.
        J Neurol Sci. 1999; 164: 172-178
        • Mancini F.
        • Sambo C.
        • Ramirez J.
        • Bennett D.
        • Haggard P.
        • Iannetti G.
        A fovea for pain at the fingertips.
        Curr Biol. 2013; 23: 496-500
        • McArthur J.C.
        • Stocks E.A.
        • Hauer P.
        • Cornblath D.R.
        • Griffin J.W.
        Epidermal nerve fiber density: Normative reference range and diagnostic efficiency.
        Arch Neurol. 1998; 55: 1513-1520
        • Moseley G.L.
        • Gallace A.
        • Di Pietro F.
        • Spence C.
        • Iannetti G.D.
        Limb-specific autonomic dysfunction in complex regional pain syndrome modulated by wearing prism glasses.
        Pain. 2013; 154: 2463-2468
        • Moseley G.L.
        • Gallace A.
        • Iannetti G.D.
        Spatially defined modulation of skin temperature and hand ownership of both hands in patients with unilateral complex regional pain syndrome.
        Brain. 2012; 135: 3676-3686
        • Moseley G.L.
        • Gallagher L.
        • Gallace A.
        Neglect-like tactile dysfunction in chronic back pain.
        Neurology. 2012; 79: 327-332
        • Moseley G.L.
        • Gallace A.
        • Spence C.
        Bodily illusions in health and disease: Physiological and clinical perspectives and the concept of a cortical “body matrix.”.
        Neurosci Biobehav Rev. 2012; 36: 34-46
        • Nielsen J.
        • Arendt-Nielsen L.
        Spatial summation of heat induced pain within and between dermatomes.
        Somatosens Mot Res. 1997; 14: 119-125
        • Price D.D.
        • McHaffie J.G.
        • Larson M.A.
        Spatial summation of heat-induced pain: Influence of stimulus area and spatial separation of stimuli on perceived pain sensation intensity and unpleasantness.
        J Neurophysiol. 1989; 62: 1270-1279
        • Quevedo A.
        • Coghill R.
        An illusion of proximal radiation of pain due to distally directed inhibition.
        J Pain. 2007; 8: 280-286
        • Quevedo A.
        • Coghill R.
        Filling-in, spatial summation, and radiation of pain: Evidence for a neural population code in the nociceptive system.
        J Neurophysiol. 2009; 102: 3544-3553
      1. Reid E: Honors thesis. Does spatial summation exist for paired noxious electrical stimuli? University of South Australia 2013. Available at: http://ura.unisa.edu.au:80/R/-?func=dbin-jump-full&object_id=114034&silo_library=GEN01.

        • Sambo C.F.
        • Liang M.
        • Cruccu G.
        • Iannetti G.D.
        Defensive peripersonal space: The blink reflex evoked by hand stimulation is increased when the hand is near the face.
        J Neurophysiol. 2012; 107: 880-889
        • Staud R.
        • Koo E.
        • Robinson M.
        • Price D.
        Spatial summation of mechanically evoked muscle pain and painful aftersensations in normal subjects and fibromyalgia patients.
        Pain. 2007; 130: 177-187
        • Weissman-Fogel I.
        • Brayer-Zwi N.
        • Defrin R.
        Spatial resolution of the pain system: A proximal-to-distal gradient of sensitivity revealed with psychophysical testing.
        Exp Brain Res. 2012; 216: 181-190
        • Yarnitsky D.
        • Arendt-Nielsen L.
        • Bouhassira D.
        • Edwards R.
        • Fillingim R.
        • Granot M.
        • Hansson P.
        • Lautenbacher S.
        • Marchand S.
        • Wilder-smith O.
        Recommendations on terminology and practice of psychophysical DNIC testing.
        Eur J Pain. 2010; 14: 339