Enhancement of pain inhibition by working memory with anodal transcranial direct current stimulation of the left dorsolateral prefrontal cortex

  • Zoha Deldar
  • Nabi Rustamov
  • Suzie Bois
  • Isabelle Blanchette
  • Mathieu Piché
Original Paper
  • 12 Downloads

Abstract

The aim of this study was to examine whether transcranial direct current stimulation (tDCS) of the dorsolateral prefrontal cortex (DLPFC) enhances pain inhibition by improving working memory (WM). Forty healthy volunteers participated in two tDCS sessions. Pain was evoked by electrical stimulation at the ankle. Participants performed an n-back task (0-back and 2-back). The experimental protocol comprised five counterbalanced conditions (0-back, 2-back, pain, 0-back with pain and 2-back with pain) that were performed twice (pre-tDCS baseline and during tDCS). Compared with the pre-tDCS baseline values, anodal tDCS decreased response times for the 2-back condition (p < 0.01) but not for the 0-back condition (p > 0.5). Anodal tDCS also decreased pain ratings marginally in the 2-back with pain condition, but not the 0-back with pain condition (p = 0.052 and p > 0.2, respectively). No effect was produced by sham tDCS for any condition (p > 0.2). These results indicate that tDCS of the left DLPFC may enhance pain inhibition by improving WM.

Keywords

Neuromodulation Nociceptive Cognition Descending modulation Anxiety 

Notes

Author contributions

ZD contributed to all aspects of the research. SB contributed to data acquisition, analyses and interpretation. NR contributed to data acquisition and interpretation. IB contributed to experimental design, data interpretation and manuscript preparation. MP contributed to all aspects of the research and obtained funding for the study.

Compliance with ethical standards

Ethical approval

All experimental procedures conformed to the standards set by the latest revision of the Declaration of Helsinki and were approved by the Research Ethics Board of Université du Québec à Trois-Rivières. All participants gave written informed consent, acknowledging their right to withdraw from the experiment without prejudice.

Conflict of interest

Zoha Deldar reports no financial or other relationship that may lead to any conflict of interest. Nabi Rustamov reports no financial or other relationship that may lead to any conflict of interest. Suzie Bois reports no financial or other relationship that may lead to any conflict of interest. Isabelle Blanchette reports no financial or other relationship that may lead to any conflict of interest. Mathieu Piché reports no financial or other relationship that may lead to any conflict of interest.

References

  1. 1.
    Legrain V, Damme SV, Eccleston C, Davis KD, Seminowicz DA, Crombez G (2009) A neurocognitive model of attention to pain: behavioral and neuroimaging evidence. Pain 144(3):230–232CrossRefPubMedGoogle Scholar
  2. 2.
    Legrain V, Mancini F, Sambo CF, Torta DM, Ronga I, Valentini E (2012) Cognitive aspects of nociception and pain: bridging neurophysiology with cognitive psychology. Neurophysiol Clin 42(5):325–336CrossRefPubMedGoogle Scholar
  3. 3.
    Berti S, Roeber U, Schröger E (2004) Bottom–up influences on working memory: behavioral and electrophysiological distraction varies with distractor strength. Exp Psychol 51(4):249–257CrossRefPubMedGoogle Scholar
  4. 4.
    Barcelo F, Escera C, Corral MJ, Periáñez JA (2006) Task switching and novelty processing activate a common neural network for cognitive control. J Cognit Neurosci 18(10):1734–1748CrossRefGoogle Scholar
  5. 5.
    McCaul KD, Malott JM (1985) Distraction and coping with pain. Pain 23(3):315CrossRefGoogle Scholar
  6. 6.
    Legrain V, Crombez G, Plaghki L, Mouraux A (2013) Shielding cognition from nociception with working memory. Cortex 49(7):1922–1934CrossRefPubMedGoogle Scholar
  7. 7.
    Torta DM, Legrain V, Mouraux A, Valentini E (2017) Attention to pain! A neurocognitive perspective on attentional modulation of pain in neuroimaging studies. CortexGoogle Scholar
  8. 8.
    Legrain V, Perchet C, Garcia-Larrea L (2009) Involuntary orienting of attention to nociceptive events: neural and behavioral signatures. J Neurophysiol 102(4):2423–2434CrossRefPubMedGoogle Scholar
  9. 9.
    Verhoeven K, Van Damme S, Eccleston C, Van Ryckeghem DM, Legrain V, Crombez G (2011) Distraction from pain and executive functioning: an experimental investigation of the role of inhibition, task switching and working memory. Eur J Pain 15(8):866–873CrossRefPubMedGoogle Scholar
  10. 10.
    Corbetta M, Shulman GL (2002) Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3(3):201–215CrossRefPubMedGoogle Scholar
  11. 11.
    Awh E, Vogel EK, Oh SH (2006) Interactions between attention and working memory. Neuroscience 139(1):201–208CrossRefPubMedGoogle Scholar
  12. 12.
    Legrain V, Crombez G, Mouraux A (2011) Controlling attention to nociceptive stimuli with working memory. PLoS ONE 6(6):e20926CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Egeth HE, Yantis S (1997) Visual attention: control, representation, and time course. Annu Rev Psychol 48(1):269–297CrossRefPubMedGoogle Scholar
  14. 14.
    Escera C, Corral MJ (2007) Role of mismatch negativity and novelty-P3 in involuntary auditory attention. J Psychophysiol 21(3–4):251–264CrossRefGoogle Scholar
  15. 15.
    Knudsen EI (2007) Fundamental components of attention. Annu Rev Neurosci 30:57–78CrossRefPubMedGoogle Scholar
  16. 16.
    Downar J, Mikulis DJ, Davis KD (2003) Neural correlates of the prolonged salience of painful stimulation. Neuroimage 20(3):1540–1551CrossRefPubMedGoogle Scholar
  17. 17.
    Bingel U, Rose M, Glascher J, Buchel C (2007) fMRI reveals how pain modulates visual object processing in the ventral visual stream. Neuron 55(1):157–167CrossRefPubMedGoogle Scholar
  18. 18.
    Yantis S, Jonides J (1990) Abrupt visual onsets and selective attention: voluntary versus automatic allocation. J Exp Psychol Hum Percept Perform 16(1):121–134CrossRefPubMedGoogle Scholar
  19. 19.
    Seminowicz DA, Davis KD (2007) Interactions of pain intensity and cognitive load: the brain stays on task. Cereb Cortex 17(6):1412–1422CrossRefPubMedGoogle Scholar
  20. 20.
    Seminowicz DA, Davis KD (2007) Pain enhances functional connectivity of a brain network evoked by performance of a cognitive task. J Neurophysiol 97(5):3651–3659CrossRefPubMedGoogle Scholar
  21. 21.
    Legrain V, Guérit J-M, Bruyer R, Plaghki L (2002) Attentional modulation of the nociceptive processing into the human brain: selective spatial attention, probability of stimulus occurrence, and target detection effects on laser evoked potentials. Pain 99(1):21–39CrossRefPubMedGoogle Scholar
  22. 22.
    Hopfinger JB, West VM (2006) Interactions between endogenous and exogenous attention on cortical visual processing. Neuroimage 31(2):774–789CrossRefPubMedGoogle Scholar
  23. 23.
    Miyake A, Friedman NP, Emerson MJ, Witzki AH, Howerter A, Wager TD (2000) The unity and diversity of executive functions and their contributions to complex “frontal lobe” tasks: a latent variable analysis. Cognit Psychol 41(1):49–100CrossRefPubMedGoogle Scholar
  24. 24.
    Van Damme S, Legrain V, Vogt J, Crombez G (2010) Keeping pain in mind: a motivational account of attention to pain. Neurosci Biobehav Rev 34(2):204–213CrossRefPubMedGoogle Scholar
  25. 25.
    Folk CL, Remington RW, Johnston JC (1992) Involuntary covert orienting is contingent on attentional control settings. J Exp Psychol Hum Percept Perform 18(4):1030–1044CrossRefPubMedGoogle Scholar
  26. 26.
    Miller EK, Cohen JD (2001) An integrative theory of prefrontal cortex function. Annu Rev Neurosci 24:167–202CrossRefPubMedGoogle Scholar
  27. 27.
    Soto D, Hodsoll J, Rotshtein P, Humphreys GW (2008) Automatic guidance of attention from working memory. Trends Cognit Sci 12(9):342–348CrossRefGoogle Scholar
  28. 28.
    Tracey I, Mantyh PW (2007) The cerebral signature for pain perception and its modulation. Neuron 55(3):377–391CrossRefPubMedGoogle Scholar
  29. 29.
    Legrain V, Crombez G, Verhoeven K, Mouraux A (2011) The role of working memory in the attentional control of pain. Pain 152(2):453–459CrossRefPubMedGoogle Scholar
  30. 30.
    Crombez G, Eccleston C, Baeyens F, Eelen P (1998) Attentional disruption is enhanced by the threat of pain. Behav Res Ther 36(2):195–204CrossRefPubMedGoogle Scholar
  31. 31.
    Lavie N, Hirst A, de Fockert JW, Viding E (2004) Load theory of selective attention and cognitive control. J Exp Psychol Gen 133(3):339–354CrossRefPubMedGoogle Scholar
  32. 32.
    Legrain V, Bruyer R, Guerit JM, Plaghki L (2005) Involuntary orientation of attention to unattended deviant nociceptive stimuli is modulated by concomitant visual task difficulty. Evidence from laser evoked potentials. Clin Neurophysiol 116(9):2165–2174CrossRefPubMedGoogle Scholar
  33. 33.
    Lavie N, Fockert JD (2006) Frontal control of attentional capture in visual search. Vis Cognit 14(4–8):863–876CrossRefGoogle Scholar
  34. 34.
    SanMiguel I, Corral M-J, Escera C (2008) When loading working memory reduces distraction: behavioral and electrophysiological evidence from an auditory-visual distraction paradigm. J Cognit Neurosci 20(7):1131–1145CrossRefGoogle Scholar
  35. 35.
    D’Esposito M, Postle BR, Rypma B (2000) Prefrontal cortical contributions to working memory: evidence from event-related fMRI studies. Exp Brain Res 133(1):3–11CrossRefPubMedGoogle Scholar
  36. 36.
    Levy R, Goldman-Rakic PS (2000) Segregation of working memory functions within the dorsolateral prefrontal cortex. Exp Brain Res 133(1):23–32CrossRefPubMedGoogle Scholar
  37. 37.
    Szmalec A, Verbruggen F, Vandierendonck A, Kemps E (2011) Control of interference during working memory updating. J Exp Psychol Hum Percept Perform 37(1):137–151CrossRefPubMedGoogle Scholar
  38. 38.
    Hester R, Garavan H (2005) Working memory and executive function: the influence of content and load on the control of attention. Mem Cognit 33(2):221–233CrossRefPubMedGoogle Scholar
  39. 39.
    Baddeley A (2003) Working memory: looking back and looking forward. Nat Rev Neurosci 4(10):829–839CrossRefPubMedGoogle Scholar
  40. 40.
    Buhle J, Wager TD (2010) Performance-dependent inhibition of pain by an executive working memory task. Pain 149(1):19–26CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Awh E, Jonides J (2001) Overlapping mechanisms of attention and spatial working memory. Elsevier, London, pp 119–126Google Scholar
  42. 42.
    Wager TD, Spicer J, Insler R, Smith EE (2014) The neural bases of distracters resistant working memory. Cognit Affect Behav Neurosci 14(1):90–105CrossRefGoogle Scholar
  43. 43.
    Berti S, Schröger E (2003) Working memory controls involuntary attention switching: evidence from an auditory distraction paradigm. Eur J Neurosci 17(5):1119–1122CrossRefPubMedGoogle Scholar
  44. 44.
    Soto D, Heinke D, Humphreys GW, Blanco MJ (2005) Early, involuntary top–down guidance of attention from working memory. J Exp Psychol Hum Percept Perform 31(2):248–261CrossRefPubMedGoogle Scholar
  45. 45.
    Jan WDF, Rees G, Frith CD, Lavie N (2001) The role of working memory in visual selective attention. Science 291(5509):1803–1806CrossRefGoogle Scholar
  46. 46.
    Berryman C, Stanton TR, Jane Bowering K, Tabor A, McFarlane A, Lorimer Moseley G (2013) Evidence for working memory deficits in chronic pain: a systematic review and meta-analysis. Pain 154(8):1181–1196CrossRefPubMedGoogle Scholar
  47. 47.
    Baker KS, Gibson S, Georgiou-Karistianis N, Roth RM, Giummarra MJ (2016) Everyday executive functioning in chronic pain: specific deficits in working memory and emotion control, predicted by mood, medications, and pain interference. Clin J Pain 32(8):673–680CrossRefPubMedGoogle Scholar
  48. 48.
    Ferreira KDS, Oliver GZ, Thomaz DC, Teixeira CT, Foss MP (2016) Cognitive deficits in chronic pain patients, in a brief screening test, are independent of comorbidities and medication use. Arq Neuropsiquiatr 74(5):361–366CrossRefGoogle Scholar
  49. 49.
    Moriarty O, McGuire BE, Finn DP (2011) The effect of pain on cognitive function: a review of clinical and preclinical research. Prog Neurobiol 93(3):385–404CrossRefPubMedGoogle Scholar
  50. 50.
    Sammer G, Brück C, Haberkamp A, Bischoff M, Blecker CR (2009) Visuospatial working memory, executive functioning, language comprehension and aging. Neuroimage 47:S109CrossRefGoogle Scholar
  51. 51.
    Mitchell KJ, Johnson MK, Raye CL, Mather M, D’Esposito M (2000) Aging and reflective processes of working memory: binding and test load deficits. Psychol Aging 15(3):527–541CrossRefPubMedGoogle Scholar
  52. 52.
    Gazzaley A, Rissman J, Cooney JW, D’Esposito M (2005) top–down suppression deficit underlies working memory impairment in normal aging. Nat Neurosci 8(10):1298–1300CrossRefPubMedGoogle Scholar
  53. 53.
    Sambataro F, Murty VP, Callicott JH, Tan H-Y, Das S, Weinberger DR, Mattay VS (2010) Age-related alterations in default mode network: impact on working memory performance. Neurobiol Aging 31(5):839–852CrossRefPubMedGoogle Scholar
  54. 54.
    Brunoni AR, Vanderhasselt MA (2014) Working memory improvement with non-invasive brain stimulation of the dorsolateral prefrontal cortex: a systematic review and meta-analysis. Brain Cognit 86:1–9CrossRefGoogle Scholar
  55. 55.
    Wolkenstein L, Plewnia C (2013) Amelioration of cognitive control in depression by transcranial direct current stimulation. Biol Psychiatry 73(7):646–651CrossRefPubMedGoogle Scholar
  56. 56.
    Andrews SC, Hoy KE, Enticott PG, Daskalakis ZJ, Fitzgerald PB (2011) Improving working memory: the effect of combining cognitive activity and anodal transcranial direct current stimulation to the left dorsolateral prefrontal cortex. Brain Stimul 4(2):84–89CrossRefPubMedGoogle Scholar
  57. 57.
    Mylius V, Jung M, Menzler K, Haag A, Khader PH, Oertel WH, Rosenow F, Lefaucheur JP (2012) Effects of transcranial direct current stimulation on pain perception and working memory. Eur J Pain 16(7):974–982CrossRefPubMedGoogle Scholar
  58. 58.
    Mariano TY, Van’t Wout M, Garnaat SL, Rasmussen SA, Greenberg BD (2016) Transcranial direct current stimulation (tDCS) targeting left dorsolateral prefrontal cortex modulates task-induced acute pain in healthy volunteers. Pain Med 17(4):737–745PubMedGoogle Scholar
  59. 59.
    Boggio PS, Ferrucci R, Rigonatti SP, Covre P, Nitsche M, Pascual-Leone A, Fregni F (2006) Effects of transcranial direct current stimulation on working memory in patients with Parkinson’s disease. J Neurol Sci 249(1):31–38CrossRefPubMedGoogle Scholar
  60. 60.
    Jo JM, Kim YH, Ko MH, Ohn SH, Joen B, Lee KH (2009) Enhancing the working memory of stroke patients using tDCS. Am J Phys Med Rehabil 88(5):404–409CrossRefPubMedGoogle Scholar
  61. 61.
    Hill AT, Fitzgerald PB, Hoy KE (2016) Effects of anodal transcranial direct current stimulation on working memory: a systematic review and meta-analysis of findings from healthy and neuropsychiatric populations. Brain Stimul 9(2):197–208CrossRefPubMedGoogle Scholar
  62. 62.
    Berryhill ME, Jones KT (2012) tDCS selectively improves working memory in older adults with more education. Neurosci Lett 521(2):148–151CrossRefPubMedGoogle Scholar
  63. 63.
    Park S-H, Seo J-H, Kim Y-H, Ko M-H (2014) Long-term effects of transcranial direct current stimulation combined with computer-assisted cognitive training in healthy older adults. NeuroReport 25(2):122–126CrossRefPubMedGoogle Scholar
  64. 64.
    Willer JC (1977) Comparative study of perceived pain and nociceptive flexion reflex in man. Pain 3(1):69–80CrossRefPubMedGoogle Scholar
  65. 65.
    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. Neuroscience 195:166–175CrossRefPubMedGoogle Scholar
  66. 66.
    Ladouceur A, Rustamov N, Dubois JD, Tessier J, Lehmann A, Descarreaux M, Rainville P, Piche M (2017) Inhibition of pain and pain-related brain activity by heterotopic noxious counter-stimulation and selective attention in chronic non-specific low back pain. Neuroscience.  https://doi.org/10.1016/j.neuroscience.2017.09.054
  67. 67.
    Ladouceur A, Tessier J, Provencher B, Rainville P, Piche M (2012) top–down attentional modulation of analgesia induced by heterotopic noxious counterstimulation. Pain 153(8):1755–1762CrossRefPubMedGoogle Scholar
  68. 68.
    Coen SJ, Aziz Q, Yágüez L, Brammer M, Williams SCR, Gregory LJ (2008) Effects of attention on visceral stimulus intensity encoding in the male human brain. Gastroenterology 135(6):2065.e1–2074.e1CrossRefGoogle Scholar
  69. 69.
    Oliveira JF, Zanao TA, Valiengo L, Lotufo PA, Bensenor IM, Fregni F, Brunoni AR (2013) Acute working memory improvement after tDCS in antidepressant-free patients with major depressive disorder. Neurosci Lett 537:60–64CrossRefPubMedGoogle Scholar
  70. 70.
    Kuo M-F, Nitsche MA (2012) Effects of transcranial electrical stimulation on cognition. Clin EEG Neurosci 43(3):192–199CrossRefPubMedGoogle Scholar
  71. 71.
    Duncan J (2001) An adaptive coding model of neural function in prefrontal cortex. Nat Rev Neurosci 2(11):820–829CrossRefPubMedGoogle Scholar
  72. 72.
    Miniussi C, Harris JA, Ruzzoli M (2013) Modelling non-invasive brain stimulation in cognitive neuroscience. Neurosci Biobehav Rev 37(8):1702–1712CrossRefPubMedGoogle Scholar
  73. 73.
    Paulus W (2011) Transcranial electrical stimulation (tES-tDCS; tRNS, tACS) methods. Neuropsychol Rehabil 21(5):602–617CrossRefPubMedGoogle Scholar
  74. 74.
    Roe JM, Nesheim M, Mathiesen NC, Moberget T, Alnaes D, Sneve MH (2016) The effects of tDCS upon sustained visual attention are dependent on cognitive load. Neuropsychologia 80:1–8CrossRefPubMedGoogle Scholar
  75. 75.
    Bikson M, Name A, Rahman A (2013) Origins of specificity during tDCS: anatomical, activity-selective, and input-bias mechanisms. Front Hum Neurosci 7:688CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Jones KT, Berryhill ME (2012) Parietal contributions to visual working memory depend on task difficulty. Front Psychiatry 3:81PubMedPubMedCentralGoogle Scholar
  77. 77.
    Wu Y-J, Tseng P, Chang C-F, Pai M-C, Hsu K-S, Lin C-C, Juan C-H (2014) Modulating the interference effect on spatial working memory by applying transcranial direct current stimulation over the right dorsolateral prefrontal cortex. Brain Cognit 91:87–94CrossRefGoogle Scholar
  78. 78.
    Buhle JT, Stevens BL, Friedman JJ, Wager TD (2012) Distraction and placebo: two separate routes to pain control. Psychol Sci 23(3):246–253CrossRefPubMedGoogle Scholar
  79. 79.
    Moore DJ, Keogh E, Eccleston C (2013) The effect of threat on attentional interruption by pain. Pain 154(1):82–88CrossRefPubMedGoogle Scholar
  80. 80.
    Sprenger C, Eippert F, Finsterbusch J, Bingel U, Rose M, Büchel C (2012) Attention modulates spinal cord responses to pain. Curr Biol CB 22(11):1019–1022CrossRefPubMedGoogle Scholar
  81. 81.
    Eippert F, Finsterbusch J, Bingel U, Buchel C (2009) Direct evidence for spinal cord involvement in placebo analgesia. Science 326(5951):404CrossRefPubMedGoogle Scholar
  82. 82.
    Bushnell MC, Duncan GH, Dubner R, Jones RL, Maixner W (1985) Attentional influences on noxious and innocuous cutaneous heat detection in humans and monkeys. J Neurosci 5(5):1103–1110PubMedGoogle Scholar
  83. 83.
    Danziger N, Fournier E, Bouhassira D, Michaud D, De BT, Santarcangelo E, Carli G, Chertock L, Willer JC (1998) Different strategies of modulation can be operative during hypnotic analgesia: a neurophysiological study. Pain 75(1):85–92CrossRefPubMedGoogle Scholar
  84. 84.
    Bouhassira D, Danziger N, Attal N, Guirimand F (2003) Comparison of the pain suppressive effects of clinical and experimental painful conditioning stimuli. Brain 126(Pt 5):1068–1078CrossRefPubMedGoogle Scholar
  85. 85.
    Terkelsen AJ, Andersen OK, Molgaard H, Hansen J, Jensen TS (2004) Mental stress inhibits pain perception and heart rate variability but not a nociceptive withdrawal reflex. Acta Physiol Scand 180(4):405–414CrossRefPubMedGoogle Scholar
  86. 86.
    Defrin R, Peleg S, Weingarden H, Heruti R, Urca G (2007) Differential effect of supraspinal modulation on the nociceptive withdrawal reflex and pain sensation. Clin Neurophysiol 118(2):427–437CrossRefPubMedGoogle Scholar
  87. 87.
    Piche M, Arsenault M, Rainville P (2009) Cerebral and cerebrospinal processes underlying counterirritation analgesia. J Neurosci 29(45):14236–14246CrossRefPubMedGoogle Scholar

Copyright information

© The Physiological Society of Japan and Springer Japan KK, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of ChiropracticUniversité du Québec à Trois-RivièresTrois-RivièresCanada
  2. 2.CogNAC Research GroupUniversité du Québec à Trois-RivièresTrois-RivièresCanada
  3. 3.Department of PsychologyUniversité du Québec à Trois-RivièresTrois-RivièresCanada

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