Advertisement

Transcranial Direct Current Stimulation of the Dorsolateral Prefrontal Cortex Alters Emotional Modulation of Spinal Nociception

Published:November 27, 2020DOI:https://doi.org/10.1016/j.jpain.2020.10.007

      Highlights

      • Transcranial stimulation of the prefrontal cortex altered spinal nociception.
      • Reducing neural excitability abolished emotional control of spinal nociception
      • Emotional modulation of pain ratings was not impacted by brain stimulation
      • Reducing neural excitability increased spinal nociception and pain ratings.

      Abstract

      Emotion has a strong modulatory effect on pain perception and spinal nociception. Pleasure inhibits pain and nociception, whereas displeasure facilitates pain and nociception. Dysregulation of this system has been implicated in development and maintenance of chronic pain. The current study sought to examine whether emotional modulation of pain could be altered through the use of transcranial direct current stimulation (tDCS) to enhance (via anodal stimulation) or depress (via cathodal stimulation) cortical excitability in the dorsolateral prefrontal cortex. Thirty-two participants (15 female, 17 male) received anodal, cathodal, and sham tDCS on three separate occasions, followed immediately by testing to examine the impact of pleasant and unpleasant images on pain and nociceptive flexion reflex (NFR) responses to electrocutaneous stimulation. Results indicated that tDCS modulated the effect of image content on NFR, F(2, 2175.06) = 3.20, P= .04, with the expected linear slope following anodal stimulation (ie, pleasant < neutral < unpleasant) but not cathodal stimulation. These findings provide novel evidence that the dorsolateral prefrontal cortex is critical to emotional modulation of spinal nociception. Moreover, the results suggest a physiological basis for a previously identified phenotype associated with risk for chronic pain and thus a potentially new target for chronic pain prevention efforts.

      Perspective

      This study demonstrated that reduction of dorsolateral prefrontal cortical excitability by transcranial direct current stimulation attenuates the impact of emotional image viewing on nociceptive reflex activity during painful electrocutaneous stimulation. This result confirms there is cortical involvement in emotional modulation of spinal nociception and opens avenues for future clinical research.

      Key words

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to The Journal of Pain
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Antal A
        • Brepohl N
        • Poreisz C
        • Boros K
        • Csifcsak G
        • Paulus W
        Transcranial direct current stimulation over somatosensory cortex decreases experimentally induced acute pain perception.
        Clin J Pain. 2008; 24: 56-63
        • Bai S
        • Dokos S
        • Ho K-A
        • Loo C
        A computational modelling study of transcranial direct current stimulation montages used in depression.
        Neuroimage. 2014; 87: 332-344
        • Baliki MN
        • Apkarian AV
        Nociception, pain, negative moods, and behavior selection.
        Neuron. 2015; 87: 474-491
        • Berna C
        • Leknes S
        • Holmes EA
        • Edwards RR
        • Goodwin GM
        • Tracey I
        Induction of depressed mood disrupts emotion regulation neurocircuitry and enhances pain unpleasantness.
        Biol Psychiatry. 2010; 67: 1083-1090
        • Boggio PS
        • Zaghi S
        • Fregni F
        Modulation of emotions associated with images of human pain using anodal transcranial direct current stimulation (tDCS).
        Neuropsychologia. 2009; 47: 212-217
        • Bradley MM
        • Lang PJ
        Measuring emotion: The self-assessment manikin and the semantic differential.
        J Behav Ther Exp Psychiatry. 1994; 25: 49-59
        • Burns JW
        • Kubilus A
        • Bruehl S
        Emotion induction moderates effects of anger management style on acute pain sensitivity.
        Pain. 2003; 106: 109-118
        • Bushnell MC
        • Ceko M
        • Low LA
        Cognitive and emotional control of pain and its disruption in chronic pain.
        Nat Rev Neurosci. 2013; 14: 502-511
        • Chan CWY
        • Dallaire M
        Subjective pain sensation is linearly correlated with the flexion reflex in man.
        Brain Res. 1989; 479: 145-150
        • Deldar Z
        • Rustamov N
        • Blanchette I
        • Piché M
        Improving working memory and pain inhibition in older persons using transcranial direct current stimulation.
        Neurosci Res. 2019; 148: 19-27
        • Deldar Z
        • Rustamov N
        • Bois S
        • Blanchette I
        • Piché M
        Enhancement of pain inhibition by working memory with anodal transcranial direct current stimulation of the left dorsolateral prefrontal cortex.
        J Physiol Sci. 2018; 68: 825-836
        • DelVentura JL
        • Terry EL
        • Bartley EJ
        • Rhudy JL
        Emotional modulation of pain and spinal nociception in persons with severe insomnia symptoms.
        Ann Behav Med. 2014; 47: 303-315
        • Doig GS
        • Simpson F
        Randomization and allocation concealment: a practical guide for researchers.
        J Crit Care. 2005; 20: 187-191
        • Ferreira-Valente MA
        • Pais-Ribeiro JL
        • Jensen MP
        Validity of four pain intensity rating scales.
        Pain. 2011; 152: 2399-2404
        • France CR
        • France JL
        • al'Absi M
        • Ring C
        • McIntyre D
        Catastrophizing is related to pain ratings, but not nociceptive flexion reflex threshold.
        Pain. 2002; 99: 459-463
        • Hadjipavlou G
        • Dunckley P
        • Behrens TE
        • Tracey I
        Determining anatomical connectivities between cortical and brainstem pain processing regions in humans: a diffusion tensor imaging study in healthy controls.
        Pain. 2006; 123: 169-178
        • Hashmi JA
        • Baliki MN
        • Huang L
        • Baria AT
        • Torbey S
        • Hermann KM
        • Schnitzer TJ
        • Apkarian A V
        Shape shifting pain: chronification of back pain shifts brain representation from nociceptive to emotional circuits.
        Brain. 2013; 136: 2751-2768
        • Hellman N
        • Kuhn BL
        • Lannon EW
        • Payne MF
        • Sturycz CA
        • Palit S
        • Shadlow JO
        • Rhudy JL
        Emotional modulation of pain and spinal nociception in sexual assault survivors.
        Psychosom Med. 2018; 80: 861-868
        • Hox JJ
        • Moerbeek M
        • van de Schoot R
        Multilevel Analysis: Techniques and Applications.
        Routledge, New York, NY2010
        • Huber F
        • Kuhn B
        • Lannon E
        • Sturycz C
        • Payne M
        • Hellman N
        • Toledo T
        • Güereca Y
        • Demuth M
        • Palit S
        (263) Less Efficient Endogenous Inhibition of Spinal Nociception Predicts Chronic Pain Onset: A Prospective Analysis from the Oklahoma Study of Native American Pain Risk (OK-SNAP).
        J Pain. 2019; 20: S40
        • Jensen MP
        • Chen C
        • Brugger AM
        Interpretation of visual analog scale ratings and change scores: a reanalysis of two clinical trials of postoperative pain.
        J Pain. 2003; 4: 407-414
        • Kuo MF
        • Nitsche MA
        Exploring prefrontal cortex functions in healthy humans by transcranial electrical stimulation.
        Neurosci Bull. 2015; 31: 198-206
        • Lang P
        • Bradley MM
        The International Affective Picture System (IAPS) in the study of emotion and attention.
        in: Coan JA Allen JJ Handb Emot Elicitation Assess. Oxford University Press, New York, NY2007
        • Lang PJ
        • Bradley MM
        • Cuthbert BN
        International Affective Picture System (IAPS): Technical Manual and Affective Ratings.
        NIMH Cent Study Emot Atten. 1997; : 39-58
        • Maeoka H
        • Matsuo A
        • Hiyamizu M
        • Morioka S
        • Ando H
        Influence of transcranial direct current stimulation of the dorsolateral prefrontal cortex on pain related emotions: A study using electroencephalographic power spectrum analysis.
        Neurosci Lett. 2012; 512: 12-16
        • Mariano TY
        • van't Wout M
        • Garnaat SL
        • Rasmussen SA
        • Greenberg BD
        Transcranial Direct Current Stimulation (tDCS) Targeting Left Dorsolateral Prefrontal Cortex Modulates Task-Induced Acute Pain in Healthy Volunteers.
        Pain Med. 2016; 17: 737-745
        • Naylor JC
        • Borckardt JJ
        • Marx CE
        • Hamer RM
        • Fredrich S
        • Reeves ST
        • George MS
        Cathodal and anodal left prefrontal tDCS and the perception of control over pain.
        Clin J Pain. 2014; 30: 693-700
        • Nitsche MA
        • Koschack J
        • Pohlers H
        • Hullemann S
        • Paulus W
        • Happe S
        Effects of frontal transcranial direct current stimulation on emotional state and processing in healthy humans.
        Front psychiatry. 2012; 3: 58
        • Nitsche MA
        • Paulus W
        Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans.
        Neurology. 2001; 57: 1899-1901
        • O'Connell NE
        • Wand BM
        • Marston L
        • Spencer S
        • Desouza LH
        Non-invasive brain stimulation techniques for chronic pain.
        Cochrane database Syst Rev. 2014; 4CD008208
        • Ossipov MH
        • Morimura K
        • Porreca F
        Descending pain modulation and chronification of pain.
        Curr Opin Support Palliat Care. 2014; 8: 143-151
        • Palit S
        • Kerr KL
        • Kuhn BL
        • DelVentura JL
        • Terry EL
        • Bartley EJ
        • Shadlow JO
        • Rhudy JL
        Examining emotional modulation of pain and spinal nociception in Native Americans: A preliminary investigation.
        Int J Psychophysiol. 2013; 90: 272-281
        • Palit S
        • Sheaff RJ
        • France CR
        • McGlone ST
        • Potter WT
        • Harkness AR
        • McNulty JL
        • Bartley EJ
        • Hoffmann R
        • Monda JK
        • Rhudy JL
        Serotonin transporter gene (5-HTTLPR) polymorphisms are associated with emotional modulation of pain but not emotional modulation of spinal nociception.
        Biol Psychol. 2011; 86: 360-369
        • Poreisz C
        • Boros K
        • Antal A
        • Paulus W
        Safety aspects of transcranial direct current stimulation concerning healthy subjects and patients.
        Brain Res Bull. 2007; 72: 208-214
      1. Price DD, McGrath PA, Rafii A, Buckingham B: The validation of visual analogue scales as ratio scale measures for chronic and experimental pain. 17:45–56, 1983.

        • Rhudy JL
        • Bartley EJ
        • Williams AE
        Habituation, sensitization, and emotional valence modulation of pain responses.
        Pain. 2010; 148: 320-327
        • Rhudy JL
        • Bartley EJ
        • Williams AE
        • McCabe KM
        • Chandler MC
        • Russell JL
        • Kerr KL
        Are there sex differences in affective modulation of spinal nociception and pain?.
        J Pain. 2010; 11: 1429-1441
        • Rhudy JL
        • Delventura JL
        • Terry EL
        • Bartley EJ
        • Olech E
        • Palit S
        • Kerr KL
        Emotional modulation of pain and spinal nociception in fibromyalgia.
        Pain. 2013; 154: 1045-1056
        • Rhudy JL
        • France CR
        Defining the nociceptive flexion reflex (NFR) threshold in human participants: A comparison of different scoring criteria.
        Pain. 2007; 128: 244-253
        • Rhudy JL
        • France CR
        Reliability and validity of a brief method to assess nociceptive flexion reflex (NFR) threshold.
        J Pain. 2011; 12: 782-791
        • Rhudy JL
        • France CR
        • Bartley EJ
        • Williams AE
        • McCabe KM
        • Russell JL
        Does pain catastrophizing moderate the relationship between spinal nociceptive processes and pain sensitivity?.
        J Pain. 2009; 10: 860-869
        • Rhudy JL
        • Meagher MW
        The role of emotion in pain modulation.
        Curr Opin Psychiatry. 2001; 14: 241-245
        • Rhudy JL
        • Williams AE
        • McCabe KM
        • Nguyen MA
        • Rambo P
        Affective modulation of nociception at spinal and supraspinal levels.
        Psychophysiology. 2005; 42: 579-587
        • Rhudy JL
        • Williams AE
        • McCabe KM
        • Rambo PL
        • Russell JL
        Emotional modulation of spinal nociception and pain: The impact of predictable noxious stimulation.
        Pain. 2006; 126: 221-233
        • Rhudy JL
        • Williams AE
        • McCabe KM
        • Russell JL
        • Maynard LJ
        Emotional control of nociceptive reactions (ECON): do affective valence and arousal play a role?.
        Pain. 2008; 136: 250-261
        • Roy M
        • Piché M
        • Chen J-I
        • Peretz I
        • Rainville P
        Cerebral and spinal modulation of pain by emotions.
        Proc Natl Acad Sci. 2009; 106: 20900-20905
        • Stagg CJ
        • Nitsche MA
        Physiological basis of transcranial direct current stimulation.
        Neuroscientist. 2011; 17: 37-53
        • Terney D
        • Bergmann I
        • Poreisz C
        • Chaieb L
        • Boros K
        • Nitsche MA
        • Paulus W
        • Antal A
        Pergolide Increases the Efficacy of Cathodal Direct Current Stimulation to Reduce the Amplitude of Laser-Evoked Potentials in Humans.
        J Pain Symptom Manage. 2008; 36: 79-91
        • Terry EL
        • Delventura JL
        • Bartley EJ
        • Vincent AL
        • Rhudy JL
        Emotional modulation of pain and spinal nociception in persons with major depressive disorder (MDD).
        Pain. 2013; 154: 2759-2768
        • Vaseghi B
        • Zoghi M
        • Jaberzadeh S
        Differential effects of cathodal transcranial direct current stimulation of prefrontal, motor and somatosensory cortices on cortical excitability and pain perception - a double-blind randomised sham-controlled study.
        Eur J Neurosci. 2015; 42: 2426-2437
        • Vaseghi B
        • Zoghi M
        • Jaberzadeh S
        How does anodal transcranial direct current stimulation of the pain neuromatrix affect brain excitability and pain perception? A randomised, double-blind, sham-control study.
        PLoS One. 2015; 10: 1-21
        • Woods AJ
        • Antal A
        • Bikson M
        • Boggio PS
        • Brunoni AR
        • Celnik P
        • Cohen LG
        • Fregni F
        • Herrmann CS
        • Kappenman ES
        • Knotkova H
        • Liebetanz D
        • Miniussi C
        • Miranda PC
        • Paulus W
        • Priori A
        • Reato D
        • Stagg C
        • Wenderoth N
        • Nitsche MA
        A technical guide to tDCS, and related non-invasive brain stimulation tools.
        Clin. Neurophysiol. 2016; 127: 1031-1048