Advertisement

Sadness Enhances the Experience of Pain and Affects Pain-Evoked Cortical Activities: An MEG Study

  • Atsuo Yoshino
    Affiliations
    Department of Psychiatry and Neurosciences, Division of Frontier Graduate School of Biomedical Sciences, Hiroshima University, 1-2-3 Kasumi, Minami-ku, Hiroshima, 734-8551, Japan
    Search for articles by this author
  • Yasumasa Okamoto
    Affiliations
    Department of Psychiatry and Neurosciences, Division of Frontier Graduate School of Biomedical Sciences, Hiroshima University, 1-2-3 Kasumi, Minami-ku, Hiroshima, 734-8551, Japan
    Search for articles by this author
  • Keiichi Onoda
    Affiliations
    Department of Neurology, Faculty of Medicine, Shimane University, 89-1, Enyacho, Izumo, 693-8501, Japan
    Search for articles by this author
  • Kazuhiro Shishida
    Affiliations
    Department of Psychiatry and Neurosciences, Division of Frontier Graduate School of Biomedical Sciences, Hiroshima University, 1-2-3 Kasumi, Minami-ku, Hiroshima, 734-8551, Japan
    Search for articles by this author
  • Shinpei Yoshimura
    Affiliations
    Department of Psychiatry and Neurosciences, Division of Frontier Graduate School of Biomedical Sciences, Hiroshima University, 1-2-3 Kasumi, Minami-ku, Hiroshima, 734-8551, Japan
    Search for articles by this author
  • Yoshihiko Kunisato
    Affiliations
    Department of Psychiatry and Neurosciences, Division of Frontier Graduate School of Biomedical Sciences, Hiroshima University, 1-2-3 Kasumi, Minami-ku, Hiroshima, 734-8551, Japan
    Search for articles by this author
  • Yoshihiko Demoto
    Affiliations
    Department of Psychiatry and Neurosciences, Division of Frontier Graduate School of Biomedical Sciences, Hiroshima University, 1-2-3 Kasumi, Minami-ku, Hiroshima, 734-8551, Japan
    Search for articles by this author
  • Go Okada
    Affiliations
    Department of Psychiatry and Neurosciences, Division of Frontier Graduate School of Biomedical Sciences, Hiroshima University, 1-2-3 Kasumi, Minami-ku, Hiroshima, 734-8551, Japan
    Search for articles by this author
  • Shigeru Toki
    Affiliations
    Department of Psychiatry and Neurosciences, Division of Frontier Graduate School of Biomedical Sciences, Hiroshima University, 1-2-3 Kasumi, Minami-ku, Hiroshima, 734-8551, Japan
    Search for articles by this author
  • Hidehisa Yamashita
    Affiliations
    Department of Psychiatry and Neurosciences, Division of Frontier Graduate School of Biomedical Sciences, Hiroshima University, 1-2-3 Kasumi, Minami-ku, Hiroshima, 734-8551, Japan
    Search for articles by this author
  • Shigeto Yamawaki
    Correspondence
    Address reprint requests to Dr. Shigeto Yamawaki, Department of Psychiatry and Neurosciences, Graduate School of Biomedical Sciences, Hiroshima University, 1-2-3 Kasumi, Minami-ku, Hiroshima 734-8551, Japan.
    Affiliations
    Department of Psychiatry and Neurosciences, Division of Frontier Graduate School of Biomedical Sciences, Hiroshima University, 1-2-3 Kasumi, Minami-ku, Hiroshima, 734-8551, Japan
    Search for articles by this author

      Abstract

      Pain is a multidimensional phenomenon. Previous psychological studies have shown that a person’s subjective pain threshold can change when certain emotions are recognized. We examined this association with magnetoencephalography. Magnetic field strength was recorded with a 306-channel neuromagnetometer while 19 healthy subjects (7 female, 12 male; age range = 20–30 years) experienced pain stimuli in different emotional contexts induced by the presentation of sad, happy, or neutral facial stimuli. Subjects also rated their subjective pain intensity. We hypothesized that pain stimuli were affected by sadness induced by facial recognition. We found: 1) the intensity of subjective pain ratings increased in the sad emotional context compared to the happy and the neutral contexts, and 2) event-related desynchronization of lower beta bands in the right hemisphere after pain stimuli was larger in the sad emotional condition than in the happy emotional condition. Previous studies have shown that event-related desynchronization in these bands could be consistently observed over the primary somatosensory cortex. These findings suggest that sadness can modulate neural responses to pain stimuli, and that brain processing of pain stimuli had already been affected, at the level of the primary somatosensory cortex, which is critical for sensory processing of pain.

      Perspective

      We found that subjective pain ratings and cortical beta rhythms after pain stimuli are influenced by the sad emotional context. These results may contribute to understanding the broader relationship between pain and negative emotion.

      Key words

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

        • Apkarian A.V.
        • Bushnell M.C.
        • Treede R.D.
        • Zubieta J.K.
        Human brain mechanisms of pain perception and regulation in health and disease.
        Eur J Pain. 2005; 9: 463-484
        • Babiloni C.
        • Capotosto P.
        • Brancucci A.
        • Del Percio C.
        • Petrini L.
        • Buttiglione M.
        • Cibelli G.
        • Romani G.
        • Rossini P.
        • Arendt-Nielsen L.
        Cortical alpha rhythms are related to the anticipation of sensorimotor interaction between painful stimuli and movements: A high-resolution EEG study.
        J Pain. 2008; 9: 902-911
        • Beck A.T.
        • Ward C.H.
        • Mendelson M.
        • Mock J.
        • Erbaugh J.
        An inventory for measuring depression.
        Arch Gen Psychiatry. 1961; 4: 561-571
        • Breslau N.
        • Lipton R.B.
        • Stewart W.F.
        • Schultz L.R.
        • Welch K.M.A.
        Comorbidity of migraine and depression: Investigating potential etiology and prognosis.
        Neurology. 2003; 60: 1308
        • Carroll L.J.
        • Cassidy J.D.
        • Côté P.
        Depression as a risk factor for onset of an episode of troublesome neck and low back pain.
        Pain. 2004; 107: 134-139
        • Chen R.
        • Yaseen Z.
        • Cohen L.G.
        • Hallett M.
        Time course of corticospinal excitability in reaction time and self-paced movements.
        Ann Neurol. 1998; 44: 317-325
        • Del Percio C.
        • Le Pera D.
        • Arendt-Nielsen L.
        • Babiloni C.
        • Brancucci A.
        • Chen A.C.N.
        • De Armas L.
        • Miliucci R.
        • Restuccia D.
        • Valeriani M.
        Distraction affects frontal alpha rhythms related to expectancy of pain: An EEG study.
        Neuroimage. 2006; 31: 1268-1277
        • Ellsworth P.C.
        • Smith C.A.
        From appraisal to emotion: Differences among unpleasant feelings.
        Motiv Emot. 1988; 12: 271-302
        • Friedman D.P.
        • Murray E.A.
        • O’Neill J.B.
        • Mishkin M.
        Cortical connections of the somatosensory fields of the lateral sulcus of macaques: Evidence for a corticolimbic pathway for touch.
        J Comp Neurol. 1986; 252: 323-347
        • Hari R.
        • Salmelin R.
        Human cortical oscillations: A neuromagnetic view through the skull.
        Trends Neurosci. 1997; 20: 44-49
        • Haxby J.V.
        • Hoffman E.A.
        • Gobbini M.I.
        The distributed human neural system for face perception.
        Trends Cogn Sci. 2000; 4: 223-232
        • Iannetti G.D.
        • Hughes N.P.
        • Lee M.C.
        • Mouraux A.
        Determinants of laser-evoked EEG responses: Pain perception or stimulus saliency?.
        J Neurophysiol. 2008; 100: 815-828
        • Inui K.
        • Tran T.D.
        • Hoshiyama M.
        • Kakigi R.
        Preferential stimulation of Adelta fibers by intra-epidermal needle electrode in humans.
        Pain. 2002; 96: 247-252
        • Inui K.
        • Tran T.D.
        • Qiu Y.
        • Wang X.
        • Hoshiyama M.
        • Kakigi R.
        Pain-related magnetic fields evoked by intra-epidermal electrical stimulation in humans.
        Clin Neurophysiol. 2002; 113: 298-304
        • Inui K.
        • Tsuji T.
        • Kakigi R.
        Temporal analysis of cortical mechanisms for pain relief by tactile stimuli in humans.
        Cereb Cortex. 2006; 16: 355-365
        • Kamachi M.
        • Bruce V.
        • Mukaida S.
        • Gyoba J.
        • Yoshikawa S.
        • Akamatsu S.
        Dynamic properties influence the perception of facial expressions.
        Perception. 2001; 30: 875-887
        • Killgore W.D.
        • Yurgelun-Todd D.A.
        Activation of the amygdala and anterior cingulate during nonconscious processing of sad versus happy faces.
        Neuroimage. 2004; 21: 1215-1223
        • Morris J.S.
        • Frith C.D.
        • Perrett D.I.
        • Rowland D.
        • Young A.W.
        • Calder A.J.
        • Dolan R.J.
        A differential neural response in the human amygdala to fearful and happy facial expressions.
        Nature. 1996; 383: 812-815
        • Mouraux A.
        • Iannetti G.D.
        Across-trial averaging of event-related EEG responses and beyond.
        Magn Reson Imaging. 2008; 26: 1041-1054
        • Ochsner K.N.
        • Ludlow D.H.
        • Knierim K.
        • Hanelin J.
        • Ramachandran T.
        • Glover G.C.
        • Mackey S.C.
        Neural correlates of individual differences in pain-related fear and anxiety.
        Pain. 2006; 120: 69-77
        • Ohara S.
        • Crone N.E.
        • Weiss N.
        • Lenz F.A.
        Analysis of synchrony demonstrates ‘pain networks’ defined by rapidly switching, task-specific, functional connectivity between pain-related cortical structures.
        Pain. 2006; 123: 244-253
        • Ohara S.
        • Crone N.E.
        • Weiss N.
        • Lenz F.A.
        Attention to a painful cutaneous laser stimulus modulates electrocorticographic event-related desynchronization in humans.
        Clin Neurophysiol. 2004; 115: 1641-1652
        • Ohara S.
        • Crone N.E.
        • Weiss N.
        • Treede R.D.
        • Lenz F.A.
        Amplitudes of laser evoked potential recorded from primary somatosensory, parasylvian and medial frontal cortex are graded with stimulus intensity.
        Pain. 2004; 110: 318-328
        • Onoda K.
        • Okamoto Y.
        • Shishida K.
        • Hashizume A.
        • Ueda K.
        • Yamashita H.
        • Yamawaki S.
        Anticipation of affective images and event-related desynchronization (ERD) of alpha activity: An MEG study.
        Brain research. 2007; 1151: 134-141
        • Penfield W.
        • Boldrey E.
        Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation.
        Brain. 1937; 60: 389-443
        • Pfurtscheller G.
        Event-related synchronization (ERS): An electrophysiological correlate of cortical areas at rest.
        Electroencephalogr Clin Neurophysiol. 1992; 83: 62-69
        • Pfurtscheller G.
        • Lopes da Silva F.H.
        Event-related EEG/MEG synchronization and desynchronization: Basic principles.
        Clin Neurophysiol. 1999; 110: 1842-1857
        • Phillips M.L.
        • Gregory L.J.
        • Cullen S.
        • Coen S.
        • Ng V.
        • Andrew C.
        • Giampietro V.
        • Bullmore E.
        • Zelaya F.
        • Amaro E.
        • Thompson D.G.
        • Hobson A.R.
        • Williams S.C.
        • Brammer M.
        • Aziz Q.
        The effect of negative emotional context on neural and behavioural responses to oesophageal stimulation.
        Brain. 2003; 126: 669-684
        • Phillips M.L.
        • Young A.W.
        • Senior C.
        • Brammer M.
        • Andrew C.
        • Calder A.J.
        • Bullmore E.T.
        • Perrett D.I.
        • Rowland D.
        • Williams S.C.
        • Gray J.A.
        • David A.S.
        A specific neural substrate for perceiving facial expressions of disgust.
        Nature. 1997; 389: 495-498
        • Ploghaus A.
        • Narain C.
        • Beckmann C.F.
        • Clare S.
        • Bantick S.
        • Wise R.
        • Matthews P.M.
        • Rawlins J.N.P.
        • Tracey I.
        Exacerbation of pain by anxiety is associated with activity in a hippocampal network.
        J Neurosci. 2001; 21: 9896-9903
        • Ploner M.
        • Freund H.J.
        • Schnitzler A.
        Pain affect without pain sensation in a patient with a postcentral lesion.
        Pain. 1999; 81: 211-214
        • Ploner M.
        • Gross J.
        • Timmermann L.
        • Pollok B.
        • Schnitzler A.
        Pain suppresses spontaneous brain rhythms.
        Cereb Cortex. 2006; 16: 537-540
        • Ploner M.
        • Schmitz F.
        • Freund H.J.
        • Schnitzler A.
        Parallel activation of primary and secondary somatosensory cortices in human pain processing.
        J Neurophysiol. 1999; 81: 3100-3104
        • Price D.D.
        Central neural mechanisms that interrelate sensory and affective dimensions of pain.
        Mol Interv. 2002; 2: 392-403
        • Price J.L.
        Comparative aspects of amygdala connectivity.
        Ann N Y Acad Sci. 2003; 985: 50-58
        • Raij T.T.
        • Forss N.
        • Stancak A.
        • Hari R.
        Modulation of motor-cortex oscillatory activity by painful Aδ-and C-fiber stimuli.
        Neuroimage. 2004; 23: 569-573
        • Shishida K.
        • Hashizume A.
        • Onoda K.
        • Okamoto Y.
        • Yamawaki S.
        Enhanced reactivity and delayed recovery of sensorimotor cortex in the novelty seeking personality.
        Neuropsychobiology. 2006; 54: 215-225
        • Spielberger C.D.
        Manual for the State-Trait Anxiety Inventory (STAI).
        Consulting Psychologists Press, Palo Alto, CA1983
        • Stancak A.
        Cortical oscillatory changes occurring during somatosensory and thermal stimulation.
        Prog Brain Res. 2006; 159: 237-252
        • Tamura Y.
        • Hoshiyama M.
        • Nakata H.
        • Hiroe N.
        • Inui K.
        • Kaneoke Y.
        • Inoue K.
        • Kakigi R.
        Functional relationship between human rolandic oscillations and motor cortical excitability: An MEG study.
        Eur J Neurosci. 2005; 21: 2555-2562
        • Torquati K.
        • Pizzella V.
        • Della Penna S.
        • Franciotti R.
        • Babiloni C.
        • Romani G.L.
        • Rossini P.M.
        “Gating” effects of simultaneous peripheral electrical stimulations on human secondary somatosensory cortex: A whole-head MEG study.
        Neuroimage. 2003; 20: 1704-1713
        • Wagner G.
        • Koschke M.
        • Leuf T.
        • Schlosser R.
        • Bar K.J.
        Reduced heat pain thresholds after sad-mood induction are associated with changes in thalamic activity.
        Neuropsychologia. 2009; 47: 980-987
        • Yoshino A.
        • Okamoto Y.
        • Onoda K.
        • Yoshimura S.
        • Kunisato Y.
        • Demoto Y.
        • Okada G.
        • Yamawaki S.
        Sadness enhances the experience of pain via neural activation in the anterior cingulate cortex and amygdala: An fMRI study.
        Neuroimage. 2010; 50: 1194-1201
        • Zelman D.C.
        • Howland E.W.
        • Nichols S.N.
        • Cleeland C.S.
        The effects of induced mood on laboratory pain.
        Pain. 1991; 46: 105-111