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Research Article| Volume 276, ISSUE 1-2, P153-158, January 15, 2009

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Hyperalgesia and laser evoked potentials alterations in hemiparkinson: Evidence for an abnormal nociceptive processing

      Abstract

      A number of patients with Parkinson's Disease (PD) complain of painful sensations that might be related not only to peripheral factors (muscle spasms, postural abnormalities) but also to an abnormal processing of nociceptive inputs in the Central Nervous System (CNS).
      To test this hypothesis, we recorded scalp CO2 laser evoked potentials (LEPs) to foot skin stimulation in 11 pain-free treated PD patients affected by hemiparkinson (during the off state), in 6 pain-free drug-naïve hemiparkinsonian patients and in 11 healthy subjects. After each LEP recording, both patients and controls were asked to rate pain due to laser stimuli.
      In all subjects, CO2 laser stimulation gave rise to a main negative N2 potential followed by a positive P2 response at vertex peaking at a latency of about 250 and 350 ms respectively which are thought to originate from several brain structures devoted to nociceptive input processing, including the cingulate gyrus and insula.
      ANOVA showed that the N2/P2 amplitude was significantly lower and pain rating significantly increased in treated PD patients than in controls in both the affected and unaffected sides, while in drug-naïve PD patients the reduction of the N2/P2 amplitude and the increase in pain rating were observed only in the affected side.
      These results suggest that in pain-free PD patients there is an abnormal nociceptive input processing that may be independent of the clinical expression of parkinsonian motor signs.

      Keywords

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      References

        • Chudler E.H.
        • Dong W.K.
        The role of the basal ganglia in nociception and pain.
        Pain. 1995; 60: 3-38
        • Tinazzi M.
        • Fiaschi A.
        • Frasson E.
        • Fiorio M.
        • Cortese F.
        • Aglioti S.M.
        Deficits of temporal discrimination in dystonia are independent from the spatial distance between the loci of tactile stimulation.
        Mov Disord. 2002; 17: 333-338
        • Aglioti S.M.
        • Fiorio M.
        • Forster B.
        • Tinazzi M.
        Temporal discrimination of cross-modal and unimodal stimuli in generalized distonia.
        Neurology. 2003; 60: 782-785
        • Fiorio M.
        • Stanzani C.
        • Rothwell J.C.
        • Bhatia K.P.
        • Moretto G.
        • Fiaschi A.
        • et al.
        Defective temporal discrimination of passive movements in Parkinson's disease.
        Neurosci Lett. 2007; 45: 312-315
        • Snider S.R.
        • Fahn S.
        • Isgreen W.P.
        • Cote L.J.
        Primary sensory symptoms in parkinsonism.
        Neurology. 1976; 26: 423-429
        • Goetz C.G.
        • Tanner Ca.M.
        • Levy M.
        • Wilson R.S.
        • Garron D.C.
        Pain in Parkinson's disease.
        Mov Disord. 1986; 1: 45-49
        • Ford B.
        Pain in Parkinson's disease.
        Clin Neurosci. 1998; 5: 63-72
        • Sage J.I.
        Pain in Parkinson's Disease.
        Curr Treat Options Neurol. 2004; 6: 191-200
        • Giuffrida R.
        • Vingerhoets F.J.G.
        • Bogousslavsky J.
        • Ghika J.
        Syndromes doulourex de la maladie de Parkinson.
        Rev Neurol. 2005; 161: 407-418
        • Tinazzi M.
        • Del Vesco C.
        • Fincati E.
        • et al.
        Pain and motor complications in Parkinson's disease.
        J Neurol Neurosurg Psychiatry. 2006; 77: 822-825
        • Djaldetti R.
        • Shifrin A.M.D.
        • Rogowski Z.
        • Sprecher E.
        • Melamed E.
        • Yamitsky D.
        Quantitative measurement of pain sensation in patients with Parkinson disease.
        Neurology. 2004; 62: 2171-2175
        • Brefel-Courbon C.
        • Payoux P.
        • Thalama C.
        • et al.
        Effect of levodopa on pain threshold in Parkinson's disease: a clinical and positron emission tomography study.
        Mov Disord. 2005; 20: 1557-1563
        • Rainville P.
        • Duncan G.H.
        • Price D.D.
        • Carrier B.
        • Bushnell M.C.
        Pain affect encoded in human anterior cingulate but not somatosensory cortex.
        Science. 1997; 277: 968-971
        • Davis K.D.
        • Kwan C.L.
        • Crawley A.P.
        • Mikulis D.J.
        Event-related fMRI of pain: entering a new era in imaging pain.
        Neuroreport. 1998; 9: 3019-3023
        • Apkarian A.V.
        Functional magnetic resonance imaging of pain consciousness: cortical networks of pain critically depend on what is implied by “pain”.
        Curr Rev Pain. 1999; 3: 308-315
        • Rainville P.
        • Hofbauer R.K.
        • Paus T.
        • Duncan G.H.
        • Bushnell M.C.
        • Price D.D.
        Cerebral mechanisms of hypnotic induction and suggestion.
        J Cogn Neurosi. 1999; 11: 110-125
        • Davis K.D.
        The neural circuitry of pain as explored with functional MRI.
        Neurol Res. 2000; 22: 313-317
        • Bromm B.
        • Lorenz J.
        Neurophysiological evaluation of pain.
        Electroenceph Clin Neurophysiol. 1998; 107: 227-253
        • Lenz F.A.
        • Rios M.
        • Chau D.
        • Krauss G.L.
        • Zirh T.A.
        • Lesser R.P.
        Painful stimuli evoke potentials recorded over the human anterior cingulate gyrus.
        J Neurophysiol. 1998; 79: 2231-2234
        • Frot M.
        • Rambaud L.
        • Guenot M.
        • Mauguiere F.
        Intracortical recordings of early pain-related CO2-laser evoked potentials in the human second somatosensory (SII) area.
        Clin Neurophysiol. 1999; 110: 133-145
        • Bentley D.E.
        • Derbyshire S.W.
        • Youell P.D.
        • Jones A.K.
        Caudal cingulate cortex involvement in pain processing: an inter-individual laser evoked potential source localisation study using realistic head models.
        Pain. 2003; 102: 265-271
        • Garcia-Larrea L.
        • Frot M.
        • Valeriani M.
        Brain generators of laser-evoked potentials: from dipoles to functional significance.
        Neurophysiol Clin-Clin Neurophysiol. 2003; 33: 279-292
        • Treede R.D.
        • Lorenz J.
        • Baumgartner U.
        Clinical usefulness of laser-evoked potentials.
        Neurophysiol Clin-Clin Neurophysiol. 2003; 33: 303-314
        • 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
        • Tinazzi M.
        • Del Vesco C.
        • Defazio G.
        • et al.
        Abnormal processing of the nociceptive input in Parkinson's disease: a study with CO2 laser evoked potentials.
        Pain. 2008;
        • Valeriani M.
        • Rambaud L.
        • Mauguière F.
        Scalp topography and dipolar source modelling of potentials evoked by CO2 laser stimulation of the hand.
        Electroenceph Clin Neurophysiol. 1996; 100: 343-353
        • Huttunen J.
        • Teravainen H.
        Pre- and postcentral cortical somatosensory evoked potentials in hemiparkinsonism.
        Mov Disord. 1993; 4: 430-436
        • Guekht A.
        • Selikhova M.
        • Serkin G.
        • Gusev E.
        Implementation of the TMS in the early stages of Parkinson's disease.
        Electromyogr Clin Neurophysiol. 2005; 45: 291-297
        • Brooks D.J.
        Detection of preclinical Parkinson's disease.
        Geriatrics. 1991; 46: 25-30
        • Fearnley J.M.
        • Lees A.J.
        Ageing and Parkinson's disease: substantia nigra regional selectivity.
        Brain. 1991; 114: 2283-2301
        • Benamer H.T.S.
        • Patterson J.
        • Grosset D.G.
        Accurate differentiation of Parkinsonism and Essential Tremor using visual assessment of [123I]FP-CIT SPET imaging: the [123I]FP-CIT SPET Study Group.
        Mov Disord. 2000; 15: 503-510
        • Marek K.L.
        • Seibyl J.P.
        • Zoghbi S.S.
        • et al.
        [123I]β CIT/SPET imaging demonstrates bilateral loss of dopamine transporters in hemiparkinson's disease.
        Neurology. 1996; 46: 231-237
        • Wenning G.K.
        • Donnemiller E.
        • Granata R.
        • Riccabona G.
        • Poewe W.
        [123I]β CIT/SPET and [123I] IBZM-SPET scanning in l-dopa-naïve Parkinson's disease.
        Mov Disord. 1998; 13: 438-445
        • Valeriani M.
        • Restuccia D.
        • Barba C.
        • Le Pera D.
        • Tonali P.
        • Mauguiere F.
        Sources of cortical responses to painful CO(2) laser skin stimulation of the hand and foot in the human brain.
        Clin Neurophysiol. 2000; 111: 1103-1112
        • Vogt B.A.
        Pain and emotion interactions in subregions of the cingulate gyrus.
        Nat Rev Neurosci. 2005; 6: 533-544
        • Buchel C.
        • Bornhovd K.
        • Quante M.
        • Glauche V.
        • Bromm B.
        • Weiller C.
        Dissociable neural responses related to pain intensity, stimulus intensity, and stimulus awareness within the anterior cingulate cortex: a parametric single-trial laser functional magnetic resonance imaging study.
        J Neurosci. 2002; 22: 970-976
        • Gerdelat-Mas A.
        • Simonetta-Moreau M.
        • Thalamas C.
        • Ory-Magne F.
        • Slaoui T.
        • Rascol O.
        • et al.
        Levodopa raises objective pain threshold in Parkinson's disease: a RIII reflex study.
        J Neurol Neurosurg Psychiatry. 2007; 78: 1140-1142
        • Schestatsky P.
        • Kumru H.
        • Valls-Solè J.
        • Valldeoriola F.
        • Marti M.
        • Tolosa E.
        • et al.
        Neurophysiologic study of central pain in patients with Parkinson disease.
        Neurology. 2007; 69: 2162-2169
        • Jurgens U.
        Afferent fibers to the cingular vocalization region in the squirrel monkey.
        Exp Neurol. 1983; 80: 395-409
        • Kemel M.L.
        • Desban M.
        • Gauchy C.
        • Glowinski J.
        • Besson M.J.
        Topographical organization of efferent projections from the cat substantia nigra pars reticulata.
        Brain Res. 1988; 455: 307-323
        • Casey K.L.
        • Beydoun A.
        • Boivie J.
        • et al.
        Laser-evoked cerebral potentials and sensory function in patients with central pain.
        Pain. 1996; 64: 485-491
        • Garcia-Larrea L.
        • Convers P.
        • Magnin M.
        • André-Obadia N.
        • Peyron R.
        • Laurent B.
        • et al.
        Laser-evoked potential abnormalities in central pain patients: the influence of spontaneous and provoked pain.
        Brain. 2002; 125: 2766-2781
        • Valeriani M.
        • Arendt-Nielsen L.
        • Le Pera D.
        • et al.
        Short-term plastic changes of the human nociceptive system following acute pain induced by capsaicin.
        Clin Neurophysiol. 2003; 114: 1879-1890
        • Arendt-Nielsen L.
        • Andersen O.K.
        • Jensen T.S.
        Brief, prolonged and repeated stimuli applied to hyperalgesic skin areas: a psychophysical study.
        Brain Res. 1996; 712: 165-167
      1. Defazio G, Berardelli A, Fabbrini G, et al. Pain as a nonmotor symptom of Parkinson's disease: evidence from a case–control study. Arch Neurol 2008;65:1191–4.