Advertisement
Research Article| Volume 19, ISSUE 8, P943-951, August 2018

Download started.

Ok

Assessment of Responsiveness to Everyday Non-Noxious Stimuli in Pain-Free Migraineurs With Versus Without Aura

      Highlights

      • Migraineurs show sensory over-responsiveness to everyday sensations.
      • Sensory over-responsiveness is more common in migraineurs with aura.
      • Attack frequency correlates with sensory over-responsiveness and pain summation.

      Abstract

      Migraineurs with aura (MWA) express higher interictal response to non-noxious and noxious experimental sensory stimuli compared with migraineurs without aura (MWoA), but whether these differences also prevail in response to everyday non-noxious stimuli is not yet explored. This is a cross-sectional study testing 53 female migraineurs (30 MWA; 23 MWoA) who underwent a wide battery of noxious psychophysical testing at a pain-free phase, and completed a Sensory Responsiveness Questionnaire and pain-related psychological questionnaires. The MWA group showed higher questionnaire-based sensory over-responsiveness (P = .030), higher magnitude of pain temporal summation (P = .031) as well as higher monthly attack frequency (P = .027) compared with the MWoA group. Overall, 45% of migraineurs described abnormal sensory (hyper- or hypo-) responsiveness; its incidence was higher among MWA (19 of 30, 63%) versus MWoA (6 of 23, 27%, P = .012), with an odds ratio of 3.58 for MWA. Sensory responsiveness scores were positively correlated with attack frequency (r = .361, P = .008) and temporal summation magnitude (r = .390, P = .004), both regardless of migraine type. MWA express higher everyday sensory responsiveness than MWoA, in line with higher response to experimental noxious stimuli. Abnormal scores of sensory responsiveness characterize people with sensory modulation dysfunction, suggesting possible underlying mechanisms overlap, and possibly high incidence of both clinical entities.

      Perspective

      This article presents findings distinguishing MWA, showing enhanced pain amplification, monthly attack frequency, and over-responsiveness to everyday sensations, compared with MWoA. Further, migraine is characterized by a high incidence of abnormal responsiveness to everyday sensation, specifically sensory over-responsiveness, that was also found related to pain.

      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

        • Ahn R.R.
        • Miller L.J.
        • Milberger S.
        • McIntosh D.N.
        Prevalence of parents' perceptions of sensory processing disorders among kindergarten children.
        Am J Occup Ther. 2004; 58: 287-293
        • Antal A.
        • Lang N.
        • Boros K.
        • Nitsche M.
        • Siebner H.R.
        • Paulus W.
        Homeostatic metaplasticity of the motor cortex is altered during headache-free intervals in migraine with aura.
        Cereb Cortex. 2008; 18: 2701-2705
        • Bar-Shalita T.
        • Cermak S.A.
        Atypical sensory modulation and psychological distress in the general population.
        Am J Occup Ther. 2016; 70: 1-9
        • Bar-Shalita T.
        • Deutsch L.
        • Honigman L.
        Ecological aspects of pain in sensory modulation disorder.
        Res Dev Disabil. 2015; 45: 157-167
        • Bar-Shalita T.
        • Seltzer Z.
        • Vatine J.J.
        • Yochman A.
        • Parush S.
        Development and psychometric properties of the Sensory Responsiveness Questionnaire (SRQ).
        Disabil Rehabil. 2009; 31: 189-201
        • Bar-Shalita T.
        • Vatine J.J.
        • Seltzer Z.
        • Parush S.
        Psychophysical correlates in adults with sensory modulation disorder.
        Disabil Rehabil. 2012; 34: 943-950
        • Bar-Shalita T.
        • Vatine J.J.
        • Yarnitsky D.
        • Parush S.
        • Weissman-Fogel I.
        Atypical central pain processing in sensory modulation disorder: Absence of temporal summation and higher after-sensation.
        Exp Brain Res. 2014; 232: 587-595
        • Bart O.
        • Bar-Shalita T.
        • Mansour H.
        • Dar R.
        Relationships among sensory responsiveness, anxiety, and ritual behaviors in children with and without atypical sensory responsiveness.
        Phys Occup Ther Pediatr. 2016; 37: 322-331
        • Ben-Sasson A.
        • Carter A.S.
        • Briggs-Gowan M.J.
        Sensory over-responsivity in elementary school: Prevalence and social-emotional correlates.
        J Abnorm Child Psychol. 2009; 37: 705-716
        • Borini C.A.
        • Gatti F.R.
        • Grezos R.M.
        • Fragoso Y.D.
        Odors as triggering and worsening factors in migraine.
        Rev Neurosc. 2008; 16: 38-40
        • Boulloche N.
        • Denuelle M.
        • Payoux P.
        • Fabre N.
        • Trotter Y.
        • Géraud G.
        Photophobia in migraine: An interictal PET study of cortical hyperexcitability and its modulation by pain.
        J Neurol Neurosurg Psychiatry. 2010; 81: 978-984
        • Brett-Green B.A.
        • Miller L.J.
        • Schoen S.A.
        • Nielsen D.M.
        An exploratory event-related potential study of multisensory integration in sensory over-responsive children.
        Brain Res. 2010; 1321: 67-77
        • Burstein R.
        • Jakubowski M.
        • Garcia-Nicas E.
        • Kainz V.
        • Bajwa Z.
        • Hargreaves R.
        • Becerra L.
        • Borsook D.
        Thalamic sensitization transforms localized pain into widespread allodynia.
        Ann Neurol. 2010; 68: 81-91
        • Conte A.
        • Barbanti P.
        • Frasca V.
        • Iacovelli E.
        • Gabriele M.
        • Giacomelli E.
        • Aurilia C.
        • Pichiorri F.
        • Gilio F.
        • Inghilleri M.
        Differences in short-term primary motor cortex synaptic potentiation as assessed by repetitive transcranial magnetic stimulation in migraine patients with and without aura.
        Pain. 2010; 148: 43-48
        • Cosentino G.
        • Fierro B.
        • Vigneri S.
        • Talamanca S.
        • Palermo A.
        • Puma A.
        • Brighina F.
        Impaired glutamatergic neurotransmission in migraine with aura? Evidence by an input-output curves transcranial magnetic stimulation study.
        Headache. 2011; 51: 726-733
        • Cucchiara B.
        • Datta R.
        • Aguirre G.K.
        • Idoko K.E.
        • Detre J.
        Measurement of visual sensitivity in migraine: Validation of two scales and correlation with visual cortex activation.
        Cephalalgia. 2015; 35: 585-592
        • de Tommaso M.
        • Difruscolo O.
        • Sardaro M.
        • Libro G.
        • Pecoraro C.
        • Serpino C.
        • Lamberti P.
        • Livrea P.
        Effects of remote cutaneous pain on trigeminal laser-evoked potentials in migraine patients.
        J Headache Pain. 2007; 8: 167-174
        • Datta R.
        • Aguirre G.K.
        • Hu S.
        • Detre J.A.
        • Cucchiara B.
        Interictal cortical hyperresponsiveness in migraine is directly related to the presence of aura.
        Cephalalgia. 2013; 33: 365-374
        • Davies P.L.
        • Chang W.P.
        • Gavin W.J.
        Maturation of sensory gating performance in children with and without sensory processing disorders.
        Int J Psychophysiol. 2009; 72: 187-197
        • Davies P.L.
        • Chang W.P.
        • Gavin W.J.
        Middle and late latency ERP components discriminate between adults, typical children, and children with sensory processing disorders.
        Front Integr Neurosci. 2010; 4: 16
        • Demarquay G.
        • Mauguière F.
        Central nervous system underpinnings of sensory hypersensitivity in migraine: Insights from neuroimaging and electrophysiological studies.
        Headache. 2016; 56: 1418-1438
        • Dunn W.
        • Little L.
        • Dean E.
        • Robertson S.
        • Evans B.
        The state of the science on sensory factors and their impact on daily life for children: A scoping review.
        OTJR (Thorofare N J). 2016; 36: 3S-26S
        • Engel-Yeger B.
        • Dunn W.
        Exploring the relationship between affect and sensory processing patterns in adults.
        Br J Occup Ther. 2011; 74: 456-464
        • Filatova E.
        • Latysheva N.
        • Kurenkov A.
        Evidence of persistent central sensitization in chronic headaches: A multi-method study.
        J Headache Pain. 2008; 9: 295-300
        • Florencio L.L.
        • Giantomassi M.C.
        • Carvalho G.F.
        • Gonçalves M.C.
        • Dach F.
        • Fernández-de-Las-Peñas C.
        • Bevilaqua-Grossi D.
        Generalized pressure pain hypersensitivity in the cervical muscles in women with migraine.
        Pain Med. 2015; 16: 1629-1634
        • Friedman D.I.
        • De ver Dye T.
        Migraine and the environment.
        Headache. 2009; 49: 941-952
        • Gierse-Plogmeier B.
        • Colak-Ekici R.
        • Wolowski A.
        • Gralow I.
        • Marziniak M.
        • Evers S.
        Differences in trigeminal and peripheral electrical pain perception in women with and without migraine.
        J Headache Pain. 2009; 10: 249-254
        • Harriott A.M.
        • Schwedt T.J.
        Migraine is associated with altered processing of sensory stimuli.
        Curr Pain Headache Rep. 2014; 18: 458
        • Hodkinson D.J.
        • Veggeberg R.
        • Kucyi A.
        • van Dijk K.R.
        • Wilcox S.L.
        • Scrivani S.J.
        • Burstein R.
        • Becerra L.
        • Borsook D.
        Cortico-cortical connections of primary sensory areas and associated symptoms in migraine.
        eNeuro. 2017; 3
        • Hodkinson D.J.
        • Wilcox S.L.
        • Veggeberg R.
        • Noseda R.
        • Burstein R.
        • Borsook D.
        • Becerra L.
        Amplitude of thalamocortical low-frequency oscillations in patients with migraine.
        J Neurosci. 2016; 36: 8026-8036
        • ICDL.
        Regulatory sensory processing disorder access 1, in Diagnostic Manual for Infancy and Early Childhood: Mental Health, Developmental, Regulatory–Sensory Processing and Language Disorders and Learning Challenges (ICDL–DMIC).
        (Bethesda, Maryland, USA)2005
        • Lauritzen M.
        Pathophysiology of the migraine aura. The spreading depression theory.
        Brain. 1994; 117: 199-210
        • Leekam S.R.
        • Nieto C.
        • Libby S.J.
        • Wing L.
        • Gould J.
        Describing the sensory abnormalities of children and adults with autism.
        J Autism Dev Disord. 2007; 37: 894-910
        • Lev R.
        • Granovsky Y.
        • Yarnitsky D.
        Enhanced pain expectation in migraine: EEG-based evidence for impaired prefrontal function.
        Headache. 2013; 53: 1054-1070
        • Maier J.
        • Sebastian I.
        • Weisbrod M.
        • Freitag C.M.
        • Resch F.
        • Bender S.
        Cortical inhibition at rest and under a focused attention challenge in adults with migraine with and without aura.
        Cephalalgia. 2011; 31: 914-924
        • Maleki N.
        • Becerra L.
        • Upadhyay J.
        • Burstein R.
        • Borsook D.
        Direct optic nerve pulvinar connections defined by diffusion MR tractography in humans: Implications for photophobia.
        Hum Brain Mapp. 2012; 33: 75-88
        • Meredith P.J.
        • Rappel G.
        • Strong J.
        • Bailey K.J.
        Sensory sensitivity and strategies for coping with pain.
        Am J Occup Ther. 2015; 69 (6904240010)
        • Miller L.J.
        • Anzalone M.E.
        • Lane S.J.
        • Cermak S.A.
        • Osten E.T.
        Concept evolution in sensory integration: A proposed nosology for diagnosis.
        Am J Occup Ther. 2007; 61: 135-140
        • Mouraux A.
        • Diukova A.
        • Lee M.C.
        • Wise R.G.
        • Iannetti G.D.
        A multisensory investigation of the functional significance of the “pain matrix.
        Neuroimage. 2011; 54: 2237-2249
        • Nahman-Averbuch H.
        • Granovsky Y.
        • Coghill R.C.
        • Yarnitsky D.
        • Sprecher E.
        • Weissman-Fogel I.
        Waning of “conditioned pain modulation”: A novel expression of subtle pronociception in migraine.
        Headache. 2013; 53: 1104-1115
        • Nguyen B.N.
        • McKendrick A.M.
        • Vingrys A.J.
        Abnormal inhibition-excitation imbalance in migraine.
        Cephalalgia. 2016; 36: 5-14
        • Noseda R.
        • Burstein R.
        Migraine pathophysiology: Anatomy of the trigeminovascular pathway and associated neurological symptoms, CSD, sensitization and modulation of pain.
        Pain. 2013; 154: S44-S53
        • Parush S.
        • Sohmer H.
        • Steinberg A.
        • Kaitz M.
        Somatosensory function in boys with ADHD and tactile defensiveness.
        Physiol Behav. 2007; 90: 553-558
        • PDM
        Psychodynamic Diagnostic Manual.
        Alliance of Psychoanalytic Organizations, Silver Spring, MD2016
        • Pietrobon D.
        • Moskowitz M.A.
        Pathophysiology of migraine.
        Annu Rev Physiol. 2013; 75: 365-391
        • Sand T.
        • Zhitniy N.
        • White L.R.
        • Stovner L.J.
        Visual evoked potential latency, amplitude and habituation in migraine: A longitudinal study.
        Clin Neurophysiol. 2008; 119: 1020-1027
        • Schwedt T.J.
        Multisensory integration in migraine.
        Curr Opin Neurol. 2013; 26: 248-253
        • Schwedt T.J.
        • Zuniga L.
        • Chong C.D.
        Low heat pain thresholds in migraineurs between attacks.
        Cephalalgia. 2015; 35: 593-599
        • Siniatchkin M.
        • Sendacki M.
        • Moeller F.
        • Wolff S.
        • Jansen O.
        • Siebner H.
        • Stephani U.
        Abnormal changes of synaptic excitability in migraine with aura.
        Cereb Cortex. 2012; 22: 2207-2216
        • Spielberger C.D.
        • O'Neil Jr, H.F.
        • Hansen D.N.
        Anxiety, drive theory, and computer-assisted learning.
        Prog Exp Pers Res. 1972; 6: 109-148
        • Sullivan M.
        • Bishop S.
        • Pivic J.
        The Pain Catastrophizing Scale: Development and validation.
        Psychol Assess. 1995; 7: 524-532
        • Tfelt-Hansen P.C.
        History of migraine with aura and cortical spreading depression from 1941 and onwards.
        Cephalalgia. 2010; 30: 780-792
        • Vanagaite J.
        • Pareja J.A.
        • Støren O.
        • White L.R.
        • Sand T.
        • Stovner L.J.
        Light-induced discomfort and pain in migraine.
        Cephalalgia. 1997; 17: 733-741
        • Vecchia D.
        • Pietrobon D.
        Migraine: A disorder of brain excitatory-inhibitory balance?.
        Trends Neurosci. 2012; 35: 507-520
        • Weissman-Fogel I.
        • Granovsky Y.
        • Bar-Shalita T.
        Sensory over-responsiveness among healthy subjects is associated with a pro-nociceptive state.
        Pain Pract. 2018; 18: 473-486
        • Weissman-Fogel I.
        • Sprecher E.
        • Granovsky Y.
        • Yarnitsky D.
        Repeated noxious stimulation of the skin enhances cutaneous pain perception of migraine patients in-between attacks: Clinical evidence for continuous sub-threshold increase in membrane excitability of central trigeminovascular neurons.
        Pain. 2003; 104: 693-700
        • Zero to Three
        Diagnostic classification of mental health and developmental disorders of infancy and early childhood, revised (DC:0–3R).
        National Center for Clinical Infant Programs, Arlington, VA2005