Short-latency afferent inhibition and somato-sensory evoked potentials during the migraine cycle: surrogate markers of a cycling cholinergic thalamo-cortical drive?
Coppola, Gianluca; Di Lenola, Davide; Abagnale, Chiaraet al.
2020 • In Journal of Headache and Pain, 21 (1), p. 34
Episodic migraine without aura; GABA; Motor cortex inhibition; Sensorimotor integration; Thalamo-cortical activation; Adolescent; Adult; Evoked Potentials, Motor/physiology; Evoked Potentials, Somatosensory/physiology; Female; Humans; Male; Median Nerve/physiopathology; Migraine Disorders/physiopathology; Motor Cortex/physiopathology; Neural Inhibition/physiology; Thalamus/physiopathology; Transcranial Magnetic Stimulation; Young Adult; Evoked Potentials, Motor; Evoked Potentials, Somatosensory; Median Nerve; Migraine Disorders; Motor Cortex; Neural Inhibition; Thalamus; Neurology (clinical); Anesthesiology and Pain Medicine; General Medicine
Abstract :
[en] ("[en] BACKGROUND: Short-latency afferent inhibition (SAI) consists of motor cortex inhibition induced by sensory afferents and depends on the excitatory effect of cholinergic thalamocortical projections on inhibitory GABAergic cortical networks. Given the electrophysiological evidence for thalamo-cortical dysrhythmia in migraine, we studied SAI in migraineurs during and between attacks and searched for correlations with somatosensory habituation, thalamocortical activation, and clinical features.
METHODS: SAI was obtained by conditioning the transcranial magnetic stimulation-induced motor evoked potential (MEP) with an electric stimulus on the median nerve at the wrist with random stimulus intervals corresponding to the latency of individual somatosensory evoked potentials (SSEP) N20 plus 2, 4, 6, or 8 ms. We recruited 30 migraine without aura patients, 16 between (MO), 14 during an attack (MI), and 16 healthy volunteers (HV). We calculated the slope of the linear regression between the unconditioned MEP amplitude and the 4-conditioned MEPs as a measure of SAI. We also measured SSEP amplitude habituation, and high-frequency oscillations (HFO) as an index of thalamo-cortical activation.
RESULTS: Compared to HV, SAI, SSEP habituation and early SSEP HFOs were significantly reduced in MO patients between attacks, but enhanced during an attack. There was a positive correlation between degree of SAI and amplitude of early HFOs in HV, but not in MO or MI.
CONCLUSIONS: The migraine cycle-dependent variations of SAI and SSEP HFOs are further evidence that facilitatory thalamocortical activation (of GABAergic networks in the motor cortex for SAI), likely to be cholinergic, is reduced in migraine between attacks, but increased ictally.","[en] ","")
Disciplines :
Neurology
Author, co-author :
Coppola, Gianluca; Department of Medico-Surgical Sciences and Biotechnologies, Sapienza University of Rome Polo Pontino, Corso della Repubblica 79, 04100, Latina, Italy. gianluca.coppola@uniroma1.it
Di Lenola, Davide; Department of Medico-Surgical Sciences and Biotechnologies, Sapienza University of Rome Polo Pontino, Corso della Repubblica 79, 04100, Latina, Italy
Abagnale, Chiara; Department of Medico-Surgical Sciences and Biotechnologies, Sapienza University of Rome Polo Pontino, Corso della Repubblica 79, 04100, Latina, Italy
Ferrandes, Fabio; Department of Medico-Surgical Sciences and Biotechnologies, Sapienza University of Rome Polo Pontino, Corso della Repubblica 79, 04100, Latina, Italy
Sebastianelli, Gabriele; Department of Medico-Surgical Sciences and Biotechnologies, Sapienza University of Rome Polo Pontino, Corso della Repubblica 79, 04100, Latina, Italy
Casillo, Francesco; Department of Medico-Surgical Sciences and Biotechnologies, Sapienza University of Rome Polo Pontino, Corso della Repubblica 79, 04100, Latina, Italy
Di Lorenzo, Cherubino; Department of Medico-Surgical Sciences and Biotechnologies, Sapienza University of Rome Polo Pontino, Corso della Repubblica 79, 04100, Latina, Italy
Serrao, Mariano; Department of Medico-Surgical Sciences and Biotechnologies, Sapienza University of Rome Polo Pontino, Corso della Repubblica 79, 04100, Latina, Italy
Evangelista, Maurizio; Università Cattolica del Sacro Cuore/CIC, Istituto di Anestesiologia, Rianimazione e Terapia del Dolore, Largo Agostino Gemelli 8, 00168, Rome, Italy
Schoenen, Jean ; Centre Hospitalier Universitaire de Liège - CHU > > Service de neurologie (CHR)
Pierelli, Francesco; Department of Medico-Surgical Sciences and Biotechnologies, Sapienza University of Rome Polo Pontino, Corso della Repubblica 79, 04100, Latina, Italy ; IRCCS - Neuromed, via Atinense, 18, 86077, Pozzilli, IS, Italy
Language :
English
Title :
Short-latency afferent inhibition and somato-sensory evoked potentials during the migraine cycle: surrogate markers of a cycling cholinergic thalamo-cortical drive?
Coppola G, Currà A, Di Lorenzo C et al (2010) Abnormal cortical responses to somatosensory stimulation in medication-overuse headache. BMC Neurol 10. https://doi.org/10.1186/1471-2377-10-126
Coppola G, Iacovelli E, Bracaglia M et al (2013) Electrophysiological correlates of episodic migraine chronification: evidence for thalamic involvement. J Headache Pain 14:76
Hubbard CS, Khan SA, Keaser ML et al (2014) Altered brain structure and function correlate with disease severity and pain catastrophizing in migraine patients. eNeuro 1:e20.14. https://doi.org/10.1523/ENEURO.0006-14.2014
Hodkinson DJ, Veggeberg R, Kucyi A et al (2016) Cortico-cortical connections of primary sensory areas and associated symptoms in migraine. Eneuro 3:ENEURO.0163-16.2016. https://doi.org/10.1523/ENEURO.0163-16.2016
Yang F-C, Chou K-H, Hsu A-L et al (2018) Altered brain functional connectome in migraine with and without restless legs syndrome: a resting-state functional MRI study. Front Neurol 9:25. https://doi.org/10.3389/fneur.2018.00025
Cosentino G, Di Marco S, Ferlisi S et al (2018) Intracortical facilitation within the migraine motor cortex depends on the stimulation intensity. A paired-pulse TMS study. J Headache Pain 19:65. https://doi.org/10.1186/s10194-018-0897-4
Cortese F, Coppola G, Di Lenola D et al (2017) Excitability of the motor cortex in patients with migraine changes with the time elapsed from the last attack. J Headache Pain 18:2. https://doi.org/10.1186/s10194-016-0712-z
Mykland MS, Bjørk MH, Stjern M et al (2019) Fluctuations of sensorimotor processing in migraine: a controlled longitudinal study of beta event related desynchronization. J Headache Pain 20:77. https://doi.org/10.1186/s10194-019-1026-8
Vuralli D, Boran HE, Cengiz B et al (2017) Somatosensory temporal discrimination remains intact in tension-type headache whereas it is disrupted in migraine attacks. Cephalalgia 37:1241-1247. https://doi.org/10.1177/0333102416677050
Alaydin HC, Vuralli D, Keceli Y et al (2019) Reduced short-latency afferent inhibition indicates impaired sensorimotor integrity during migraine attacks. Headache 59:906-914. https://doi.org/10.1111/head.13554
Turco CV, El-Sayes J, Savoie MJ et al (2018) Short- and long-latency afferent inhibition; uses, mechanisms and influencing factors. Brain Stimul 11:59-74. https://doi.org/10.1016/j.brs.2017.09.009
Coppola G, Vandenheede M, Di Clemente L et al (2005) Somatosensory evoked high-frequency oscillations reflecting thalamo-cortical activity are decreased in migraine patients between attacks. Brain 128:98-103. https://doi.org/10.1093/brain/awh334
Coppola G, De Pasqua V, Pierelli F, Schoenen J (2012) Effects of repetitive transcranial magnetic stimulation on somatosensory evoked potentials and high frequency oscillations in migraine. Cephalalgia 32:700-709. https://doi.org/10.1177/0333102412446313
Porcaro C, Di Lorenzo G, Seri S et al (2017) Impaired brainstem and thalamic high-frequency oscillatory EEG activity in migraine between attacks. Cephalalgia 37:915-926. https://doi.org/10.1177/0333102416657146
Brighina F, Giglia G, Scalia S et al (2005) Facilitatory effects of 1 Hz rTMS in motor cortex of patients affected by migraine with aura. Exp Brain Res 161:34-38. https://doi.org/10.1007/s00221-004-2042-7
Pierelli F, Iacovelli E, Bracaglia M et al (2013) Abnormal sensorimotor plasticity in migraine without aura patients. Pain 154:1738-1742
Cosentino G, Fierro B, Vigneri S et al (2014) Cyclical changes of cortical excitability and metaplasticity in migraine: evidence from a repetitive transcranial magnetic stimulation study. Pain 155:1070-1078
Di Lazzaro V, Pilato F, Dileone M et al (2005) Dissociated effects of diazepam and lorazepam on short-latency afferent inhibition. J Physiol 569:315-323. https://doi.org/10.1113/jphysiol.2005.092155
Fischer M, Orth M (2011) Short-latency sensory afferent inhibition: conditioning stimulus intensity, recording site, and effects of 1 Hz repetitive TMS. Brain Stimul 4:202-209. https://doi.org/10.1016/J.BRS.2010.10.005
Coppola G, Bracaglia M, Di Lenola D et al (2016) Lateral inhibition in the somatosensory cortex during and between migraine without aura attacks: correlations with thalamocortical activity and clinical features. Cephalalgia 36:568-578. https://doi.org/10.1177/0333102415610873
Curio G (2000) Linking 600-Hz "spikelike" EEG/MEG wavelets ('σ-bursts') to cellular substrates: concepts and caveats. J Clin Neurophysiol 17:377-396
Porcaro C, Coppola G, Lorenzo GD et al (2009) Hand somatosensory subcortical and cortical sources assessed by functional source separation: an EEG study. Hum Brain Mapp 30. https://doi.org/10.1002/hbm.20533
Oliviero A, Molina León A, Holler I et al (2005) Reduced sensorimotor inhibition in the ipsilesional motor cortex in a patient with chronic stroke of the paramedian thalamus. Clin Neurophysiol 116:2592-2598. https://doi.org/10.1016/j.clinph.2005.07.015
Kojima S, Onishi H, Miyaguchi S et al (2015) Effects of cathodal transcranial direct current stimulation to primary somatosensory cortex on short-latency afferent inhibition. Neuroreport 26:634-637. https://doi.org/10.1097/WNR.0000000000000402
Di Lazzaro V, Pilato F, Dileone M et al (2007) Segregating two inhibitory circuits in human motor cortex at the level of GABAA receptor subtypes: a TMS study. Clin Neurophysiol 118:2207-2214. https://doi.org/10.1016/J.CLINPH.2007.07.005
Di Lazzaro V, Oliviero A, Pilato F et al (2005) Neurophysiological predictors of long term response to AChE inhibitors in AD patients. J Neurol Neurosurg Psychiatry 76:1064-1069. https://doi.org/10.1136/jnnp.2004.051334
Di Lazzaro V, Oliviero A, Profice P et al (2000) Muscarinic receptor blockade has differential effects on the excitability of intracortical circuits in the human motor cortex. Exp Brain Res 135:455-461. https://doi.org/10.1007/s002210000543
Nardone R, Bergmann J, Christova M et al (2012) Short latency afferent inhibition differs among the subtypes of mild cognitive impairment. J Neural Transm 119:463-471. https://doi.org/10.1007/s00702-011-0725-3
Manganelli F, Ragno M, Cacchiò G et al (2008) Motor cortex cholinergic dysfunction in CADASIL: a transcranial magnetic demonstration. Clin Neurophysiol 119:351-355. https://doi.org/10.1016/j.clinph.2007.10.011
Kawasaki Y, Fujiki M, Ooba H et al (2012) Short latency afferent inhibition associated with cortical compression and memory impairment in patients with chronic subdural hematoma. Clin Neurol Neurosurg 114:976-980. https://doi.org/10.1016/j.clineuro.2012.02.037
Di Lorenzo F, Martorana A, Ponzo V et al (2013) Cerebellar theta burst stimulation modulates short latency afferent inhibition in Alzheimer's disease patients. Front Aging Neurosci 5:2. https://doi.org/10.3389/fnagi.2013.00002
Valeriani M, Rinalduzzi S, Vigevano F (2005) Multilevel somatosensory system disinhibition in children with migraine. Pain 118:137-144. https://doi.org/10.1016/j.pain.2005.08.026
Ugawa Y, Genba-Shimizu K, Kanazawa I (1996) Somatosensory evoked potential recovery (SEP-R) in various neurological disorders. Electroencephalogr Clin Neurophysiol - Evoked Potentials 100:62-67. https://doi.org/10.1016/0168-5597(95)00195-6
Udupa K, Ni Z, Gunraj C, Chen R (2009) Interactions between short latency afferent inhibition and long interval intracortical inhibition. Exp Brain Res 199:177-183. https://doi.org/10.1007/s00221-009-1997-9
Nardone R, Bergmann J, De Blasi P et al (2010) Cholinergic dysfunction and amnesia in patients with Wernicke-Korsakoff syndrome: a transcranial magnetic stimulation study. J Neural Transm 117:385-391. https://doi.org/10.1007/s00702-009-0347-1
Lapitskaya N, Gosseries O, De Pasqua V et al (2013) Abnormal corticospinal excitability in patients with disorders of consciousness. Brain Stimul 6:590-597. https://doi.org/10.1016/j.brs.2013.01.002
Celebi O, Temuçin ÇM, Elibol B, Saka E (2014) Cognitive profiling in relation to short latency afferent inhibition of frontal cortex in multiple system atrophy. Parkinsonism Relat Disord 20:632-636. https://doi.org/10.1016/j.parkreldis.2014.03.012
Nardone R, Bergmann J, Brigo F et al (2013) Functional evaluation of central cholinergic circuits in patients with Parkinson's disease and REM sleep behavior disorder: a TMS study. J Neural Transm 120:413-422. https://doi.org/10.1007/s00702-012-0888-6
Farmer K, Cady R, Bleiberg J, Reeves D (2000) A pilot study to measure cognitive efficiency during migraine. Headache 40:657-661
Farmer K, Cady R, Bleiberg J et al (2001) Sumatriptan nasal spray and cognitive function during migraine: results of an open-label study. Headache 41:377-384
Gil-Gouveia R, Oliveira A, Martins I (2015) Cognitive dysfunction during migraine attacks: a study on migraine without aura. Cephalalgia 35:662-674
Koppen H, Palm-Meinders I, Kruit M et al (2011) The impact of a migraine attack and its after-effects on perceptual organization, attention, and working memory. Cephalalgia 31:1419-1427
Le Pira F, Lanaia F, Zappalà G et al (2004) Relationship between clinical variables and cognitive performances in migraineurs with and without aura. Funct Neurol 19:101-105
Suhr JA, Seng EK (2012) Neuropsychological functioning in migraine: clinical and research implications. Cephalalgia 32:39-54
Yetkin-Ozden S, Ekizoglu E, Baykan B (2015) Face recognition in patients with migraine. Pain Pract 15:319-322