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The Journal of Headache and Pain

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Open Access 01-12-2024 | Aura | Research

Different vulnerability of fast and slow cortical oscillations to suppressive effect of spreading depolarization: state-dependent features potentially relevant to pathogenesis of migraine aura

Authors: Tatiana M. Medvedeva, Maria P. Smirnova, Irina V. Pavlova, Lyudmila V. Vinogradova

Published in: The Journal of Headache and Pain | Issue 1/2024

Abstract

Background

Spreading depolarization (SD), underlying mechanism of migraine aura and potential activator of pain pathways, is known to elicit transient local silencing cortical activity. Sweeping across the cortex, the electrocorticographic depression is supposed to underlie spreading negative symptoms of migraine aura. Main information about the suppressive effect of SD on cortical oscillations was obtained in anesthetized animals while ictal recordings in conscious patients failed to detect EEG depression during migraine aura. Here, we investigate the suppressive effect of SD on spontaneous cortical activity in awake animals and examine whether the anesthesia modifies the SD effect.

Methods

Spectral and spatiotemporal characteristics of spontaneous cortical activity following a single unilateral SD elicited by amygdala pinprick were analyzed in awake freely behaving rats and after induction of urethane anesthesia.

Results

In wakefulness, SD transiently suppressed cortical oscillations in all frequency bands except delta. Slow delta activity did not decline its power during SD and even increased it afterwards; high-frequency gamma oscillations showed the strongest and longest depression under awake conditions. Unexpectedly, gamma power reduced not only during SD invasion the recording cortical sites but also when SD occupied distant subcortical/cortical areas. Contralateral cortex not invaded by SD also showed transient depression of gamma activity in awake animals. Introduction of general anesthesia modified the pattern of SD-induced depression: SD evoked the strongest cessation of slow delta activity, milder suppression of fast oscillations and no distant changes in gamma activity.

Conclusion

Slow and fast cortical oscillations differ in their vulnerability to SD influence, especially in wakefulness. In the conscious brain, SD produces stronger and spatially broader depression of fast cortical oscillations than slow ones. The frequency-specific effects of SD on cortical activity of awake brain may underlie some previously unexplained clinical features of migraine aura.

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Goadsby PJ, Holland PR, Martins-Oliveira M, Hoffmann J, Schankin C, Akerman S (2017) Pathophysiology of Migraine: A Disorder of Sensory Processing. Physiol Rev 97(2):553–622CrossRefPubMedPubMedCentral

Charles A (2018) The migraine aura. CONTINUUM: Lifelong Learn Neurol 24(4):1009–22

Bolay H, Vuralli D, Goadsby PJ (2019) Aura and Head pain: relationship and gaps in the translational models. J Headache Pain 20(1):94CrossRefPubMedPubMedCentral

Leao A (1944) Spreading depression of activity in the cerebral cortex. J Neurophysiol 7:359–90CrossRef

Lindquist BE, Shuttleworth CW (2017) Evidence that adenosine contributes to Leao’s spreading depression in vivo. J Cereb Blood Flow Metab 37(5):1656–1669CrossRefPubMed

Eikermann-Haerter K, Negro A, Ayata C (2013) Spreading depression and the clinical correlates of migraine. Rev Neurosci 24(4):353–363CrossRefPubMed

Lauritzen M, Trojaborg W, Olesen J (1981) EEG during attacks of common and classical migraine. Cephalalgia 1(2):63–66CrossRefPubMed

Tolner EA, Chen SP, Eikermann-Haerter K (2019) Current understanding of cortical structure and function in migraine. Cephalalgia 39(13):1683–99CrossRefPubMedPubMedCentral

Hartings JA, Wilson JA, Hinzman JM, Pollandt S, Dreier JP, DiNapoli V et al (2014) Spreading depression in continuous electroencephalography of brain trauma. Ann Neurol 76(5):681–694CrossRefPubMed

10.

Kentar M, Díaz-Peregrino R, Trenado C, Sánchez-Porras R, San-Juan D, Ramírez-Cuapio FL et al (2022) Spatial and temporal frequency band changes during infarct induction, infarct progression, and spreading depolarizations in the gyrencephalic brain. Front Neurosci 16:1025967CrossRefPubMedPubMedCentral

11.

Drenckhahn C, Winkler MKL, Major S, Scheel M, Kang EJ, Pinczolits A et al (2012) Correlates of spreading depolarization in human scalp electroencephalography. Brain 135(3):853–868CrossRefPubMedPubMedCentral

12.

Kudo C, Toyama M, Boku A, Hanamoto H, Morimoto Y, Sugimura M et al (2013) Anesthetic effects on susceptibility to cortical spreading depression. Neuropharmacology 67:32–36CrossRefPubMed

13.

Hertle DN, Dreier JP, Woitzik J, Hartings JA, Bullock R, Okonkwo DO et al (2012) Effect of analgesics and sedatives on the occurrence of spreading depolarizations accompanying acute brain injury. Brain 135(8):2390–2398CrossRefPubMed

14.

Tepe N, Filiz A, Dilekoz E, Akcali D, Sara Y, Charles A et al (2015) The thalamic reticular nucleus is activated by cortical spreading depression in freely moving rats: prevention by acute valproate administration. Eur J Neurosci 41(1):120–128CrossRefPubMed

15.

Houben T, Loonen IC, Baca SM, Schenke M, Meijer JH, Ferrari MD et al (2017) Optogenetic induction of cortical spreading depression in anesthetized and freely behaving mice. J Cereb Blood Flow & Metab 37(5):1641–55CrossRef

16.

Akcali D, Sayin A, Sara Y, Bolay H (2010) Does single cortical spreading depression elicit pain behaviour in freely moving rats? Cephalalgia 30(10):1195–1206CrossRefPubMed

17.

Siegfried B, Shibata M, Huston JP (1977) Electrophysiological concomitants of eating induced from neocortex and hippocampus by electrical stimulation and injection of KCl or norepinephrine. Brain Res 121(1):97–112CrossRefPubMed

18.

Vinogradova LV, Rysakova MP, Pavlova IV (2020) Small damage of brain parenchyma reliably triggers spreading depolarization. Neurol Res 42(1):76–82CrossRefPubMed

19.

Sugimoto K, Yang J, Fischer P, Takizawa T, Mulder IA, Qin T et al (2023) Optogenetic spreading depolarizations do not worsen acute ischemic stroke outcome. Stroke 54(4):1110–1119CrossRefPubMed

20.

Fifková E (1966) Spreading depression in subcortical structures in rabbit. Brain Res 2(1):61–70CrossRefPubMed

21.

Smirnova MP, Medvedeva TM, Pavlova IV, Vinogradova LV (2022) Region-specific vulnerability of the amygdala to injury-induced spreading depolarization. Biomedicines 10(9):2183CrossRefPubMedPubMedCentral

22.

Vinogradova LV, Koroleva VI, Bures J (1991) Re-entry waves of Leao’s spreading depression between neocortex and caudate nucleus. Brain Res 538(1):161–164CrossRefPubMed

23.

Hadjikhani N, Ward N, Boshyan J, Napadow V, Maeda Y, Truini A et al (2013) The missing link: Enhanced functional connectivity between amygdala and visceroceptive cortex in migraine. Cephalalgia 33(15):1264–1268CrossRefPubMedPubMedCentral

24.

Chen Z, Chen X, Liu M, Dong Z, Ma L, Yu S (2017) Altered functional connectivity of amygdala underlying the neuromechanism of migraine pathogenesis. J Headache Pain 18(1):7CrossRefPubMedPubMedCentral

25.

Neeb L, Bastian K, Villringer K, Israel H, Reuter U, Fiebach JB (2017) Structural gray matter alterations in chronic migraine: implications for a progressive disease? Headache: J Head Face Pain 57(3):400–16CrossRef

26.

Lee CH, Park H, Lee MJ, Park B (2023) Whole-brain functional gradients reveal cortical and subcortical alterations in patients with episodic migraine. Hum Brain Mapp 44(6):2224–2233CrossRefPubMedPubMedCentral

27.

Eikermann-Haerter K, Yuzawa I, Qin T, Wang Y, Baek K, Kim YR et al (2011) Enhanced subcortical spreading depression in familial hemiplegic migraine type 1 mutant mice. J Neurosci 31(15):5755–5763CrossRefPubMedPubMedCentral

28.

Herrero MT, Insausti R, Gonzalo LM (1991) Cortically projecting cells in the periaqueductal gray matter of the rat. A retrograde fluorescent tracer study. Brain Res 543(2):201–12. https://doi.org/10.1016/0006-8993(91)90029-uCrossRefPubMed

29.

Dai W, Liu RH, Qiu E, Liu Y, Chen Z, Chen X, Ao R, Zhuo M, Yu S (2021) Cortical mechanisms in migraine. Mol Pain 17:17448069211050246. https://doi.org/10.1177/17448069211050246CrossRefPubMedPubMedCentral

30.

Paxinos G, Watson C (1982) The Rat Brain in Stereotaxic Coordinates. Elsevier, Am sterdam

31.

Hall SD, Barnes GR, Hillebrand A, Furlong PL, Singh KD, Holliday IE (2004) Spatio-temporal imaging of cortical desynchronization in migraine visual aura: a magnetoencephalography case study. Headache: J Head Face Pain 44(3):204–8CrossRef

32.

Seri S, Cerquiglini A, Guidetti V (1993) Computerized EEG topography in childhood migraine between and during attacks. Cephalalgia 13(1):53–56. https://doi.org/10.1046/j.1468-2982.1993.1301053.xCrossRefPubMed

33.

Chastan N, Lebas A, Legoff F, Parain D, Guyant-Marechal L (2016) Clinical and electroencephalographic abnormalities during the full duration of a sporadic hemiplegic migraine attack. Clin Neurophysiol 46(4–5):307–311. https://doi.org/10.1016/j.neucli.2016.03.004CrossRef

34.

Unekawa M, Tomita Y, Toriumi H, Masamoto K, Kanno I, Suzuki N (2013) Potassium-induced cortical spreading depression bilaterally suppresses the electroencephalogram but only ipsilaterally affects red blood cell velocity in intraparenchymal capillaries. J Neurosci Res 91(4):578–584. https://doi.org/10.1002/jnr.23184CrossRefPubMed

35.

Vinogradova LV, Suleymanova EM, Medvedeva TM (2021) Transient loss of interhemispheric functional connectivity following unilateral cortical spreading depression in awake rats. Cephalalgia 41(3):353–365. https://doi.org/10.1177/0333102420970172CrossRefPubMed

36.

Hertle DN, Heer M, Santos E, Schöll M, Kowoll CM, Dohmen C et al (2016) Changes in electrocorticographic beta frequency components precede spreading depolarization in patients with acute brain injury. Clin Neurophysiol 127(7):2661–2667CrossRefPubMed

37.

Bureš J, Burešová O, Fifková E, Rabending G (1965) Reversible deafferentation of cerebral cortex by thalamic spreading depression. Exp Neurol 12(1):55–67CrossRefPubMed

38.

Bureš J, Hartmann G, Lukyanova LD (1967) Blockade of thalamocortical and pyramidal pathways by striatal spreading depression in rats. Exp Neurol 18(4):404–415CrossRefPubMed

39.

Fu X, Chen M, Lu J, Li P (2022) Cortical spreading depression induces propagating activation of the thalamus ventral posteromedial nucleus in awake mice. J Headache Pain 23(1):15. https://doi.org/10.1186/s10194-021-01370-zCrossRefPubMedPubMedCentral

40.

Vinogradova LV, Kuznetsova GD, Coenen AM (2009) Unilateral cortical spreading depression induced by sound in rats. Brain Res 1286:201–207. https://doi.org/10.1016/j.brainres.2009.06.047CrossRefPubMed

41.

Vinogradova LV (2015) Comparative potency of sensory-induced brainstem activation to trigger spreading depression and seizures in the cortex of awake rats: Implications for the pathophysiology of migraine aura. Cephalalgia 35(11):979–986CrossRefPubMed

42.

Westberg KG, Kolta A (2011) The trigeminal circuits responsible for chewing. Int Rev Neurobiol 97:77–98. https://doi.org/10.1016/B978-0-12-385198-7.00004-7CrossRefPubMed

43.

Hansen JM, Baca SM, VanValkenburgh P, Charles A (2013) Distinctive anatomical and physiological features of migraine aura revealed by 18 years of recording. Brain 136(12):3589–3595CrossRefPubMed

44.

Bowyer SM, Tepley N, Papuashvili N, Kato S, Barkley GL, Welch KM, Okada YC (1999) Analysis of MEG signals of spreading cortical depression with propagation constrained to a rectangular cortical strip. II Gyrencephalic Swine Model Brain Res 843(1–2):79–86. https://doi.org/10.1016/s0006-8993(99)01893-4CrossRefPubMed

45.

Santos E, Schöll M, Sánchez-Porras R, Dahlem MA, Silos H, Unterberg A, Dickhaus H, Sakowitz OW (2014) Radial, spiral and reverberating waves of spreading depolarization occur in the gyrencephalic brain. Neuroimage 99:244–55. https://doi.org/10.1016/j.neuroimage.2014.05.021CrossRefPubMed

Title: Different vulnerability of fast and slow cortical oscillations to suppressive effect of spreading depolarization: state-dependent features potentially relevant to pathogenesis of migraine aura
Authors: Tatiana M. Medvedeva
Maria P. Smirnova
Irina V. Pavlova
Lyudmila V. Vinogradova
Publication date: 01-12-2024
Publisher: Springer Milan
Keywords: Aura
Migraine
Affective Disorder
Affective Disorder
Published in: The Journal of Headache and Pain / Issue 1/2024
Print ISSN: 1129-2369
Electronic ISSN: 1129-2377
DOI: https://doi.org/10.1186/s10194-023-01706-x

At a glance: The STEP trials

Springer Medicine

Different vulnerability of fast and slow cortical oscillations to suppressive effect of spreading depolarization: state-dependent features potentially relevant to pathogenesis of migraine aura

Abstract

Background

Methods

Results

Conclusion

At a glance: The STEP trials

Springer Medicine

Abstract

Background

Methods

Results

Conclusion

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