This study aims to investigate whether intranetwork dynamic functional connectivity and causal interactions of the salience network is altered in the interictal term of migraine. Thirty-two healthy controls, 37 migraineurs without aura, and 20 migraineurs with aura were recruited. Participants underwent a T1-weighted scan and resting-state fMRI protocol inside a 1.5T MR scanner. We obtained average spatial maps of resting-state networks using group independent component analysis, which yielded subject-specific time series through a dual regression approach. Salience network regions of interest (bilateral insulae and prefrontal cortices, dorsal anterior cingulate cortex) were obtained from the group average map through cluster-based thresholding. To describe intranetwork connectivity, average and dynamic conditional correlation was calculated. Causal interactions between the default-mode, dorsal attention, and salience network were characterised by spectral Granger's causality. Time-averaged correlation was lower between the right insula and prefrontal cortex in migraine without aura vs with aura and healthy controls (P < 0.038, P < 0.037). Variance of dynamic conditional correlation was higher in migraine with aura vs healthy controls and migraine with aura vs without aura between the right insula and dorsal anterior cingulate cortex (P < 0.011, P < 0.026), and in migraine with aura vs healthy controls between the dorsal anterior cingulate and left prefrontal cortex (P < 0.021). Causality was weaker in the <0.05 Hz frequency range between the salience and dorsal attention networks in migraine with aura (P < 0.032). Overall, migraineurs with aura exhibit more fluctuating connections in the salience network, which also affect network interactions, and could be connected to altered cortical excitability and increased sensory gain.

Central European Institute of Technology Brno Czech Republic

Department of Neurology Albert Szent Györgyi Clinical Center University of Szeged Szeged Hungary

Department of Radiology Albert Szent Györgyi Clinical Center University of Szeged Szeged Hungary

MTA SZTE Neuroscience Research Group Szeged Hungary

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Antal A, Temme J, Nitsche MA, Varga ET, Lang N, Paulus W. Altered motion perception in migraineurs: evidence for interictal cortical hyperexcitability. Cephalalgia 2005;25:788–94.

Barnett L, Seth AK. The MVGC multivariate Granger causality toolbox: a new approach to Granger-causal inference. J Neurosci Methods 2014;223:50–68.

Beckmann CF, Smith SM. Probabilistic independent component analysis for functional magnetic resonance imaging. IEEE Trans Med Imaging 2004;23:137–52.

Bollerslev T. Generalized autoregressive conditional heteroskedasticity. J Econom 1986;31:307–27.

Bosma RL, Kim JA, Cheng JC, Rogachov A, Hemington KS, Osborne NR, Oh J, Davis KD. Dynamic pain connectome functional connectivity and oscillations reflect multiple sclerosis pain. PAIN 2018;159:2267–76.

Brennan KC, Pietrobon D. A systems neuroscience approach to migraine. Neuron 2018;97:1004–21.

Buzsaki G, Draguhn A. Neuronal oscillations in cortical networks. Science 2004;304:1926–9.

Chang C, Glover GH. Time-frequency dynamics of resting-state brain connectivity measured with fMRI. Neuroimage 2010;50:81–98.

Charles AC, Baca SM. Cortical spreading depression and migraine. Nat Rev Neurol 2013;9:637–44.

Cheng JC, Bosma RL, Hemington KS, Kucyi A, Lindquist MA, Davis KD. Slow-5 dynamic functional connectivity reflects the capacity to sustain cognitive performance during pain. Neuroimage 2017;157:61–8.

Choe AS, Nebel MB, Barber AD, Cohen JR, Xu Y, Pekar JJ, Caffo B, Lindquist MA. Comparing test-retest reliability of dynamic functional connectivity methods. Neuroimage 2017;158:155–75.

Chong CD, Schwedt TJ, Hougaard A. Brain functional connectivity in headache disorders: a narrative review of MRI investigations. J Cereb Blood flow Metab 2019;39:650–69.

Cohen JR. The behavioral and cognitive relevance of time-varying, dynamic changes in functional connectivity. Neuroimage 2018;180:515–25.

Coppola G, Bracaglia M, Di Lenola D, Di Lorenzo C, Serrao M, Parisi V, Di Renzo A, Martelli F, Fadda A, Schoenen J, Pierelli F. Visual evoked potentials in subgroups of migraine with aura patients. J Headache Pain 2015;16:92.

Downar J, Crawley AP, Mikulis DJ, Davis KD. A cortical network sensitive to stimulus salience in a neutral behavioral context across multiple sensory modalities. J Neurophysiol 2002;87:615–20.

Engle R. Dynamic conditional correlation. J Business Econ Stat 2002;20:339–50.

Farago P, Tuka B, Toth E, Szabo N, Kiraly A, Csete G, Szok D, Tajti J, Pardutz A, Vecsei L, Kincses ZT. Interictal brain activity differs in migraine with and without aura: resting state fMRI study. J Headache Pain 2017;18:8.

Gohel SR, Biswal BB. Functional integration between brain regions at rest occurs in multiple-frequency bands. Brain Connect 2015;5:23–34.

Goto M, Abe O, Miyati T, Yamasue H, Gomi T, Takeda T. Head motion and correction methods in resting-state functional MRI. Magn Reson Med Sci 2016;15:178–86.

Granger CWJ. Investigating causal relations by econometric models and cross-spectral methods. Econometrica 1969;37:424–38.

Griffanti L, Douaud G, Bijsterbosch J, Evangelisti S, Alfaro-Almagro F, Glasser MF, Duff EP, Fitzgibbon S, Westphal R, Carone D, Beckmann CF, Smith SM. Hand classification of fMRI ICA noise components. Neuroimage 2017;154:188–205.

Jiang T. Brainnetome: a new -ome to understand the brain and its disorders. Neuroimage 2013;80:263–72.

Kaminski M, Ding M, Truccolo WA, Bressler SL. Evaluating causal relations in neural systems: granger causality, directed transfer function and statistical assessment of significance. Biol Cybern 2001;85:145–57.

Legrain V, Iannetti GD, Plaghki L, Mouraux A. The pain matrix reloaded: a salience detection system for the body. Prog Neurobiol 2011;93:111–24.

Levar N, Van Doesum TJ, Denys D, Van Wingen GA. Anterior cingulate GABA and glutamate concentrations are associated with resting-state network connectivity. Sci Rep 2019;9:2116.

Lindquist MA, Xu Y, Nebel MB, Caffo BS. Evaluating dynamic bivariate correlations in resting-state fMRI: a comparison study and a new approach. Neuroimage 2014;101:531–46.

Liu Z, Zhang Y, Bai L, Yan H, Dai R, Zhong C, Wang H, Wei W, Xue T, Feng Y, You Y, Tian J. Investigation of the effective connectivity of resting state networks in Alzheimer's disease: a functional MRI study combining independent components analysis and multivariate Granger causality analysis. NMR Biomed 2012;25:1311–20.

Mantegazza M, Cestele S. Pathophysiological mechanisms of migraine and epilepsy: similarities and differences. Neurosci Lett 2018;667:92–102.

McKendrick AM, Battista J, Snyder JS, Carter OL. Visual and auditory perceptual rivalry in migraine. Cephalalgia 2011;31:1158–69.

Morgan VL, Abou-Khalil B, Rogers BP. Evolution of functional connectivity of brain networks and their dynamic interaction in temporal lobe epilepsy. Brain Connect 2015;5:35–44.

Nickerson LD, Smith SM, Ongur D, Beckmann CF. Using dual regression to investigate network shape and amplitude in functional connectivity analyses. Front Neurosci 2017;11:115.

Pietrobon D, Moskowitz MA. Pathophysiology of migraine. Annu Rev Physiol 2013;75:365–91.

Sauvage A, Hubert G, Touboul J, Ribot J. The hemodynamic signal as a first-order low-pass temporal filter: evidence and implications for neuroimaging studies. Neuroimage 2017;155:394–405.

Scholz J, Klein MC, Behrens TE, Johansen-Berg H. Training induces changes in white-matter architecture. Nat Neurosci 2009;12:1370–1.

Seth AK, Barrett AB, Barnett L. Granger causality analysis in neuroscience and neuroimaging. J Neurosci 2015;35:3293–7.

Smith SM. Fast robust automated brain extraction. Hum Brain Mapp 2002;17:143–55.

Smith SM, Fox PT, Miller KL, Glahn DC, Fox PM, Mackay CE, Filippini N, Watkins KE, Toro R, Laird AR, Beckmann CF. Correspondence of the brain's functional architecture during activation and rest. Proc Natl Acad Sci U S A 2009;106:13040–5.

Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, Niazy RK, Saunders J, Vickers J, Zhang Y, De Stefano N, Brady JM, Matthews PM. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 2004;23(suppl 1):S208–219.

Sridharan D, Levitin DJ, Menon V. A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks. Proc Natl Acad Sci U S A 2008;105:12569–74.

Szabo N, Farago P, Kiraly A, Vereb D, Csete G, Toth E, Kocsis K, Kincses B, Tuka B, Pardutz A, Szok D, Tajti J, Vecsei L, Kincses ZT. Evidence for plastic processes in migraine with aura: a diffusion weighted MRI study. Front Neuroanat 2017;11:138.

Szabo N, Kincses ZT, Pardutz A, Tajti J, Szok D, Tuka B, Kiraly A, Babos M, Voros E, Bomboi G, Orzi F, Vecsei L. White matter microstructural alterations in migraine: a diffusion-weighted MRI study. PAIN 2012;153:651–6.

Tagliazucchi E, von Wegner F, Morzelewski A, Brodbeck V, Laufs H. Dynamic BOLD functional connectivity in humans and its electrophysiological correlates. Front Hum Neurosci 2012;6:339.

Tibber MS, Kelly MG, Jansari A, Dakin SC, Shepherd AJ. An inability to exclude visual noise in migraine. Invest Ophthalmol Vis Sci 2014;55:2539–46.

Tu Y, Fu Z, Zeng F, Maleki N, Lan L, Li Z, Park J, Wilson G, Gao Y, Liu M, Calhoun V, Liang F, Kong J. Abnormal thalamocortical network dynamics in migraine. Neurology 2019;92:e2706-16.

Vidaurre D, Smith SM, Woolrich MW. Brain network dynamics are hierarchically organized in time. Proc Natl Acad Sci U S A 2017;114:12827–32.

Wen X, Rangarajan G, Ding M. Is Granger causality a viable technique for analyzing fMRI data? PLoS one 2013;8:e67428.

Winkler AM, Ridgway GR, Webster MA, Smith SM, Nichols TE. Permutation inference for the general linear model. Neuroimage 2014;92:381–97.

Xia M, Wang J, He Y. BrainNet viewer: a network visualization tool for human brain connectomics. PLoS One 2013;8:e68910.

Younis S, Hougaard A, Vestergaard MB, Larsson HBW, Ashina M. Migraine and magnetic resonance spectroscopy: a systematic review. Curr Opin Neurol 2017;30:246–62.

Yu D, Yuan K, Luo L, Zhai J, Bi Y, Xue T, Ren X, Zhang M, Ren G, Lu X. Abnormal functional integration across core brain networks in migraine without aura. Mol Pain 2017;13:1744806917737461.

Zhou Y, Friston KJ, Zeidman P, Chen J, Li S, Razi A. The hierarchical organization of the default, dorsal attention and salience networks in adolescents and young adults. Cereb Cortex 2018;28:726–37.