Skip to main content

Table 1 Functional connectivity MRI during the interictal phase of migraine compared with non-migraine controls

From: Functional connectivity studies in migraine: what have we learned?

Study

Population and method

Findings

Mainero, 2011 Ann Neurol [1]

Origin: USA.

17 migraine (8 MA and 9 MO) patients were compared to 17 age- and sex-matched controls.

Migraine versus controls

PAG: increased FC with right ventrolateral prefrontal cortex, right supramarginal gyrus, right anterior insula, right postcentral gyrus (S1), right thalamus, left angular gyrus, left supramarginal gyrus/parietal operculum (S2), and bilateral precentral gyrus (M1). Decreased FC with right dorsolateral prefrontal cortex, right lateral prefrontal cortex, right anterior cingulate, left dorsomedial prefrontal cortex, left medial prefrontal cortex, and left anterior insula.

Seed-based approach using FSL. Seeds were used for PAG.

Yuan K, 2012 PLoS One [3]

Origin: China.

21 MO patients were compared to 21 age- and sex-matched controls.

MO versus controls

Right ACC: increased FC with bilateral orbitofrontal cortex.

Left ACC: increased FC with bilateral orbitofrontal cortex and right dorsolateral prefrontal cortex.

Seed-based approach using FSL. Seed were bilaterally placed in anterior cingulate cortex (ACC).

Russo A, 2012 Cephalalgia [4]

Origin: Italy.

14 MO patients were compared to 14 age- and sex-matched controls.

MO versus controls

FPN: decreased FC with right middle frontal gyrus and right dorsal ACC.

ICA-based approach using MATLAB to examine fronto-parietal network (FPN).

Jin C, 2012 NMR Biomed [5]

Origin: China.

21 MO were compared with 21 age- and sex-matched controls.

Seed-based approach using FSL. Seeds were used for left medial prefrontal cortex (PFC), left dorsal ACC, right occipital lobe, cerebellum and brainstem.

MO versus controls

Dorsal ACC: increased FC of bilateral middle temporal lobe, orbitofrontal cortex, and left dorsolateral prefrontal cortex.

Right occipital lobe: increased FC of left dorsolateral prefrontal cortex and right middle cingulate cortex.

Left medial PFC: increased FC of bilateral dorsolateral prefrontal cortex.

Right cerebellum: increased FC with the right medial PFC.

Brainstem: no changes were detected.

Xue T, 2012 PLoS One [6]

Origin: China.

23 MO patients were compared with 23 age- and sex-matched controls.

MO versus controls

Right CEN: increased FC with right middle frontal gyrus and right anterior insula.

Left CEN: increased FC with left inferior frontal gyrus.

SN: decreased FC with right supplementary motor area.

DMN: increased FC with right anterior insula.

ICA-based and seed-based approach using FSL. Seed were used for default mode network (DMN), central executive network (CEN) and salience network (SN).

Xue T, 2013 NMR Biomed [7]

Origin: China.

18 MO patients were compared with 18 age- and sex-matched controls.

MO versus controls

Left ACC: increased FC with bilateral frontal lobe and left parietal lobe.

Right thalamus: increased FC with bilateral caudate, left temporal lobe and right putamen.

Left PFC: increased FC with right precuneus and bilateral parietal lobe.

Right PFC: increased FC with bilateral parietal lobe and left temporal lobe.

Right insula: increased FC with left temporal pole, right frontal lobe, and left parietal lobe.

Seed-based approach using MATLAB. Seeds were used for left ACC, right thalamus, bilateral PFC and right insula.

Tessitore A, 2013 J Headache Pain [8]

Origin: Italy.

20 MO patients were compared with 20 age- and sex-matched controls.

MO versus controls

DMN: decreased FC with left superior prefrontal gyrus and left temporal pole.

ICA-based approach using FSL to identify DMN among a total of 40 networks.

Schwedt TJ, 2013 Headache [9]

Origin: USA.

20 chronic migraine patients were compared with 20 controls.

Chronic migraine versus controls

Anterior insula: atypical FC with pulvinar, middle temporal cortex, mediodorsal thalamus, precuneus, PAG, cingulate cortex, and inferior parietal cortex.

Amygdala: atypical FC with superior frontal cortex and occipital cortex.

Seed-based approach using in-house developed software. Seeds were placed in ACC and bilaterally anterior insula and amygdala.

Hadjikhani, 2013 Cephalalgia [10]

Origin: USA.

22 migraine (11 MA and 11 MO) patients were compared to 20 healthy controls.

Migraine versus controls

Amygdala: increased FC with anterior insula, secondary somatosensory cortex (S2) and thalamus.

Seed-based approach using FSL. Seeds were placed in right and left amygdala.

Yuan K, 2013 J Pain [11]

Origin: China.

40 MO patients were compared to 40 age- and sex-matched controls.

MO versus controls

Right caudate: increased FC with left insula and left putamen.

Left caudate: increased FC with bilateral hippocampal gyrus, left amygdala, left insula and left putamen.

Right nucleaus accumbens: increased FC with bilateral parahippocampal gyrus, bilateral ACC, bilateral orbitofrontal cortex, and left posterior cingulate cortex.

Seed-based approach using FSL. Seeds were used subregions of the basal ganglia (bilateral caudate and right nucleus accumbens).

Moulton EA, 2014 PLoS One [12]

Origin: USA.

12 MO patients were compared with 12 age- and sex-matched controls.

MO versus controls

Hypothalamus: increased FC with right precentral gyrus, right middle frontal gyrus, left superior parietal gyrus/supramarginal gyrus, left inferior temporal gyrus, right planum polare, left temporal pole, left middle temporal gyrus, left parahippocampal gyrus, left superior temporal gyrus, bilateral hippocampus, left caudate, right nucleus coeruleus, bilateral pontine nuclei, left cerebellar crus I and II, bilateral cerebellar lobule V, right cerebellar lobules V and VI, left vermal lobules VIIIa and VIIIb and left dentate nucleus.

Decreased FC with right precentral gyrus, left frontal pole, left paracingulate gyrus, right superior frontal gyrus, right fusiform gyrus and left lingual gyrus.

Seed-based approach using FSL. Seeds were used for hypothalamus.

Tessitore A, 2015 Headache [13]

Origin: Italy.

20 MA and 20 MO patients were compared to 20 age- and sex-matched controls.

MA versus controls

Right ECN: Decreased FC with right middle frontal gyrus and dorsal ACC.

ICA-based approach using FSL to identify executive control network (ECN) among a total of 40 networks.

MO versus controls

Right ECN: Decreased FC with right middle frontal gyrus and dorsal ACC.

Zhang J, 2016J Headache Pain [14]

Origin: China.

22 MO patients were compared with 22 healthy matched controls.

MO versus controls

DMN: increased FC with left posterior cingulate cortex and left precuneus.

ICA-based approach using MATLAB to identify DMN among a total of 20 networks.

Coppola G, 2016 J Headache Pain [15]

Origin: Italy.

18 MO patients were compared to 19 healthy volunteers.

MO versus controls

DMN: decreased FC with a network composed of the visuospatial system and medial visual cortical areas.

ICA-based approach using MATLAB, where a total of 39 networks were identified.

Niddam DM, 2016 Cephalalgia [16]

Origin: Taiwan.

26 MA and 26 MO patients were compared with 26 age- and sex-matched controls.

MA versus controls

Left DAN: increased FC with right orbital gyrus, left rectal gyrus, right fusiform gyrus, right middle temporal gyrus and right parahippocampal gyrus.

Left SN: decreased FC with bilateral cuneus, left superior occipital gyrus, right lingual gyrus, left fusiform gyrus and left middle temporal gyrus.

Right cuneus: increased FC with left cingulate gyrus, bilateral precuneus and bilateral posterior cingulate. Decreased FC with bilateral insula, bilateral middle frontal gyrus, bilateral claustrum, bilateral lentiform nucleus, right inferior frontal gyrus, bilateral cingulate gyrus and bilateral superior frontal gyrus.

Seed-based approach using MATLAB. Seeds were used for DMN (posterior cingulate cortex), dorsal attention network (DAN) (middle frontal gyrus), SN (anterior insula) and right cuneus.

MO versus controls

Left DAN: increased FC with right middle temporal gyrus, right parahippocampal gyrus, right middle occipital gyrus and right fusiform gyrus.

MA versus MO

Left SN: decreased FC with bilateral cuneus, bilateral lingual gyrus, left middle temporal gyrus and middle occipital gyrus.

Right cuneus: increased FC with left middle frontal gyrus, bilateral cingulate gyrus and right precuneus. Decreased FC with bilateral insula, bilateral claustrum, right lentiform nucleus, right inferior frontal gyrus and left middle frontal gyrus.

Tedeschi G, 2016Cephalalgia [17]

Origin: Italy.

20 MA and 20 MO patients were compared to 20 healthy controls.

MA versus MO

VN: increased FC with right lingual gyrus.

ICA-based approach using FSL to examine visual network (VN) among a total of 40 networks.

MA versus MO/controls

VN: no changes were found.

Chen Z, 2016 J Headache Pain [18]

Origin: China.

18 episodic migraine,16 chronic migraine and 44 medication overuse headache (MOH) + chronic migraine patients were compared to 32 normal controls.

Episodic migraine versus controls

Right MdNS: increased FC with right ACC and decreased FC with right insula.

Left MdNS: increased FC with right precentral gyrus and decreased FC with right insula.

Seed-based approach using MATLAB. Seeds were bilaterally placed in the marginal division of neostriatum (MdNS).

Chronic migraine versus controls

Right MdNS: increased FC with right middle temporal gyrus.

Left MdNS: increased FC with bilateral middle frontal gyrus and left hippocampus.

MOH + chronic migraine versus controls

Right MdNS: increased FC with right interior temporal gyrus and left parahippocampal gyrus.

Left MdNS: increased FC with right middle frontal gyrus.

Hodkinson DJ, 2016 eNeuro [19]

Origin: USA

40 migraine patients were compared to 40 matched healthy controls.

Migraine versus controls

V1: reduced anticorrelation to precuneus and decreased positive correlations to inferior occipital cortex/middle occipital cortex.

Seed-based approarch using M MATLAB. Seeds were used for networks of vision (V1), audition (primary auditory cortex) and somatosensation (S1).

Primary auditory cortex: reduced anticorrelation to PFC, dorsolateral PFC, precuneus, posterior cingulate cortex and lateral parietal cortex. Decreased positive correlations to insula, opercular cortex, posterior central sulcus and anterior temporal lobe.

S1: No changes were found.

Androulakis M, 2017 Neurology [20]

Origin: USA.

29 chronic migraine patients were compared to 29 age- and sex-matched controls.

Overall connectivity was decreased in all three networks in the chronic migraine group compared to controls.

Seed-based approach using MATLAB. Seeds were used for SN, CEN and DMN.

Changes were associated with moderate to severe headache and allodynia.

Lo Buono V, 2017 J Headache Pain [21]

Origin: Italy.

14 MA patients, 14 MO patients and 14 matched controls.

MA versus MO

DMN: increased FC of bilateral central opercular cortex, right insular cortex, bilateral first and second Heschl’s gyrus, left superior temporal gyrus, bilateral lingual gyrus, right occpipital fusiform gyrus, and left occipital pole.

ICA-based approach using FSL. DMN was examined.

MA versus controls

DMN: Increased FC of bilateral Heschl’s gyrus, bilateral planum temporale, and left superior temporal gyrus.

MO versus controls

DMN: Increased FC of bilateral lingual gyrus, occcipital fusiform gyrus, occipital pole, and cingulate gyrus.

Hougaard A, 2017 Eur J Neurol [22]

Origin: Denmark.

40 MA patients were compared to 40 age- and sex-matched controls.

Seed-based approach

No difference was found in any examined network.

Seed-based and ICA-based approaches using FSL. Seeds were used for DMN, primary visual cortex, lateral geniculate nucleus, PAG, amygdala, inferior frontal gyrus, superior parietal lobule, inferior parietal lobule, pars opercularis, visual area V2, V3A, V4 and V5.

ICA-based approach

No changes were detected in 30 analysed networks.

Chen Z, 2017 J Headache Pain [23]

Origin: China.

18 episodic migraine patients (15 MO, 3 MA) were compared with 18 healthy controls.

Episodic migraine versus controls

Right ventrolateral PAG: decreased FC with left precentral gyrus.

Left ventrolateral PAG: decreased FC with left precentral gyrus, left middle frontal gyrus, left inferior frontal gyrus, bilateral middle temporal gyrus, right superior frontal gyrus and right supplementary motor area.

Left dorsolateral PAG: decreased FC with right pars triangularis of inferior frontal gyrus and the medial superior frontal gyrus.

Seed-based approach using MATLAB. Seeds were used for PAG, incl. Bilateral ventrolateral PAG, lateral PAG, dorsolateral PAG, and dorsomedial PAG.

Chen Z, 2017 J Headache Pain [24]

Origin: China.

18 episodic migraine and 16 chronic migraine patients were compared to 18 normal controls.

Episodic migraine versus controls

Left amygdala: increased FC with left middle cingulate gyrus and left precuneus.

Right amygdala: no change.

Seed-based approach using MATLAB. Seed were bilaterally placed in amygdala.

Chronic migraine versus controls

Left amygdala: no change.

Right amygdala: decreased FC with right inferior occipital lobe and right middle occipital lobe.

Chronic versus episodic migraine

Left amygdala: inferior temporal gyrus, right orbital part of superior frontal gyrus, left fusiform, right postcentral gyrus, left rectus, right amygdala and left precentral gyrus.

Right amygdala: inferior temporal gyrus, left middle cingulate gyrus, left orbital part of medial frontal gyrus, left temporal pole, right orbital part of inferior frontal gyrus, right anterior cingulate gyrus and left orbital part of inferior frontal gyrus.

Yu D, 2017 Mol Pain [25]

Origin: China.

31 MO patients were compared with 31 age- and education-matched controls.

MO versus controls

Right ACC: decreased FC with PFC and posterior cingulate cortex.

Left PFC: decreased FC with left insula and posterior parietal cortex.

Seed-based and ICA-based approaches using FSL. Seeds were used for DMN (medial PFC and posterior cingulate cortex), CEN (dorsloteral PFC and posterior parietal cortex) and SN (frontoinsular cortex and ACC).

No increased FC was found.

Zhang J, 2017 J Neurol [26]

Origin: China.

30 MO patients were compared to 31 healthy controls.

MO versus controls

Left S1: increased FC with left anterior parietal lobe, right superior parietal lobe, right S1, bilateral premotor cortex, right inferior frontal gyrus, right insula, right temporal lobe, left primary motor cortex and right middle occipital gyrus.

Right S1: decreased FC with bilateral premotor cortex, bilateral superior frontal gyrus, bilateral ACC, pons, left insula, bilateral S1, bilateral paracentral lobule, right temporal lobe, right cerebellum lobule VIIIb and left inferior parietal lobule.

Seed-based approach using MATLAB. Seeds were bilaterally placed in primary somatosensory cortex (S1).

  1. MA Migraine with aura, MO Migraine without aura, FSL FMRIB Software Library, FC Functional connectivity, ACC Anterior cingulate cortex, ICA Independent component analysis, CEN Central executive network, DAN Dorsal attention network, DMN Default mode network, ECN Executive control network, FPN Fronto-parietal network, PAG Periaqueductal gray, PFC Prefrontal cortex, SN Salience network, VN Visual network, MdNS Marginal division of neostriatum