Neuroimaging investigation of memory changes in migraine: a systematic review

DAVID, Mírian Celly Medeiros Miranda; SANTOS, Bárbara Sousa dos; BARROS, Waleska Maria Almeida; SILVA, Taynara Rayane Lins da; FRANCO, Carlúcia Ithamar Fernandes; MATOS, Rhowena Jane Barbosa de

doi:10.1590/0004-282X20200025

Mírian Celly Medeiros Miranda DAVID

Universidade Federal de Pernambuco, Programa de Pós-Graduação em Neuropsiquiatria e Ciências do Comportamento, Recife PE, Brazil.

http://orcid.org/0000-0002-7152-8852

Bárbara Sousa dos SANTOS

Universidade Estadual da Paraíba, Departamento de Fisioterapia, Campina Grande PB, Brazil.

http://orcid.org/0000-0002-0987-9520

Waleska Maria Almeida BARROS

Universidade Federal de Pernambuco, Programa de Pós-Graduação em Neuropsiquiatria e Ciências do Comportamento, Recife PE, Brazil.

http://orcid.org/0000-0002-9033-8165

Taynara Rayane Lins da SILVA

Universidade Escritor Osman da Costa Lins, Vitória de Santo Antão PB, Brazil.

http://orcid.org/0000-0002-2396-5847

Carlúcia Ithamar Fernandes FRANCO

Universidade Estadual da Paraíba, Departamento de Fisioterapia, Campina Grande PB, Brazil.

http://orcid.org/0000-0001-6653-8864

Rhowena Jane Barbosa de MATOS

Universidade Federal de Pernambuco, Programa de Pós-Graduação em Neuropsiquiatria e Ciências do Comportamento, Recife PE, Brazil.

Universidade Federal de Pernambuco, Centro Acadêmico de Vitória, Núcleo de Educação Física e Ciências do Esporte, Vitória de Santo Antão PB, Brazil.

http://orcid.org/0000-0001-5914-7304

Correspondence: Mírian Celly Medeiros Miranda David; E-mail: miriancelly@hotmail.com

Conflict of interest: The authors declare there is no conflict of interest.

Source: Research data. The percentage values correspond to the percentage of agreement between the reviewers. Selected articles: 1=Wang et al.³⁵35. Wang N, Huang HL, Zhou H, Yu CY. Cognitive impairment and quality of life in patients with migraine-associated vertigo. Eur Rev Med Pharmacol Sci. 2016 Dec;20(23):4913-7.; 2=Schwedt et al.³⁶36. Schwedt TJ, Chong CD, Chiang CC, Baxter L, Schlaggar BL, Dodick DW. Enhanced pain-induced activity of pain-processing regions in a case-control study of episodic migraine. Cephalalgia. 2014 Oct;34(12):947-58. https://doi.org/10.1177/0333102414526069
https://doi.org/https://doi.org/10.1177/... ; 3=Liu et al.³⁷37. Liu J, Zhao L, Nan J, Li G, Xiong S, von Deneena KM, et al. The trade-off between wiring cost and network topology in white matter structural networks in health and migraine. Exp Neurol. 2013 Oct;248:196-204. https://doi.org/10.1016/j.expneurol.2013.04.012
https://doi.org/https://doi.org/10.1016/... ; 4=Coppola et al.³⁸38. Coppola G, Di Renzo A, Tinelli E, Iacovelli E, Lepre C, Di Lorenzo C, et al. Evidence for brain morphometric changes during the migraine cycle: a magnetic resonance-based morphometry study. Cephalalgia. 2015 Aug;35(9):783-91. https://doi.org/10.1177/0333102414559732
https://doi.org/https://doi.org/10.1177/... ; 5=Tso et al.³⁹39. Tso AR, Trujillo A, Guo CC, Goadsby PJ, Seeley WW. The anterior insula shows heightened interictal intrinsic connectivity in migraine without aura. Neurology. 2015 Mar;84(10):1043-50. https://doi.org/10.1212/WNL.0000000000001330
https://doi.org/https://doi.org/10.1212/... ; 6=Hougaard et al.⁴⁰40. Hougaard A, Amin FM, Hoffmann MB, Rostrup E, Larsson HB, Asghar MS, et al. Interhemispheric differences of fMRI responses to visual stimuli in patients with side fixed migraine aura. Hum Brain Mapp. 2014 Jun;35(6):2714-23. https://doi.org/10.1002/hbm.22361
https://doi.org/https://doi.org/10.1002/... ; 7=Yang et al.⁴¹41. Yang FC, Chou KH, Hsu AL, Fuh JL, Lirng J, Kao HW, et al. Altered brain functional connectome in migraine with and without restless legs syndrome: a resting-state functional MRI study. Front Neurol. 2018 Jan;9:25. https://doi.org/10.3389/fneur.2018.00025
https://doi.org/https://doi.org/10.3389/... ; 8=Maleki et al.⁴²42. Maleki N, Becerra L, Brawn J, McEwen B, Burstein R, Borsook D. Common hippocampal structural and functional changes in migraine. Brain Struct Funct. 2013 Jul;218(4):903-12. https://doi.org/10.1007/s00429-012-0437-y
https://doi.org/https://doi.org/10.1007/... ; 9=Eck et al.⁴³43. Eck J, Richter M, Straube T, Miltner WH, Weiss T. Affective brain regions are activated during the processing of pain-related words in migraine patients. Pain. 2011 May;152(5):1104-13. https://doi.org/10.1016/j.pain.2011.01.026
https://doi.org/https://doi.org/10.1016/... .

Authors (year)	Subjects	Sex	Age	Migraine type	Migraine duration	Pain intensity	Attacks frequency (days/month)	Medication	Cognition	Anxiety	Depression
Coppola et al. (2015)³⁸38. Coppola G, Di Renzo A, Tinelli E, Iacovelli E, Lepre C, Di Lorenzo C, et al. Evidence for brain morphometric changes during the migraine cycle: a magnetic resonance-based morphometry study. Cephalalgia. 2015 Aug;35(9):783-91. https://doi.org/10.1177/0333102414559732 https://doi.org/https://doi.org/10.1177/...	39 (E:24; C:15)	E: 19F, 5M; C: 11F, 4M	E: interictal (31.6±7.6), Ictal (33.3±12.1); C: 28.6±4.0)	Migraine without aura (24)	Interictal: 16.5±6.6 years; Ictal: 13.1±9.9 years	VAS Interictal: 7.5±0.8; Ictal: 7.4±0.6	Interictal: 3.4±2.4; Ictal: 4.0±3.4	Abortive medications, except in the neuroimaging session.	X	X	X
Maleki et al. (2013)⁴²42. Maleki N, Becerra L, Brawn J, McEwen B, Burstein R, Borsook D. Common hippocampal structural and functional changes in migraine. Brain Struct Funct. 2013 Jul;218(4):903-12. https://doi.org/10.1007/s00429-012-0437-y https://doi.org/https://doi.org/10.1007/...	30 (E: 20; C: 10)	E: 14F, 6M; C:7F, 3M	E: LF (40.2±3.6); HF (43.9±3.4); C: 39.1±3.2)	Episodic LF migraine (1-2 days/month): 10 subjects; HF (8-14 days/month): 10 subjects	X	NRS: LF (7.7±2.4); HF: (7.2±1.8)	LF: 1.7±0.5; HF: 9.3±2.6	Triptans	X	X	BDI: LF (2.1±2.5); HF (1.9±2.4)
Schwedt et al. (2014)³⁶36. Schwedt TJ, Chong CD, Chiang CC, Baxter L, Schlaggar BL, Dodick DW. Enhanced pain-induced activity of pain-processing regions in a case-control study of episodic migraine. Cephalalgia. 2014 Oct;34(12):947-58. https://doi.org/10.1177/0333102414526069 https://doi.org/https://doi.org/10.1177/...	51 (E: 24; C: 27)	E: 19F, 5M; C: 22F, 5M	E: 36.2±11.3; C: 33.7±12.5	Migraine with aura (8) and without aura (16)	15.0±9.3 years.	X	6.5±3.0	No prophylactic medication for at least eight weeks. No overuse of abortive medicines for migraine.	X	STAI: State - 25.4±25.7; Trait ‒ 29.3±31.0	BDI: 2.8±4.7
Tso et al. (2015)³⁹39. Tso AR, Trujillo A, Guo CC, Goadsby PJ, Seeley WW. The anterior insula shows heightened interictal intrinsic connectivity in migraine without aura. Neurology. 2015 Mar;84(10):1043-50. https://doi.org/10.1212/WNL.0000000000001330 https://doi.org/https://doi.org/10.1212/...	30 (E:15; C: 15)	E: 12F, 3M; C: 12F, 3M	E: 33.1±9.4; C: 32.6±8.5	Migraine without aura (15)	X	X	6 (2-12)	No preventive medication for migraine. No individual used analgesics >8 days/month	X	X	X
Wang et al. (2016)³⁵35. Wang N, Huang HL, Zhou H, Yu CY. Cognitive impairment and quality of life in patients with migraine-associated vertigo. Eur Rev Med Pharmacol Sci. 2016 Dec;20(23):4913-7.	80 (E: 40; C: 40)*	E: 23 F, 17M; C: 22F, 18M	E: 42.2±15.4; C: 43.5±16.2	Migraine with aura (24) and without aura (16)	4.7 ±2.5 months	X	X	X	↓ MMSE, ROCF, TMT, VFT	Exclusion criteria, but not evaluated	Exclusion criteria, but not evaluated
Hougaard et al. (2014)⁴⁰40. Hougaard A, Amin FM, Hoffmann MB, Rostrup E, Larsson HB, Asghar MS, et al. Interhemispheric differences of fMRI responses to visual stimuli in patients with side fixed migraine aura. Hum Brain Mapp. 2014 Jun;35(6):2714-23. https://doi.org/10.1002/hbm.22361 https://doi.org/https://doi.org/10.1002/...	40 (E: 20; C: 20)	E: 15F, 5M; C: 15F, 5M	E: 35.0 (20.7-55.0); C: 35.1(20.6-54.7)	Migraine with aura (20)	20.8±11.3 years	X	2.3±2.0 (1-8)	No daily or prophylactic medication for migraine	X	X	X
Yang et al. (2018)⁴¹41. Yang FC, Chou KH, Hsu AL, Fuh JL, Lirng J, Kao HW, et al. Altered brain functional connectome in migraine with and without restless legs syndrome: a resting-state functional MRI study. Front Neurol. 2018 Jan;9:25. https://doi.org/10.3389/fneur.2018.00025 https://doi.org/https://doi.org/10.3389/...	41 (E: 22; C: 19)*	E: 19F, 3M; C: 17F, 2M	E: 32.4±7.7; C: 33.5±9.1	Migraine with aura (11) and without aura (11)	11.9±7.4 years	X	6.1±5.8	Pause in prophylactic medication for migraine (B-blocker or flunarizine) for at least 2 days before imaging	X	HADS: 12.5±7.1	BDI: 8.4±5.9
Liu et al. (2013)³⁷37. Liu J, Zhao L, Nan J, Li G, Xiong S, von Deneena KM, et al. The trade-off between wiring cost and network topology in white matter structural networks in health and migraine. Exp Neurol. 2013 Oct;248:196-204. https://doi.org/10.1016/j.expneurol.2013.04.012 https://doi.org/https://doi.org/10.1016/...	52 (E: 26; C: 26)	E: 26F, 0M; C: 26F, 0M	E: 34.6±4.5; C: 33.3±3.04	Migraine without aura (26)	12.9±3.4 years	NRS: 4.1±0.8	5.2±2.9	There was no restriction of medication, and no details were given about the medications used	X	X	X
Eck et al. (2011)⁴³43. Eck J, Richter M, Straube T, Miltner WH, Weiss T. Affective brain regions are activated during the processing of pain-related words in migraine patients. Pain. 2011 May;152(5):1104-13. https://doi.org/10.1016/j.pain.2011.01.026 https://doi.org/https://doi.org/10.1016/...	20 (E: 10; C: 10)	E: 9F, 1M; C: 9F, 1M	E: 37.9±4.7; C: 37.8±4.8	Migraine with aura (4) and without aura (6)	X	X	X	X	X	X	X

Authors (year)	Memory type	Ictal/interictal condition	Neuroimaging instruments	Task/Test at imaging	Results	Consequence to memory
Coppola et al. (2015)³⁸38. Coppola G, Di Renzo A, Tinelli E, Iacovelli E, Lepre C, Di Lorenzo C, et al. Evidence for brain morphometric changes during the migraine cycle: a magnetic resonance-based morphometry study. Cephalalgia. 2015 Aug;35(9):783-91. https://doi.org/10.1177/0333102414559732 https://doi.org/https://doi.org/10.1177/...	Not specified	Ictal (10) and Interictal (14)	MRI, 3T, weighted in T1. They did not characterize the pulse sequence.	Not applicable	Reduction of gray matter density in the mass of the right inferior parietal lobe, right inferior temporal gyrus, right superior temporal gyrus and left temporal pole in individuals in the interictal phase. Increased gray matter density in the right lenticular nucleus, bilateral insula and left temporal pole in the ictal phase.	Dysfunction in memory processing by affecting regions, such as the inferior parietal lobe and upper temporal gyrus, areas that interconnect visual and auditory processing, perception and memory.
Wang et al. (2016)³⁵35. Wang N, Huang HL, Zhou H, Yu CY. Cognitive impairment and quality of life in patients with migraine-associated vertigo. Eur Rev Med Pharmacol Sci. 2016 Dec;20(23):4913-7.	Not specified	Interictal	MRI, 3T, Flair weighted with spin echo pulse sequence, and T2.	Not applicable	More lesions in the deep white matter in the brain, in the lateral periphery of the ventricles and in the total white matter of the brain when compared to the control group.	Cognitive impairment, including memory, related to lesions of the brain white matter.
Liu et al. (2013)³⁷37. Liu J, Zhao L, Nan J, Li G, Xiong S, von Deneena KM, et al. The trade-off between wiring cost and network topology in white matter structural networks in health and migraine. Exp Neurol. 2013 Oct;248:196-204. https://doi.org/10.1016/j.expneurol.2013.04.012 https://doi.org/https://doi.org/10.1016/...	Memory of pain	X	Diffusion tensor imaging tractography, MRI, 3T, gradient echo sequence.	Not applicable	Changes in white matter; increase of the clustering coefficient but decrease in the modularity of the networks; altered connection strength on insula, amygdala, cingulate gyrus, hippocampus, parahippocampal gyrus, striatum, prefrontal dorsolateral cortex, pre-central gyrus, inferior parietal gyrus, occipital cortices and temporal cortices.	Neurological reorganization and degeneration in terms of learning and memory, especially related to pain.

Authors (year)	Memory type	Ictal/interictal condition	Neuroimaging instruments	Task/Test at imaging	Results	Consequence to memory
Maleki et al. (2013)⁴²42. Maleki N, Becerra L, Brawn J, McEwen B, Burstein R, Borsook D. Common hippocampal structural and functional changes in migraine. Brain Struct Funct. 2013 Jul;218(4):903-12. https://doi.org/10.1007/s00429-012-0437-y https://doi.org/https://doi.org/10.1007/...	Not specified	X	fMRI, 3T, T1 weighted, echo gradient sequence.	Painful thermal stimulation	Decreased functional connectivity with the hippocampus in the contralateral supramarginal gyrus, bilateral temporal pole, contralateral orbitofrontal, bilateral nucleus accumbens, bilateral anterior insula, bilateral medial frontal, contralateral paracingulate in individuals having a high frequency of migraine when compared to individuals having a low frequency of attacks.	Reduced connectivity of the hippocampus to other brain areas indicates possible memory-processing failure.
Schwedt et al. (2014)³⁶36. Schwedt TJ, Chong CD, Chiang CC, Baxter L, Schlaggar BL, Dodick DW. Enhanced pain-induced activity of pain-processing regions in a case-control study of episodic migraine. Cephalalgia. 2014 Oct;34(12):947-58. https://doi.org/10.1177/0333102414526069 https://doi.org/https://doi.org/10.1177/...	Memory of pain	X	fMRI, 3T, T1 weighted with echo gradient sequence and T2 weighted with spin echo sequence.	Painful thermal stimulation	Individuals having migraine had greater activation induced by pain in the lentiform nucleus, fusiform gyrus, subthalamic nucleus, hippocampus, mid-cingulate cortex, premotor, somatosensory and dorsolateral prefrontal cortex and less activation in pre-central gyrus and superior temporal gyrus.	Most regions with increased pain induced activation participate in cognitive aspects of pain perception, such as attention to pain and memory related to pain.
Tso et al. (2015)³⁹39. Tso AR, Trujillo A, Guo CC, Goadsby PJ, Seeley WW. The anterior insula shows heightened interictal intrinsic connectivity in migraine without aura. Neurology. 2015 Mar;84(10):1043-50. https://doi.org/10.1212/WNL.0000000000001330 https://doi.org/https://doi.org/10.1212/...	Not specified	Interictal (out of 72 hours before or after an attack).	fMRI, 3T, T2* weighted with planar echo sequence. Coregistration was performed with T1 weighted and echo gradient sequence.	Resting state	Higher connectivity between the calcarine cortex, the Heschl gyrus and the right dorsal anterior insula. The anterior right ventral insula presented increased connectivity with the left ventral medial part in patients with migraine, as well as with the left temporal lobe and the amygdala.	Alteration in the connectivity of the dorsal anterior insula would lead to a modification in the function of organizing and sustaining cognitive processing.
Hougaard et al. (2014)⁴⁰40. Hougaard A, Amin FM, Hoffmann MB, Rostrup E, Larsson HB, Asghar MS, et al. Interhemispheric differences of fMRI responses to visual stimuli in patients with side fixed migraine aura. Hum Brain Mapp. 2014 Jun;35(6):2714-23. https://doi.org/10.1002/hbm.22361 https://doi.org/https://doi.org/10.1002/...	Visuospatial memory	Interictal	fMRI-BOLD, 3T, T1 weighted with echo gradient sequence.	Visual Stimulation	Increased signs in the inferior frontal gyrus, superior parietal lobe; inferior parietal lobe and intraparietal sulcus, as well as the occipital cortex areas.	Impairment of the functional network involved in oculomotor control, orientation of movement, perception of movement, visual attention, and visuospatial memory.
Yang et al. (2018)⁴¹41. Yang FC, Chou KH, Hsu AL, Fuh JL, Lirng J, Kao HW, et al. Altered brain functional connectome in migraine with and without restless legs syndrome: a resting-state functional MRI study. Front Neurol. 2018 Jan;9:25. https://doi.org/10.3389/fneur.2018.00025 https://doi.org/https://doi.org/10.3389/...	Not specified	Interictal ‒ individuals without symptoms of migraine two days before the application of the imaging technique.	fMRI-BOLD, 3T. Anatomical scan T1 weighted with echo gradient sequence. Spontaneous activity measured in T2 weighted with echo gradient sequence.	Resting state	Patients having migraine presented several weaker neural connections than control. The most affected functional brain networks were dorsal attention, salience, default mode, visual and fronto-parietal modes.	Changes in the dorsal attention network may manifest as memory deficits during and between migraine attacks.
Eck et al. (2011)⁴³43. Eck J, Richter M, Straube T, Miltner WH, Weiss T. Affective brain regions are activated during the processing of pain-related words in migraine patients. Pain. 2011 May;152(5):1104-13. https://doi.org/10.1016/j.pain.2011.01.026 https://doi.org/https://doi.org/10.1016/...	Memory of pain	X	fMRI, 1.5T, weighted in T1 and T2. They did not characterize the pulse sequence.	Verbal descriptors of pain.	Adjectives related to pain provoked increased activations in the left orbitofrontal cortex and anterior insula during imaging, and in the right secondary somatosensory cortex and posterior insula during distraction when compared to negative adjectives.	The involvement of ventrolateral, dorsolateral and rostrolateral and prefrontal structures may be related to the demands of imagination, including processes of working memory and long-term memory.

[1] Correspondence: Mírian Celly Medeiros Miranda David; E-mail: miriancelly@hotmail.com

Brasil

Brasil

Neuroimaging investigation of memory changes in migraine: a systematic review

Investigação por neuroimagem das alterações de memória na enxaqueca: uma revisão sistemática

ABSTRACT

Background:

Methods:

Results:

Conclusions: