Regulation of amygdala by rtfMRI-NF technique in improving insomnia disorder

Share this content in WeChat

• Clinical Articles •

ZHANG Miao WU Xiaoling LI Zhonglin ZOU Zhi ZHOU Jing SHEN Yu QI Fei GU Yu'ang JIA Shulei DOU Shewei YAN Fengshan LI Yongli

Cite this article as: ZHANG M, WU X L, LI Z L, et al. Regulation of amygdala by rtfMRI-NF technique in improving insomnia disorder[J]. Chin J Magn Reson Imaging, 2023, 14(7): 5-9. DOI:10.12015/issn.1674-8034.2023.07.002.

Abstract

[Abstract] Objective To investigate the effect of real-time functional magnetic resonance imaging neurofeedback (rtfMRI-NF) on amygdala in patients with insomnia disorder (ID).Materials and Methods Twenty-nine patients with ID were recruited, and the rtfMRI-NF technique was used for intervention for 3 weeks (once per week). Rest-state functional magnetic resonance imaging data and Pittsburgh Sleep Quality Index (PSQI), Insomnia severity index scale (ISI), Hamilton Depression Scale (HAMD), Beck Depression Inventory (BDI), Hamilton Anxiety Scale (HAMA) were collected before and after the intervention. The bilateral amygdala was used as the seed point to calculate functional connectivity (FC) between the amygdala and the whole brain voxels. The paired t-test was used to compare the statistically significant difference brain areas before and after the intervention, and the FC values of the statistically significant difference brain areas after the intervention were extracted to conduct correlation analysis with clinical scale scores.Results PSQI, ISI, HAMA and HAMD scores of patients with ID were lower after rtfMRI-NF technique intervention than before intervention (P＜0.05), and there was no statistical significance in BDI scores compared with before intervention. After intervention, the FC values of the left amygdala with left middle temporal gyrus, left medial frontal gyrus, right precuneus and right precuneus increased in patients with ID. FC values decreased in the left amygdala with right parietal gyrus, right superior temporal gyrus, and left middle frontal gyrus (GRF correction, voxel level P＜0.001, mass level P＜0.05). And after intervention, the FC values of the left amygdala with the right precuneus were negatively correlated with PSQI scores (r=-0.477, P＜0.01), and the FC values of the left amygdala with the right top gyrus were negatively correlated with HAMA scores (r=-0.586, P＜0.01).Conclusions rtfMRI-NF technology can improve the sleep quality and emotional state of the patients with ID, and the mechanism may be related to the changes of functional connections between the left amygdala with the default network, emotional regulation, and cognitive brain regions.

[Keywords] insomnia disorder；real-time functional magnetic resonance imaging neurofeedback；amygdala；functional connectivity；rest-state functional magnetic resonance imaging；magnetic resonance imaging

Contributor Information

ZHANG Miao¹ WU Xiaoling² LI Zhonglin¹ ZOU Zhi¹ ZHOU Jing³ SHEN Yu¹ QI Fei¹ GU Yu'ang⁴ JIA Shulei⁴ DOU Shewei¹ YAN Fengshan¹ LI Yongli^3*

¹ Department of Medical Imaging, Zhengzhou University People's Hospital/Henan Provincial People's Hospital, Zhengzhou 450003, China

² Department of Nuclear Medicine, Henan Proincial People's Hospital, Zhengzhou University People's Hospital, Zhengzhou 450003, China

³ Department of Health Management, Henan Proincial People's Hospital, Zhengzhou University People's Hospital, Zhengzhou 450003, China

⁴ Department of Medical Imaging, Henan Provincial People's Hospital, Xinxiang Medical University, Zhengzhou 450000, China

Corresponding author: Li YL, E-mail: shyliyongli@126.com

Conflicts of interest None.

Publication Information

ACKNOWLEDGMENTS National Natural Science Foundation of China (No. 82071884); Young and Middle-Aged Health Science and Technology Innovation Talent Project of Henan Province (No. YXKC2020004); Science and Technology Research Project of Henan Provincial (No. 222102310198).

Received 2023-01-19

Accepted 2023-06-25

DOI: 10.12015/issn.1674-8034.2023.07.002

Text

References

[1]

CHUNG K F, YEUNG W F, HO F Y, et al. Cross-cultural and comparative epidemiology of insomnia: the Diagnostic and statistical manual (DSM), International classification of diseases (ICD) and International classification of sleep disorders (ICSD)[J]. Sleep Med, 2015, 16(4): 477-482. DOI: 10.1016/j.sleep.2014.10.018.

[2]

RIEMANN D, KRONE L B, WULFF K, et al. Sleep, insomnia, and depression[J]. Neuropsychopharmacology, 2020, 45(1): 74-89. DOI: 10.1038/s41386-019-0411-y.

[3]

PALAGINI L, HERTENSTEIN E, RIEMANN D, et al. Sleep, insomnia and mental health[J/OL]. J Sleep Res, 2022, 31(4): e13628 [2023-01-18]. https://onlinelibrary.wiley.com/doi/10.1111/jsr.12661. DOI: 10.1111/jsr.13628.

[4]

LI L Q, GAN Y, ZHOU X G, et al. Insomnia and the risk of hypertension: a meta-analysis of prospective cohort studies[J/OL]. Sleep Med Rev, 2021, 56: 101403 [2023-01-18]. https://linkinghub.elsevier.com/retrieve/pii/S1087-0792(20)30146-5. DOI: 10.1016/j.smrv.2020.101403.

[5]

CHASENS E R, IMES C C, KARIUKI J K, et al. Sleep and metabolic syndrome[J]. Nurs Clin North Am, 2021, 56(2): 203-217. DOI: 10.1016/j.cnur.2020.10.012.

[6]

HUANG B H, DUNCAN M J, CISTULLI P A, et al. Sleep and physical activity in relation to all-cause, cardiovascular disease and cancer mortality risk[J]. Br J Sports Med, 2022, 56(13): 718-724. DOI: 10.1136/bjsports-2021-104046.

[7]

Chinese Sleep Research Society. China guidelines for diagnosis and treatment of insomnia[J]. Natl Med J China, 2017, 97(24): 1844-1856. DOI: 10.3760/cma.j.issn.0376-2491.2017.24.002.

[8]

ZHAO W R, LI C Y, CHEN J J, et al. Insomnia disorder and hyperarousal: evidence from resting-state and sleeping EEG[J]. Sci Sin Vitae, 2020, 50(3): 270-286. DOI: org/10.1360/SSV-2019-0234.

[9]

THIBAULT R T, MACPHERSON A, LIFSHITZ M, et al. Neurofeedback with fMRI: a critical systematic review[J/OL]. Neuroimage, 2018, 172: 786-807 [2023-01-18]. https://linkinghub.elsevier.com/retrieve/pii/S1053-8119(17)31095-9. DOI: 10.1016/j.neuroimage.2017.12.071.

[10]

ZHU Y S, GAO H, TONG L, et al. Emotion regulation of Hippocampus using real-time fMRI neurofeedback in healthy human[J/OL]. Front Hum Neurosci, 2019, 13: 242 [2023-01-18]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6660260/. DOI: 10.3389/fnhum.2019.00242.

[11]

ZOU Z, LI Z L, ZHOU J, et al. Research progress on the regulation target of real-time functional magnetic resonance imaging neurofeedback[J]. Chin J Magn Reson Imaging, 2020, 11(8): 684-687. DOI: 10.12015/issn.1674-8034.2020.08.022.

[12]

DUDEK E, DODELL-FEDER D. The efficacy of real-time functional magnetic resonance imaging neurofeedback for psychiatric illness: a meta-analysis of brain and behavioral outcomes[J/OL]. Neurosci Biobehav Rev, 2021, 121: 291-306 [2023-01-18]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7856210/. DOI: 10.1016/j.neubiorev.2020.12.020.

[13]

BAGLIONI C, SPIEGELHALDER K, REGEN W, et al. Insomnia disorder is associated with increased amygdala reactivity to insomnia-related stimuli[J]. Sleep, 2014, 37(12): 1907-1917. DOI: 10.5665/sleep.4240.

[14]

SCHIEL J E, HOLUB F, PETRI R, et al. Affect and arousal in insomnia: through a lens of neuroimaging studies[J/OL]. Curr Psychiatry Rep, 2020, 22(9): 44 [2023-01-18]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7359160/. DOI: 10.1007/s11920-020-01173-0.

[15]

BARREIROS A R, ALMEIDA I, BAÍA B C, et al. Amygdala modulation during emotion regulation training with fMRI-based neurofeedback[J/OL]. Front Hum Neurosci, 2019, 13: 89 [2023-01-18]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6444080/. DOI: 10.3389/fnhum.2019.00089.

[16]

LI X D, LI Z L, ZOU Z, et al. Real-time fMRI neurofeedback training changes brain degree centrality and improves sleep in chronic insomnia disorder: a resting-state fMRI study[J/OL]. Front Mol Neurosci, 2022, 15: 825286 [2023-01-18]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8904428/. DOI: 10.3389/fnmol.2022.825286.

[17]

WATANABE T, SASAKI Y, SHIBATA K, et al. Advances in fMRI real-time neurofeedback: (trends in cognitive sciences 21, 997-1010, 2017)[J/OL]. Trends Cogn Sci, 2018, 22(8): 738 [2023-01-18]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6054802/. DOI: 10.1016/j.tics.2018.05.007.

[18]

FEDE S J, DEAN S F, MANUWEERA T, et al. A guide to literature informed decisions in the design of real time fMRI neurofeedback studies: a systematic review[J/OL]. Front Hum Neurosci, 2020, 14: 60 [2023-01-18]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7052377/. DOI: 10.3389/fnhum.2020.00060.

[19]

BACKHAUS J, JUNGHANNS K, BROOCKS A, et al. Test-retest reliability and validity of the Pittsburgh Sleep Quality Index in primary insomnia[J]. J Psychosom Res, 2002, 53(3): 737-740. DOI: 10.1016/s0022-3999(02)00330-6.

[20]

GAO W, CHEN S D, BISWAL B, et al. Temporal dynamics of spontaneous default-mode network activity mediate the association between reappraisal and depression[J]. Soc Cogn Affect Neurosci, 2018, 13(12): 1235-1247. DOI: 10.1093/scan/nsy092.

[21]

PAN J H, ZHAN L Y, HU C L, et al. Emotion regulation and complex brain networks: association between expressive suppression and efficiency in the Fronto-parietal network and default-mode network[J/OL]. Front Hum Neurosci, 2018, 12: 70 [2023-01-18]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5890121/. DOI: 10.3389/fnhum.2018.00070.

[22]

LUNSFORD-AVERY J R, DAMME K S F, ENGELHARD M M, et al. Sleep/wake regularity associated with default mode network structure among healthy adolescents and young adults[J/OL]. Sci Rep, 2020, 10(1): 509 [2023-01-18]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6965093/. DOI: 10.1038/s41598-019-57024-3.

[23]

JACKSON R L, BAJADA C J, RICE G E, et al. An emergent functional parcellation of the temporal cortex[J/OL]. Neuroimage, 2018, 170: 385-399 [2023-01-18]. https://linkinghub.elsevier.com/retrieve/pii/S1053-8119(17)30316-6. DOI: 10.1016/j.neuroimage.2017.04.024.

[24]

CIPOLLI C, FERRARA M, DE GENNARO L, et al. Beyond the neuropsychology of dreaming: insights into the neural basis of dreaming with new techniques of sleep recording and analysis[J/OL]. Sleep Med Rev, 2017, 35: 8-20 [2023-01-18]. https://linkinghub.elsevier.com/retrieve/pii/S1087-0792(16)30067-3. DOI: 10.1016/j.smrv.2016.07.005.

[25]

YAN C Q, WANG X, HUO J W, et al. Abnormal global brain functional connectivity in primary insomnia patients: a resting-state functional MRI study[J/OL]. Front Neurol, 2018, 9: 856 [2023-01-18]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6224336/. DOI: 10.3389/fneur.2018.00856.

[26]

DIXON M L, THIRUCHSELVAM R, TODD R, et al. Emotion and the prefrontal cortex: an integrative review[J]. Psychol Bull, 2017, 143(10): 1033-1081. DOI: 10.1037/bul0000096.

[27]

HERMANN A, SCHÄFER A, WALTER B, et al. Emotion regulation in spider phobia: role of the medial prefrontal cortex[J]. Soc Cogn Affect Neurosci, 2009, 4(3): 257-267. DOI: 10.1093/scan/nsp013.

[28]

WANG J J, BECKER B, WANG L J, et al. Corresponding anatomical and coactivation architecture of the human precuneus showing similar connectivity patterns with macaques[J/OL]. Neuroimage, 2019, 200: 562-574 [2023-01-18]. https://linkinghub.elsevier.com/retrieve/pii/S1053-8119(19)30563-4. DOI: 10.1016/j.neuroimage.2019.07.001.

[29]

YAO P. Functional brain imaging characteristics of insomnia patients with different sleep duration[D]. Hohhot: Inner Mongolia Medical University, 2020.

[30]

MARQUES D R, GOMES A A, CLEMENTE V, et al. Unbalanced resting-state networks activity in psychophysiological insomnia[J]. Sleep Biol Rhythms, 2017, 15(2): 167-177. DOI: 10.1007/s41105-017-0096-8.

[31]

HE X X, LI X, FU J L, et al. The morphometry of left cuneus mediating the genetic regulation on working memory[J]. Hum Brain Mapp, 2021, 42(11): 3470-3480. DOI: 10.1002/hbm.25446.

[32]

WANG Z Y, FEI X, LIU X T, et al. REM sleep is associated with distinct global cortical dynamics and controlled by occipital cortex[J/OL]. Nat Commun, 2022, 13(1): 6896 [2023-01-18]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9653484/. DOI: 10.1038/s41467-022-34720-9.

[33]

KAY D, BUYSSE D. Hyperarousal and beyond: new insights to the pathophysiology of insomnia disorder through functional neuroimaging studies[J/OL]. [2023-01-18]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5366822/.BrainSci, 2017, 7(12): 23. DOI: 10.3390/brainsci7030023.

[34]

WOLPERT D M, GOODBODY S J, HUSAIN M. Maintaining internal representations: the role of the human superior parietal lobe[J]. Nat Neurosci, 1998, 1(6): 529-533. DOI: 10.1038/2245.

[35]

DUTTA A, MCKIE S, DEAKIN J F. Resting state networks in major depressive disorder[J]. Psychiatry Res, 2014, 224(3): 139-151. DOI: 10.1016/j.pscychresns.2014.10.003.

[36]

WANG Y L, JIANG P, TANG S, et al. Left superior temporal sulcus morphometry mediates the impact of anxiety and depressive symptoms on sleep quality in healthy adults[J]. Soc Cogn Affect Neurosci, 2021, 16(5): 492-501. DOI: 10.1093/scan/nsab012.

[37]

YE Y X, WANG C Y, LAN X F, et al. Abnormal amygdala functional connectivity in MDD patients with insomnia complaints[J/OL]. Psychiatry Res Neuroimaging, 2023, 328: 111578 [2023-01-18]. https://linkinghub.elsevier.com/retrieve/pii/S0925-4927(22)00135-4. DOI: 10.1016/j.pscychresns.2022.111578.

[38]

SONG P H, LIN H, LIU C Y, et al. Transcranial magnetic stimulation to the middle frontal gyrus during attention modes induced dynamic module reconfiguration in brain networks[J/OL]. Front Neuroinform, 2019, 13: 22 [2023-01-18]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6456710/. DOI: 10.3389/fninf.2019.00022.

[39]

CHAI Y. Effect of sleep deprivation on negative mood and its neural mechanism[D]. Guangzhou: Sun Yat-sen University, 2020. DOI: 10.27231/d.cnki.gnmyc.2020.000023.

[40]

SORGER B, SCHARNOWSKI F, LINDEN D E J, et al. Control freaks: towards optimal selection of control conditions for fMRI neurofeedback studies[J/OL]. Neuroimage, 2019, 186: 256-265 [2023-01-18]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6338498/. DOI: 10.1016/j.neuroimage.2018.11.004.

PREV SCMR white paper: Interpretation of rapid CMR for clinical indications

NEXT Prediction of IDH mutations in glioma based on MRI multiparametric image fusion and DenseNet network

LINK

Tel & Fax: +8610-67113815 E-mail: editor@cjmri.cn