Immediate brain network changes in AIS patients treated with electroacupuncture by observing resting-state functional magnetic resonance imaging

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• Clinical Article •

ZHU Li YU Chengxin ZHAO Changjiang XIONG Xiong CHEN Long ZHANG Can CHEN Jiangjin

Cite this article as: ZHU L, YU C X, ZHAO C J, et al. Immediate brain network changes in AIS patients treated with electroacupuncture by observing resting-state functional magnetic resonance imaging[J]. Chin J Magn Reson Imaging, 2024, 15(6): 42-48. DOI:10.12015/issn.1674-8034.2024.06.006.

Abstract

[Abstract] Objective To investigate the changes of immediate sensory motor network (SMN) and default mode network (DMN) in patients with acute ischemic stroke (AIS) using resting-state functional magnetic resonance imaging (rs-fMRI) and independent component analysis (ICA).Materials and Methods Twenty-seven patients with AIS and 27 healthy controls (HCs) were included in the study. Each subject was assessed on relevant clinical scales and baseline data were collected, followed by immediate electroacupuncture stimulation for AIS, and relevant rs-fMRI data were collected. Then, the SMN and DMN network components were extracted using the ICA method. The functional connectivity values of patients and healthy controls were compared, as well as the changes in functional connectivity before and after acupuncture; bias correlation analysis was performed between the change values and the corresponding changes in clinical scale scores; and then the differential brain regions were used as seed points to calculate their functional connectivity (FC) with the whole brain.Results Before acupuncture, functional connectivity increased in the left prefrontal lobe of the AIS group comparable to the healthy control group (P<0.001), and decreased in the left subparietal lobule (Z=4.38, P<0.001) and the right posterior cingulate gyrus (Z=4.87, P<0.001); the FC values of the left subparietal lobule (P<0.001), the left posterior cingulate gyrus (P<0.001), and the left frontal lobe (P<0.001) increased, increased FC values in some cerebellar regions (P<0.001). After acupuncture, the functional connectivity of the right prefrontal lobe in the AIS group significantly increased (P<0.001) and strongly and positively correlated with the difference of (Fugl-Meyer Assessment, FMA) score (r=0.842, P<0.001); the FC values of the right thalamus (Z=4.38, P<0.001) and the left frontal lobe in the AIS group significantly increased (P<0.001), and the FC values of some cerebellar regions increased.Conclusions AIS patients have abnormal brain activity in the limbic system (posterior cingulate gyrus, hippocampus)-thalamus-cortex (subparietal lobule-frontal lobe) neural circuit; electroacupuncture can immediately modulate the brain spontaneous activity of AIS patients, which involves the brain areas related to motor completion, and it may be a potential target brain area for electroacupuncture treatment of AIS.

[Keywords] acute ischemic stroke；resting-state functional magnetic resonance imaging；magnetic resonance imaging；electroacupuncture therapy；immediate effects；frontal lobe

Contributor Information

ZHU Li^{1,
2}   YU Chengxin^{1,
2*}   ZHAO Changjiang^{1,
2}   XIONG Xiong^{1,
2}   CHEN Long^{1,
2}   ZHANG Can^{1,
2}   CHEN Jiangjin^{1,
2}

¹ The First College of Clinical Medical Science, China Three Gorges University, Yichang 443000, China

² Department of Radiology, Yichang Central People's Hospital, Yichang, Hubei 443000, China

Corresponding author: YU C X, E-mail: ycyucx@163.com

Conflicts of interest None.

Publication Information

Received 2023-01-22

Accepted 2024-05-31

DOI: 10.12015/issn.1674-8034.2024.06.006

Text

References

[1]

FEIGIN V L, OWOLABI M O. Pragmatic solutions to reduce the global burden of stroke: a world stroke organization-lancet neurology commission[J]. Lancet Neurol, 2023. DOI: 10.1016/S1474-4422(23)00277-6.

[2]

BATHLA G, AJMERA P, MEHTA P M, et al. Advances in acute ischemic stroke treatment: Current status and future directions[J]. AJNR Am J Neuroradiol, 2023, 44(7): 750-758. DOI: 10.3174/ajnr.A7872.

[3]

MA H, CAMPBELL B, PARSONS M W, et al. Thrombolysis guided by perfusion imaging up to 9 hours after onset of stroke[J].N Engl J Med, 2019, 380(19): 1795-1803. DOI: 10.1056/NEJMoa1813046.

[4]

BIRCH S, ROBINSON N. Acupuncture as a post-stroke treatment option: A narrative review of clinical guideline recommendations[J/OL]. Phytomedicine, 2022, 104: 154297 [2024-01-22]. https://doi.org/10.1016/j.phymed.2022.154297. DOI: 10.1016/j.phymed.2022.154297.

[5]

QU Q M, JIA J. Interpretation and prospect of stroke rehabilitation guidelines[J]. Chinese Journal of Medicine, 2022, 57(5): 487-490. DOI: 10.3969/j.issn.1008-1070.2022.05.007.

[6]

ZHANG F N, LIU H L, LI Z. Net Meta-analysis of the Effects of Acupuncture and Repetitive Transcranial Magnetic Stimulation on Upper Extremity Motor Function and the Ability to Perform Activities of Daily Living in Stroke Patients: The 13th National Congress of Sports Science[C]. Tianjin, China, Sports Medicine Section Presentation, 2023.

[7]

FENG X L. Effects of electroacupuncture at different time intervals on patients with wind-phlegm stasis type acute ischemic stroke[D]. Nanjing: Nanjing University of Chinese Medicine, 2016.

[8]

JIANG Y, QIAN J, MA T H, et al. Analysis of the efficacy of different electroacupuncture parameters in the treatment of peripheral facial paralysis[J]. Shanghai J Acup Moxib, 2024, 43(2): 225-232. DOI: 10.13460/j.issn.1005-0957.2023.13.0035.

[9]

SUN J F, HE J K, MA Y, et al. Immediate brain effects of electroacupuncture at auricular concha in the treatment of first-episode depression using the resting-state fMRI technology[J]. Shanghai J Acup Moxib, 2023, 42(5): 477-484. DOI: 10.13460/j.issn.1005-0957.2023.05.0477.

[10]

PENG Y Y, LUAN L. Therapeutic effect of electroacupuncture with different intensity currents in the treatment of primary trigeminal neuralgia[J]. Hubei Journal of TCM FEB, 2015, 37(2): 61-62.

[11]

BALASUBRAMANIAN C K, LI C, BOWDEN M G, et al. Dimensionality and item-difficulty hierarchy of the lower extremity fugl-meyer assessment in individuals with subacute and chronic stroke[J]. Arch Phys Med Rehabil, 2016, 97(4): 582-589. DOI: 10.1016/j.apmr.2015.12.012.

[12]

TAO L, FU Q H, PEI J. Application of motor function scales in patients with post-stroke limb hemiplegia[J]. Chin J Acu and Mox, 2021, 10(2): 77-82. DOI: 10.3877/cma.j.issn.2095-3240.2021.02.012.

[13]

INAGAKI H K, CHEN S, RIDDER M C, et al. A midbrain-thalamus-cortex circuit reorganizes cortical dynamics to initiate movement[J]. Cell, 2022, 185(6): 1065-1081. DOI: 10.1016/j.cell.2022.02.006.

[14]

PANG R, WANG D, CHEN T S R, et al. Reorganization of prefrontal network in stroke patients with dyskinesias: evidence from resting‐state functional near‐infrared spectroscopy[J/OL]. J Biophotonics, 2022, 15(7): e202200014 [2024-01-22]. https://pubmed.ncbi.nlm.nih.gov./35324088/. DOI: 10.1002/jbio.202200014.

[15]

OLAFSON E, RUSSELLO G, JAMISON K W, et al. Frontoparietal network activation is associated with motor recovery in ischemic stroke patients[J/OL]. Commun Biol, 2022, 5(1): 993 [2024-01-22]. https://doi.org/10.1038/s42003-022-03950-4. DOI: 10.1038/s42003-022-03950-4.

[16]

URBIN M A, HONG X, LANG C E, et al. Resting-state functional connectivity and its association with multiple domains of upper-extremity function in chronic stroke[J]. Neurorehabil Neural Repair, 2014, 28(8): 761-769. DOI: 10.1177/1545968314522349.

[17]

GUO M, XU G J, YU Q R, et al. Post-stroke motor dysfunction is associated with structural damage to the corpus callosum connecting interhemispheric homotopic brain regions[J]. Chin J Magn Reson Imag, 2022, 13(6): 28-35. DOI: 10.12015/issn.1674-8034.2022.06.006.

[18]

LARIVIÈRE S, WARD N S, BOUDRIAS M. Disrupted functional network integrity and flexibility after stroke: Relation to motor impairments[J]. Neuroimage Clin, 2018, 19: 883-891. DOI: 10.1016/j.nicl.2018.06.010.

[19]

LIU B, TIAN Q, GU Y. Robust vestibular self-motion signals in macaque posterior cingulate region[J/OL]. eLife, 2021, 10: e64569 [2024-01-22]. https://doi.org/10.7554/eLife.64569. DOI: 10.7554/eLife.64569.

[20]

CARUANA F, GERBELLA M, AVANZINI P, et al. Motor and emotional behaviours elicited by electrical stimulation of the human cingulate cortex[J]. Brain, 2018, 141(10): 3035-3051. DOI: 10.1093/brain/awy219.

[21]

SI X, XIANG S, ZHANG L, et al. Acupuncture with deqi modulates the hemodynamic response and functional connectivity of the prefrontal-motor cortical network[J/OL]. Front Neurosci, 2021, 15: 693623 [2024-01-22]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8415569/. DOI: 10.3389/fnins.2021.693623.

[22]

LIU H, CHEN L, ZHANG G, et al. Scalp acupuncture enhances the functional connectivity of visual and cognitive-motor function network of patients with acute ischemic stroke[J]. Evid Based Complement Alternat Med, 2020, 2020: 1-11. DOI: 10.1155/2020/8836794.

[23]

VICENTINI J E, WEILER M, CASSEB R F, et al. Subacute functional connectivity correlates with cognitive recovery six months after stroke[J/OL]. Neuroimage Clin, 2021, 29: 102538 [2024-01-22]. https://doi.org/10.1016/j.nicl.2020.102538. DOI: 10.1016/j.nicl.2020.102538.

[24]

WU C W, LIN S N, HSU L, et al. Synchrony between default-mode and sensorimotor networks facilitates motor function in stroke rehabilitation: A pilot fMRI study[J/OL]. Front Neurosci, 2020, 14: 548 [2024-01-22]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7325875/. DOI: 10.3389/fnins.2020.00548.

[25]

MEIRHAEGHE N, SOHN H, JAZAYERI M. A precise and adaptive neural mechanism for predictive temporal processing in the frontal cortex[J]. Neuron, 2021, 109(18): 2995-3011. DOI: 10.1016/j.neuron.2021.08.025.

[26]

WEBLER R D, FOX J, MCTEAGUE L M, et al. DLPFC stimulation alters working memory related activations and performance: An interleaved TMS-fMRI study[J]. Brain Stimul, 2022, 15(3): 823-832. DOI: 10.1016/j.brs.2022.05.014.

[27]

MENON V, D'ESPOSITO M. The role of PFC networks in cognitive control and executive function[J]. Neuropsychopharmacology, 2022, 47(1): 90-103. DOI: 10.1038/s41386-021-01152-w.

[28]

WANG W W, WU X. Anatomy, physiology and cingulate epilepsy of the cingulate gyrus[J]. Chinese Journal of Modern Neurologic Diseases, 2018, 18(5): 315-323. DOI: 10.3969/j.issn.1672-6731.2018.05.004.

[29]

KRAVITZ D J, SALEEM K S, BAKER C I, et al. A new neural framework for visuospatial processing[J]. Nat Rev Neurosci, 2011, 12(4): 217-230. DOI: 10.1038/nrn3008.

[30]

KIRIYAMA I, MIKI H, KIKUCHI K, et al. Topographic analysis of the inferior parietal lobule in high-resolution 3D MR imaging[J]. AJNR Am J Neuroradiol, 2009, 30(3): 520-524. DOI: 10.3174/ajnr.A1417.

[31]

LIU F, CHEN C, BAI Z, et al. Specific subsystems of the inferior parietal lobule are associated with hand dysfunction following stroke: A cross‐sectional resting‐statefMRI study[J]. CNS Neurosci Ther, 2022, 28(12): 2116-2128. DOI: 10.1111/cns.13946.

[32]

TOMIYAMA H, MURAYAMA K, NEMOTO K, et al. Functional connectivity between pre-supplementary motor area and inferior parietal lobule associated with impaired motor response inhibition in first-degree relatives of patients with obsessive-compulsive disorder[J]. Cerebral Cortex, 2023, 33(12): 7531-7539. DOI: 10.1093/cercor/bhad058.

[33]

ARLEO A, BAREŠ M, BERNARD J A, et al. Consensus paper: Cerebellum and ageing[J]. Cerebellum, 2023, 23(2): 802-832. DOI: 10.1007/s12311-023-01577-7.

[34]

FRANÇA C, DE ANDRADE D C, TEIXEIRA M J, et al. Cerebellum as a possible target for neuromodulation after stroke[J]. Brain Stimul, 2018, 11(5): 1175-1176. DOI: 10.1016/j.brs.2018.04.017.

[35]

KHAN M A, GHAFOOR U, YOO H, et al. Acupuncture enhances brain function in patients with mild cognitive impairment: evidence from a functional-near infrared spectroscopy study[J]. Neural Regen Res, 2022, 17(8): 1850-1856. DOI: 10.4103/1673-5374.332150.

[36]

BUIJS R M, VAN EDEN C G. The integration of stress by the hypothalamus, amygdala and prefrontal cortex: balance between the autonomic nervous system and the neuroendocrine system[J]. Prog Brain Res, 2000, 126: 117-132. DOI: 10.1016/S0079-6123(00)26011-1.

[37]

SAKATANI K, KITAGAWA T, AOYAMA N, et al. Effects of acupuncture on autonomic nervous function and prefrontal cortex activity[J]. Adv Exp Med Biol, 2010, 662: 455-460. DOI: 10.1007/978-1-4419-1241-1_65.

[38]

LI K, WANG J, HU Z, et al. Gating attractor dynamics of frontal cortex under acupuncture via recurrent neural network[J]. IEEE J Biomed Health Inform, 2022, 26(8): 3836-3847. DOI: 10.1109/JBHI.2022.3158963.

[39]

CHEN L, QU Y, CAO J, et al. The increased inter‐brain neural synchronization in prefrontal cortex between simulated patient and acupuncturist during acupuncture stimulation: Evidence from functional near-infrared spectroscopy hyperscanning[J]. Hum Brain Mapp, 2023, 44(3): 980-988. DOI: 10.1002/hbm.26120.

[40]

CAO J, QU Y, CHEN L, et al. The regulations on cortical activation and functional connectivity of the dorsolateral prefrontal cortex-primary somatosensory cortex elicited by acupuncture with reinforcing-reducing manipulation[J/OL]. Front Hum Neurosci, 2023, 17: 1159378 [2024-01-22]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10188977/. DOI: 10.3389/fnhum.2023.1159378.

[41]

XING Y K, WANG K D, LI X. Mechanisms and research progress of the thalamus primordial nucleus in the regulation of body motor function[J]. Chinese Journal of Pathophysiology, 2022, 38(3): 559-565. DOI: 10.3969/j.issn.1000-4718.2022.03.022.

[42]

GIULIANI C. The flavonoid quercetin induces AP-1 activation in FRTL-5 Thyroid Cells[J/OL]. Antioxidants, 2019, 8(5): 112 [2024-01-22]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6562732/. DOI: 10.3390/antiox8050112.

[43]

BEVAN M D. Motor control: A basal ganglia feedback circuit for action suppression[J/OL]. Curr Biol, 2021, 31(4): R191-R193 [2024-01-22]. https://pubmed.ncbi.nlm.nih.gov/33621506/. DOI: 10.1016/j.cub.2020.11.067.

[44]

BALDASSARRE A, RAMSEY L, RENGACHARY J, et al. Dissociated functional connectivity profiles for motor and attention deficits in acute right-hemisphere stroke[J]. Brain, 2016, 139(7): 2024-2038. DOI: 10.1093/brain/aww107.

[45]

TULADHAR A M, SNAPHAAN L, SHUMSKAYA E, et al. Default mode network connectivity in stroke patients[J/OL]. PloS One, 2013, 8(6): e66556 [2024-01-22]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3688936/. DOI: 10.1371/journal.pone.0066556.

[46]

WANG D Y, ZHANG B Y, LI T, et al. Progress of the neuromodulation mechanism of acupuncture on brain networks[J]. Shanghai J Acup Moxib, 2021, 40(6): 781-785. DOI: 10.13460/j.issn.1005-0957.2021.13.0011.

[47]

WANG Y, LU M, LIU R, et al. Acupuncture alters brain's dynamic functional network connectivity in stroke patients with motor dysfunction: A randomised controlled neuroimaging trial[J]. Neural Plasticity, 2023, 2023: 1-14. DOI: 10.1155/2023/8510213.

[48]

ZHANG J, LU C, WU X, et al. Neuroplasticity of acupuncture for stroke: An evidence-based review of MRI[J]. Neural Plasticity, 2021, 2021: 1-14. DOI: 10.1155/2021/2662585.

[49]

FANG J, JIN Z, WANG Y, et al. The salient characteristics of the central effects of acupuncture needling: Limbic‐paralimbic‐neocortical network modulation[J]. Hum Brain Mapp, 2009, 30(4): 1196-1206. DOI: 10.1002/hbm.20583.

[50]

LI Y, YU Z, WU P, et al. Ability of an altered functional coupling between resting-state networks to predict behavioral outcomes in subcortical ischemic stroke: A longitudinal study[J/OL]. Front Aging Neurosci, 2022, 14: 933567 [2024-01-22]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9520312/. DOI: 10.3389/fnagi.2022.933567.

[51]

WU P, ZHOU Y, LIAO C, et al. Structural changes induced by acupuncture in the recovering brain after ischemic stroke[J]. Evid Based Complement Alternat Med, 2018, 2018: 1-8. DOI: 10.1155/2018/5179689.

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