AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
PDF (5 MB)
Collect
Submit Manuscript AI Chat Paper
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Research Article | Open Access

Cortico–subcortical spatiotemporal dynamics in Parkinson’s disease can be modulated by transcranial alternating current stimulation

School of Life Science, Beijing Institute of Technology, Beijing 100081, China
School of Mechatronical Engineering, Beijing Institute of Technology, Beijing 100081, China
School of Medical Technology, Beijing Institute of Technology, Beijing 100081, China
Parkinson Medical Center, Beijing Rehabilitation Hospital, Capital Medical University, Beijing 100144, China
Show Author Information

Abstract

Objective:

We investigated changes in cortico–subcortical spatiotemporal dynamics to explore the treatment mechanisms of transcranial alternating current stimulation (tACS) in patients with Parkinson’s disease (PD).

Methods:

Resting-state functional magnetic resonance imaging (rs-fMRI) data were collected from 20 patients with PD and 20 normal controls (NC). Each patient with PD received successive multidisciplinary intensive rehabilitation treatment and tACS treatment over a one-year interval. Individual functional brain network mapping and co-activation pattern (CAP) analysis were performed to characterize cortico–subcortical dynamics.

Results:

The same tACS electrode placement stimulated different proportions of functional brain networks across the participants. CAP analysis revealed that the visual network, attentional network, and default mode network co-activated with the thalamus, accumbens, and amygdala, respectively. The pattern characterized by the de-activation of the visual network and the activation of the thalamus showed a significantly low amplitude in the patients with PD than in NCs, and this amplitude increased after tACS treatment. Furthermore, the co-occurrence of cortico–subcortical CAPs was significantly higher in patients with PD than in NCs and decreased after tACS treatment.

Conclusions:

This study investigated cortico–subcortical spatiotemporal dynamics in patients with PD and further revealed the tACS treatment mechanism. These findings contribute to understanding cortico–subcortical dynamics and exploring noninvasive neuromodulation targets of cortico–subcortical circuits in brain diseases, such as PD, Alzheimer’s disease, and depression.

References

[1]
Kalia LV, Lang AE. Parkinson’s disease. Lancet 2015, 386(9996): 896–912.
[2]
Seppi K, Ray Chaudhuri K, Coelho M, et al. Update on treatments for nonmotor symptoms of Parkinson’s disease-an evidence-based medicine review. Mov Disord 2019, 34(2): 180–198.
[3]
Liu TT, Yan Y, Ai J, et al. Disrupted rich-club organization of brain structural networks in Parkinson’s disease. Brain Struct Funct 2021, 226(7): 2205–2217.
[4]
Oswal A, Cao CY, Yeh CH, et al. Neural signatures of hyperdirect pathway activity in Parkinson’s disease. Nat Commun 2021, 12(1): 5185.
[5]
Campbell MC, Koller JM, Snyder AZ, et al. CSF proteins and resting-state functional connectivity in Parkinson disease. Neurology 2015, 84(24): 2413–2421.
[6]
Litvak V, Jha A, Eusebio A, et al. Resting oscillatory cortico-subthalamic connectivity in patients with Parkinson’s disease. Brain 2011, 134(Pt 2): 359–374.
[7]
Deuschl G, Schade-Brittinger C, Krack P, et al. A randomized trial of deep-brain stimulation for Parkinson's disease. N Engl J Med 2006, 355(9): 896–908.
[8]
Fenoy AJ, Simpson RK Jr. Risks of common complications in deep brain stimulation surgery: management and avoidance. J Neurosurg 2014, 120(1): 132–139.
[9]
Ko JH, Spetsieris PG, Eidelberg D. Network structure and function in parkinson’s disease. Cereb Cortex 2018, 28(12): 4121–4135.
[10]
Gaynor LM, Kühn AA, Dileone M, et al. Suppression of beta oscillations in the subthalamic nucleus following cortical stimulation in humans. Eur J Neurosci 2008, 28(8): 1686–1695.
[11]
Liu AL, Vöröslakos M, Kronberg G, et al. Immediate neurophysiological effects of transcranial electrical stimulation. Nat Commun 2018, 9(1): 5092.
[12]
Dagan M, Herman T, Harrison R, et al. Multitarget transcranial direct current stimulation for freezing of gait in Parkinson’s disease. Mov Disord 2018, 33(4): 642–646.
[13]
Simpson MW, Mak M. The effect of transcranial direct current stimulation on upper limb motor performance in Parkinson’s disease: a systematic review. J Neurol 2020, 267(12): 3479–3488.
[14]
Doruk D, Gray Z, Bravo GL, et al. Effects of tDCS on executive function in Parkinson’s disease. Neurosci Lett 2014, 582: 27–31.
[15]
Huang H, Watts RL, Montgomery EB Jr. Effects of deep brain stimulation frequency on bradykinesia of Parkinson’s disease. Mov Disord 2014, 29(2): 203–206.
[16]
Krause MR, Vieira PG, Csorba BA, et al. Transcranial alternating current stimulation entrains single-neuron activity in the primate brain. Proc Natl Acad Sci USA 2019, 116(12): 5747–5755.
[17]
Johnson L, Alekseichuk I, Krieg J, et al. Dose-dependent effects of transcranial alternating current stimulation on spike timing in awake nonhuman Primates. Sci Adv 2020, 6(36): eaaz2747.
[18]
Brittain JS, Probert-Smith P, Aziz TZ, et al. Tremor suppression by rhythmic transcranial current stimulation. Curr Biol 2013, 23(5): 436–440.
[19]
Joundi RA, Jenkinson N, Brittain JS, et al. Driving oscillatory activity in the human cortex enhances motor performance. Curr Biol 2012, 22(5): 403–407.
[20]
Asamoah B, Khatoun A, Mc Laughlin M. tACS motor system effects can be caused by transcutaneous stimulation of peripheral nerves. Nat Commun 2019, 10: 266.
[21]
Ju H, Lee,. Transcranial alternating current stimulation rescues motor deficits in a mouse model of Parkinson’s disease via the production of glial cell line-derived neurotrophic factor. Brain Stimul 2022, 15(3): 645–653.
[22]
Guerra A, Colella D, Giangrosso M, et al. Driving motor cortex oscillations modulates bradykinesia in Parkinson’s disease. Brain 2022, 145(1): 224–236.
[23]
Del Felice A, Castiglia L, Formaggio E, et al. Personalized transcranial alternating current stimulation (tACS) and physical therapy to treat motor and cognitive symptoms in Parkinson’s disease: a randomized cross-over trial. Neuroimage Clin 2019, 22: 101768.
[24]
Shill HA, Obradov S, Katsnelson Y, et al. A randomized, double-blind trial of transcranial electrostimulation in early Parkinson’s disease. Mov Disord 2011, 26(8): 1477–1480.
[25]
Biswal BB, Mennes M, Zuo XN, et al. Toward discovery science of human brain function. Proc Natl Acad Sci USA 2010, 107(10): 4734–4739.
[26]
Helmich RC, Derikx LC, Bakker M, et al. Spatial remapping of cortico-striatal connectivity in parkinson’s disease. Cereb Cortex 2010, 20(5): 1175–1186.
[27]
Kucyi A, Hove MJ, Esterman M, et al. Dynamic brain network correlates of spontaneous fluctuations in attention. Cereb Cortex 2017, 27(3): 1831–1840.
[28]
Liu TT, Wang L, Suo DJ, et al. Resting-state functional MRI of healthy adults: temporal dynamic brain coactivation patterns. Radiology 2022, 304(3): 624–632.
[29]
Kim J, Criaud M, Cho SS, et al. Abnormal intrinsic brain functional network dynamics in Parkinson’s disease. Brain 2017, 140(11): 2955–2967.
[30]
Favaretto C, Allegra M, Deco G, et al. Subcortical-cortical dynamical states of the human brain and their breakdown in stroke. Nat Commun 2022, 13(1): 5069.
[31]
Li ML, Wang DH, Ren JX, et al. Performing group-level functional image analyses based on homologous functional regions mapped in individuals. PLoS Biol 2019, 17(3): e2007032.
[32]
Liu TT, Shi ZY, Zhang J, et al. Individual functional parcellation revealed compensation of dynamic limbic network organization in healthy ageing. Hum Brain Mapp 2023, 44(2): 744–761.
[33]
Li ML, Dahmani L, Hubbard CS, et al. Individualized functional connectome identified generalizable biomarkers for psychiatric symptoms in transdiagnostic patients. Neuropsychopharmacology 2023, 48(4): 633–641.
[34]
Lynch CJ, Elbau IG, Ng TH, et al. Automated optimization of TMS coil placement for personalized functional network engagement. Neuron 2022, 110(20): 3263–3277.e4.
[35]
Si QQ, Gan CT, Zhang H, et al. Altered dynamic functional network connectivity in levodopa-induced dyskinesia of Parkinson’s disease. CNS Neurosci Ther 2023, 29(1): 192–201.
[36]
Zhang CX, Deng J, Li Y, et al. Abnormal pulmonary function in early parkinson’s disease: a preliminary prospective observational study. Lung 2022, 200(3): 325–329.
[37]
Postuma RB, Berg D, Stern M, et al. MDS clinical diagnostic criteria for Parkinson's disease. Mov Disord 2015, 30(12): 1591–1599.
[38]
Hoehn MM, Yahr MD. Parkinsonism: onset, progression and mortality. Neurology 1967, 17(5): 427–442.
[39]
Goetz CG, Fahn S, Martinez-Martin P, et al. Movement Disorder Society-sponsored revision of the Unified Parkinson’s Disease Rating Scale (MDS-UPDRS): process, format, and clinimetric testing plan. Mov Disord 2007, 22(1): 41–47.
[40]
Podsiadlo D, Richardson S. The timed “Up & Go”: a test of basic functional mobility for frail elderly persons. J Am Geriatr Soc 1991, 39(2): 142–148.
[41]
Folstein MF, Folstein SE, McHugh PR. “Mini-mental state”. A practical method for grading cognitive state of patients for clinician. J Psychiatr Res 1975, 12(3): 189–198.
[42]
Nasreddine ZS, Phillips NA, Bédirian V, et al. The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc 2005, 53(4): 695–699.
[43]
Maier W, Buller R, Philipp M, et al. The Hamilton Anxiety Scale: reliability, validity and sensitivity to change in anxiety and depressive disorders. J Affect Disord 1988, 14(1): 61–68.
[44]
Hamilton M. A rating scale for depression. J Neurol Neurosurg Psychiatry 1960, 23(1): 56–62.
[45]
Chen KK, Jin ZH, Gao L, et al. Efficacy of short-term multidisciplinary intensive rehabilitation in patients with different Parkinson’s disease motor subtypes: a prospective pilot study with 3-month follow-up. Neural Regen Res 2021, 16(7): 1336–1343.
[46]
Power JD, Barnes KA, Snyder AZ, et al. Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. NeuroImage 2012, 59(3): 2142–2154.
[47]
Wang DH, Buckner RL, Fox MD, et al. Parcellating cortical functional networks in individuals. Nat Neurosci 2015, 18(12): 1853–1860.
[48]
Wagner TA, Zahn M, Grodzinsky AJ, et al. Three-dimensional head model Simulation of transcranial magnetic stimulation. IEEE Trans Biomed Eng 2004, 51(9): 1586–1598.
[49]
Liu X, Zhang NY, Chang CT, et al. Co-activation patterns in resting-state fMRI signals. NeuroImage 2018, 180(Pt B): 485–494.
[50]
Singleton SP, Luppi AI, Carhart-Harris RL, et al. Receptor-informed network control theory links LSD and psilocybin to a flattening of the brain’s control energy landscape. Nat Commun 2022, 13(1): 5812.
[51]
Hadoush H, Banihani SA, Khalil H, et al. Dopamine, BDNF and motor function postbilateral anodal transcranial direct current stimulation in Parkinson’s disease. Neurodegener Dis Manag 2018, 8(3): 171–179.
[52]
Hadoush H, Al-Jarrah M, Khalil H, et al. Bilateral anodal transcranial direct current stimulation effect on balance and fearing of fall in patient with Parkinson’s disease. NeuroRehabilitation 2018, 42(1): 63–68.
[53]
Helfrich RF, Schneider TR, Rach S, et al. Entrainment of brain oscillations by transcranial alternating current stimulation. Curr Biol 2014, 24(3): 333–339.
[54]
Soleimani G, Kupliki R, Bodurka J, et al. How structural and functional MRI can inform dual-site tACS parameters: a case study in a clinical population and its pragmatic implications. Brain Stimul 2022, 15(2): 337–351.
[55]
Herweg NA, Solomon EA, Kahana MJ. Theta oscillations in human memory. Trends Cogn Sci 2020, 24(3): 208–227.
[56]
Groenewegen HJ, Wright CI, Beijer AVJ. The nucleus accumbens: Gateway for limbic structures to reach the motor system? In: Holstege G, Bandler R, Saper CB, Eds. Emotional Motor System. Progress in Brain Research. 107. Amsterdam: Elsevier Science Bv, 1996, pp 485–511.
[57]
Pasman EP, McKeown MJ, Garg S, et al. Brain connectivity during simulated balance in older adults with and without Parkinson’s disease. Neuroimage Clin 2021, 30: 102676.
[58]
Sesack SR, Grace AA. Cortico-basal Ganglia reward network: microcircuitry. Neuropsychopharmacology 2010, 35(1): 27–47.
[59]
Tremblay C, Rahayel S, Vo A, et al. Brain atrophy progression in Parkinson’s disease is shaped by connectivity and local vulnerability. Brain Commun 2021, 3(4): fcab269.
[60]
He H, Liang L, Tang T, et al. Progressive brain changes in Parkinson’s disease: a meta-analysis of structural magnetic resonance imaging studies. Brain Res 2020, 1740: 146847.
[61]
Halassa MM, Kastner S. Thalamic functions in distributed cognitive control. Nat Neurosci 2017, 20(12): 1669–1679.
[62]
Behrens TE, Johansen-Berg H, Woolrich MW, et al. Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat Neurosci 2003, 6(7): 750–757.
[63]
Müller F, Niso G, Samiee S, et al. A thalamocortical pathway for fast rerouting of tactile information to occipital cortex in congenital blindness. Nat Commun 2019, 10(1): 5154.
[64]
Antón-Bolaños N, Espinosa A, López-Bendito G. Developmental interactions between thalamus and cortex: a true love reciprocal story. Curr Opin Neurobiol 2018, 52: 33–41.
[65]
Steiner L, Federspiel A, Slavova N, et al. Functional topography of the thalamo-cortical system during development and its relation to cognition. Neuroimage 2020, 223: 117361.
[66]
Setzer B, Fultz NE, Gomez DEP, et al. A temporal sequence of thalamic activity unfolds at transitions in behavioral arousal state. Nat Commun 2022, 13(1): 5442.
[67]
Kosciessa JQ, Lindenberger U, Garrett DD. Thalamocortical excitability modulation guides human perception under uncertainty. Nat Commun 2021, 12(1): 2430.
[68]
Born G, Schneider-Soupiadis FA, Erisken S, et al. Corticothalamic feedback sculpts visual spatial integration in mouse thalamus. Nat Neurosci 2021, 24(12): 1711–1720.
[69]
Lin JF, Zhang LJ, Guo RH, et al. The influence of visual deprivation on the development of the thalamocortical network: evidence from congenitally blind children and adults. Neuroimage 2022, 264: 119722.
[70]
Zou GY, Xu J, Zhou SQ, et al. Functional MRI of arousals in nonrapid eye movement sleep. Sleep 2020, 43(2): zsz218.
[71]
Salgado S, Kaplitt MG. The nucleus accumbens: a comprehensive review. Stereotact Funct Neurosurg 2015, 93(2): 75–93.
[72]
Bayassi-Jakowicka M, Lietzau G, Czuba E, et al. Neuroplasticity and multilevel system of connections determine the integrative role of nucleus accumbens in the brain reward system. Int J Mol Sci 2021, 22(18): 9806.
[73]
Richard JM, Castro DC, Difeliceantonio AG, et al. Mapping brain circuits of reward and motivation: in the footsteps of Ann Kelley. Neurosci Biobehav Rev 2013, 37(9 Pt A): 1919–1931.
[74]
Ikeda Y, Funayama T, Tateno A, et al. Bupropion increases activation in nucleus accumbens during anticipation of monetary reward. Psychopharmacology 2019, 236(12): 3655–3665.
[75]
Kinugawa K, Mano T, Yamatani Y, et al. Pain-related abnormal neuronal synchronization of the nucleus accumbens in parkinson’s disease. Brain Sci 2022, 12(1): 84.
[76]
Barbosa P, Hapuarachchi B, Djamshidian A, et al. Lower nucleus accumbens α-synuclein load and D3 receptor levels in Parkinson’s disease with impulsive compulsive behaviours. Brain 2019, 142(11): 3580–3591.
[77]
Carriere N, Besson P, Dujardin K, et al. Apathy in Parkinson’s disease is associated with nucleus accumbens atrophy: a magnetic resonance imaging shape analysis. Mov Disord 2014, 29(7): 897–903.
[78]
Martinez-Horta S, Sampedro F, Pagonabarraga J, et al. Non-demented Parkinson’s disease patients with apathy show decreased grey matter volume in key executive and reward-related nodes. Brain Imaging Behav 2017, 11(5): 1334–1342.
[79]
Wang EW, Du GW, Lewis MM, et al. Multimodal MRI evaluation of parkinsonian limbic pathologies. Neurobiol Aging 2019, 76: 194–200.
[80]
Hanganu A, Bedetti C, Degroot C, et al. Mild cognitive impairment is linked with faster rate of cortical thinning in patients with Parkinson’s disease longitudinally. Brain 2014, 137(Pt 4): 1120–1129.
[81]
Planche V, Munsch F, Pereira B, et al. Anatomical predictors of cognitive decline after subthalamic stimulation in Parkinson’s disease. Brain Struct Funct 2018, 223(7): 3063–3072.
[82]
Zhang H, Shan AD, Gan CT, et al. Impaired interhemispheric synchrony in Parkinson’s disease patients with apathy. J Affect Disord 2022, 318: 283–290.
[83]
Sun HB, Zou J, Sun ZY, et al. Numerical investigations on the resistance and longitudinal motion stability of a high-speed planing trimaran. J Mar Sci Eng 2020, 8: 830.
[84]
Chen LL, Wang JL, Xia MR, et al. Altered functional connectivity of nucleus accumbens subregions associates with non-motor symptoms in Parkinson’s disease. CNS Neurosci Ther 2022, 28(12): 2308–2318.
[85]
Baggio HC, Segura B, Garrido-Millan JL, et al. Resting-state frontostriatal functional connectivity in Parkinson’s disease-related apathy. Mov Disord 2015, 30(5): 671–679.
[86]
Hammes J, Theis H, Giehl K, et al. Dopamine metabolism of the nucleus accumbens and fronto-striatal connectivity modulate impulse control. Brain 2019, 142(3): 733–743.
[87]
Jia XQ, Wang ZJ, Yang T, et al. Entorhinal cortex atrophy in early, drug-naive parkinson’s disease with mild cognitive impairment. Aging Dis 2019, 10(6): 1221–1232.
[88]
Yoon EJ, Monchi O. Probable REM sleep behavior disorder is associated with longitudinal cortical thinning in Parkinson’s disease. NPJ Parkinsons Dis 2021, 7(1): 19.
[89]
van Mierlo TJ, Chung C, Foncke EM, et al. Depressive symptoms in Parkinson’s disease are related to decreased hippocampus and amygdala volume. Mov Disord 2015, 30(2): 245–252.
[90]
Zhang, Haobo. The relationship of anxious and depressive symptoms in Parkinson’s disease with voxel-based neuroanatomical and functional connectivity measures. J Affect Disord 2019, 245: 580–588.
Brain Science Advances
Pages 114-135
Cite this article:
Liu T, Yan Z, Han Z, et al. Cortico–subcortical spatiotemporal dynamics in Parkinson’s disease can be modulated by transcranial alternating current stimulation. Brain Science Advances, 2023, 9(2): 114-135. https://doi.org/10.26599/BSA.2023.9050009

662

Views

39

Downloads

3

Crossref

Altmetrics

Received: 11 January 2023
Revised: 06 March 2023
Accepted: 30 March 2023
Published: 05 June 2023
© The authors 2023.

This article is published with open access at journals.sagepub.com/home/BSA

Creative Commons Non Commercial CC BY-NC: This article is distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 License (http://www.creativecommons.org/licenses/by-nc/4.0/) which permits non-commercial use, reproduction and distribution of the work without further permission provided the original work is attributed as specified on the SAGE and Open Access pages (https://us.sagepub.com/en-us/nam/open-access-at-sage).

Return