Neuro-Navigated RTMS Improves Sleep and Cognitive Impairment Via Regulating Sleep-Related Networks' Spontaneous Activity in AD Spectrum Patients

Overview

Journal Clin Interv Aging

Publisher Dove Medical Press

Specialty Geriatrics

Date 2023 Aug 21

PMID 37601952

Authors

Shengqi You

Tingyu Lv

Ruomeng Qin

Zheqi Hu

Zhihong Ke

Weina Yao

Hui Zhao

Feng Bai

Affiliations

Soon will be listed here.

Abstract

Study Objectives: By examining spontaneous activity changes of sleep-related networks in patients with the Alzheimer's disease (AD) spectrum with or without insomnia disorder (ID) over time via neuro-navigated repetitive transcranial magnetic stimulation (rTMS), we revealed the effect and mechanism of rTMS targeting the left-angular gyrus in improving the comorbidity symptoms of the AD spectrum with ID.

Methods: A total of 34 AD spectrum patients were recruited in this study, including 18 patients with ID and the remaining 16 patients without ID. All of them were measured for cognitive function and sleep by using the cognitive and sleep subscales of the neuropsychiatric inventory. The amplitude of low-frequency fluctuation changes in sleep-related networks was revealed before and after neuro-navigated rTMS treatment between these two groups, and the behavioral significance was further explored.

Results: Affective auditory processing and sensory-motor collaborative sleep-related networks with hypo-spontaneous activity were observed at baseline in the AD spectrum with ID group, while substantial increases in activity were evident at follow-up in these subjects. In addition, longitudinal affective auditory processing, sensory-motor and default mode collaborative sleep-related networks with hyper-spontaneous activity were also revealed at follow-up in the AD spectrum with ID group. In particular, longitudinal changes in sleep-related networks were associated with improvements in sleep quality and episodic memory scores in AD spectrum with ID patients.

Conclusion: We speculated that left angular gyrus-navigated rTMS therapy may enhance the memory function of AD spectrum patients by regulating the spontaneous activity of sleep-related networks, and it was associated with memory consolidation in the hippocampus-cortical circuit during sleep.

Clinical Trial Registration: The study was registered at the Chinese Clinical Trial Registry, registration ID: ChiCTR2100050496, China.

References

Si X, Zhou W, Hong B . Cooperative cortical network for categorical processing of Chinese lexical tone. Proc Natl Acad Sci U S A. 2017; 114(46):12303-12308. PMC: 5699060. DOI: 10.1073/pnas.1710752114. View

Katzman R, Zhang M, Wang Z, Liu W, Yu E, Wong S . A Chinese version of the Mini-Mental State Examination; impact of illiteracy in a Shanghai dementia survey. J Clin Epidemiol. 1988; 41(10):971-8. DOI: 10.1016/0895-4356(88)90034-0. View

Fernandez-Mendoza J, Vela-Bueno A, Vgontzas A, Jose Ramos-Platon M, Olavarrieta-Bernardino S, Bixler E . Cognitive-emotional hyperarousal as a premorbid characteristic of individuals vulnerable to insomnia. Psychosom Med. 2010; 72(4):397-403. DOI: 10.1097/PSY.0b013e3181d75319. View

Trost W, Fruhholz S, Cochrane T, Cojan Y, Vuilleumier P . Temporal dynamics of musical emotions examined through intersubject synchrony of brain activity. Soc Cogn Affect Neurosci. 2015; 10(12):1705-21. PMC: 4666110. DOI: 10.1093/scan/nsv060. View

Pannese A, Grandjean D, Fruhholz S . Amygdala and auditory cortex exhibit distinct sensitivity to relevant acoustic features of auditory emotions. Cortex. 2016; 85:116-125. DOI: 10.1016/j.cortex.2016.10.013. View

Yeo B, Krienen F, Sepulcre J, Sabuncu M, Lashkari D, Hollinshead M . The organization of the human cerebral cortex estimated by intrinsic functional connectivity. J Neurophysiol. 2011; 106(3):1125-65. PMC: 3174820. DOI: 10.1152/jn.00338.2011. View

Bliwise D . Sleep in normal aging and dementia. Sleep. 1993; 16(1):40-81. DOI: 10.1093/sleep/16.1.40. View

Yang Z, Sheng X, Qin R, Chen H, Shao P, Xu H . Cognitive Improvement via Left Angular Gyrus-Navigated Repetitive Transcranial Magnetic Stimulation Inducing the Neuroplasticity of Thalamic System in Amnesic Mild Cognitive Impairment Patients. J Alzheimers Dis. 2022; 86(2):537-551. DOI: 10.3233/JAD-215390. View

Lin Y, Jiang W, Shan P, Lu M, Wang T, Li R . The role of repetitive transcranial magnetic stimulation (rTMS) in the treatment of cognitive impairment in patients with Alzheimer's disease: A systematic review and meta-analysis. J Neurol Sci. 2019; 398:184-191. DOI: 10.1016/j.jns.2019.01.038. View

10.

Jessen F, Amariglio R, van Boxtel M, Breteler M, Ceccaldi M, Chetelat G . A conceptual framework for research on subjective cognitive decline in preclinical Alzheimer's disease. Alzheimers Dement. 2014; 10(6):844-52. PMC: 4317324. DOI: 10.1016/j.jalz.2014.01.001. View

11.

Irwin M, Vitiello M . Implications of sleep disturbance and inflammation for Alzheimer's disease dementia. Lancet Neurol. 2019; 18(3):296-306. DOI: 10.1016/S1474-4422(18)30450-2. View

12.

Fransson P . Spontaneous low-frequency BOLD signal fluctuations: an fMRI investigation of the resting-state default mode of brain function hypothesis. Hum Brain Mapp. 2005; 26(1):15-29. PMC: 6871700. DOI: 10.1002/hbm.20113. View

13.

Guo Z, Jiang Z, Jiang B, McClure M, Mu Q . High-Frequency Repetitive Transcranial Magnetic Stimulation Could Improve Impaired Working Memory Induced by Sleep Deprivation. Neural Plast. 2020; 2019:7030286. PMC: 6930796. DOI: 10.1155/2019/7030286. View

14.

Xu J, Dong H, Li N, Wang Z, Guo F, Wei J . Weighted RSA: An Improved Framework on the Perception of Audio-visual Affective Speech in Left Insula and Superior Temporal Gyrus. Neuroscience. 2021; 469:46-58. DOI: 10.1016/j.neuroscience.2021.06.002. View

15.

Joe E, Ringman J . Cognitive symptoms of Alzheimer's disease: clinical management and prevention. BMJ. 2019; 367:l6217. DOI: 10.1136/bmj.l6217. View

16.

Albert M, DeKosky S, Dickson D, Dubois B, Feldman H, Fox N . The diagnosis of mild cognitive impairment due to Alzheimer's disease: recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimers Dement. 2011; 7(3):270-9. PMC: 3312027. DOI: 10.1016/j.jalz.2011.03.008. View

17.

Lauriola M, Esposito R, Delli Pizzi S, de Zambotti M, Londrillo F, Kramer J . Sleep changes without medial temporal lobe or brain cortical changes in community-dwelling individuals with subjective cognitive decline. Alzheimers Dement. 2016; 13(7):783-791. PMC: 5749240. DOI: 10.1016/j.jalz.2016.11.006. View

18.

Fogel S, Ray L, Fang Z, Silverbrook M, Naci L, Owen A . While you were sleeping: Evidence for high-level executive processing of an auditory narrative during sleep. Conscious Cogn. 2022; 100:103306. DOI: 10.1016/j.concog.2022.103306. View

19.

Tahmasian M, Noori K, Samea F, Zarei M, Spiegelhalder K, Eickhoff S . A lack of consistent brain alterations in insomnia disorder: An activation likelihood estimation meta-analysis. Sleep Med Rev. 2018; 42:111-118. PMC: 7965842. DOI: 10.1016/j.smrv.2018.07.004. View

20.

Fasiello E, Gorgoni M, Scarpelli S, Alfonsi V, Strambi L, De Gennaro L . Functional connectivity changes in insomnia disorder: A systematic review. Sleep Med Rev. 2021; 61:101569. DOI: 10.1016/j.smrv.2021.101569. View