Left lateral parietal rTMS improves cognition and modulates resting brain connectivity in patients with Alzheimer’s disease: Possible role of BDNF and oxidative stress

Velioğlu, Halil Aziz; Hanoğlu, Lütfü; Bayraktaroğlu, Zübeyir; Toprak, Guven; Güler, Eray Metin; Bektay, Muhammed Yunus; Mutlu-Burnaz, Ozlem; Yuluğ, Burak

doi:10.1016/j.nlm.2021.107410

Cited by 36 publications

(49 citation statements)

References 97 publications

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“…Our patients in the rTMS group scored significantly higher on the PVLT total score and its immediate recall subscale score. This is in line with findings that AD patients performed better on visual recognition memory after a 2-week 20 Hz rTMS treatment applied over the left lateral parietal cortex ( Velioglu et al, 2021 ). In healthy people, transcranial direct current stimulation applied over the parietal cortex improves verbal episodic memory during the retrieval phase ( Manenti et al, 2013 ).…”

Section: Discussionsupporting

confidence: 91%

“…The result that some cognition improvements were accomplished after a 2-week rTMS treatment could be supported by the finding that a 2-week rTMS treatment applied over the left lateral parietal cortex could improve cognition and modulate the functional connectivity of the brain network in AD patients ( Velioglu et al, 2021 ). AD patients’ cognition decline might be related to disrupted integration and segregation in their large-scale brain networks ( Dai and He, 2014 ), including the parietal memory network ( Hu et al, 2019 ), inferring that connectivity between different brain regions was abnormally disturbed and that rTMS might strengthen residual brain tissue connectivity.…”

Section: Discussionmentioning

confidence: 94%

“…In AD patients, the integrity of the parietal memory network including the inferior parietal lobule was disrupted ( Greene and Killiany, 2010 ; Hu et al, 2019 ). After a 2-week rTMS treatment (1,640 pulses, 20 Hz, 100 MT, one session per day and 5 days per week) applied over the left lateral parietal cortex, AD patients performed better on visual recognition memory and clock drawing test, indicating that high-frequency rTMS treatment could improve cognition and modulate functional connectivity of the brain network ( Velioglu et al, 2021 ). Evidence also showed that in prodromal AD patients, a 2-week 20 Hz rTMS treatment applied over the precuneus enhanced their episodic memory and neural activity ( Koch et al, 2018 ).…”

Section: Introductionmentioning

confidence: 99%

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Precision Repetitive Transcranial Magnetic Stimulation Over the Left Parietal Cortex Improves Memory in Alzheimer’s Disease: A Randomized, Double-Blind, Sham-Controlled Study

Jia

Yang

et al. 2021

Front. Aging Neurosci.

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ObjectiveWe aim to study the effect of precision repetitive transcranial magnetic stimulation (rTMS) over the left parietal cortex on the memory and cognitive function in Alzheimer’s disease (AD).MethodsBased on the resting-state functional magnetic resonance imaging, the left parietal cortex site with the highest functional connectivity to the hippocampus was selected as the target of rTMS treatment. Sixty-nine AD patients were randomized to either rTMS or sham treatment (five sessions/week for a total of 10 sessions). The Mini-Mental State Examination (MMSE), 12-Word Philadelphia Verbal Learning Test (PVLT), and Clinical Dementia Rating (CDR) were assessed at baseline and after the last session.ResultsAfter a 2-week treatment, compared to patients in the sham group, those in the rTMS group scored significantly higher on PVLT total score and its immediate recall subscale score. Moreover, in the rTMS group, there were significant improvements after the 2-week treatment, which were manifested in MMSE total score and its time orientation and recall subscale scores, as well as PVLT total score and its immediate recall and short delay recall subscale scores. In the sham group, the PVLT total score was significantly improved.ConclusionThe target site of the left parietal cortex can improve AD patients’ cognitive function, especially memory, providing a potential therapy.

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Section: Discussionsupporting

confidence: 91%

Section: Discussionmentioning

confidence: 94%

Section: Introductionmentioning

confidence: 99%

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Precision Repetitive Transcranial Magnetic Stimulation Over the Left Parietal Cortex Improves Memory in Alzheimer’s Disease: A Randomized, Double-Blind, Sham-Controlled Study

Jia

Yang

et al. 2021

Front. Aging Neurosci.

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“…Although results from healthy young and old adults demonstrate the potential for rTMS to improve memory abilities, similar findings have not been reported yet for AD and (a)MCI. Although new clinical trials are proceeding at the time of this writing [94], only one recent study was identified applying rTMS to AG in individuals with mild to severe AD [56]. Velioglu and colleagues administered ten sessions of 20 Hz rTMS at 100% MT to left angular gyrus [56].…”

Section: Rtms Of Ag: MCI and Admentioning

confidence: 99%

“…Although new clinical trials are proceeding at the time of this writing [94], only one recent study was identified applying rTMS to AG in individuals with mild to severe AD [56]. Velioglu and colleagues administered ten sessions of 20 Hz rTMS at 100% MT to left angular gyrus [56]. Visual recognition memory performance and the clock drawing test improved after stimulation, but there were no other cognitive benefits reported.…”

Section: Rtms Of Ag: MCI and Admentioning

confidence: 99%

Stimulating Memory: Reviewing Interventions Using Repetitive Transcranial Magnetic Stimulation to Enhance or Restore Memory Abilities

2021

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Human memory systems are imperfect recording devices that are affected by age and disease, but recent findings suggest that the performance of these systems may be modifiable through interventions using non-invasive brain stimulation such as repetitive transcranial magnetic stimulation (rTMS). The translational potential of these rTMS interventions is clear: memory problems are the most common cognitive complaint associated with healthy aging, while pathological conditions such as Alzheimer’s disease are often associated with severe deficits in memory. Therapies to improve memory or treat memory loss could enhance independence while reducing costs for public health systems. Despite this promise, several important factors limit the generalizability and translational potential of rTMS interventions for memory. Heterogeneity of protocol design, rTMS parameters, and outcome measures present significant challenges to interpretation and reproducibility. However, recent advances in cognitive neuroscience, including rTMS approaches in addition to a new understanding of functional brain networks and related insights, may offer methodological tools necessary to design new interventional studies with enhanced experimental rigor, improved reproducibility, and greater likelihood of successful translation to clinical settings. In this review, we first discuss the current state of the literature on memory modulation with rTMS, then offer a commentary on developments in cognitive neuroscience that are relevant to rTMS interventions, and finally close by offering several recommendations for the design of future investigations using rTMS to modulate human memory performance.

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Effectiveness of Personalized Hippocampal Network–Targeted Stimulation in Alzheimer Disease

Jung,

Jang,

Park

et al. 2024

JAMA Netw Open

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ImportanceRepetitive transcranial magnetic stimulation (rTMS) has emerged as a safe and promising intervention for Alzheimer disease (AD).ObjectiveTo investigate the effect of a 4-week personalized hippocampal network–targeted rTMS on cognitive and functional performance, as well as functional connectivity in AD.Design, Setting, and ParticipantsThis randomized clinical trial, which was sham-controlled and masked to participants and evaluators, was conducted between May 2020 and April 2022 at a single Korean memory clinic. Eligible participants were between ages 55 and 90 years and had confirmed early AD with evidence of an amyloid biomarker. Participants who met the inclusion criteria were randomly assigned to receive hippocampal network–targeted rTMS or sham stimulation. Participants received 4-week rTMS treatment, with assessment conducted at weeks 4 and 8. Data were analyzed between April 2022 and January 2024.InterventionsEach patient received 20 sessions of personalized rTMS targeting the left parietal area, functionally connected to the hippocampus, based on fMRI connectivity analysis over 4 weeks. The sham group underwent the same procedure, excluding actual magnetic stimulation. A personalized 3-dimensional printed frame to fix the TMS coil to the optimal target site was produced.Main Outcomes and MeasuresThe primary outcome was the change in the AD Assessment Scale-Cognitive Subscale test (ADAS-Cog) after 8 weeks from baseline. Secondary outcomes included changes in the Clinical Dementia Rating-Sum of Boxes (CDR-SOB) and Seoul-Instrumental Activity Daily Living (S-IADL) scales, as well as resting-state fMRI connectivity between the hippocampus and cortical areas.ResultsAmong 30 participants (18 in the rTMS group; 12 in the sham group) who completed the 8-week trial, the mean (SD) age was 69.8 (9.1) years; 18 (60%) were female. As the primary outcome, the change in ADAS-Cog at the eighth week was significantly different between the rTMS and sham groups (coefficient [SE], −5.2 [1.6]; P = .002). The change in CDR-SOB (−4.5 [1.4]; P = .007) and S-IADL (1.7 [0.7]; P = .004) were significantly different between the groups favoring rTMS groups. The fMRI connectivity analysis revealed that rTMS increased the functional connectivity between the hippocampus and precuneus, with its changes associated with improvements in ADAS-Cog (r = −0.57; P = .005).Conclusions and RelevanceThis randomized clinical trial demonstrated the positive effects of rTMS on cognitive and functional performance, and the plastic changes in the hippocampal-cortical network. Our results support the consideration of rTMS as a potential treatment for AD.Trial RegistrationClinicalTrials.gov Identifier: NCT04260724

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Left lateral parietal rTMS improves cognition and modulates resting brain connectivity in patients with Alzheimer’s disease: Possible role of BDNF and oxidative stress

Cited by 36 publications

References 97 publications

Precision Repetitive Transcranial Magnetic Stimulation Over the Left Parietal Cortex Improves Memory in Alzheimer’s Disease: A Randomized, Double-Blind, Sham-Controlled Study

Precision Repetitive Transcranial Magnetic Stimulation Over the Left Parietal Cortex Improves Memory in Alzheimer’s Disease: A Randomized, Double-Blind, Sham-Controlled Study

Stimulating Memory: Reviewing Interventions Using Repetitive Transcranial Magnetic Stimulation to Enhance or Restore Memory Abilities

Effectiveness of Personalized Hippocampal Network–Targeted Stimulation in Alzheimer Disease

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