Deep brain stimulation for Alzheimer’s disease – current status and next steps

References

• Hebert LE, Weuve J, Scherr PA, et al. Alzheimer disease in the United States (2010-2050) estimated using the 2010 census. Neurology. 2013;80(19):1778–1783. doi: 10.1212/WNL.0b013e31828726f5
   PubMed Web of Science ®Google Scholar
• Querfurth HW, LaFerla FM. Alzheimer’s disease. N Engl J Med. 2010;362(4):329–344. doi: 10.1056/NEJMra0909142
   PubMed Web of Science ®Google Scholar
• Selkoe DJ, Hardy J. The amyloid hypothesis of Alzheimer’s disease at 25 years. EMBO Mol Med. 2016;8(6):595–608. doi: 10.15252/emmm.201606210
   PubMed Web of Science ®Google Scholar
• Rajah Kumaran K, Yunusa S, Perimal E, et al. Insights into the pathophysiology of Alzheimer’s disease and potential therapeutic targets: a Current perspective. J Alzheimers Dis. 2023;91(2):507–530. doi: 10.3233/JAD-220666
   PubMed Web of Science ®Google Scholar
• Busche MA, Hyman BT. Synergy between amyloid-beta and tau in Alzheimer’s disease. Nat Neurosci. 2020;23(10):1183–1193. doi: 10.1038/s41593-020-0687-6
   PubMed Web of Science ®Google Scholar
• Jack CR Jr., Knopman DS, Jagust WJ, et al. Tracking pathophysiological processes in Alzheimer’s disease: an updated hypothetical model of dynamic biomarkers. Lancet Neurol. 2013;12(2):207–216. doi: 10.1016/S1474-4422(12)70291-0
   PubMed Web of Science ®Google Scholar
• Birks J. Cholinesterase inhibitors for Alzheimer’s disease. Cochrane Database Syst Rev. 2006;2016(3):CD005593. doi: 10.1002/14651858.CD005593
   Google Scholar
• McShane R, Areosa Sastre A, Minakaran N. Memantine for dementia. Cochrane Database Syst Rev. 2006;2:CD003154. doi: 10.1002/14651858.CD003154.pub5
   PubMedGoogle Scholar
• Palop JJ, Mucke L. Network abnormalities and interneuron dysfunction in Alzheimer disease. Nat Rev Neurosci. 2016;17(12):777–792. doi: 10.1038/nrn.2016.141
   PubMed Web of Science ®Google Scholar
• Bloudek LM, Spackman DE, Blankenburg M, et al. Review and meta-analysis of biomarkers and diagnostic imaging in Alzheimer’s disease. J Alzheimers Dis. 2011;26(4):627–645. doi: 10.3233/JAD-2011-110458
   PubMed Web of Science ®Google Scholar
• Contreras JA, Avena-Koenigsberger A, Risacher SL, et al. Resting state network modularity along the prodromal late onset Alzheimer’s disease continuum. NeuroImage Clin. 2019;22:101687. doi: 10.1016/j.nicl.2019.101687
   PubMed Web of Science ®Google Scholar
• Vogel JW, Corriveau-Lecavalier N, Franzmeier N, et al. Connectome-based modelling of neurodegenerative diseases: towards precision medicine and mechanistic insight. Nat Rev Neurosci. 2023;24(10):620–639. doi: 10.1038/s41583-023-00731-8
   PubMed Web of Science ®Google Scholar
• Bero AW, Yan P, Roh JH, et al. Neuronal activity regulates the regional vulnerability to amyloid-beta deposition. Nat Neurosci. 2011;14(6):750–756. doi: 10.1038/nn.2801
   PubMed Web of Science ®Google Scholar
• Busche MA, Chen X, Henning HA, et al. Critical role of soluble amyloid-beta for early hippocampal hyperactivity in a mouse model of Alzheimer’s disease. Proc Natl Acad Sci USA. 2012;109(22):8740–8745. doi: 10.1073/pnas.1206171109
   PubMed Web of Science ®Google Scholar
• Busche MA, Wegmann S, Dujardin S, et al. Tau impairs neural circuits, dominating amyloid-beta effects, in Alzheimer models in vivo. Nat Neurosci. 2019;22(1):57–64. doi: 10.1038/s41593-018-0289-8
   PubMed Web of Science ®Google Scholar
• Wu JW, Hussaini SA, Bastille IM, et al. Neuronal activity enhances tau propagation and tau pathology in vivo. Nat Neurosci. 2016;19(8):1085–1092. doi: 10.1038/nn.4328
   PubMed Web of Science ®Google Scholar
• Senova S, Fomenko A, Gondard E, et al. Anatomy and function of the fornix in the context of its potential as a therapeutic target. J Neurol Neurosurg Psychiatry. 2020;91(5):547–559. doi: 10.1136/jnnp-2019-322375
   PubMed Web of Science ®Google Scholar
• Mevel K, Chetelat G, Eustache F, et al. The default mode network in healthy aging and Alzheimer’s disease. Int J Alzheimers Dis. 2011;2011:535816. doi: 10.4061/2011/535816
   PubMedGoogle Scholar
• Rios AS, Oxenford S, Neudorfer C, et al. Optimal deep brain stimulation sites and networks for stimulation of the fornix in Alzheimer’s disease. Nat Commun. 2022;13(1):7707. doi: 10.1038/s41467-022-34510-3
   PubMed Web of Science ®Google Scholar
• Lozano AM, Lipsman N. Probing and regulating dysfunctional circuits using deep brain stimulation. Neuron. 2013;77(3):406–424. doi: 10.1016/j.neuron.2013.01.020
   PubMed Web of Science ®Google Scholar
• Gazes Y, Li P, Sun E, et al. Age specificity in fornix-to-hippocampus association. Brain Imaging Behav. 2019;13(5):1444–1452. doi: 10.1007/s11682-018-9958-1
   PubMed Web of Science ®Google Scholar
• Antonenko D, Kulzow N, Cesarz ME, et al. Hippocampal pathway plasticity is associated with the ability to form novel memories in older adults. Front Aging Neurosci. 2016;8:61. doi: 10.3389/fnagi.2016.00061
   PubMed Web of Science ®Google Scholar
• Stratmann K, Heinsen H, Korf HW, et al. Precortical phase of Alzheimer’s disease (AD)-related tau cytoskeletal pathology. Brain Pathol. 2016;26(3):371–386. doi: 10.1111/bpa.12289
   PubMed Web of Science ®Google Scholar
• Thierry M, Boluda S, Delatour B, et al. Human subiculo-fornico-mamillary system in Alzheimer’s disease: tau seeding by the pillar of the fornix. Acta Neuropathol. 2020;139(3):443–461. doi: 10.1007/s00401-019-02108-7
   PubMed Web of Science ®Google Scholar
• Fletcher E, Raman M, Huebner P, et al. Loss of fornix white matter volume as a predictor of cognitive impairment in cognitively normal elderly individuals. JAMA Neurol. 2013;70(11):1389–1395. doi: 10.1001/jamaneurol.2013.3263
   PubMed Web of Science ®Google Scholar
• Bartus RT, Dean RL 3rd, Beer B, et al. The cholinergic hypothesis of geriatric memory dysfunction. Science. 1982;217(4558):408–414. doi: 10.1126/science.7046051
   PubMed Web of Science ®Google Scholar
• Carlsen J, Zaborszky L, Heimer L. Cholinergic projections from the basal forebrain to the basolateral amygdaloid complex: a combined retrograde fluorescent and immunohistochemical study. J Comp Neurol. 1985;234(2):155–167. doi: 10.1002/cne.902340203
   PubMed Web of Science ®Google Scholar
• Sillito AM, Kemp JA. Cholinergic modulation of the functional organization of the cat visual cortex. Brain Res. 1983;289(1–2):143–155. doi: 10.1016/0006-8993(83)90015-X
   PubMed Web of Science ®Google Scholar
• Hardenacke K, Kuhn J, Lenartz D, et al. Stimulate or degenerate: deep brain stimulation of the nucleus basalis meynert in Alzheimer dementia. World Neurosurg. 2013;80(3–4):S27 e35–43. doi: 10.1016/j.wneu.2012.12.005
   PubMed Web of Science ®Google Scholar
• McCormick DA. Actions of acetylcholine in the cerebral cortex and thalamus and implications for function. Prog Brain Res. 1993;98:303–308.
   PubMed Web of Science ®Google Scholar
• Sassin I, Schultz C, Thal DR, et al. Evolution of Alzheimer’s disease-related cytoskeletal changes in the basal nucleus of meynert. Acta Neuropathol. 2000;100(3):259–269. doi: 10.1007/s004019900178
   PubMed Web of Science ®Google Scholar
• Iraizoz I, Guijarro JL, Gonzalo LM, et al. Neuropathological changes in the nucleus basalis correlate with clinical measures of dementia. Acta Neuropathol. 1999;98(2):186–196. doi: 10.1007/s004010051068
   PubMed Web of Science ®Google Scholar
• Ovsepian SV, Herms J. Cholinergic neurons-keeping check on amyloid beta in the cerebral cortex. Front Cell Neurosci. 2013;7:252. doi: 10.3389/fncel.2013.00252
   PubMedGoogle Scholar
• Bierer LM, Haroutunian V, Gabriel S, et al. Neurochemical correlates of dementia severity in Alzheimer’s disease: relative importance of the cholinergic deficits. J Neurochem. 1995;64(2):749–760. doi: 10.1046/j.1471-4159.1995.64020749.x
   PubMed Web of Science ®Google Scholar
• Menardi A, Rossi S, Koch G, et al. Toward noninvasive brain stimulation 2.0 in Alzheimer’s disease. Ageing Res Rev. 2022;75:101555. doi: 10.1016/j.arr.2021.101555
   PubMed Web of Science ®Google Scholar
• Koch G, Casula EP, Bonni S, et al. Precuneus magnetic stimulation for Alzheimer’s disease: a randomized, sham-controlled trial. Brain. 2022;145(11):3776–3786. doi: 10.1093/brain/awac285
   PubMed Web of Science ®Google Scholar
• Benussi A, Cantoni V, Cotelli MS, et al. Exposure to gamma tACS in Alzheimer’s disease: a randomized, double-blind, sham-controlled, crossover, pilot study. Brain Stimul. 2021;14(3):531–540. doi: 10.1016/j.brs.2021.03.007
   PubMed Web of Science ®Google Scholar
• Hamani C, McAndrews MP, Cohn M, et al. Memory enhancement induced by hypothalamic/fornix deep brain stimulation. Ann Neurol. 2008;63(1):119–123. doi: 10.1002/ana.21295
   PubMed Web of Science ®Google Scholar
• Hariz M, Lees AJ, Blomstedt Y, et al. Serendipity and observations in functional neurosurgery: from James Parkinson’s stroke to Hamani’s & Lozano’s flashbacks. Stereotact Funct Neurosurg. 2022;100(4):201–209. doi: 10.1159/000525794
   PubMed Web of Science ®Google Scholar
• Luo Y, Sun Y, Tian X, et al. Deep brain stimulation for Alzheimer’s disease: stimulation parameters and potential mechanisms of action. Front Aging Neurosci. 2021;13:619543. doi: 10.3389/fnagi.2021.619543
   PubMed Web of Science ®Google Scholar
• Laxton AW, Tang-Wai DF, MP M, et al. A phase I trial of deep brain stimulation of memory circuits in Alzheimer’s disease. Ann Neurol. 2010;68(4):521–534. doi: 10.1002/ana.22089
   PubMed Web of Science ®Google Scholar
• Mayeux R, Sano M, Wood AJJ. Treatment of Alzheimer’s disease. N Engl J Med. 1999;341(22):1670–1679. doi: 10.1056/NEJM199911253412207
   PubMed Web of Science ®Google Scholar
• Smith GS, Laxton AW, Tang-Wai DF, et al. Increased cerebral metabolism after 1 year of deep brain stimulation in Alzheimer disease. Arch Neurol. 2012;69(9):1141–1148. doi: 10.1001/archneurol.2012.590
   PubMed Web of Science ®Google Scholar
• Sankar T, Chakravarty MM, Bescos A, et al. Deep brain stimulation influences brain structure in Alzheimer’s disease. Brain Stimul. 2015;8(3):645–654. doi: 10.1016/j.brs.2014.11.020
   PubMed Web of Science ®Google Scholar
• Stone SS, Teixeira CM, Devito LM, et al. Stimulation of entorhinal cortex promotes adult neurogenesis and facilitates spatial memory. J Neurosci. 2011;31(38):13469–13484. doi: 10.1523/JNEUROSCI.3100-11.2011
   PubMed Web of Science ®Google Scholar
• Lozano AM, Fosdick L, Chakravarty MM, et al. A phase II study of fornix deep brain stimulation in mild Alzheimer’s disease. J Alzheimers Dis. 2016;54(2):777–787. doi: 10.3233/JAD-160017
   PubMed Web of Science ®Google Scholar
• Schneider LS, Kennedy RE, Wang G, et al. Differences in Alzheimer disease clinical trial outcomes based on age of the participants. Neurology. 2015;84(11):1121–1127. doi: 10.1212/WNL.0000000000001376
   PubMed Web of Science ®Google Scholar
• Ponce FA, Asaad WF, Foote KD, et al. Bilateral deep brain stimulation of the fornix for Alzheimer’s disease: surgical safety in the ADvance trial. J Neurosurg. 2016;125(1):75–84. doi: 10.3171/2015.6.JNS15716
   PubMed Web of Science ®Google Scholar
• Germann J, Elias GJB, Boutet A, et al. Brain structures and networks responsible for stimulation-induced memory flashbacks during forniceal deep brain stimulation for Alzheimer’s disease. Alzheimers Dement. 2021;17(5):777–787. doi: 10.1002/alz.12238
   PubMed Web of Science ®Google Scholar
• Deeb W, Salvato B, Almeida L, et al. Fornix-region deep brain stimulation-induced memory flashbacks in Alzheimer’s disease. N Engl J Med. 2019;381(8):783–785. doi: 10.1056/NEJMc1905240
   PubMed Web of Science ®Google Scholar
• Lv Q, Du A, Wei W, et al. Deep brain stimulation: a potential treatment for dementia in Alzheimer’s disease (AD) and Parkinson’s disease dementia (PDD). Front Neurosci. 2018;12:360. doi: 10.3389/fnins.2018.00360
   PubMed Web of Science ®Google Scholar
• You Z, Wu YY, Wu R, et al. Efforts of subthalamic nucleus deep brain stimulation on cognitive spectrum: from explicit to implicit changes in the patients with Parkinson’s disease for 1 year. CNS Neurosci Ther. 2020;26(9):972–980. doi: 10.1111/cns.13392
   PubMed Web of Science ®Google Scholar
• Leplus A, Lauritzen I, Melon C, et al. Chronic fornix deep brain stimulation in a transgenic Alzheimer’s rat model reduces amyloid burden, inflammation, and neuronal loss. Brain Struct Funct. 2019;224(1):363–372. doi: 10.1007/s00429-018-1779-x
   PubMed Web of Science ®Google Scholar
• Koubeissi MZ, Kahriman E, Syed TU, et al. Low-frequency electrical stimulation of a fiber tract in temporal lobe epilepsy. Ann Neurol. 2013;74(2):223–231. doi: 10.1002/ana.23915
   PubMed Web of Science ®Google Scholar
• Stypulkowski PH, Stanslaski SR, Giftakis JE. Modulation of hippocampal activity with fornix deep brain stimulation. Brain Stimul. 2017;10(6):1125–1132. doi: 10.1016/j.brs.2017.09.002
   PubMed Web of Science ®Google Scholar
• Hescham S, Lim LW, Jahanshahi A, et al. Deep brain stimulation of the forniceal area enhances memory functions in experimental dementia: the role of stimulation parameters. Brain Stimul. 2013;6(1):72–77. doi: 10.1016/j.brs.2012.01.008
   PubMed Web of Science ®Google Scholar
• Iaccarino HF, Singer AC, Martorell AJ, et al. Gamma frequency entrainment attenuates amyloid load and modifies microglia. Nature. 2016;540(7632):230–235. doi: 10.1038/nature20587
   PubMed Web of Science ®Google Scholar
• Soula M, Martin-Avila A, Zhang Y, et al. Forty-hertz light stimulation does not entrain native gamma oscillations in Alzheimer’s disease model mice. Nat Neurosci. 2023;26(4):570–578. doi: 10.1038/s41593-023-01270-2
   PubMed Web of Science ®Google Scholar
• Benear SL, Ngo CT, Olson IR. Dissecting the fornix in basic memory processes and neuropsychiatric disease: a review. Brain Connect. 2020;10(7):331–354. doi: 10.1089/brain.2020.0749
   PubMed Web of Science ®Google Scholar
• Benabid AL, Pollak P, Louveau A, et al. Combined (thalamotomy and stimulation) stereotactic surgery of the VIM thalamic nucleus for bilateral Parkinson disease. Appl Neurophysiol. 1987;50(1–6):344–346. doi: 10.1159/000100803
   PubMedGoogle Scholar
• Turnbull IM, McGeer PL, Beattie L, et al. Stimulation of the basal nucleus of Meynert in senile dementia of Alzheimer’s type. A preliminary report. Appl Neurophysiol. 1985;48(1–6):216–221. doi: 10.1159/000101130
   PubMedGoogle Scholar
• Freund HJ, Kuhn J, Lenartz D, et al. Cognitive functions in a patient with Parkinson-dementia syndrome undergoing deep brain stimulation. Arch Neurol. 2009;66(6):781–785. doi: 10.1001/archneurol.2009.102
   PubMed Web of Science ®Google Scholar
• Buzsaki G, Bickford RG, Ponomareff G, et al. Nucleus basalis and thalamic control of neocortical activity in the freely moving rat. J Neurosci. 1988;8(11):4007–4026. doi: 10.1523/JNEUROSCI.08-11-04007.1988
   PubMed Web of Science ®Google Scholar
• Kuhn J, Hardenacke K, Lenartz D, et al. Deep brain stimulation of the nucleus basalis of meynert in Alzheimer’s dementia. Mol Psychiatry. 2015;20(3):353–360. doi: 10.1038/mp.2014.32
   PubMed Web of Science ®Google Scholar
• Kuhn J, Hardenacke K, Shubina E, et al. Deep brain stimulation of the nucleus basalis of meynert in early stage of Alzheimer’s dementia. Brain Stimul. 2015;8(4):838–839. doi: 10.1016/j.brs.2015.04.002
   PubMed Web of Science ®Google Scholar
• Qi XL, Liu R, Singh B, et al. Nucleus basalis stimulation enhances working memory by stabilizing stimulus representations in primate prefrontal cortical activity. Cell Rep. 2021;36(5):109469. doi: 10.1016/j.celrep.2021.109469
   PubMed Web of Science ®Google Scholar
• Liu R, Crawford J, Callahan PM, et al. Intermittent stimulation in the nucleus basalis of meynert improves sustained attention in rhesus monkeys. Neuropharmacology. 2018;137:202–210. doi: 10.1016/j.neuropharm.2018.04.026
   PubMed Web of Science ®Google Scholar
• Liu R, Crawford J, Callahan PM, et al. Intermittent stimulation of the nucleus basalis of meynert improves working memory in adult monkeys. Curr Biol. 2017;27(17):2640–2646 e2644. doi: 10.1016/j.cub.2017.07.021
   PubMed Web of Science ®Google Scholar
• Koulousakis P, van den Hove D, Visser-Vandewalle V, et al. Cognitive improvements after intermittent deep brain stimulation of the nucleus basalis of meynert in a transgenic rat model for alzheimer’s disease: a preliminary approach. J Alzheimers Dis. 2020;73(2):461–466. doi: 10.3233/JAD-190919
   PubMed Web of Science ®Google Scholar
• Mann A, Gondard E, Tampellini D, et al. Chronic deep brain stimulation in an Alzheimer’s disease mouse model enhances memory and reduces pathological hallmarks. Brain Stimul. 2018;11(2):435–444. doi: 10.1016/j.brs.2017.11.012
   PubMed Web of Science ®Google Scholar
• Fell J, Staresina BP, Do Lam AT, et al. Memory modulation by weak synchronous deep brain stimulation: a pilot study. Brain Stimul. 2013;6(3):270–273. doi: 10.1016/j.brs.2012.08.001
   PubMed Web of Science ®Google Scholar
• Suthana N, Haneef Z, Stern J, et al. Memory enhancement and deep-brain stimulation of the entorhinal area. N Engl J Med. 2012;366(6):502–510. doi: 10.1056/NEJMoa1107212
   PubMed Web of Science ®Google Scholar
• Titiz AS, Hill MRH, Mankin EA, et al. Theta-burst microstimulation in the human entorhinal area improves memory specificity. Elife. 2017;6. doi: 10.7554/eLife.29515
   PubMed Web of Science ®Google Scholar
• Ezzyat Y, Wanda PA, Levy DF, et al. Closed-loop stimulation of temporal cortex rescues functional networks and improves memory. Nat Commun. 2018;9(1):365. doi: 10.1038/s41467-017-02753-0
   PubMedGoogle Scholar
• Scharre DW, Weichart E, Nielson D, et al. Deep brain stimulation of frontal lobe networks to treat Alzheimer’s disease. J Alzheimers Dis. 2018;62(2):621–633. doi: 10.3233/JAD-170082
   PubMed Web of Science ®Google Scholar
• Liu Z, Shu K, Geng Y, et al. Deep brain stimulation of fornix in Alzheimer’s disease: from basic research to clinical practice. Eur J Clin Invest. 2023;53(8):e13995. doi: 10.1111/eci.13995
   PubMed Web of Science ®Google Scholar
• Jeong J. EEG dynamics in patients with Alzheimer’s disease. Clin Neurophysiol. 2004;115(7):1490–1505. doi: 10.1016/j.clinph.2004.01.001
   PubMed Web of Science ®Google Scholar
• van Dyck CH, Swanson CJ, Aisen P, et al. Lecanemab in early Alzheimer’s disease. N Engl J Med. 2023;388(1):9–21. doi: 10.1056/NEJMoa2212948
   PubMed Web of Science ®Google Scholar
• Grossman N, Bono D, Dedic N, et al. Noninvasive deep brain stimulation via temporally interfering electric fields. Cell. 2017;169(6):1029–1041 e1016. doi: 10.1016/j.cell.2017.05.024
   PubMed Web of Science ®Google Scholar
• Philip NS, Arulpragasam AR. Reaching for the unreachable: low intensity focused ultrasound for non-invasive deep brain stimulation. Neuropsychopharmacology. 2023;48(1):251–252. doi: 10.1038/s41386-022-01386-2
   PubMed Web of Science ®Google Scholar
• Violante IR, Alania K, Cassara AM, et al. Non-invasive temporal interference electrical stimulation of the human hippocampus. Nat Neurosci. 2023;26(11): 1994–2004.
   PubMed Web of Science ®Google Scholar
• Boutet A, Madhavan R, Elias GJB, et al. Predicting optimal deep brain stimulation parameters for Parkinson’s disease using functional MRI and machine learning. Nat Commun. 2021;12(1):3043. doi: 10.1038/s41467-021-23311-9
   PubMed Web of Science ®Google Scholar