Transcranial Magnetic Stimulation to Address Mild Cognitive Impairment in the Elderly: A Randomized Controlled Study

Hellen Livia Drumond Marra, Martin Luiz Myczkowski, Cláudia Maia Memória, Débora Arnaut, Philip Leite Ribeiro, Carlos Gustavo Sardinha Mansur, Rodrigo Lancelote Alberto, Bianca Boura Bellini, Adriano Alves Fernandes da Silva, Gabriel Tortella, Daniel Ciampi de Andrade, Manoel Jacobsen Teixeira, Orestes Vicente Forlenza, Marco Antonio Marcolin, Hellen Livia Drumond Marra, Martin Luiz Myczkowski, Cláudia Maia Memória, Débora Arnaut, Philip Leite Ribeiro, Carlos Gustavo Sardinha Mansur, Rodrigo Lancelote Alberto, Bianca Boura Bellini, Adriano Alves Fernandes da Silva, Gabriel Tortella, Daniel Ciampi de Andrade, Manoel Jacobsen Teixeira, Orestes Vicente Forlenza, Marco Antonio Marcolin

Abstract

Transcranial magnetic stimulation (TMS) is a noninvasive brain stimulation technique with potential to improve memory. Mild cognitive impairment (MCI), which still lacks a specific therapy, is a clinical syndrome associated with increased risk of dementia. This study aims to assess the effects of high-frequency repetitive TMS (HF rTMS) on everyday memory of the elderly with MCI. We conducted a double-blinded randomized sham-controlled trial using rTMS over the left dorsolateral prefrontal cortex (DLPFC). Thirty-four elderly outpatients meeting Petersen's MCI criteria were randomly assigned to receive 10 sessions of either active TMS or sham, 10 Hz rTMS at 110% of motor threshold, 2,000 pulses per session. Neuropsychological assessment at baseline, after the last session (10th) and at one-month follow-up, was applied. ANOVA on the primary efficacy measure, the Rivermead Behavioural Memory Test, revealed a significant group-by-time interaction (p = 0.05), favoring the active group. The improvement was kept after one month. Other neuropsychological tests were heterogeneous. rTMS at 10 Hz enhanced everyday memory in elderly with MCI after 10 sessions. These findings suggest that rTMS might be effective as a therapy for MCI and probably a tool to delay deterioration.

Figures

Figure 1
Figure 1
Flow diagram of referred and enrolled patients.
Figure 2
Figure 2
Comparison of RBMT means scores in T0, T1, and T2. Two-way ANOVA for repeated measures. Timing of procedures: T0: baseline cognitive assessment and 1st rTMS; T1: 10th rTMS session and 2nd cognitive assessment; T2: 30 days after T1 and 3rd cognitive assessment. Student's t-test for comparison of rTMS versus sham basal means, p = 0.292.
Figure 3
Figure 3
Comparison of logical memory II means scores in T0, T1, and T2. Two-way ANOVA for repeated measures. Timing of procedures: T0: baseline cognitive assessment and 1st rTMS; T1: 10th rTMS session and 2nd cognitive assessment; T2: 30 days after T1 and 3rd cognitive assessment. Student's t-test for comparison of rTMS versus sham basal means, p = 0.087.
Figure 4
Figure 4
Comparison of letter-number sequencing means scores in T0, T1, and T2. Two-way ANOVA for repeated measures. Timing of procedures: T0: baseline cognitive assessment and 1st rTMS; T1: 10th rTMS session and 2nd cognitive assessment; T2: 30 days after T1 and 3rd cognitive assessment. Student's t-test for comparison of rTMS versus sham basal means, p = 0.211.
Figure 5
Figure 5
Comparison of Trail Making Test B means scores in T0, T1, and T2. Two-way ANOVA for repeated measures. Timing of procedures: T0: baseline cognitive assessment and 1st rTMS; T1: 10th rTMS session and 2nd cognitive assessment; T2: 30 days after T1 and 3rd cognitive assessment. Mann-Whitney-Wilcoxon test for comparison of rTMS versus sham basal means, p = 0.986.
Figure 6
Figure 6
Comparison of semantic verbal fluency/animal naming means scores in T0, T1, and T2. Two-way ANOVA for repeated measures. Timing of procedures: T0: baseline cognitive assessment and 1st rTMS; T1: 10th rTMS session and 2nd cognitive assessment; T2: 30 days after T1 and 3rd cognitive assessment. Student's t-test for comparison of rTMS versus sham basal means, p = 0.081.

References

    1. Petersen R. C., Negash S. Mild cognitive impairment: an overview. CNS Spectrums. 2008;13(1):45–53.
    1. Petersen R. C., Smith G. E., Waring S. C., Ivnik R. J., Tangalos E. G., Kokmen E. Mild cognitive impairment: clinical characterization and outcome. Archives of Neurology. 1999;56(3):303–308. doi: 10.1001/archneur.56.3.303.
    1. Cotelli M., Calabria M., Manenti R., et al. Brain stimulation improves associative memory in an individual with amnestic mild cognitive impairment. Neurocase. 2012;18(3):217–223. doi: 10.1080/13554794.2011.588176.
    1. Cotelli M., Manenti R., Zanetti O., Miniussi C. Non-pharmacological intervention for memory decline. Frontiers in Human Neuroscience. 2012;6, article 46 doi: 10.3389/fnhum.2012.00046.
    1. Irish M., Lawlor B. A., Coen R. F., O'Mara S. M. Everyday episodic memory in amnestic mild cognitive impairment: a preliminary investigation. BMC Neuroscience. 2011;12, article 80 doi: 10.1186/1471-2202-12-80.
    1. Kelley B. J., Petersen R. C. Alzheimer’s disease and mild cognitive impairment. Neurologic Clinics. 2007;25(3):577–609. doi: 10.1016/j.ncl.2007.03.008.
    1. Jicha G. A., Parisi J. E., Dickson D. W., et al. Neuropathologic outcome of mild cognitive impairment following progression to clinical dementia. Archives of Neurology. 2006;63(5):674–681. doi: 10.1001/archneur.63.5.674.
    1. Sperling R. A., Aisen P. S., Beckett L. A., et al. Toward defining the preclinical stages of Alzheimer's disease: recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimer's and Dementia. 2011;7(3):280–292. doi: 10.1016/j.jalz.2011.03.003.
    1. Summers M. J., Saunders N. L. J. Neuropsychological measures predict decline to alzheimer's dementia from mild cognitive impairment. Neuropsychology. 2012;26(4):498–508. doi: 10.1037/a0028576.
    1. Small G. W., Bookheimer S. Y., Thompson P. M., et al. Current and future uses of neuroimaging for cognitively impaired patients. The Lancet Neurology. 2008;7(2):161–172. doi: 10.1016/s1474-4422(08)70019-x.
    1. Chapman R. M., Mapstone M., McCrary J. W., et al. Predicting conversion from mild cognitive impairment to Alzheimer's disease using neuropsychological tests and multivariate methods. Journal of Clinical and Experimental Neuropsychology. 2011;33(2):187–199. doi: 10.1080/13803395.2010.499356.
    1. Kazui H., Matsuda A., Hirono N., et al. Everyday memory impairment of patients with mild cognitive impairment. Dementia and Geriatric Cognitive Disorders. 2005;19(5-6):331–337. doi: 10.1159/000084559.
    1. Sandrini M., Brambilla M., Manenti R., Rosini S., Cohen L. G., Cotelli M. Noninvasive stimulation of prefrontal cortex strengthens existing episodic memories and reduces forgetting in the elderly. Frontiers in Aging Neuroscience. 2014;6, article 289 doi: 10.3389/fnagi.2014.00289.
    1. Yassuda M. S., Flaks M. K., Viola L. F., et al. Psychometric characteristics of the Rivermead Behavioural Memory Test (RBMT) as an early detection instrument for dementia and mild cognitive impairment in Brazil. International Psychogeriatrics. 2010;22(6):1003–1011. doi: 10.1017/s1041610210001055.
    1. Cabeza R., Anderson N. D., Locantore J. K., McIntosh A. R. Aging gracefully: compensatory brain activity in high-performing older adults. NeuroImage. 2002;17(3):1394–1402. doi: 10.1006/nimg.2002.1280.
    1. Simons J. S., Spiers H. J. Prefrontal and medial temporal lobe interactions in long-term memory. Nature Reviews Neuroscience. 2003;4(8):637–648. doi: 10.1038/nrn1178.
    1. Cabeza R., Ciaramelli E., Olson I. R., Moscovitch M. The parietal cortex and episodic memory: an attentional account. Nature Reviews Neuroscience. 2008;9(8):613–625. doi: 10.1038/nrn2459.
    1. Turriziani P., Smirni D., Zappalà G., Mangano G. R., Oliveri M., Cipolotti L. Enhancing memory performance with rTMS in healthy subjects and individuals with Mild Cognitive Impairment: the role of the right dorsolateral prefrontal cortex. Frontiers in Human Neuroscience. 2012;6, article 62 doi: 10.3389/fnhum.2012.00062.
    1. Manenti R., Cotelli M., Miniussi C. Successful physiological aging and episodic memory: a brain stimulation study. Behavioural Brain Research. 2011;216(1):153–158. doi: 10.1016/j.bbr.2010.07.027.
    1. Cabeza R., Grady C. L., Nyberg L., et al. Age-related differences in neural activity during memory encoding and retrieval: a positron emission tomography study. Journal of Neuroscience. 1997;17(1):391–400.
    1. Tulving E., Kapur S., Craik F. I. M., Moscovitch M., Houle S. Hemispheric encoding/retrieval asymmetry in episodic memory: positron emission tomography findings. Proceedings of the National Academy of Sciences of the United States of America. 1994;91(6):2016–2020. doi: 10.1073/pnas.91.6.2016.
    1. Voytek B., Gazzaley A. Stimulating the aging brain. Annals of Neurology. 2013;73(1):1–3. doi: 10.1002/ana.23790.
    1. George M. S., Padberg F., Schlaepfer T. E., et al. Controversy: repetitive transcranial magnetic stimulation or transcranial direct current stimulation shows efficacy in treating psychiatric diseases (depression, mania, schizophrenia, obsessive-complusive disorder, panic, posttraumatic stress disorder) Brain Stimulation. 2009;2(1):14–21. doi: 10.1016/j.brs.2008.06.001.
    1. Wassermann E. M., Epstein C., Ziemann U., Walsh V., Paus T., Lisanby S. Handbook of Tanscranial Stimulation. Oxford, UK: Oxford University Press; 2008.
    1. Jahanshahi M., Rothwell J. Transcranial magnetic stimulation studies of cognition: an emerging field. Experimental Brain Research. 2000;131(1):1–9. doi: 10.1007/s002219900224.
    1. Pascual-Leone A., Valls-Solé J., Wassermann E. M., Hallett M. Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. Brain. 1994;117(4):847–858. doi: 10.1093/brain/117.4.847.
    1. Maeda F., Keenan J. P., Tormos J. M., Topka H., Pascual-Leone A. Modulation of corticospinal excitability by repetitive transcranial magnetic stimulation. Clinical Neurophysiology. 2000;111(5):800–805. doi: 10.1016/s1388-2457(99)00323-5.
    1. Morris J. C. The Clinical Dementia Rating (CDR): current version and scoring rules. Neurology. 1993;43(11):2412–2414.
    1. Siebner H. R., Hartwigsen G., Kassuba T., Rothwell J. C. How does transcranial magnetic stimulation modify neuronal activity in the brain? Implications for studies of cognition. Cortex. 2009;45(9):1035–1042. doi: 10.1016/j.cortex.2009.02.007.
    1. Hoogendam J. M., Ramakers G. M. J., Di Lazzaro V. Physiology of repetitive transcranial magnetic stimulation of the human brain. Brain Stimulation. 2010;3(2):95–118. doi: 10.1016/j.brs.2009.10.005.
    1. Siebner H. R., Rothwell J. Transcranial magnetic stimulation: new insights into representational cortical plasticity. Experimental Brain Research. 2003;148(1):1–16. doi: 10.1007/s00221-002-1234-2.
    1. Luber B., McClintock S. M., Lisanby S. H. Applications of transcranial magnetic stimulation and magnetic seizure therapy in the study and treatment of disorders related to cerebral aging. Dialogues in Clinical Neuroscience. 2013;15(1):87–98.
    1. Rossi S., Hallett M., Rossini P. M., et al. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clinical Neurophysiology. 2009;120(12):2008–2039. doi: 10.1016/j.clinph.2009.08.016.
    1. Nardone R., Tezzon F., Höller Y., Golaszewski S., Trinka E., Brigo F. Transcranial magnetic stimulation (TMS)/repetitive TMS in mild cognitive impairment and Alzheimer's disease. Acta Neurologica Scandinavica. 2014;129(6):351–366. doi: 10.1111/ane.12223.
    1. Ziemann U., Paulus W., Nitsche M. A., et al. Consensus: motor cortex plasticity protocols. Brain Stimulation. 2008;1(3):164–182. doi: 10.1016/j.brs.2008.06.006.
    1. Thickbroom G. W. Transcranial magnetic stimulation and synaptic plasticity: experimental framework and human models. Experimental Brain Research. 2007;180(4):583–593. doi: 10.1007/s00221-007-0991-3.
    1. Lefaucheur J. P., André-Obadia N., Antal A., et al. Evidence-based guidelines on the therapeutic use of repetitive transcranial magnetic stimulation (rTMS) Clinical Neurophysiology. 2014;125(11):2150–2206. doi: 10.1016/j.clinph.2014.05.021.
    1. Lisanby S. H., Luber B., Perera T., Sackeim H. A. Transcranial magnetic stimulation: applications in basic neuroscience and neuropsychopharmacology. International Journal of Neuropsychopharmacology. 2000;3(3):259–273. doi: 10.1017/s1461145700002005.
    1. Demirtas-Tatlidede A., Vahabzadeh-Hagh A. M., Pascual-Leone A. Can noninvasive brain stimulation enhance cognition in neuropsychiatric disorders? Neuropharmacology. 2013;64:566–578. doi: 10.1016/j.neuropharm.2012.06.020.
    1. Huerta P. T., Volpe B. T. Transcranial magnetic stimulation, synaptic plasticity and network oscillations. Journal of NeuroEngineering and Rehabilitation. 2009;6(1, article 7) doi: 10.1186/1743-0003-6-7.
    1. Gazzaley A., D'Esposito M. Top-down modulation and normal aging. Annals of the New York Academy of Sciences. 2007;1097:67–83. doi: 10.1196/annals.1379.010.
    1. Gershon A. A., Dannon P. N., Grunhaus L. Transcranial magnetic stimulation in the treatment of depression. American Journal of Psychiatry. 2003;160(5):835–845. doi: 10.1176/appi.ajp.160.5.835.
    1. Cheeran B., Talelli P., Mori F., et al. A common polymorphism in the brain-derived neurotrophic factor gene (BDNF) modulates human cortical plasticity and the response to rTMS. Journal of Physiology. 2008;586(23):5717–5725. doi: 10.1113/jphysiol.2008.159905.
    1. Manenti R., Cotelli M., Calabria M., Maioli C., Miniussi C. The role of the dorsolateral prefrontal cortex in retrieval from long-term memory depends on strategies: a repetitive transcranial magnetic stimulation study. Neuroscience. 2010;166(2):501–507. doi: 10.1016/j.neuroscience.2009.12.037.
    1. Solé-Padullés C., Bartrés-Faz D., Junqué C., et al. Repetitive transcranial magnetic stimulation effects on brain function and cognition among elders with memory dysfunction. A randomized sham-controlled study. Cerebral Cortex. 2006;16(10):1487–1493. doi: 10.1093/cercor/bhj083.
    1. Lisanby S. H., Gutman D., Luber B., Schroeder C., Sackeim H. A. Sham TMS: intracerebral measurement of the induced electrical field and the induction of motor-evoked potentials. Biological Psychiatry. 2001;49(5):460–463. doi: 10.1016/s0006-3223(00)01110-0.
    1. Mills K. R., Boniface S. J., Schubert M. Magnetic brain stimulation with a double coil: the importance of coil orientation. Electroencephalography and Clinical Neurophysiology/Evoked Potentials Section. 1992;85(1):17–21. doi: 10.1016/0168-5597(92)90096-T.
    1. Rossi S., Miniussi C., Pasqualetti P., Babiloni C., Rossini P. M., Cappa S. F. Age-related functional changes of prefrontal cortex in long-term memory: a repetitive transcranial magnetic stimulation study. The Journal of Neuroscience. 2004;24(36):7939–7944. doi: 10.1523/jneurosci.0703-04.2004.
    1. Manenti R., Cotelli M., Robertson I. H., Miniussi C. Transcranial brain stimulation studies of episodic memory in young adults, elderly adults and individuals with memory dysfunction: a review. Brain Stimulation. 2012;5(2):103–109. doi: 10.1016/j.brs.2012.03.004.
    1. Guse B., Falkai P., Wobrock T. Cognitive effects of high-frequency repetitive transcranial magnetic stimulation: a systematic review. Journal of Neural Transmission. 2010;117(1):105–122. doi: 10.1007/s00702-009-0333-7.
    1. Nasreddine Z. S., Phillips N. A., Bédirian V., et al. The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. Journal of the American Geriatrics Society. 2005;53(4):695–699. doi: 10.1111/j.1532-5415.2005.53221.x.
    1. Sheikh J. I., Yesavage J. A. Geriatric depression scale (GDS): recent evidence and development of a shorter version. Clinical Gerontologist. 1986;5(1-2):165–173. doi: 10.1300/j018v05n01_09.
    1. Hamilton M. A rating scale for depression. Journal of Neurology, Neurosurgery, and Psychiatry. 1960;23:56–62. doi: 10.1136/jnnp.23.1.56.
    1. Hamilton M. The assessment of anxiety states by rating. The British Journal of Medical Psychology. 1959;32(1):50–55. doi: 10.1111/j.2044-8341.1959.tb00467.x.
    1. Jorm A. F., Korten A. E. Assessment of cognitive decline in the elderly by informant interview. British Journal of Psychiatry. 1988;152:209–213. doi: 10.1192/bjp.152.2.209.
    1. Hindmarch I., Lehfeld H., De Jongh P., Erzigkeit H. The Bayer: activities of daily living scale (B-ADL) Dementia and Geriatric Cognitive Disorders. 1998;9(2):20–26.
    1. Folstein M. F., Folstein S. E., Mchugh P. R. ‘Mini-mental state’. A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research. 1975;12(3):189–198.
    1. Wilson B., Cockburn J., Baddeley A., Hiorns R. The development and validation of a test battery for detecting and monitoring everyday memory problems. Journal of Clinical and Experimental Neuropsychology. 1989;11(6):855–870. doi: 10.1080/01688638908400940.
    1. Adachi H., Shinagawa S., Komori K., et al. Comparison of the utility of everyday memory test and the Alzheimer's Disease Assessment Scale-Cognitive part for evaluation of mild cognitive impairment and very mild Alzheimer's disease. Psychiatry and Clinical Neurosciences. 2013;67(3):148–153. doi: 10.1111/pcn.12034.
    1. Van Balen H. G. G., Westzaan P. S. H., Mulder T. Stratified norms for the rivermead behavioural memory test. Neuropsychological Rehabilitation. 1996;6(3):203–217. doi: 10.1080/713755507.
    1. Wechsler D. I. Examiner's Manual: Wechsler Adult Intelligence Scale—Revised. New York, NY, USA: The Psychological Corporation; 1981.
    1. Malloy-Diniz L. F. M., Cruz M. F., Torres V. M., Cosenza R. M. O teste de aprendizagem auditivo-verbal de Rey: normas para uma população brasileira. Revista Brasileira de Neurologia. 2000;36:79–83.
    1. Malloy-Diniz L. F., Lasmar V. A. P., Gazinelli L. D. S. R., Fuentes D., Salgado J. V. The Rey Auditory-Verbal Learning Test: applicability for the brazilian elderly population. Revista Brasileira de Psiquiatria. 2007;29(4):324–329. doi: 10.1590/s1516-44462006005000053.
    1. Savage R. M., Gouvier W. D. Rey auditory-verbal learning test: the effects of age and gender, and norms for delayed recall and story recognition trials. Archives of Clinical Neuropsychology. 1992;7(5):407–414. doi: 10.1016/0887-6177(92)90153-e.
    1. Wechsler D. WAIS-III: Administration and Scoring Manual. San Antonio, Tex, USA: The Psychological Corporation; 1997.
    1. Hill B. D., Elliott E. M., Shelton J. T., Pella R. D., O'Jile J. R., Gouvier W. D. Can we improve the clinical assessment of working memory? An evaluation of the WAIS-III using a working memory criterion construct. Journal of Clinical and Experimental Neuropsychology. 2010;32(3):315–323. doi: 10.1080/13803390903032529.
    1. Tombaugh T. N. Trail Making test A and B: normative data stratified by age and education. Archives of Clinical Neuropsychology. 2004;19(2):203–214. doi: 10.1016/s0887-6177(03)00039-8.
    1. Reynolds C. R. Comprehensive Trail Making Test: Examiner’s Manual. Austin, Tex, USA: Pro-Ed; 2002.
    1. Mezzich J. E., Moses J. A., Jr. Efficient screening for brain dysfunction. Biological Psychiatry. 1980;15(2):333–337.
    1. Reitan R. M. Validity of the Trail Making test as an indicator of organic brain damage. Perceptual and Motor Skills. 1958;8(3):271–276. doi: 10.2466/PMS.8.7.271-276.
    1. Tombaugh T. N., Kozak J., Rees L. Normative data stratified by age and education for two measures of verbal fluency: FAS and animal naming. Archives of Clinical Neuropsychology. 1999;14(2):167–177. doi: 10.1016/s0887-6177(97)00095-4.
    1. Trenerry M. R., Crosson B., DeBoe J., Leber W. R. The Stroop Neuropsychological Screening Test. Odessa, Ukraine: Psychological Assessment Resources; 1989.
    1. First M. B., Spitzer R. L., Gibbon M., Willian J. B. W. Structured Clinical Interview for DSM IV Axis I disorders—Research version—Non-Patient Edition (SCID-I/NP) New York, NY, USA: Biometrics Research Department; 2002.
    1. Loo C. K., Taylor J. L., Gandevia S. C., McDarmont B. N., Mitchell P. B., Sachdev P. S. Transcranial magnetic stimulation (TMS) in controlled treatment studies: are some ‘sham’ forms active? Biological Psychiatry. 2000;47(4):325–331. doi: 10.1016/s0006-3223(99)00285-1.
    1. Wassermann E. M., Pascual-Leone A., Valls-Solé J., Toro C., Cohen L. G., Hallett M. Topography of the inhibitory and excitatory responses to transcranial magnetic stimulation in a hand muscle. Electroencephalography and Clinical Neurophysiology. 1993;89(6):424–433.
    1. Bolló-Gasol S., Piñol-Ripoll G., Cejudo-Bolivar J. C., Llorente-Vizcaino A., Peraita-Adrados H. Ecological assessment of mild cognitive impairment and Alzheimer disease using the Rivermead Behavioural Memory Test. Neurología. 2013;29(6):339–345. doi: 10.1016/j.nrl.2013.07.004.
    1. Loo C. K., Sachdev P., Elsayed H., et al. Effects of a 2- to 4-week course of repetitive Transcranial Magnetic Stimulation (rTMS) on neuropsychologic functioning, electroencephalogram, and auditory threshold in depressed patients. Biological Psychiatry. 2001;49(7):615–623. doi: 10.1016/s0006-3223(00)00996-3.
    1. Loo C. K., Mitchell P. B., Croker V. M., et al. Double-blind controlled investigation of bilateral prefrontal transcranial magnetic stimulation for the treatment of resistant major depression. Psychological Medicine. 2003;33(1):33–40. doi: 10.1017/s0033291702006839.
    1. Nahas Z., Li X., Kozel F. A., et al. Safety and benefits of distance-adjusted prefrontal transcranial magnetic stimulation in depressed patients 55–75 years of age: a pilot study. Depression and Anxiety. 2004;19(4):249–256. Erratum in: F. R. Daro, B. B. Bellini, Z. H. Nahas, D. E. Bohning, M. S. George, M. A. Marcolin, Depression and Anxiety, vol. 27, no. 1, p. 90, 2010.
    1. Stokes M. G., Chambers C. D., Gould I. C., et al. Distance-adjusted motor threshold for transcranial magnetic stimulation. Clinical Neurophysiology. 2007;118(7):1617–1625. doi: 10.1016/j.clinph.2007.04.004.
    1. Daro F. R., Bellini B. B., Nahas Z. H., Bohning D. E., George M. S., Marcolin M. A. Safety and benefits of distance-adjusted prefrontal transcranial magnetic stimulation in depressed patients 55–75 years of age: a pilot study. Depression and Anxiety. 2010;27(1):p. 90. doi: 10.1002/da.20652. Erratum.
    1. Nahas Z., Li X., Kozel F. A., et al. Safety and benefits of distance-adjusted prefrontal transcranial magnetic stimulation in depressed patients 55–75 years of age: a pilot study. Depression and Anxiety. 2004;19(4):249–256. doi: 10.1002/da.20015. Erratum to Depression and Anxiety, vol. 27, no. 1, p. 90, 2010.
    1. Janicak P. G., Dowd S. M., Martis B., et al. Repetitive transcranial magnetic stimulation versus electroconvulsive therapy for major depression: preliminary results of a randomized trial. Biological Psychiatry. 2002;51(8):659–667. doi: 10.1016/s0006-3223(01)01354-3.
    1. Robertson E. M., Théoret H., Pascual-Leone A. Studies in cognition: the problems solved and created by transcranial magnetic stimulation. Journal of Cognitive Neuroscience. 2003;15(7):948–960. doi: 10.1162/089892903770007344.
    1. Petersen R. C., Doody R., Kurz A., et al. Current concepts in mild cognitive impairment. Archives of Neurology. 2001;58(12):1985–1992. doi: 10.1001/archneur.58.12.1985.
    1. Schönfeldt-Lecuona C., Lefaucheur J.-P., Cardenas-Morales L., Wolf R. C., Kammer T., Herwig U. The value of neuronavigated rTMS for the treatment of depression. Neurophysiologie Clinique/Clinical Neurophysiology. 2010;40(1):37–43. doi: 10.1016/j.neucli.2009.06.004.
    1. Ahdab R., Ayache S. S., Brugières P., Goujon C., Lefaucheur J. P. Comparison of ‘standard’ and ‘navigated’ procedures of TMS coil positioning over motor, premotor and prefrontal targets in patients with chronic pain and depression. Neurophysiologie Clinique. 2010;40(1):27–36. doi: 10.1016/j.neucli.2010.01.001.
    1. Beam W., Borckardt J. J., Reeves S. T., George M. S. An efficient and accurate new method for locating the F3 position for prefrontal TMS applications. Brain Stimulation. 2009;2(1):50–54. doi: 10.1016/j.brs.2008.09.006.
    1. Vallence A.-M., Goldsworthy M. R. Can noninvasive brain stimulation enhance function in the ageing brain? Journal of Neurophysiology. 2014;111(1):1–3. doi: 10.1152/jn.00088.2013.
    1. Gangitano M., Valero-Cabré A., Tormos J. M., Mottaghy F. M., Romero J. R., Pascual-Leone Á. Modulation of input-output curves by low and high frequency repetitive transcranial magnetic stimulation of the motor cortex. Clinical Neurophysiology. 2002;113(8):1249–1257. doi: 10.1016/s1388-2457(02)00109-8.
    1. Touge T., Gerschlager W., Brown P., Rothwell J. C. Are the after-effects of low-frequency rTMS on motor cortex excitability due to changes in the efficacy of cortical synapses? Clinical Neurophysiology. 2001;112(11):2138–2145. doi: 10.1016/s1388-2457(01)00651-4.
    1. Chen R., Classen J., Gerloff C., et al. Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology. 1997;48(5):1398–1403. doi: 10.1212/wnl.48.5.1398.
    1. Clark V. P., Parasuraman R. Neuroenhancement: enhancing brain and mind in health and in disease. NeuroImage. 2014;85:889–894. doi: 10.1016/j.neuroimage.2013.08.071.
    1. McKendrick R., Ayaz H., Olmstead R., Parasuraman R. Enhancing dual-task performance with verbal and spatial working memory training: continuous monitoring of cerebral hemodynamics with NIRS. NeuroImage. 2014;85:1014–1026. doi: 10.1016/j.neuroimage.2013.05.103.
    1. Bentwich J., Dobronevsky E., Aichenbaum S., et al. Beneficial effect of repetitive transcranial magnetic stimulation combined with cognitive training for the treatment of Alzheimer's disease: a proof of concept study. Journal of Neural Transmission. 2011;118(3):463–471. doi: 10.1007/s00702-010-0578-1.
    1. Vallar G., Bolognini N. Behavioural facilitation following brain stimulation: implications for neurorehabilitation. Neuropsychological Rehabilitation. 2011;21(5):618–649. doi: 10.1080/09602011.2011.574050.

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