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Transcranial magnetic stimulation improves cognition over time in Parkinson's disease

  • Author Footnotes
    1 authors contributed equally to the manuscript.
    Jessica Trung
    Footnotes
    1 authors contributed equally to the manuscript.
    Affiliations
    CIUSSS Centre-Sud-de-l’Île-de-Montréal, Centre de Recherche de l’Institut Universitaire de Gériatrie de Montréal, Montréal, QC, Canada
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  • Author Footnotes
    1 authors contributed equally to the manuscript.
    Alexandru Hanganu
    Footnotes
    1 authors contributed equally to the manuscript.
    Affiliations
    CIUSSS Centre-Sud-de-l’Île-de-Montréal, Centre de Recherche de l’Institut Universitaire de Gériatrie de Montréal, Montréal, QC, Canada

    Department of Clinical Neurosciences and Department of Radiology, University of Calgary, Calgary, AB, Canada

    Hotchkiss Brain Institute, Cumming School of Medicine, Calgary, AB, Canada

    Department of Psychology, University of Montreal, Montreal, QC, Canada
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  • Stevan Jobert
    Affiliations
    CIUSSS Centre-Sud-de-l’Île-de-Montréal, Centre de Recherche de l’Institut Universitaire de Gériatrie de Montréal, Montréal, QC, Canada
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  • Clotilde Degroot
    Affiliations
    CIUSSS Centre-Sud-de-l’Île-de-Montréal, Centre de Recherche de l’Institut Universitaire de Gériatrie de Montréal, Montréal, QC, Canada

    McGill University, Montreal, QC, Canada
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  • Beatriz Mejia-Constain
    Affiliations
    CIUSSS Centre-Sud-de-l’Île-de-Montréal, Centre de Recherche de l’Institut Universitaire de Gériatrie de Montréal, Montréal, QC, Canada
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  • Mekale Kibreab
    Affiliations
    Department of Clinical Neurosciences and Department of Radiology, University of Calgary, Calgary, AB, Canada

    Hotchkiss Brain Institute, Cumming School of Medicine, Calgary, AB, Canada
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  • Marie-Andrée Bruneau
    Affiliations
    CIUSSS Centre-Sud-de-l’Île-de-Montréal, Centre de Recherche de l’Institut Universitaire de Gériatrie de Montréal, Montréal, QC, Canada
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  • Anne-Louise Lafontaine
    Affiliations
    Movement Disorders Unit, McGill University Health Center, Montreal, QC, Canada
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  • Antonio Strafella
    Affiliations
    Department of Medicine, Division of Neurology, University of Toronto, ON, Canada
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  • Oury Monchi
    Correspondence
    Corresponding author. Department of Clinical Neurosciences, University of Calgary, 3330 Hospital DR NW, Calgary, Alberta, T2N 4N1, Canada.
    Affiliations
    CIUSSS Centre-Sud-de-l’Île-de-Montréal, Centre de Recherche de l’Institut Universitaire de Gériatrie de Montréal, Montréal, QC, Canada

    Department of Clinical Neurosciences and Department of Radiology, University of Calgary, Calgary, AB, Canada

    Hotchkiss Brain Institute, Cumming School of Medicine, Calgary, AB, Canada

    McGill University, Montreal, QC, Canada
    Search for articles by this author
  • Author Footnotes
    1 authors contributed equally to the manuscript.

      Highlights

      • Active TMS improves global cognitive performance over time in patients with Parkinson's disease and MCI.
      • There is no significant difference between the active and sham TMS groups.
      • Active and sham TMS improves attention but only active TMS improves visuospatial abilities.
      • TMS has no effect on executive performance, language or memory.
      • The potential sham TMS effect cannot be excluded.

      Abstract

      Introduction

      Cognitive impairment can occur in the early phase of Parkinson's disease and increases the risk of developing dementia. Cognitive deficits were shown to be associated with functional alterations in the dorsolateral prefrontal cortex (DLPFC) and caudate nucleus. Two previous transcranial magnetic stimulation studies over the left DLPFC showed short-term improvement in cognitive performance and focused on specific task.

      Methods

      28 patients with idiopathic Parkinson's disease and mild cognitive impairment received intermittent “theta burst” stimulation (iTBS) (active, N = 14; or sham, N = 14) over the left DLPFC, twice a day for three days with 1–2 days in between. Detailed neuropsychological assessment of five cognitive domains was performed before iTBS and on days 1, 10, and 30 after the last iTBS session. Composite Z-scores were calculated for each domain and for overall cognition.

      Results

      Our results showed an increase in overall cognition up to one month in both groups but this effect was only significant in the active group. Improvements were seen in the attention domain for both groups and in the visuospatial domain in the active group only. No significant differences were found between the groups.

      Conclusion

      These preliminary findings suggest that active iTBS might improve overall cognitive performance in patients with Parkinson's disease with mild cognitive impairment and that this effect can last up to one month. This cognitive improvement, is likely mediated by improvement on visuospatial abilities. Further studies are needed to explore the potential of iTBS as a therapeutical tool to slow cognitive decline in patients with Parkinson's disease.

      Keywords

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      References

        • Mayeux R.
        Epidemiology of neurodegeneration.
        Annu. Rev. Neurosci. 2003; https://doi.org/10.1146/annurev.neuro.26.043002.094919
        • Janvin C.C.
        • Larsen J.P.
        • Aarsland D.
        • Hugdahl K.
        Subtypes of mild cognitive impairment in Parkinson's disease: progression to dementia.
        Mov. Disord. 2006; 21: 1343-1349https://doi.org/10.1002/mds.20974
        • Monchi O.
        • Petrides M.
        • Mejia-Constain B.
        • Strafella A.P.
        Cortical activity in Parkinson's disease during executive processing depends on striatal involvement.
        Brain. 2007; 130: 233-244https://doi.org/10.1093/brain/awl326
        • Cools R.
        • Stefanova E.
        • Barker R.A.
        • Robbins T.W.
        • Owen A.M.
        Dopaminergic modulation of high‐level cognition in Parkinson's disease: the role of the prefrontal cortex revealed by PET.
        Brain. 2002; 125: 584-594https://doi.org/10.1093/brain/awf052
        • Monchi O.
        • Stoessl A.J.
        Imaging neural correlates of mild cognitive impairment in Parkinson's disease.
        Lancet Neurol. 2012; 11: 653-655https://doi.org/10.1016/s1474-4422(12)70162-x
        • Nagano-Saito A.
        • Habak C.
        • Mejía-Constaín B.
        • Degroot C.
        • Monetta L.
        • Jubault T.
        • Bedetti C.
        • Lafontaine A.-L.
        • Chouinard S.
        • Soland V.
        Effect of mild cognitive impairment on the patterns of neural activity in early Parkinson's disease.
        Neurobiol. Aging. 2014; 35: 223-231
        • Strafella A.P.
        • Paus T.
        • Barrett J.
        • Dagher A.
        Repetitive transcranial magnetic stimulation of the human prefrontal cortex induces dopamine release in the caudate nucleus.
        J. Neurosci. 2001; 21: RC157
        • Ko J.H.
        • Monchi O.
        • Ptito A.
        • Bloomfield P.
        • Houle S.
        • Strafella A.P.
        Theta burst stimulation‐induced inhibition of dorsolateral prefrontal cortex reveals hemispheric asymmetry in striatal dopamine release during a set‐shifting task–a TMS–[11C] raclopride PET study.
        Eur. J. Neurosci. 2008; 28: 2147-2155
        • Rektorova I.
        • Megova S.
        • Bares M.
        • Rektor I.
        Cognitive functioning after repetitive transcranial magnetic stimulation in patients with cerebrovascular disease without dementia: a pilot study of seven patients.
        J. Neurol. Sci. 2005; (229–230): 157-161
        • Blumenfeld R.S.
        • Lee T.G.
        • D'Esposito M.
        The effects of lateral prefrontal transcranial magnetic stimulation on item memory encoding.
        Neuropsychologia. 2014; 53: 197-202
        • Sedláčková S.
        • Rektorová I.
        • Srovnalová H.
        • Rektor I.
        Effect of high frequency repetitive transcranial magnetic stimulation on reaction time, clinical features and cognitive functions in patients with Parkinson's disease.
        J. Neural Transm. 2009; 116: 1093-1101
        • Arai N.
        • Müller-Dahlhaus F.
        • Murakami T.
        • Bliem B.
        • Lu M.-K.
        • Ugawa Y.
        • Ziemann U.
        State-dependent and timing-dependent bidirectional associative plasticity in the human SMA-M1 network.
        J. Neurosci. 2011; 31: 15376-15383
        • Boggio P.S.
        • Fregni F.
        • Bermpohl F.
        • Mansur C.G.
        • Rosa M.
        • Rumi D.O.
        • Barbosa E.R.
        • Odebrecht Rosa M.
        • Pascual-Leone A.
        • Rigonatti S.P.
        • Marcolin M.A.
        • Araujo Silva M.T.
        Effect of repetitive TMS and fluoxetine on cognitive function in patients with Parkinson's disease and concurrent depression.
        Mov. Disord. 2005; 20: 1178-1184
        • Epstein C.M.
        • Evatt M.L.
        • Funk A.
        • Girard-Siqueira L.
        • Lupei N.
        • Slaughter L.
        • Athar S.
        • Green J.
        • McDonald W.
        • DeLong M.R.
        An open study of repetitive transcranial magnetic stimulation in treatment-resistant depression with Parkinson's disease.
        Clin. Neurophysiol. 2007; 118: 2189-2194
        • Huang Y.-Z.
        • Edwards M.J.
        • Rounis E.
        • Bhatia K.P.
        • Rothwell J.C.
        Theta burst stimulation of the human motor cortex.
        Neuron. 2005; 45: 201-206
        • Cheng C.-M.
        • Juan C.-H.
        • Chen M.-H.
        • Chang C.-F.
        • Lu H.J.
        • Su T.-P.
        • Lee Y.-C.
        • Li C.-T.
        Different forms of prefrontal theta burst stimulation for executive function of medication-resistant depression: evidence from a randomized sham-controlled study.
        Prog. Neuro Psychopharmacol. Biol. Psychiatr. 2016; 66: 35-40
        • Munneke M.A.M.
        • Rongen J.J.
        • Overeem S.
        • Schelhaas H.J.
        • Zwarts M.J.
        • Stegeman D.F.
        Cumulative effect of 5 daily sessions of theta burst stimulation on corticospinal excitability in amyotrophic lateral sclerosis.
        Muscle Nerve. 2013; 48: 733-738
        • Valero‐Cabré A.
        • Pascual‐Leone A.
        • Rushmore R.J.
        Cumulative sessions of repetitive transcranial magnetic stimulation (rTMS) build up facilitation to subsequent TMS-mediated behavioural disruptions.
        Eur. J. Neurosci. 2008; 27: 765-774
        • Dubois B.
        • Burn D.
        • Goetz C.
        • Aarsland D.
        • Brown R.G.
        • Broe G.A.
        • Dickson D.
        • Duyckaerts C.
        • Cummings J.
        • Gauthier S.
        • Korczyn A.
        • Lees A.
        • Levy R.
        • Litvan I.
        • Mizuno Y.
        • McKeith I.G.
        • Olanow C.W.
        • Poewe W.
        • Sampaio C.
        • Tolosa E.
        • Emre M.
        Diagnostic procedures for Parkinson's disease dementia: recommendations from the movement disorder society task force.
        Mov. Disord. 2007; 22: 2314-2324https://doi.org/10.1002/mds.21844
        • De la Fuente-Fernández R.
        • Ruth T.J.
        • Sossi V.
        • Schulzer M.
        • Calne D.B.
        • Stoessl A.J.
        Expectation and dopamine release: mechanism of the placebo effect in Parkinson's disease.
        Science. 2001; 293 (80-): 1164-1166
        • Troster A.I.
        • Paolo A.M.
        • Lyons K.E.
        • Glatt S.L.
        • Hubble J.P.
        • Koller W.C.
        The influence of depression on cognition in Parkinson's disease A pattern of impairment distinguishable from Alzheimer's disease.
        Neurology. 1995; 45: 672-676
        • Strafella A.P.
        • Ko J.H.
        • Monchi O.
        Therapeutic application of transcranial magnetic stimulation in Parkinson's disease: the contribution of expectation.
        Neuroimage. 2006; 31: 1666-1672
        • Meck W.H.
        • Benson A.M.
        Dissecting the brain's internal clock: how frontal–striatal circuitry keeps time and shifts attention.
        Brain Cogn. 2002; 48: 195-211
        • Lupien S.J.
        • McEwen B.S.
        • Gunnar M.R.
        • Heim C.
        Effects of stress throughout the lifespan on the brain, behaviour and cognition.
        Nat. Rev. Neurosci. 2009; https://doi.org/10.1038/nrn2639
        • Falleti M.
        • Maruff P.
        • Collie A.
        • Darby D.
        Practice effects associated with the repeated assessment of cognitive function using the CogState battery at 10-minute, one week and one month test-retest intervals.
        J. Clin. Exp. Neuropsychol. 2006; https://doi.org/10.1080/13803390500205718
        • Beglinger L.J.
        • Gaydos B.
        • Tangphao-Daniels O.
        • Duff K.
        • Kareken D.A.
        • Crawford J.
        • Fastenau P.S.
        • Siemers E.R.
        Practice effects and the use of alternate forms in serial neuropsychological testing.
        Arch. Clin. Neuropsychol. 2005; https://doi.org/10.1016/j.acn.2004.12.003
        • Goldberg T.E.
        • Harvey P.D.
        • Wesnes K.A.
        • Snyder P.J.
        • Schneider L.S.
        Practice effects due to serial cognitive assessment: implications for preclinical Alzheimer's disease randomized controlled trials.
        Alzheimer's Dementia Diagn. Assess. Dis. Monit. 2015; https://doi.org/10.1016/j.dadm.2014.11.003
        • van den Heuvel O.A.
        • Van Gorsel H.C.
        • Veltman D.J.
        • Van Der Werf Y.D.
        Impairment of executive performance after transcranial magnetic modulation of the left dorsal frontal‐striatal circuit.
        Hum. Brain Mapp. 2013; 34: 347-355
        • Andersen R.A.
        • Snyder L.H.
        • Bradley D.C.
        • Xing J.
        Multimodal representation of space in the posterior parietal cortex and its use in planning movements.
        Annu. Rev. Neurosci. 1997; https://doi.org/10.1146/annurev.neuro.20.1.303
        • Buschman T.J.
        • Miller E.K.
        Top-down versus bottom-up control of attention in the prefrontal and posterior parietal cortices.
        Science. 2007; 315 (80-.): 1860-1862
        • Sohn M.-H.
        • Ursu S.
        • Anderson J.R.
        • Stenger V.A.
        • Carter C.S.
        The role of prefrontal cortex and posterior parietal cortex in task switching.
        Proc. Natl. Acad. Sci. 2000; 97: 13448-13453