Neurometabolic correlates of posturography in normal aging and older adults with mild cognitive impairment: Evidence from a 1H-MRS study

Oron Levin, Wouter A J Vints, Gal Ziv, Gintarė Katkutė, Simona Kušleikienė, Kristina Valatkevičienė, Samrat Sheoran, Margarita Drozdova-Statkevičienė, Rymantė Gleiznienė, Mati Pääsuke, Vilma Dudonienė, Uwe Himmelreich, Vida J Česnaitienė, Nerijus Masiulis, Oron Levin, Wouter A J Vints, Gal Ziv, Gintarė Katkutė, Simona Kušleikienė, Kristina Valatkevičienė, Samrat Sheoran, Margarita Drozdova-Statkevičienė, Rymantė Gleiznienė, Mati Pääsuke, Vilma Dudonienė, Uwe Himmelreich, Vida J Česnaitienė, Nerijus Masiulis

Abstract

Proton magnetic resonance spectroscopy (1H-MRS) holds promise for revealing and understanding neurodegenerative processes associated with cognitive and functional impairments in aging. In the present study, we examined the neurometabolic correlates of balance performance in 42 cognitively intact older adults (healthy controls - HC) and 26 older individuals that were diagnosed with mild cognitive impairment (MCI). Neurometabolite ratios of total N-acetyl aspartate (tNAA), glutamate-glutamine complex (Glx), total choline (tCho) and myo-inositol (mIns) relative to total creatine (tCr) were assessed using single voxel 1H-MRS in four different brain regions. Regions of interest were the left hippocampus (HPC), dorsal posterior cingulate cortex (dPCC), left sensorimotor cortex (SM1), and right dorsolateral prefrontal cortex (dlPFC). Center-of-pressure velocity (Vcop) and dual task effect (DTE) were used as measures of balance performance. Results indicated no significant group differences in neurometabolite ratios and balance performance measures. However, our observations revealed that higher tCho/tCr and mIns/tCr in hippocampus and dPCC were generic predictors of worse balance performance, suggesting that neuroinflammatory processes in these regions might be a driving factor for impaired balance performance in aging. Further, we found that higher tNAA/tCr and mIns/tCr and lower Glx/tCr in left SM1 were predictors of better balance performance in MCI but not in HC. The latter observation hints at the possibility that individuals with MCI may upregulate balance control through recruitment of sensorimotor pathways.

Keywords: Aging; Balance control; Brain neurometabolites; Dual-task effect; Postural stability.

Conflict of interest statement

Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Copyright © 2022 The Author(s). Published by Elsevier Inc. All rights reserved.

Figures

Fig. 1
Fig. 1
(A-B) Illustration of stance conditions and representative CoP trajectory. (C) Voxel placement in the dorsal posterior cingulate cortex (dPCC), left hippocampus (HPC), left primary sensorimotor cortex (SM1), and right dorsolateral prefrontal cortex (dlPFC). (D) Representative spectra (black) and LCModel fits (red) for PRESS data from right dlPFC. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
Fig. 2
Fig. 2
Group differenced in sway velocity as function of task (single-task verses dual-task) during Tandem Romberg stance with eyes open. AP = Anteroposterior, ML = Medio-lateral, Vcop = Center of Pressure velocity.

References

    1. Agrawal Y., Smith P.E., Rosenberg P.B. Vestibular impairment, cognitive decline and Alzheimer’s disease: balancing the evidence. Aging Mental Health. 2020;24:705–708.
    1. Allan L.M., Ballard C.G., Rowan E.N., Kenny R.A. Incidence and prediction of falls in dementia: a prospective study in older people. PLoS One. 2009;4:e5521.
    1. Ansai J.H., Andrade L.P., Masse F.A.A., Goncalves J., Takahashi A.C.M., Vale F.A.C., Rebelatto J.R. Risk factors for falls in older adults with mild cognitive impairment and mild Alzheimer disease. J. Geriatr. Phys. Ther. 2019;42:116–121.
    1. Bahureksa L., Najafi B., Saleh A., Sabbagh M., Coon D., Mohler M.J., Schwenk M. The impact of mild cognitive impairment on gait and balance: a systematic review and meta-analysis of studies using instrumented assessment. Gerontology. 2017;63:67–83.
    1. Ben Salem D., Walker P.M., Aho S., Tavernier B., Giroud M., Tzourio C., Ricolfi F., Brunotte F. Brain flexibility and balance and gait performances mark morphological and metabolic abnormalities in the elderly. J. Clin. Neurosci. 2008;15:1360–1365.
    1. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B. 1995;57:289–300.
    1. Boisgontier M.P., Beets I.A., Duysens J., Nieuwboer A., Krampe R.T., Swinnen S.P. Age-related differences in attentional cost associated with postural dual tasks: increased recruitment of generic cognitive resources in older adults. Neurosci. Biobehav. Rev. 2013;37:1824–1837.
    1. Boisgontier M.P., Cheval B., Chalavi S., van Ruitenbeek P., Leunissen I., Levin O., Nieuwboer A., Swinnen S.P. Individual differences in brainstem and basal ganglia predict postural control and balance loss in young and older adults. Neurobiol. Aging. 2017;50:47–59.
    1. Bugnariu N., Fung J. Aging and selective sensorimotor strategies in the regulation of upright balance. J. Neuroeng. Rehabil. 2007;4:19.
    1. Chantanachai T., Sturnieks D.L., Lord S.R., Payne N., Webster L., Taylor M.E. Risk factors for falls in older people with cognitive impairment living in the community: systematic review and meta-analysis. Ageing Res. Rev. 2021;71
    1. Chantanachai T., Taylor M.E., Lord S.R., Menant J., Delbaere K., Sachdev P.S., Kochan N.A., Brodaty H., Sturnieks D.L. Risk factors for falls in community-dwelling older people with mild cognitive impairment: a prospective one-year study. PeerJ. 2022;10:e13484.
    1. Cleeland C., Pipingas A., Scholey A., White D. Neurochemical changes in the aging brain: a systematic review. Neurosci. Biobehav. Rev. 2019;98:306–319.
    1. Delbaere K., Kochan N.A., Close J.C., Menant J.C., Sturnieks D.L., Brodaty H., Sachdev P.S., Lord S.R. Mild cognitive impairment as a predictor of falls in community-dwelling older people. Am. J. Geriatr. Psychiatry. 2012;20:845–853.
    1. Deschamps T., Beauchet O., Annweiler C., Cornu C., Mignardot J.B. Postural control and cognitive decline in older adults: position versus velocity implicit motor strategy. Gait Posture. 2014;39:628–630.
    1. Ding B., Chen K.M., Ling H.W., Zhang H., Chai W.M., Li X., Wang T. Diffusion tensor imaging correlates with proton magnetic resonance spectroscopy in posterior cingulate region of patients with Alzheimer’s disease. Dement. Geriatr. Cogn. Disord. 2008;25:218–225.
    1. Ding X.Q., Maudsley A.A., Sabati M., Sheriff S., Schmitz B., Schütze M., Bronzlik P., Kahl K.G., Lanfermann H. Physiological neuronal decline in healthy aging human brain - An in vivo study with MRI and short echo-time whole-brain1H MR spectroscopic imaging. Neuroimage. 2016;137:45–51.
    1. Donker S.F., Roerdink M., Greven A.J., Beek P.J. Regularity of center-of-pressure trajectories depends on the amount of attention invested in postural control. Exp. Brain Res. 2007;181:1–11.
    1. Doumas M., Smolders C., Krampe R.T. Task prioritization in aging: effects of sensory information on concurrent posture and memory performance. Exp. Brain Res. 2008;187:275–281.
    1. Drozdova-Statkevičienė M., Česnaitienė V.J., Pukėnas K., Levin O., Masiulis N. Sway regularity and sway activity in older adults’ upright stance are differentially affected by dual task. Neurosci. Lett. 2018;666:153–157.
    1. Drozdova-Statkevičienė M., Česnaitienė V.J., Levin O., Pauwels L., Pukėnas K., Helsen W.F., Staes F., Masiulis N. The beneficial effects of acute strength training on sway activity and sway regularity in healthy older men: evidence from a posturography study. Neurosci. Lett. 2021;749
    1. Eylers V.V., Maudsley A.A., Bronzlik P., Dellani P.R., Lanfermann H., Ding X.Q. Detection of Normal Aging Effects on Human Brain Metabolite Concentrations and Microstructure with Whole-Brain MR Spectroscopic Imaging and Quantitative MR Imaging. AJNR Am. J. Neuroradiol. 2016;37:447–454.
    1. Gao F., Edden R.A.E., Li M., Puts N.A.J., Wang G., Liu C., Zhao B., Wang H., Bai X., Zhao C., Wang X., Barker P.B. Magnetic resonance spectroscopy detects an age-related decline in brain GABA levels. Neuroimage. 2013;78:75–82.
    1. Gonçalves J., Ansai J.H., Masse F., Vale F., Takahashi A., Andrade L.P. Dual-task as a predictor of falls in older people with mild cognitive impairment and mild Alzheimer’s disease: a prospective cohort study. Braz. J. Phys. Ther. 2018;22:417–423.
    1. Graff-Radford J., Boeve B.F., Murray M.E., Ferman T.J., Tosakulwong N., Lesnick T.G., Maroney-Smith M., Senjem M.L., Gunter J., Smith G.E., Knopman D.S., Jack C.R., Jr, Dickson D.W., Petersen R.C., Kantarci K. Regional proton magnetic resonance spectroscopy patterns in dementia with Lewy bodies. Neurobiol. Aging. 2014;35:1483–1490.
    1. Granacher U., Bridenbaugh S.A., Muehlbauer T., Wehrle A., Kressig R.W. Age-related effects on postural control under multi-task conditions. Gerontology. 2011;57:247–255.
    1. Grossman E.J., Kirov I.I., Gonen O., Novikov D.S., Davitz M.S., Lui Y.W., Grossman R.I., Inglese M., Fieremans E. N-acetyl-aspartate levels correlate with intra-axonal compartment parameters from diffusion MRI. Neuroimage. 2015;118:334–343.
    1. Harris J.L., Yeh H.-W., Swerdlow R.H., Choi I.-Y., Lee P., Brooks W.M. High-field proton magnetic resonance spectroscopy reveals metabolic effects of normal brain aging. Neurobiol. Aging. 2014;35:1686–1694.
    1. Huang C.Y., Lin L.L., Hwang I.S. Age-related differences in reorganization of functional connectivity for a dual task with increasing postural destabilization. Front. Aging Neurosci. 2017;9:96.
    1. Huxhold O., Li S.-C., Schmiedek F., Lindenberger U. Dual-tasking postural control: aging and the effects of cognitive demand in conjunction with focus of attention. Brain Res. Bull. 2006;69:294–305.
    1. Ide R., Ota M., Hada Y., Watanabe S., Takahashi T., Tamura M., Nemoto K., Arai T. Dynamic balance deficit and the neural network in Alzheimer’s disease and mild cognitive impairment. Gait Posture. 2022;93:252–258.
    1. Jacob A., Tward D.J., Resnick S., Smith P.F., Lopez C., Rebello E., Wei E.X., Tilak Ratnanather J., Agrawal Y. Vestibular function and cortical and sub-cortical alterations in an aging population. Heliyon. 2020;6:e04728.
    1. Kantarci K. Proton MRS in mild cognitive impairment. J. Magn. Reson. Imaging. 2013;37:770–777.
    1. Kantarci K., Smith G.E., Ivnik R.J., Petersen R.C., Boeve B.F., Knopman D.S., Tangalos E.G., Jack C.R., Jr. 1H magnetic resonance spectroscopy, cognitive function, and apolipoprotein e genotype in normal aging, mild cognitive impairment and Alzheimer’s disease. J. Int. Neuropsychol. Soc. 2002;8:934–942.
    1. Kantarci K., Weigand S.D., Petersen R.C., Boeve B.F., Knopman D.S., Gunter J., Reyes D., Shiung M., O'Brien P.C., Smith G.E., Ivnik R.J., Tangalos E.G., Jack C.R., Jr. Longitudinal 1H MRS changes in mild cognitive impairment and Alzheimer’s disease. Neurobiol. Aging. 2007;28:1330–1339.
    1. Langer K., Cohen R.A., Porges E.C., Williamson J.B., Woods A.J. Circulating cytokines predict 1H-Proton MRS cerebral metabolites in healthy older adults. Front. Aging Neurosci. 2021;13
    1. Levin O., Weerasekera A., King B.R., Heise K.F., Sima D.M., Chalavi S., Maes C., Peeters R., Sunaert S., Cuypers K., Van Huffel S., Mantini D., Himmelreich U., Swinnen S.P. Sensorimotor cortex neurometabolite levels as correlate of motor performance in normal aging: evidence from a 1H-MRS study. Neuroimage. 2019;202
    1. Lin A., Andronesi O., Bogner W., Choi I.Y., Coello E., Cudalbu C., Juchem C., Kemp G.J., Kreis R., Krššák M., Lee P., Maudsley A.A., Meyerspeer M., Mlynarik V., Near J., Öz G., Peek A.L., Puts N.A., Ratai E.M., Tkáč I., Mullins P.G. Minimum Reporting Standards for in vivo Magnetic Resonance Spectroscopy (MRSinMRS): experts’ consensus recommendations. NMR Biomed. 2021;34:e4484.
    1. Lind A., Boraxbekk C.-J., Petersen E.T., Paulson O.B., Siebner H.R., Marsman A. Regional myo-inositol, creatine, and choline levels are higher at older age and scale negatively with visuospatial working memory: a cross-sectional proton MR spectroscopy study at 7 Tesla on normal cognitive ageing. J. Neurosci. 2020;40:8149–8159.
    1. Lind A., Boraxbekk C.J., Petersen E.T., Paulson O.B., Andersen O., Siebner H.R., Marsman A. Do glia provide the link between low-grade systemic inflammation and normal cognitive ageing? A 1H magnetic resonance spectroscopy study at 7 Tesla. J. Neurochem. 2021;159:185–196.
    1. Liu H., Zhang D., Lin H., Zhang Q., Zheng L., Zheng Y., Yin X., Li Z., Liang S., Huang S. Meta-analysis of neurochemical changes estimated via magnetic resonance spectroscopy in mild cognitive impairment and Alzheimer’s disease. Front. Aging Neurosci. 2021;13
    1. Liu-Ambrose T.Y., Ashe M.C., Graf P., Beattie B.L., Khan K.M. Increased risk of falling in older community-dwelling women with mild cognitive impairment. Phys. Ther. 2008;88:1482–1491.
    1. Lyros E., Ragoschke-Schumm A., Kostopoulos P., Sehr A., Backens M., Kalampokini S., Decker Y., Lesmeister M., Liu Y., Reith W., Fassbender K. Normal brain aging and Alzheimer’s disease are associated with lower cerebral pH: an in vivo histidine 1H-MR spectroscopy study. Neurobiol. Aging. 2020;87:60–69.
    1. Marsh A.P., Geel S.E. The effect of age on the attentional demands of postural control. Gait Posture. 2000;12:105–113.
    1. Marusic U., Taube W., Morrison S.A., Biasutti L., Grassi B., De Pauw K., Meeusen R., Pisot R., Ruffieux J. Aging effects on prefrontal cortex oxygenation in a posture-cognition dual-task: an fNIRS pilot study. Eur. Rev. Aging Phys. Act. 2019;16:2.
    1. Metastasio A., Rinaldi P., Tarducci R., Mariani E., Feliziani F.T., Cherubini A., Pelliccioli G.P., Gobbi G., Senin U., Mecocci P. Conversion of MCI to dementia: role of proton magnetic resonance spectroscopy. Neurobiol. Aging. 2006;27:926–932.
    1. Micarelli A., Liguori C., Viziano A., Izzi F., Placidi F., Alessandrini M. Integrating postural and vestibular dimensions to depict impairment in moderate-to severe obstructive sleep apnea syndrome patients. J. Sleep Res. 2017;26:487–494.
    1. Micarelli A., Viziano A., Della-Morte D., Augimeri I., Alessandrini M. Degree of functional impairment associated with vestibular hypofunction among older adults with cognitive decline. Otol. Neurotol. 2018;39:e392–e400.
    1. Mignardot J.B., Beauchet O., Annweiler C., Cornu C., Deschamps T. Postural sway, falls, and cognitive status: a cross-sectional study among older adults. J. Alzheimers Dis. 2014;41:431–439.
    1. Mitolo M., Stanzani-Maserati M., Capellari S., Testa C., Rucci P., Poda R., Oppi F., Gallassi R., Sambati L., Rizzo G., Parchi P., Evangelisti S., Talozzi L., Tonon C., Lodi R., Liguori R. Predicting conversion from mild cognitive impairment to Alzheimer’s disease using brain 1H-MRS and volumetric changes: a two- year retrospective follow-up study. Neuroimage Clin. 2019;23
    1. Montero-Odasso M., Bergman H., Phillips N.A., Wong C.H., Sourial N., Chertkow H. Dual-tasking and gait in people with mild cognitive impairment. The effect of working memory. BMC Geriatr. 2009;9:41.
    1. Morse C.I., Thom J.M., Davis M.G., Fox K.R., Birch K.M., Narici M.V. Reduced plantarflexor specific torque in the elderly is associated with a lower activation capacity. Eur. J. Appl. Physiol. 2004;92:219–226.
    1. Nikolaidis A., Baniqued P.L., Kranz M.B., Scavuzzo C.J., Barbey A.K., Kramer A.F., Larsen R.J. Multivariate associations of fluid intelligence and NAA. Cereb. Cortex. 2017;27:2607–2616.
    1. Oeltzschner G., Wijtenburg S.A., Mikkelsen M., Edden R., Barker P.B., Joo J.H., Leoutsakos J.S., Rowland L.M., Workman C.I., Smith G.S. Neurometabolites and associations with cognitive deficits in mild cognitive impairment: a magnetic resonance spectroscopy study at 7 Tesla. Neurobiol. Aging. 2019;73:211–218.
    1. Olson B.L., Holshouser B.A., Britt W., 3rd, Mueller C., Baqai W., Patra S., Petersen F., Kirsch W.M. Longitudinal metabolic and cognitive changes in mild cognitive impairment patients. Alzheimer Dis. Assoc. Disord. 2008;22:269–277.
    1. Parra M.A., Pattan V., Wong D., Beaglehole A., Lonie J., Wan H.I., Honey G., Hall J., Whalley H.C., Lawrie S.M. Medial temporal lobe function during emotional memory in early Alzheimer’s disease, mild cognitive impairment and healthy ageing: an fMRI study. BMC Psychiatry. 2013;13:76.
    1. Petersen R.C. Mild cognitive impairment: transition between aging and Alzheimer’s disease. Neurologia. 2000;15:93–101.
    1. Petersen R.C., Caracciolo B., Brayne C., Gauthier S., Jelic V., Fratiglioni L. Mild cognitive impairment: a concept in evolution. J. Inter Med. 2014;275:214–228.
    1. Petrigna L., Gentile A., Mani D., Pajaujiene S., Zanotto T., Thomas E., Paoli A., Palma A., Bianco A. Dual-task conditions on static postural control in older adults: a systematic review and meta-analysis. J. Aging Phys. Act. 2021;29:162–177.
    1. Porges E.C., Woods A.J., Edden R.A., Puts N.A., Harris A.D., Chen H., Garcia A.M., Seider T.R., Lamb D.G., Williamson J.B., Cohen R.A. Frontal gamma-aminobutyric acid concentrations are associated with cognitive performance in older adults. Biol. Psychiatry Cogn. Neurosci. Neuroimaging. 2017;2:38–44.
    1. Ranchet M., Morgan J.C., Akinwuntan A.E., Devos H. Cognitive workload across the spectrum of cognitive impairments: a systematic review of physiological measures. Neurosci. Biobehav. Rev. 2017;80:516–537.
    1. Reyngoudt H., Claeys T., Vlerick L., Verleden S., Acou M., Deblaere K., De Deene Y., Audenaert K., Goethals I., Achten E. Age-related differences in metabolites in the posterior cingulate cortex and hippocampus of normal ageing brain: a 1H-MRS study. Eur. J. Radiol. 2012;81:e223–e231.
    1. Roman-Liu D. Age-related changes in the range and velocity of postural sway. Arch. Gerontol. Geriatr. 2018;77:68–80.
    1. Seidler R.D., Bernard J.A., Burutolu T.B., Fling B.W., Gordon M.T., Gwin J.T., Kwak Y., Lipps D.B. Motor control and aging: links to age-related brain structural, functional, and biochemical effects. Neurosci. Biobehav. Rev. 2010;34:721–733.
    1. Semenov Y.R., Bigelow R.T., Xue Q., Lac S.D., Agrawal Y. Association between vestibular and cognitive function in US adults: data from the national health and nutrition examination survey. J. Gerontol. A Biol. Sci. Med. Sci. 2016;71:243–250.
    1. Shin B.M., Han S.J., Jung J.H., Kim J.E., Fregni F. Effect of mild cognitive impairment on balance. J. Neurol. Sci. 2011;305:121–125.
    1. Sparto P.J., Rosso A.L., Divecha A.A., Metti A.L., Rosano C. Shared neural substrates of cognitive function and postural control in older adults. Alzheimers Dement. 2020;16:621–629.
    1. Stins J.F., Beek P.J. A critical evaluation of the cognitive penetrability of posture. Exp. Aging Res. 2012;38:208–219.
    1. Stins J.F., Michielsen M.E., Roerdink M., Beek P.J. Sway regularity reflects attentional involvement in postural control: effects of expertise, vision and cognition. Gait Posture. 2009;30:106–109.
    1. Sugihara Y., Matsuura T., Kubo Y., Ohgomori T. Activation of the prefrontal cortex and improvement of cognitive performance with standing on one leg. Neuroscience. 2021;477:50–62.
    1. Swan L., Otani H., Loubert P.V. Reducing postural sway by manipulating the difficulty levels of a cognitive task and a balance task. Gait Posture. 2007;26:470–474.
    1. Tangen G.G., Engedal K., Bergland A., Moger T.A., Mengshoel A.M. Relationships between balance and cognition in patients with subjective cognitive impairment, mild cognitive impairment, and Alzheimer disease. Phys. Ther. 2014;94:1123–1134.
    1. Targosz-Gajniak M.G., Siuda J.S., Wicher M.M., Banasik T.J., Bujak M.A., Augusciak-Duma A.M., Opala G. Magnetic resonance spectroscopy as a predictor of conversion of mild cognitive impairment to dementia. J. Neurol. Sci. 2013;335:58–63.
    1. Taylor M.E., Ketels M.M., Delbaere K., Lord S.R., Mikolaizak A.S., Close J.C. Gait impairment and falls in cognitively impaired older adults: an explanatory model of sensorimotor and neuropsychological mediators. Age Ageing. 2012;41:665–669.
    1. Taylor M.E., Delbaere K., Lord S.R., Mikolaizak A.S., Brodaty H., Close J.C. Neuropsychological, physical, and functional mobility measures associated with falls in cognitively impaired older adults. J. Gerontol. A Biol. Sci. Med. Sci. 2014;69:987–995.
    1. Taylor M.E., Lord S.R., Delbaere K., Kurrle S.E., Mikolaizak A.S., Close J.C.T. Reaction time and postural sway modify the effect of executive function on risk of falls in older people with mild to moderate cognitive impairment. Am. J. Geriatr. Psychiatry. 2017;25:397–406.
    1. Teasdale N., Simoneau M. Attentional demands for postural control: the effects of aging and sensory reintegration. Gait Posture. 2001;14:203–210.
    1. Tumati S., Opmeer E.M., Marsman J.C., Martens S., Reesink F.E., De Deyn P.P., Aleman A. Lower choline and myo-inositol in temporo-parietal cortex is associated with apathy in amnestic MCI. Front. Aging Neurosci. 2018;10:106.
    1. Van Impe A., Coxon J.P., Goble D.J., Doumas M., Swinnen S.P. White matter fractional anisotropy predicts balance performance in older adults. Neurobiol. Aging. 2012;33:1900–1912.
    1. Vints W., Kušleikiene S., Sheoran S., Šarkinaite M., Valatkevičiene K., Gleizniene R., Kvedaras M., Pukenas K., Himmelreich U., Cesnaitiene V.J., Levin O., Verbunt J., Masiulis N. Inflammatory blood biomarker kynurenine is linked with elevated neuroinflammation and neurodegeneration in older adults: evidence from two 1H-MRS post-processing analysis methods. Front. Psych. 2022;13
    1. Wang Y., Huang X., Feng Y., Luo Q., He Y., Guo Q., Feng Y., Wang H., Yin S. Resting-state electroencephalography and P300 evidence: age-related vestibular loss as a risk factor contributes to cognitive decline. J. Alzheimers Dis. 2022;86:1107–1121.
    1. Wang H., Tan L., Wang H.F., Liu Y., Yin R.H., Wang W.Y., Chang X.L., Jiang T., Yu J.T. Magnetic resonance spectroscopy in Alzheimer’s disease: systematic review and meta-analysis. J. Alzheimers Dis. 2015;46:1049–1070.
    1. Waragai M., Moriya M., Nojo T. Decreased N-acetyl aspartate/myo-inositol ratio in the posterior cingulate cortex shown by magnetic resonance spectroscopy may be one of the risk markers of preclinical Alzheimer’s disease: a 7-year follow-up study. J. Alzheimers Dis. 2017;60:1411–1427.
    1. Ward N.S., Frackowiak R.S.J. Age-related changes in the neural correlates of motor performance. Brain. 2003;126:873–888.
    1. Weerasekera A., Levin O., Clauwaert A., Heise K.F., Hermans L., Peeters R., Mantini D., Cuypers K., Leunissen I., Himmelreich U., Swinnen S.P. Neurometabolic correlates of reactive and proactive motor inhibition in young and older adults: evidence from multiple regional 1H-MR spectroscopy. Cereb. Cortex Commun. 2020;1:tgaa028.
    1. Wei E.X., Oh E.S., Harun A., Ehrenburg M., Agrawal Y. Vestibular loss predicts poorer spatial cognition in patients with Alzheimer’s disease. J. Alzheimers Dis. 2018;61:995–1003.
    1. Wei E.X., Oh E.S., Harun A., Ehrenburg M., Xue Q.L., Simonsick E., Agrawal Y. Increased prevalence of vestibular loss in mild cognitive impairment and Alzheimer’s disease. Curr. Alzheimer Res. 2019;16:1143–1150.
    1. Wijtenburg S.A., McGuire S.A., Rowland L.M., Sherman P.M., Lancaster J.L., Tate D.F., Hardies L.J., Patel B., Glahn D.C., Hong L.E., Fox P.T., Kochunov P. Relationship between fractional anisotropy of cerebral white matter and metabolite concentrations measured using (1)H magnetic resonance spectroscopy in healthy adults. Neuroimage. 2013;66:161–168.
    1. Winter A.D. Human balance and posture control during standing and walking. Gait Posture. 1995;3:193–214.
    1. Wittenberg E., Thompson J., Nam C.S., Franz J.R. Neuroimaging of human balance control: a systematic review. Front. Hum. Neurosci. 2017;11:170.
    1. Yoon B., Choi S.H., Jeong J.H., Park K.W., Kim E.J., Hwang J., Jang J.W., Kim H.J., Hong J.Y., Lee J.M., Kang J.H., Yoon S.J. Balance and mobility performance along the Alzheimer’s disease spectrum. J. Alzheimers Dis. 2020;73:633–644.
    1. Zahr N.M., Mayer D., Pfefferbaum A., Sullivan E.V. Low striatal glutamate levels underlie cognitive decline in the elderly: evidence from in vivo molecular spectroscopy. Cereb. Cortex. 2008;8:2241–2250.
    1. Zahr N.M., Mayer D., Rohlfing T., Chanraud S., Gu M., Sullivan E.V., Pfefferbaum A. In vivo glutamate measured with magnetic resonance spectroscopy: behavioral correlates in aging. Neurobiol. Aging. 2013;34:1265–1276.
    1. Zanigni S., Testa C., Calandra-Buonaura G., Sambati L., Guarino M., Gabellini A., Evangelisti S., Cortelli P., Lodi R., Tonon C. The contribution of cerebellar proton magnetic resonance spectroscopy in the differential diagnosis among parkinsonian syndromes. Parkinsonism Relat. Disord. 2015;21:929–937.
    1. Zhang B., Ferman T.J., Boeve B.F., Smith G.E., Maroney-Smith M., Spychalla A.J., Knopman D.S., Jack C.R., Jr, Petersen R.C., Kantarci K. MRS in mild cognitive impairment: early differentiation of dementia with Lewy bodies and Alzheimer’s disease. J. Neuroimaging. 2015;25:269–274.
    1. Zhao L., Teng J., Mai W., Su J., Yu B., Nong X., Li C., Wei Y., Duan G., Deng X., Deng D., Chen S. A pilot study on the cutoff value of related brain metabolite in Chinese elderly patients with mild cognitive impairment using MRS. Front. Aging Neurosci. 2021;13
    1. Zöllner H.J., Považan M., Hui S., Tapper S., Edden R., Oeltzschner G. Comparison of different linear-combination modeling algorithms for short-TE proton spectra. NMR Biomed. 2021;34:e4482.

Source: PubMed

Sponsors et collaborateurs

Les conditions médicales

Interventions en matière de drogue

3
S'abonner