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Erschienen in:

01.06.2019 | Original Paper

Neural Scaffolding as the Foundation for Stable Performance of Aging Cerebellum

verfasst von: Pavel Filip, Cécile Gallea, Stéphane Lehéricy, Ovidiu Lungu, Martin Bareš

Erschienen in: The Cerebellum | Ausgabe 3/2019

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Abstract

Although recently conceptualized as a neural node essential for a vast spectrum of associative and cognitive processes, the cerebellum has largely eluded attention in the research of aging, where it is marginalized mainly to structural analyses. In the current cross-sectional study of 67 healthy subjects of various ages (20 to 76 years), we sought to provide a comprehensive, multimodal account of age-related changes in the cerebellum during predictive motor timing, which was previously shown to engage this structure. We combined behavioral assessments of performance with functional MRI and voxel-based morphometry using an advanced method to avoid cerebellar deformation and registration imprecisions inherent to the standard processing at the whole-brain level. Higher age was surprisingly associated with stable behavioral performance during predictive motor timing, despite the massive decrease of infratentorial gray matter volume of a far higher extent than in the supratentorial region, affecting mainly the posterior cerebellar lobe. Nonetheless, this very area showed extensive hyperactivation directly correlated with age. The same region had decreased connectivity with the left caudate and increased connectivity with the left fusiform gyrus, the right pallidum, the hippocampus, and the lingual gyrus. Hence, we propose to extend the scaffolding theory of aging, previously limited mainly to the frontal cortices, to include also the cerebellum, which is likewise suffering from atrophy to a far greater extent than the rest of the brain and is similarly counteracting it by bilateral hyperactivation.
Literatur
1.
Zurück zum Zitat Seidler RD, Bernard JA, Burutolu TB, Fling BW, Gordon MT, Gwin JT, et al. Motor control and aging: links to age-related brain structural, functional, and biochemical effects. Neurosci Biobehav Rev. 2010;34(5):721–33.CrossRefPubMed Seidler RD, Bernard JA, Burutolu TB, Fling BW, Gordon MT, Gwin JT, et al. Motor control and aging: links to age-related brain structural, functional, and biochemical effects. Neurosci Biobehav Rev. 2010;34(5):721–33.CrossRefPubMed
3.
Zurück zum Zitat Harper S. Economic and social implications of aging societies. Science. 2014;346(6209):587–91.CrossRefPubMed Harper S. Economic and social implications of aging societies. Science. 2014;346(6209):587–91.CrossRefPubMed
4.
Zurück zum Zitat Naccarato M, Calautti C, Jones PS, Day DJ, Carpenter TA, Baron JC. Does healthy aging affect the hemispheric activation balance during paced index-to-thumb opposition task? An fMRI study. Neuroimage. 2006;32(3):1250–6.CrossRefPubMed Naccarato M, Calautti C, Jones PS, Day DJ, Carpenter TA, Baron JC. Does healthy aging affect the hemispheric activation balance during paced index-to-thumb opposition task? An fMRI study. Neuroimage. 2006;32(3):1250–6.CrossRefPubMed
6.
Zurück zum Zitat Stoodley CJ, Schmahmann JD. Functional topography in the human cerebellum: a meta-analysis of neuroimaging studies. Neuroimage. 2009;44(2):489–501.CrossRefPubMed Stoodley CJ, Schmahmann JD. Functional topography in the human cerebellum: a meta-analysis of neuroimaging studies. Neuroimage. 2009;44(2):489–501.CrossRefPubMed
7.
Zurück zum Zitat Filip P, Lungu OV, Manto M-U, Bareš M. Linking essential tremor to the cerebellum: physiological evidence. Cerebellum. 2016;15(6):774–80.CrossRefPubMed Filip P, Lungu OV, Manto M-U, Bareš M. Linking essential tremor to the cerebellum: physiological evidence. Cerebellum. 2016;15(6):774–80.CrossRefPubMed
9.
Zurück zum Zitat Bernard JA, Seidler RD. Moving forward: age effects on the cerebellum underlie cognitive and motor declines. Neurosci Biobehav Rev. 2014;42:193–207.CrossRefPubMed Bernard JA, Seidler RD. Moving forward: age effects on the cerebellum underlie cognitive and motor declines. Neurosci Biobehav Rev. 2014;42:193–207.CrossRefPubMed
10.
Zurück zum Zitat Raz N, Gunning-Dixon F, Head D, Williamson A, Acker JD. Age and sex differences in the cerebellum and the ventral pons: a prospective MR study of healthy adults. Am J Neuroradiol. 2001;22(6):1161–7.PubMedPubMedCentral Raz N, Gunning-Dixon F, Head D, Williamson A, Acker JD. Age and sex differences in the cerebellum and the ventral pons: a prospective MR study of healthy adults. Am J Neuroradiol. 2001;22(6):1161–7.PubMedPubMedCentral
16.
Zurück zum Zitat Filip P, Lošák J, Kašpárek T, Vaníček J, Bareš M. Neural network of predictive motor timing in the context of gender differences. Neural Plast. 2016;2016:1–9.CrossRef Filip P, Lošák J, Kašpárek T, Vaníček J, Bareš M. Neural network of predictive motor timing in the context of gender differences. Neural Plast. 2016;2016:1–9.CrossRef
17.
Zurück zum Zitat Filip P, Gallea C, Lehéricy S, Bertasi E, Popa T, Mareček R, et al. Disruption in cerebellar and basal ganglia networks during a visuospatial task in cervical dystonia. Mov Disord. 2017;32(5):757–68.CrossRefPubMed Filip P, Gallea C, Lehéricy S, Bertasi E, Popa T, Mareček R, et al. Disruption in cerebellar and basal ganglia networks during a visuospatial task in cervical dystonia. Mov Disord. 2017;32(5):757–68.CrossRefPubMed
18.
Zurück zum Zitat Husárová I, Mikl M, Lungu OV, Mareček R, Vaníček J, Bareš M. Similar circuits but different connectivity patterns between the cerebellum, basal ganglia, and supplementary motor area in early Parkinson’s disease patients and controls during predictive motor timing. J Neuroimaging. 2013;23(4):452–62.CrossRefPubMed Husárová I, Mikl M, Lungu OV, Mareček R, Vaníček J, Bareš M. Similar circuits but different connectivity patterns between the cerebellum, basal ganglia, and supplementary motor area in early Parkinson’s disease patients and controls during predictive motor timing. J Neuroimaging. 2013;23(4):452–62.CrossRefPubMed
19.
Zurück zum Zitat Schmahmann JD, Sherman JC. The cerebellar cognitive affective syndrome. Brain J Neurol. 1998;121(4):561–79.CrossRef Schmahmann JD, Sherman JC. The cerebellar cognitive affective syndrome. Brain J Neurol. 1998;121(4):561–79.CrossRef
22.
Zurück zum Zitat Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 1971;9(1):97–113.CrossRefPubMed Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 1971;9(1):97–113.CrossRefPubMed
24.
Zurück zum Zitat Filip P, Lungu OV, Shaw DJ, Kasparek T, Bareš M. The mechanisms of movement control and time estimation in cervical dystonia patients. Neural Plast. 2013;2013:1–10.CrossRef Filip P, Lungu OV, Shaw DJ, Kasparek T, Bareš M. The mechanisms of movement control and time estimation in cervical dystonia patients. Neural Plast. 2013;2013:1–10.CrossRef
26.
Zurück zum Zitat Schuirmann DJ. A comparison of the two one-sided tests procedure and the power approach for assessing the equivalence of average bioavailability. J Pharmacokinet Biopharm. 1987;15(6):657–80.CrossRefPubMed Schuirmann DJ. A comparison of the two one-sided tests procedure and the power approach for assessing the equivalence of average bioavailability. J Pharmacokinet Biopharm. 1987;15(6):657–80.CrossRefPubMed
27.
Zurück zum Zitat Bares M, Lungu O, Liu T, Waechter T, Gomez CM, Ashe J. Impaired predictive motor timing in patients with cerebellar disorders. Exp Brain Res Exp. 2007;180(2):355–65.CrossRef Bares M, Lungu O, Liu T, Waechter T, Gomez CM, Ashe J. Impaired predictive motor timing in patients with cerebellar disorders. Exp Brain Res Exp. 2007;180(2):355–65.CrossRef
28.
Zurück zum Zitat Friston KJ, Buechel C, Fink GR, Morris J, Rolls E, Dolan RJ. Psychophysiological and modulatory interactions in neuroimaging. Neuroimage. 1997;6(3):218–29.CrossRefPubMed Friston KJ, Buechel C, Fink GR, Morris J, Rolls E, Dolan RJ. Psychophysiological and modulatory interactions in neuroimaging. Neuroimage. 1997;6(3):218–29.CrossRefPubMed
29.
Zurück zum Zitat Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, et al. A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage. 2005;25(4):1325–35.CrossRefPubMed Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, et al. A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage. 2005;25(4):1325–35.CrossRefPubMed
30.
Zurück zum Zitat Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage. 2002;15(1):273–89.CrossRefPubMed Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage. 2002;15(1):273–89.CrossRefPubMed
32.
Zurück zum Zitat Welford AT, Norris AH, Shock NW. Speed and accuracy of movement and their changes with age. Acta Psychol. 1969;30(C):3–15.CrossRef Welford AT, Norris AH, Shock NW. Speed and accuracy of movement and their changes with age. Acta Psychol. 1969;30(C):3–15.CrossRef
36.
Zurück zum Zitat Stoodley CJ. The cerebellum and cognition: evidence from functional imaging studies. Cerebellum. 2012;11(2):352–65.CrossRefPubMed Stoodley CJ. The cerebellum and cognition: evidence from functional imaging studies. Cerebellum. 2012;11(2):352–65.CrossRefPubMed
37.
Zurück zum Zitat Cabeza R. Hemispheric asymmetry reduction in older adults: the HAROLD model. Psychol Aging. 2002;17(1):85–100.CrossRefPubMed Cabeza R. Hemispheric asymmetry reduction in older adults: the HAROLD model. Psychol Aging. 2002;17(1):85–100.CrossRefPubMed
38.
Zurück zum Zitat Ward NS, Frackowiak RSJ. Age-related changes in the neural correlates of motor performance. Brain J Neurol. 2003;126(0 4):873–88.CrossRef Ward NS, Frackowiak RSJ. Age-related changes in the neural correlates of motor performance. Brain J Neurol. 2003;126(0 4):873–88.CrossRef
41.
Zurück zum Zitat Driver J, Spence C. Multisensory perception: beyond modularity and convergence. Curr Biol. 2000;10(20):R731–5.CrossRefPubMed Driver J, Spence C. Multisensory perception: beyond modularity and convergence. Curr Biol. 2000;10(20):R731–5.CrossRefPubMed
42.
Zurück zum Zitat Schroeter ML, Zysset S, Kruggel F, Von Cramon DY. Age dependency of the hemodynamic response as measured by functional near-infrared spectroscopy. Neuroimage. 2003;19(3):555–64.CrossRefPubMed Schroeter ML, Zysset S, Kruggel F, Von Cramon DY. Age dependency of the hemodynamic response as measured by functional near-infrared spectroscopy. Neuroimage. 2003;19(3):555–64.CrossRefPubMed
43.
Zurück zum Zitat Huettel SA, Singerman JD, McCarthy G. The effects of aging upon the hemodynamic response measured by functional MRI. Neuroimage. 2001;13(1):161–75.CrossRefPubMed Huettel SA, Singerman JD, McCarthy G. The effects of aging upon the hemodynamic response measured by functional MRI. Neuroimage. 2001;13(1):161–75.CrossRefPubMed
46.
Zurück zum Zitat Buckner RL, Krienen FM, Castellanos A, Diaz JC, Yeo BT. The organization of the human cerebellum estimated by intrinsic functional connectivity. J Neurophysiol. 2011;106(5):2322–45. Buckner RL, Krienen FM, Castellanos A, Diaz JC, Yeo BT. The organization of the human cerebellum estimated by intrinsic functional connectivity. J Neurophysiol. 2011;106(5):2322–45.
Metadaten
Titel
Neural Scaffolding as the Foundation for Stable Performance of Aging Cerebellum
verfasst von
Pavel Filip
Cécile Gallea
Stéphane Lehéricy
Ovidiu Lungu
Martin Bareš
Publikationsdatum
01.06.2019
Verlag
Springer US
Erschienen in
The Cerebellum / Ausgabe 3/2019
Print ISSN: 1473-4222
Elektronische ISSN: 1473-4230
DOI
https://doi.org/10.1007/s12311-019-01015-7

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