Abstract
Declines in both cortical grey matter and bimanual coordination performance are evident in healthy ageing. However, the relationship between ageing, bimanual performance, and grey matter loss remains unclear, particularly across the whole adult lifespan. Therefore, participants (N = 93, range 20–80 years) performed a complex Bimanual Tracking Task, and structural brain images were obtained using magnetic resonance imaging. Analyses revealed that age correlated negatively with task performance. Voxel-based morphometry analysis revealed that age was associated with grey matter declines in task-relevant cortical areas and that grey matter in these areas was negatively associated with task performance. However, no evidence for a mediating effect of grey matter in age-related bimanual performance decline was observed. We propose a new hypothesis that functional compensation may account for the observed absence of mediation, which is in line with the observed pattern of increased inter-individual variance in performance with age.
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References
Ashburner J, Friston KJ (2000) Voxel-based morphometry—the methods. Neuroimage 11:805–821. doi:10.1006/nimg.2000.0582
Bangert AS, Reuter-Lorenz PA, Walsh CM, Schachter AB, Seidler RD (2010) Bimanual coordination and aging: neurobehavioral implications. Neuropsychologia 48:1165–1170. doi:10.1016/j.neuropsychologia.2009.11.013
Beets IA, Gooijers J, Boisgontier MP, Pauwels L, Coxon JP, Wittenberg G, Swinnen SP (2014) Reduced neural differentiation between feedback conditions after bimanual coordination training with and without augmented visual feedback. Cereb Cortex. doi:10.1093/cercor/bhu005
Brett M, Anton JL, valabregue R, Poline JB (2002) Region of interest analysis using an SPM toolbox [abstract]. Presented at the 8th international conference on functional mapping of the human brain, Sendai, Japan, 2–6 June 2002. Available on CD-ROM in NeuroImage, vol 16, No 2, abstract 497
Courchesne E et al (2000) Normal brain development and aging: quantitative analysis at in vivo MR imaging in healthy volunteers. Radiology 216:672–682. doi:10.1148/radiology.216.3.r00au37672
Dijkerman HC, de Haan EH (2007) Somatosensory processes subserving perception and action. Behav Brain Sci 30:189–201. doi:10.1017/S0140525X07001392 (discussion 201–139)
Ferreira D et al (2013) Cognitive decline is mediated by gray matter changes during middle-age. Neurobiol Aging. doi:10.1016/j.neurobiolaging.2013.10.095
Goble DJ, Coxon JP, Wenderoth N, Van Impe A, Swinnen SP (2009) Proprioceptive sensibility in the elderly: degeneration, functional consequences and plastic-adaptive processes. Neurosci Biobehav Rev 33:271–278. doi:10.1016/j.neubiorev.2008.08.012
Goble DJ, Coxon JP, Van Impe A, De Vos J, Wenderoth N, Swinnen SP (2010) The neural control of bimanual movements in the elderly: brain regions exhibiting age-related increases in activity, frequency-induced neural modulation, and task-specific compensatory recruitment. Hum Brain Mapp 31:1281–1295. doi:10.1002/hbm.20943
Good CD, Johnsrude IS, Ashburner J, Henson RN, Friston KJ, Frackowiak RS (2001) A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage 14:21–36. doi:10.1006/nimg.2001.0786
Gunning-Dixon FM, Brickman AM, Cheng JC, Alexopoulos GS (2009) Aging of cerebral white matter: a review of MRI findings. Int J Geriatr Psychiatry 24:109–117. doi:10.1002/gps.2087
Hafkemeijer A, Altmann-Schneider I, de Craen AJ, Slagboom PE, van der Grond J, Rombouts SA (2014) Associations between age and gray matter volume in anatomical brain networks in middle-aged to older adults. Aging Cell 13:1068–1074. doi:10.1111/acel.12271
Hayes AF (2013) Introduction to mediation, moderation, and conditional process analysis; a regression-based approach. Methodology in the social sciences. The Guilford Press, New York
Hultsch DF, MacDonald SW, Dixon RA (2002) Variability in reaction time performance of younger and older adults. J Gerontol B Psychol Sci Soc Sci 57:P101–P115
Jenkinson M, Smith S (2001) A global optimisation method for robust affine registration of brain images. Med Image Anal 5:143–156
Jenkinson M, Bannister P, Brady M, Smith S (2002) Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17:825–841
Jenkinson M, Beckmann CF, Behrens TE, Woolrich MW, Smith SM (2012) Fsl Neuroimage 62:782–790. doi:10.1016/j.neuroimage.2011.09.015
Jernigan TL, Archibald SL, Fennema-Notestine C, Gamst AC, Stout JC, Bonner J, Hesselink JR (2001) Effects of age on tissues and regions of the cerebrum and cerebellum. Neurobiol Aging 22:581–594
Nichols TE, Holmes AP (2001) Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp 15:1–25
Nichols T, Brett M, Andersson J, Wager T, Poline JB (2005) Valid conjunction inference with the minimum statistic. Neuroimage 25:653–660. doi:10.1016/j.neuroimage.2004.12.005
Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113
Patenaude B, Smith SM, Kennedy DN, Jenkinson M (2011) A Bayesian model of shape and appearance for subcortical brain segmentation. Neuroimage 56:907–922. doi:10.1016/j.neuroimage.2011.02.046
Pauwels L, Vancleef K, Swinnen SP, Beets IA (2015) Challenge to promote change: both young and older adults benefit from contextual interference. Front Aging Neurosci 7:157. doi:10.3389/fnagi.2015.00157
Pfefferbaum A, Rohlfing T, Rosenbloom MJ, Chu W, Colrain IM, Sullivan EV (2013) Variation in longitudinal trajectories of regional brain volumes of healthy men and women (ages 10–85 years) measured with atlas-based parcellation of MRI. Neuroimage 65:176–193. doi:10.1016/j.neuroimage.2012.10.008
Raz N et al (1997) Selective aging of the human cerebral cortex observed in vivo: differential vulnerability of the prefrontal gray matter. Cereb Cortex 7:268–282
Raz N, Gunning-Dixon F, Head D, Rodrigue KM, Williamson A, Acker JD (2004) Aging, sexual dimorphism, and hemispheric asymmetry of the cerebral cortex: replicability of regional differences in volume. Neurobiol Aging 25:377–396. doi:10.1016/S0197-4580(03)00118-0
Raz N et al (2005) Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. Cereb Cortex 15:1676–1689. doi:10.1093/cercor/bhi044
Reuter-Lorenz PA, Cappell KA (2008) Neurocognitive aging and the compensation hypothesis. Curr Dir Psychol Sci 17:177–182
Ridgway G, Barnes J, Pepple T, Fox N (2011) Estimation of total intracranial volume; a comparison of methods. Alzheimer’s Dement 7:S62–S63
Rorden C, Brett M (2000) Stereotaxic display of brain lesions. Behav Neurol 12:191–200
Salat DH et al (2004) Thinning of the cerebral cortex in aging. Cereb Cortex 14:721–730. doi:10.1093/cercor/bhh032
Salthouse TA (2011) Neuroanatomical substrates of age-related cognitive decline. Psychol Bull 137:753–784. doi:10.1037/a0023262
Seidler RD et al (2010) Motor control and aging: links to age-related brain structural, functional, and biochemical effects. Neurosci Biobehav Rev 34:721–733. doi:10.1016/j.neubiorev.2009.10.005
Serbruyns L et al (2013) Bimanual motor deficits in older adults predicted by diffusion tensor imaging metrics of corpus callosum subregions. Brain Struct Funct. doi:10.1007/s00429-013-0654-z
Serbruyns L et al (2015a) Bimanual motor deficits in older adults predicted by diffusion tensor imaging metrics of corpus callosum subregions. Brain Struct Funct 220:273–290. doi:10.1007/s00429-013-0654-z
Serbruyns L et al (2015b) Subcortical volumetric changes across the adult lifespan: subregional thalamic atrophy accounts for age-related sensorimotor performance declines. Cortex 65:128–138. doi:10.1016/j.cortex.2015.01.003
Serrien DJ, Swinnen SP, Stelmach GE (2000) Age-related deterioration of coordinated interlimb behavior. J Gerontol B Psychol Sci Soc Sci 55:P295–P303
Sisti HM et al (2011) Testing multiple coordination constraints with a novel bimanual visuomotor task. PLoS One 6:e23619. doi:10.1371/journal.pone.0023619
Sisti HM et al (2012) Microstructural organization of corpus callosum projections to prefrontal cortex predicts bimanual motor learning. Learn Mem 19:351–357. doi:10.1101/lm.026534.112
Smith SM (2002) Fast robust automated brain extraction. Hum Brain Mapp 17:143–155. doi:10.1002/hbm.10062
Solesio-Jofre E, Serbruyns L, Woolley DG, Mantini D, Beets IA, Swinnen SP (2014) Aging effects on the resting state motor network and interlimb coordination. Hum Brain Mapp. doi:10.1002/hbm.22450
Sowell ER, Peterson BS, Thompson PM, Welcome SE, Henkenius AL, Toga AW (2003) Mapping cortical change across the human life span. Nat Neurosci 6:309–315. doi:10.1038/nn1008
Swinnen SP, Jardin K, Verschueren S, Meulenbroek R, Franz L, Dounskaia N, Walter CB (1998) Exploring interlimb constraints during bimanual graphic performance: effects of muscle grouping and direction. Behav Brain Res 90:79–87
Tisserand DJ, Pruessner JC, Sanz Arigita EJ, van Boxtel MP, Evans AC, Jolles J, Uylings HB (2002) Regional frontal cortical volumes decrease differentially in aging: an MRI study to compare volumetric approaches and voxel-based morphometry. Neuroimage 17:657–669
Wishart LR, Lee TD, Murdoch JE, Hodges NJ (2000) Effects of aging on automatic and effortful processes in bimanual coordination. J Gerontol B Psychol Sci Soc Sci 55:P85–P94
Woolrich MW et al (2009) Bayesian analysis of neuroimaging data in FSL. Neuroimage 45:S173–S186. doi:10.1016/j.neuroimage.2008.10.055
World-Medical-Association (1964, 2008) World Medical Association Declaration of Helsinki: Ethical principles for medical research involving human subjects
Zhang Y, Brady M, Smith S (2001) Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Trans Med Imaging 20:45–57. doi:10.1109/42.906424
Acknowledgments
This work was supported by the Interuniversity Attraction Poles Programme initiated by the Belgian Science Policy (P7/11); Research Fund KU Leuven (C16/15/070.); and FWO Vlaanderen (G.0721.12, G0708.14).
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van Ruitenbeek, P., Serbruyns, L., Solesio-Jofre, E. et al. Cortical grey matter content is associated with both age and bimanual performance, but is not observed to mediate age-related behavioural decline. Brain Struct Funct 222, 437–448 (2017). https://doi.org/10.1007/s00429-016-1226-9
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DOI: https://doi.org/10.1007/s00429-016-1226-9