Abstract
Aging is associated with cognitive decline and decreased capacity to inhibit distracting information. Video game training holds promise to increase inhibitory mechanisms in older adults. In the current study, we tested the impact of 3D-platform video game training on performance in an antisaccade task and on related changes in grey matter within the frontal eye fields (FEFs) of older adults. An experimental group (VID group) engaged in 3D-platform video game training over a period of 6 months, while an active control group was trained on piano lessons (MUS group), and a no-contact control group did not participate in any intervention (CON group). Increased performance in oculomotor inhibition, as measured by the antisaccade task, and increased grey matter in the right FEF was observed uniquely in the VID group. These results demonstrate that 3D-platform video game training can improve inhibitory control known to decline with age.
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References
Andres P, Van der Linden M (2000) Age-related differences in supervisory attentional system functions. J Gerontol Ser B Psychol Sci Soc Sci 55(6):P373–P380. https://doi.org/10.1093/geronb/55.6.P373
Anguera JA, Boccanfuso J, Rintoul JL, Al-Hashimi O, Faraji F, Janowich J, Gazzaley A (2013) Video game training enhances cognitive control in older adults. Nature 501(7465):97–101. https://doi.org/10.1038/nature12486
Antoniades CA, Demeyere N, Kennard C, Humphreys GW, Hu MT (2015) Antisaccades and executive dysfunction in early drug-naive Parkinson’s disease: The discovery study. Mov Disord 30(6):843–847
Ashburner J, Friston KJ (2000) Voxel-based morphometry—the methods. NeuroImage 11(6):805–821. https://doi.org/10.1006/nimg.2000.0582
Basak C, Boot WR, Voss MW, Kramer AF (2008) Can training in a real-time strategy video game attenuate cognitive decline in older adults? Psychol Aging 23(4):765–777. https://doi.org/10.1037/a0013494
Bohbot VD, Lerch J, Thorndycraft B, Iaria G, Zijdenbos AP (2007) Gray matter differences correlate with spontaneous strategies in a human virtual navigation task. J Neurosci 27(38):10078–10083. https://doi.org/10.1523/JNEUROSCI.1763-07.2007
Bowling AC, Hindman EA, Donnelly JF (2012) Prosaccade errors in the antisaccade task: differences between corrected and uncorrected errors and links to neuropsychological tests. Exp Brain Res 216(2):169–179. https://doi.org/10.1007/s00221-011-2921-7
Boxer AL, Garbutt S, Seeley WW, Jafari A, Heuer HW, Mirsky J, Miller BL (2012) Saccade abnormalities in autopsy-confirmed frontotemporal lobar degeneration and alzheimer disease. Arch Neurol 69(4):509–517. https://doi.org/10.1001/archneurol.2011.1021
Butler KM, Zacks RT, Henderson JM (1999) Suppression of reflexive saccades in younger and older adults: age comparisons on an antisaccade task. Memory Cognition 27(4):584–591. https://doi.org/10.3758/BF03211552
Castel AD, Pratt J, Drummond E (2005) The effects of action video game experience on the time course of inhibition of return and the efficiency of visual search. Acta Physiol (Oxf) 119(2):217–230. https://doi.org/10.1016/j.actpsy.2005.02.004
Chisholm JD, Kingstone A (2012) Improved top-down control reduces oculomotor capture: the case of action video game players. Atten Percept Psychophys 74(2):257–262. https://doi.org/10.3758/s13414-011-0253-0
Cormier SM, Hagman JD (2014) Transfer of learning: contemporary research and applications. Elsevier Science, Consulté à l’adresse. https://books.google.ca/books?id=p_vSAwAAQBAJ
Crawford TJ, Higham CS, Renvoize T, Patel J, Dale M, Suriya A, Tetley S (2005) Inhibitory control of saccadic eye movements and cognitive impairment in Alzheimer’s disease. Biol Psychiatry 57:1052–1060
Eskildsen SF, Coupé P, Fonov V, Manjón JV, Leung KK, Guizard N, Collins DL (2012) BEaST: brain extraction based on nonlocal segmentation technique. NeuroImage 59(3):2362–2373. https://doi.org/10.1016/j.neuroimage.2011.09.012
Ettinger U, Antonova E, Crawford TJ, Mitterschiffthaler MT, Goswani S, Sharma T, Kumari V (2005) Structural neural correlates of prosaccade and antisaccade eye movements in healthy humans. Neuroimage 24:487–494
Everling S, Fischer B (1998) The antisaccade: a review of basic research and clinical studies. Neuropsychologia 36(9):885–899. https://doi.org/10.1016/S0028-3932(98)00020-7
Feng J, Spence I, Pratt J (2007) Playing an action video game reduces gender differences in spatial cognition. Psychol Sci 18(10):850–855. https://doi.org/10.1111/j.1467-9280.2007.01990
Filippi M, Horsfield M, Hajnal J, Narayana P, Udupa J, Yousry T, Zijdenbos A (1998) Quantitative assessment of magnetic resonance imaging lesion load in multiple sclerosis. J Neurol Neurosurg Psychiatry 64(Suppl 1):S88–S93
Gozli DG, Bavelier D, Pratt J (2014) The effect of action video game playing on sensorimotor learning: evidence from a movement tracking task. Hum Mov Sci 38:152–162. https://doi.org/10.1016/j.humov.2014.09.004
Green CS, Bavelier D (2003) Action video game modifies visual selective attention. Nature 423(6939):534–537. https://doi.org/10.1038/nature01647
Green CS, Bavelier D (2007) Action-video-game experience alters the spatial resolution of vision. Psychol Sci 18(1):88–94. https://doi.org/10.1111/j.1467-9280.2007.01853.x
Hallett PE (1978) Primary and secondary saccades to goals defined by instructions. Vis Res 18(10):1279–1296. https://doi.org/10.1016/0042-6989(78)90218-3
Hasher L, Zacks RT, May CP (1999) Inhibitory control, circadian arousal, and age. In: Attention and performance XVII: cognitive regulation of performance: interaction of theory and application. pp 653–675
Hellmuth J, Mirsky J, Heuer HW, Matlin A, Jafari A, Garbutt S, Boxer AL (2012) Multicenter validation of a bedside antisaccade task as a measure of executive function. Neurology 78(23):1824–1831. https://doi.org/10.1212/WNL.0b013e318258f785
Hood AJ, Amador SC, Cain AE, Briand KA, Al-Refai AH, Schiess MC, Sereno AB (2007) Levodopa slows prosaccades and improves antisaccades: an eye movement study in Parkinson’s disease. J Neurol Neurosurg Psychiatry 78(6):565–570
Hutton SB, Ettinger U (2006) The antisaccade task as a research tool in psychopathology: a critical review. Psychophysiology 43(3):302–313
Iaria G, Petrides M, Dagher A, Pike B, Bohbot VD (2003) Cognitive strategies dependent on the hippocampus and caudate nucleus in human navigation: variability and change with practice. J Neurosci 23(13):5945. https://doi.org/10.1523/JNEUROSCI.23-13-05945.2003
Kaufman LD, Pratt J, Levine B, Black SE (2012) Executive deficits detected in mild Alzheimer’s disease using the antisaccade task. Brain Behav 2:15–21
Konishi K, Bohbot VD (2013) Spatial navigational strategies correlate with gray matter in the hippocampus of healthy older adults tested in a virtual maze. Front Aging Neurosci 5:1. https://doi.org/10.3389/fnagi.2013.00001
Kühn S, Gleich T, Lorenz RC, Lindenberger U, Gallinat J (2014) Playing Super Mario induces structural brain plasticity: gray matter changes resulting from training with a commercial video game. Mol Psychiatry 19(2):265–271. https://doi.org/10.1038/mp.2013.120
Miller EK (2000) The prefontral cortex and cognitive control. Nat Rev Neurosci 1(1):59–65. https://doi.org/10.1038/35036228
Mirsky JB, Heuer HW, Jafari A, Kramer JH, Schenk AK, Viskontas IV, Boxer AL (2011) Anti-saccade performance predicts executive function and brain structure in normal elders. Cognit Behav Neurol 24(2):50–58. https://doi.org/10.1097/WNN.0b013e318223f6c6
Munoz DP, Everling S (2004) Look away: the anti-saccade task and the voluntary control of eye movement. Nat Rev Neurosci 5(3):218–228. https://doi.org/10.1038/nrn1345
Nasreddine ZS, Phillips NA, Bédirian V, Charbonneau S, Whitehead V, Collin I, Chertkow H (2005) The montreal cognitive assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc 53(4):695–699. https://doi.org/10.1111/j.1532-5415.2005.53221
Nieuwenhuis S, Ridderinkhof KR, de Jong R, Kok A, van der Molen MW (2000) Inhibitory inefficiency and failures of intention activation: age-related decline in the control of saccadic eye movements. Psychol Aging 15(4):635–647. https://doi.org/10.1037/0882-7974.15.4.635
Nieuwenhuis S, Broerse A, Nielen MMA, Jong R (2004) A goal activation approach to the study of executive function: an application to antisaccade tasks. Neurocognit Mech Perform Monit Inhib Control 56(2):198–214. https://doi.org/10.1016/j.bandc.2003.12.002
Olincy A, Ross R, Youngd D, Freedman R (1997) Age diminishes performance on an antisaccade eye movement task. Neurobiol Aging 18(5):483–489. https://doi.org/10.1016/S0197-4580(97)00109-7
Sadedin SP, Pope B, Oshlack A (2012) Bpipe: a tool for running and managing bioinformatics pipelines. Bioinformatics 28(11):1525–1526. https://doi.org/10.1093/bioinformatics/bts167
Strobach T, Frensch PA, Schubert T (2012) Video game practice optimizes executive control skills in dual-task and task switching situations. Acta Physiol (Oxf) 140(1):13–24. https://doi.org/10.1016/j.actpsy.2012.02.001
Sweeney JA, Rosano C, Berman RA, Luna B (2001) Inhibitory control of attention declines more than working memory during normal aging. Neurobiol Aging 22(1):39–47. https://doi.org/10.1016/S0197-4580(00)00175-5
Wecker NS, Kramer JH, Wisniewski A, Delis DC, Kaplan E (2000) Age effects on executive ability. Neuropsychology 14(3):409–414. https://doi.org/10.1037/0894-4105.14.3.409
West GL, Stevens SA, Pun C, Pratt J (2008) Visuospatial experience modulates attentional capture: evidence from action video game players. J Vis 8(16):13–13. https://doi.org/10.1167/8.16.13
West GL, Al-Aidroos N, Pratt J (2013) Action video game experience affects oculomotor performance. Acta Physiol (Oxf) 142(1):38–42. https://doi.org/10.1016/j.actpsy.2011.08.005
West GL, Drisdelle BL, Konishi K, Jackson J, Jolicoeur P, Bohbot VD (2015) Habitual action video game playing is associated with caudate nucleus-dependent navigational strategies. Proc R Soc B Biol Sci 282(1808):20142952–20142952. https://doi.org/10.1098/rspb.2014.2952
West GL, Konishi K, Diarra M, Benady-Chorney J, Drisdelle BL, Dahmani L, Bohbot VD (2017a) Impact of video games on plasticity of the hippocampus. Mol Psychiatry. https://doi.org/10.1038/mp.2017.155
West GL, Zendel BR, Konishi K, Benady-Chorney J, Bohbot VD et al (2017b) Playing Super Mario 64 increases hippocampal grey matter in older adults. PLOS ONE 12(12):e0187779. https://doi.org/10.1371/journal.pone.0187779
Winocur G, Craik FIM, Levine B, Robertson IH, Binns MA, Alexander M, Stuss DT (2007) Cognitive rehabilitation in the elderly: overview and future directions. J Int Neuropsychol Soc 13(01):166–171. https://doi.org/10.1017/S1355617707070191
Wolfe PL, Lehockey KA (2016) Neuropsychological assessment of driving capacity. Arch Clin Neuropsychol 31(6):517–529. https://doi.org/10.1093/arclin/acw050
Yoon U, Fonov VS, Perusse D, Evans AC (2009) The effect of template choice on morphometric analysis of pediatric brain data. NeuroImage 45(3):769–777. https://doi.org/10.1016/j.neuroimage.2008.12.046
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This project was supported by a Canadian Institutes of Health Research Grant: http://www.cihr-irsc.gc.ca/e/193.html to Sylvie Belleville and a Natural science and engineering research council of Canada grant to Greg L West (436140-2013): http://www.nserc-crsng.gc.ca/index_eng.asp.
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Diarra, M., Zendel, B.R., Benady-Chorney, J. et al. Playing Super Mario increases oculomotor inhibition and frontal eye field grey matter in older adults. Exp Brain Res 237, 723–733 (2019). https://doi.org/10.1007/s00221-018-5453-6
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DOI: https://doi.org/10.1007/s00221-018-5453-6