期刊论文详细信息
BMC Neuroscience
Effects of a cognitive training on spatial learning and associated functional brain activations
Brigitte Röder2  Thomas Wolbers1  Anna Stenzel2  Kathrin Holzschneider2  Kirsten Hötting2 
[1] German Center for Neurodegenerative Diseases, Leipziger Str. 44, 39120 Magdeburg, Germany;Biological Psychology and Neuropsychology, University of Hamburg, Von-Melle-Park 11, 20146 Hamburg, Germany
关键词: Prevention;    Humans;    fMRI;    Spatial memory;    Cognition;    Cognitive training;    Physical activity;    Exercise;   
Others  :  1140213
DOI  :  10.1186/1471-2202-14-73
 received in 2012-11-16, accepted in 2013-07-10,  发布年份 2013
PDF
【 摘 要 】

Background

Both cognitive and physical exercise have been discussed as promising interventions for healthy cognitive aging. The present study assessed the effects of cognitive training (spatial vs. perceptual training) and physical training (endurance training vs. non-endurance training) on spatial learning and associated brain activation in 33 adults (40–55 years). Spatial learning was assessed with a virtual maze task, and at the same time neural correlates were measured with functional magnetic resonance imaging (fMRI).

Results

Only the spatial training improved performance in the maze task. These behavioral gains were accompanied by a decrease in frontal and temporal lobe activity. At posttest, participants of the spatial training group showed lower activity than participants of the perceptual training group in a network of brain regions associated with spatial learning, including the hippocampus and parahippocampal gyrus. No significant differences were observed between the two physical intervention groups.

Conclusions

Functional changes in neural systems associated with spatial navigation can be induced by cognitive interventions and seem to be stronger than effects of physical exercise in middle-aged adults.

【 授权许可】

   
2013 Hötting et al.; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20150324152414820.pdf 896KB PDF download
Figure 6. 84KB Image download
Figure 5. 42KB Image download
Figure 4. 52KB Image download
Figure 3. 50KB Image download
Figure 2. 35KB Image download
Figure 1. 67KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

【 参考文献 】
  • [1]Hedden T, Gabrieli JD: Insights into the ageing mind: a view from cognitive neuroscience. Nat Rev Neurosci 2004, 5(2):87-96.
  • [2]Gow AJ, Johnson W, Pattie A, Whiteman MC, Starr J, Deary IJ: Mental ability in childhood and cognitive aging. Gerontology 2008, 54(3):177-186.
  • [3]Deary IJ, Gow AJ, Pattie A, Starr JM: Cohort Profile: The Lothian Birth Cohorts of 1921 and 1936. Int J Epidemiol 2012, 41(6):1576-1584.
  • [4]Fillit H, Nash DT, Rundek T, Zuckerman A: Cardiovascular risk factors and dementia. Am J Geriatr Pharmacother 2008, 6(2):100-118.
  • [5]Witte AV, Fobker M, Gellner R, Knecht S, Flöel A: Caloric restriction improves memory in elderly humans. Proc Natl Acad Sci USA 2009, 106(4):1255-1260.
  • [6]Scarmeas N, Stern Y, Tang MX, Mayeux R, Luchsinger JA: Mediterranean diet and risk for Alzheimer's disease. Ann Neurol 2006, 59(6):912-921.
  • [7]Hillman CH, Erickson KI, Kramer AF: Be smart, exercise your heart: exercise effects on brain and cognition. Nat Rev Neurosci 2008, 9(1):58-65.
  • [8]Kramer AF, Willis SL: Enhancing the cognitive vitality of older adults. Curr Dir Psychol Sci 2002, 11:173-176.
  • [9]Abbott RD, White LR, Ross GW, Masaki KH, Curb JD, Petrovitch H: Walking and dementia in physically capable elderly men. JAMA 2004, 292(12):1447-1453.
  • [10]Rovio S, Kareholt I, Helkala EL, Viitanen M, Winblad B, Tuomilehto J, Soininen H, Nissinen A, Kivipelto M: Leisure-time physical activity at midlife and the risk of dementia and Alzheimer's disease. Lancet Neurol 2005, 4(11):705-711.
  • [11]Blumenthal JA, Madden DJ: Effects of aerobic exercise training, age, and physical fitness on memory-search performance. Psychol Aging 1988, 3(3):280-285.
  • [12]Chodzko-Zajko WJ, Schuler P, Solomon J, Heinl B, Ellis NR: The influence of physical fitness on automatic and effortful memory changes in aging. Int J Aging Hum Dev 1992, 35(4):265-285.
  • [13]Erickson KI, Prakash RS, Voss MW, Chaddock L, Hu L, Morris KS, White SM, Wojcicki TR, McAuley E, Kramer AF: Aerobic fitness is associated with hippocampal volume in elderly humans. Hippocampus 2009, 19(10):1030-1039.
  • [14]Erickson KI, Raji CA, Lopez OL, Becker JT, Rosano C, Newman AB, Gach HM, Thompson PM, Ho AJ, Kuller LH: Physical activity predicts gray matter volume in late adulthood: the Cardiovascular Health Study. Neurology 2010, 75(16):1415-1422.
  • [15]Rosano C, Venkatraman VK, Guralnik J, Newman AB, Glynn NW, Launer L, Taylor CA, Williamson J, Studenski S, Pahor M, et al.: Psychomotor speed and functional brain MRI 2 years after completing a physical activity treatment. J Gerontol A Biol Sci Med Sci 2010, 65(6):639-647.
  • [16]Colcombe SJ, Kramer AF, Erickson KI, Scalf P, McAuley E, Cohen NJ, Webb A, Jerome GJ, Marquez DX, Elavsky S: Cardiovascular fitness, cortical plasticity, and aging. Proc Natl Acad Sci U S A 2004, 101(9):3316-3321.
  • [17]Colcombe SJ, Erickson KI, Scalf PE, Kim JS, Prakash R, McAuley E, Elavsky S, Marquez DX, Hu L, Kramer AF: Aerobic exercise training increases brain volume in aging humans. J Gerontol A Biol Sci Med Sci 2006, 61(11):1166-1170.
  • [18]Colcombe S, Kramer AF: Fitness effects on the cognitive function of older adults: a meta-analytic study. Psychol Sci 2003, 14(2):125-130.
  • [19]Kramer AF, Hahn S, Cohen NJ, Banich MT, McAuley E, Harrison CR, Chason J, Vakil E, Bardell L, Boileau RA, et al.: Ageing, fitness and neurocognitive function. Nature 1999, 400(6743):418-419.
  • [20]Ruscheweyh R, Willemer C, Kruger K, Duning T, Warnecke T, Sommer J, Volker K, Ho HV, Mooren F, Knecht S, et al.: Physical activity and memory functions: an interventional study. Neurobiol Aging 2011, 32(7):1304-1319.
  • [21]Hötting K, Reich B, Holzschneider K, Kauschke K, Schmidt T, Reer R, Braumann KM, Röder B: Differential cognitive effects of cycling versus stretching/coordination training in middle-aged adults. Health Psychol 2012, 31(2):145-155.
  • [22]Lautenschlager NT, Cox KL, Flicker L, Foster JK, van Bockxmeer FM, Xiao J, Greenop KR, Almeida OP: Effect of physical activity on cognitive function in older adults at risk for Alzheimer disease: a randomized trial. JAMA 2008, 300(9):1027-1037.
  • [23]Stroth S, Hille K, Spitzer M, Reinhardt R: Aerobic endurance exercise benefits memory and affect in young adults. Neuropsychol Rehabil 2009, 19(2):223-243.
  • [24]Pereira AC, Huddleston DE, Brickman AM, Sosunov AA, Hen R, McKhann GM, Sloan R, Gage FH, Brown TR, Small SA: An in vivo correlate of exercise-induced neurogenesis in the adult dentate gyrus. Proc Natl Acad Sci U S A 2007, 104(13):5638-5643.
  • [25]Erickson KI, Voss MW, Prakash RS, Basak C, Szabo A, Chaddock L, Kim JS, Heo S, Alves H, White SM, et al.: Exercise training increases size of hippocampus and improves memory. Proc Natl Acad Sci U S A 2011, 108(7):3017-3022.
  • [26]Burdette JH, Laurienti PJ, Espeland MA, Morgan A, Telesford Q, Vechlekar CD, Hayasaka S, Jennings JM, Katula JA, Kraft RA, et al.: Using network science to evaluate exercise-associated brain changes in older adults. Front Aging Neurosci 2010, 2:23.
  • [27]Voss MW, Prakash RS, Erickson KI, Basak C, Chaddock L, Kim JS, Alves H, Heo S, Szabo AN, White SM, et al.: Plasticity of brain networks in a randomized intervention trial of exercise training in older adults. Front Aging Neurosci 2010, 2:article 21.
  • [28]Dahlin E, Neely AS, Larsson A, Backman L, Nyberg L: Transfer of learning after updating training mediated by the striatum. Science 2008, 320(5882):1510-1512.
  • [29]Edwards JD, Wadley VG, Vance DE, Wood K, Roenker DL, Ball KK: The impact of speed of processing training on cognitive and everyday performance. Aging Ment Health 2005, 9(3):262-271.
  • [30]Boron JB, Turiano NA, Willis SL, Schaie KW: Effects of cognitive training on change in accuracy in inductive reasoning ability. J Gerontol B Psychol Sci Soc Sci 2007, 62(3):P179-186.
  • [31]Persson J, Reuter-Lorenz PA: Gaining control: training executive function and far transfer of the ability to resolve interference. Psychol Sci 2008, 19(9):881-888.
  • [32]Lövden M, Backman L, Lindenberger U, Schaefer S, Schmiedek F: A theoretical framework for the study of adult cognitive plasticity. Psychol Bull 2010, 136(4):659-676.
  • [33]Feng J, Spence I, Pratt J: Playing an action video game reduces gender differences in spatial cognition. Psychol Sci 2007, 18(10):850-855.
  • [34]Iaria G, Petrides M, Dagher A, Pike B, Bohbot VD: Cognitive strategies dependent on the hippocampus and caudate nucleus in human navigation: variability and change with practice. J Neurosci 2003, 23(13):5945-5952.
  • [35]Willis SL, Schaie KW: Training the elderly on the ability factors of spatial orientation and inductive reasoning. Psychol Aging 1986, 1(3):239-247.
  • [36]Lövden M, Schaefer S, Noack H, Bodammer NC, Kuhn S, Heinze HJ, Duzel E, Backman L, Lindenberger U: Spatial navigation training protects the hippocampus against age-related changes during early and late adulthood. Neurobiol Aging 2012, 33(3):620.e9-620.e22.
  • [37]Woollett K, Maguire EA: Acquiring "the Knowledge" of London's Layout Drives Structural Brain Changes. Curr Biol 2011, 21(24):2109-2114.
  • [38]Poldrack RA: Imaging brain plasticity: conceptual and methodological issues–a theoretical review. Neuroimage 2000, 12(1):1-13.
  • [39]Kelly AM, Garavan H: Human functional neuroimaging of brain changes associated with practice. Cereb Cortex 2005, 15(8):1089-1102.
  • [40]Rauchs G, Orban P, Balteau E, Schmidt C, Degueldre C, Luxen A, Maquet P, Peigneux P: Partially segregated neural networks for spatial and contextual memory in virtual navigation. Hippocampus 2008, 18(5):503-518.
  • [41]Ohnishi T, Matsuda H, Hirakata M, Ugawa Y: Navigation ability dependent neural activation in the human brain: an fMRI study. Neurosci Res 2006, 55(4):361-369.
  • [42]Gould E, Beylin A, Tanapat P, Reeves A, Shors TJ: Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci 1999, 2(3):260-265.
  • [43]van Praag H, Kempermann G, Gage FH: Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 1999, 2(3):266-270.
  • [44]Kesslak JP, So V, Choi J, Cotman CW, Gomez-Pinilla F: Learning upregulates brain-derived neurotrophic factor messenger ribonucleic acid: a mechanism to facilitate encoding and circuit maintenance? Behav Neurosci 1998, 112(4):1012-1019.
  • [45]Vaynman S, Ying Z, Gomez-Pinilla F: Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition. Eur J Neurosci 2004, 20(10):2580-2590.
  • [46]Uysal N, Tugyan K, Kayatekin BM, Acikgoz O, Bagriyanik HA, Gonenc S, Ozdemir D, Aksu I, Topcu A, Semin I: The effects of regular aerobic exercise in adolescent period on hippocampal neuron density, apoptosis and spatial memory. Neurosci Lett 2005, 383(3):241-245.
  • [47]van Praag H, Shubert T, Zhao C, Gage FH: Exercise enhances learning and hippocampal neurogenesis in aged mice. J Neurosci 2005, 25(38):8680-8685.
  • [48]Kempermann G, Fabel K, Ehninger D, Babu H, Leal-Galicia P, Garthe A, Wolf SA: Why and how physical activity promotes experience-induced brain plasticity. Front Neurosci 2010, 4:189.
  • [49]Kempermann G: The neurogenic reserve hypothesis: what is adult hippocampal neurogenesis good for? Trends Neurosci 2008, 31(4):163-169.
  • [50]Fabel K, Wolf SA, Ehninger D, Babu H, Leal-Galicia P, Kempermann G: Additive effects of physical exercise and environmental enrichment on adult hippocampal neurogenesis in mice. Front Neurosci 2009, 3:50.
  • [51]Fabre C, Chamari K, Mucci P, Masse-Biron J, Prefaut C: Improvement of cognitive function by mental and/or individualized aerobic training in healthy elderly subjects. Int J Sports Med 2002, 23(6):415-421.
  • [52]Rovio S, Spulber G, Nieminen LJ, Niskanen E, Winblad B, Tuomilehto J, Nissinen A, Soininen H, Kivipelto M: The effect of midlife physical activity on structural brain changes in the elderly. Neurobiol Aging 2010, 31(11):1927-1936.
  • [53]Wolbers T, Buchel C: Dissociable retrosplenial and hippocampal contributions to successful formation of survey representations. J Neurosci 2005, 25(13):3333-3340.
  • [54]Holzschneider K, Wolbers T, Röder B, Hötting K: Cardiovascular fitness modulates brain activation associated with spatial learning. Neuroimage 2012, 59(3):3003-3014.
  • [55]Ekstrom AD, Kahana MJ, Caplan JB, Fields TA, Isham EA, Newman EL, Fried I: Cellular networks underlying human spatial navigation. Nature 2003, 425(6954):184-188.
  • [56]Burgess N, Maguire EA, O'Keefe J: The human hippocampus and spatial and episodic memory. Neuron 2002, 35(4):625-641.
  • [57]Epstein RA: Parahippocampal and retrosplenial contributions to human spatial navigation. Trends Cogn Sci 2008, 12(10):388-396.
  • [58]Hartley T, Maguire EA, Spiers HJ, Burgess N: The well-worn route and the path less traveled: distinct neural bases of route following and wayfinding in humans. Neuron 2003, 37(5):877-888.
  • [59]Shelton AL, Gabrieli JD: Neural correlates of encoding space from route and survey perspectives. J Neurosci 2002, 22(7):2711-2717.
  • [60]Lehrl S: Mehrfachwahl-Wortschatz-Intelligenztest MWT-B. Balingen, Germany: Spitta Verlag; 2005.
  • [61]Lehrl S, Triebig G, Fischer B: Multiple choice vocabulary test MWT as a valid and short test to estimate premorbid intelligence. Acta Neurol Scand 1995, 91(5):335-345.
  • [62]Helmstädter C, Lendt M, Lux S: Verbaler Lern- und Merkfähigkeitstest (VLMT). Göttingen, Germany: Hogrefe; 2001.
  • [63]Bäumler G: Farbe-Wort-Interferenztest (FWIT) nach J.R. Stroop. Göttingen, Germany: Hogrefe; 1985.
  • [64]Stroop JR: Studies of interference in serial verbal reaction. J Exp Psychol 1935, 18:643-662.
  • [65]King JA, Burgess N, Hartley T, Vargha-Khadem F, O'Keefe J: Human hippocampus and viewpoint dependence in spatial memory. Hippocampus 2002, 12(6):811-820.
  • [66]Wolbers T, Wiener JM, Mallot HA, Buchel C: Differential recruitment of the hippocampus, medial prefrontal cortex, and the human motion complex during path integration in humans. J Neurosci 2007, 27(35):9408-9416.
  • [67]Karni A, Sagi D: Where Practice Makes Perfect in Texture Discrimination: Evidence for Primary Visual Cortex Plasticity. PNAS 1991, 88(11):4966-4970.
  • [68]Fahle M, Daum I: Perceptual learning in amnesia. Neuropsychologia 2002, 40(8):1167-1172.
  • [69]Team RDC: R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2011.
  • [70]Ashburner J, Friston KJ: Unified segmentation. Neuroimage 2005, 26(3):839-851.
  • [71]Wolbers T, Weiller C, Buchel C: Neural foundations of emerging route knowledge in complex spatial environments. Brain Res Cogn Brain Res 2004, 21(3):401-411.
  • [72]Lancaster JL, Rainey LH, Summerlin JL, Freitas CS, Fox PT, Evans AC, Toga AW, Mazziotta JC: Automated labeling of the human brain: a preliminary report on the development and evaluation of a forward-transform method. Hum Brain Mapp 1997, 5(4):238-242.
  • [73]Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M: Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 2002, 15(1):273-289.
  • [74]Nielsen FA: The Brede database: a small database for functional neuroimaging. Neuroimage 2003, 19(Supplement):e1788.
  • [75]Barnett SM, Ceci SJ: When and where do we apply what we learn? A taxonomy for far transfer. Psychol Bull 2002, 128(4):612-637.
  • [76]Tronel S, Fabre A, Charrier V, Oliet SH, Gage FH, Abrous DN: Spatial learning sculpts the dendritic arbor of adult-born hippocampal neurons. Proc Natl Acad Sci U S A 2010, 107(17):7963-7968.
  • [77]Waller D: Individual differences in spatial learning from computer-simulated environments. J Exp Psychol Appl 2000, 6(4):307-321.
  • [78]Ojemann GA, Schoenfield-McNeill J, Corina DP: Anatomic subdivisions in human temporal cortical neuronal activity related to recent verbal memory. Nat Neurosci 2002, 5(1):64-71.
  • [79]Amorapanth PX, Widick P, Chatterjee A: The neural basis for spatial relations. J Cogn Neurosci 2010, 22(8):1739-1753.
  • [80]Jordan K, Schadow J, Wuestenberg T, Heinze HJ, Jäncke L: Different cortical activations for subjects using allocentric or egocentric strategies in a virtual navigation task. Neuroreport 2004, 15(1):135-140.
  • [81]Iaria G, Lanyon LJ, Fox CJ, Giaschi D, Barton JJ: Navigational skills correlate with hippocampal fractional anisotropy in humans. Hippocampus 2008, 18(4):335-339.
  • [82]Maguire EA, Gadian DG, Johnsrude IS, Good CD, Ashburner J, Frackowiak RS, Frith CD: Navigation-related structural change in the hippocampi of taxi drivers. Proc Natl Acad Sci U S A 2000, 97(8):4398-4403.
  • [83]Moffat SD, Kennedy KM, Rodrigue KM, Raz N: Extrahippocampal contributions to age differences in human spatial navigation. Cereb Cortex 2007, 17(6):1274-1282.
  • [84]Maguire EA, Burgess N, Donnett JG, Frackowiak RS, Frith CD, O'Keefe J: Knowing where and getting there: a human navigation network. Science 1998, 280(5365):921-924.
  • [85]Moffat SD, Elkins W, Resnick SM: Age differences in the neural systems supporting human allocentric spatial navigation. Neurobiol Aging 2006, 27(7):965-972.
  • [86]Antonova E, Parslow D, Brammer M, Dawson GR, Jackson SH, Morris RG: Age-related neural activity during allocentric spatial memory. Memory 2009, 17(2):125-143.
  • [87]Wood JN, Grafman J: Human prefrontal cortex: processing and representational perspectives. Nat Rev Neurosci 2003, 4(2):139-147.
  • [88]Voelcker-Rehage C, Godde B, Staudinger UM: Physical and motor fitness are both related to cognition in old age. Eur J Neurosci 2010, 31(1):167-176.
  • [89]Liu-Ambrose T, Nagamatsu LS, Voss MW, Khan KM, Handy TC: Resistance training and functional plasticity of the aging brain: a 12-month randomized controlled trial. Neurobiol Aging 2012, 33(8):1690-1698.
  • [90]Moffat SD, Zonderman AB, Resnick SM: Age differences in spatial memory in a virtual environment navigation task. Neurobiol Aging 2001, 22(5):787-796.
  • [91]Driscoll I, Hamilton DA, Yeo RA, Brooks WM, Sutherland RJ: Virtual navigation in humans: the impact of age, sex, and hormones on place learning. Horm Behav 2005, 47(3):326-335.
  文献评价指标  
  下载次数:34次 浏览次数:11次