Training-induced brain structure changes in the elderly

Janina Boyke, Joenna Driemeyer, Christian Gaser, Christian Büchel, Arne May, Janina Boyke, Joenna Driemeyer, Christian Gaser, Christian Büchel, Arne May

Abstract

It has been suggested that learning is associated with a transient and highly selective increase in brain gray matter in healthy young volunteers. It is not clear whether and to what extent the aging brain is still able to exhibit such structural plasticity. We built on our original study, now focusing on healthy senior citizens. We observed that elderly persons were able to learn three-ball cascade juggling, but with less proficiency compared with 20-year-old adolescents. Similar to the young group, gray-matter changes in the older brain related to skill acquisition were observed in area hMT/V5 (middle temporal area of the visual cortex). In addition, elderly volunteers who learned to juggle showed transient increases in gray matter in the hippocampus on the left side and in the nucleus accumbens bilaterally.

Figures

Figure 1.
Figure 1.
Flow chart of volunteer recruitment. Only 10 of 44 individuals were able to juggle 60 s at time point 2. Fifteen volunteers were fluent jugglers and accomplished between 40 and 60 s. We therefore compared the data of 25 individuals of the jugglers group who had the best results in endurance juggling (mean time, 56.7 s) with the data sets of the 25 controls.
Figure 2.
Figure 2.
Time point (before intervention, after intervention) by group (jugglers, controls) interaction analysis, testing for greater changes in the jugglers group. Gray-matter increase is shown superimposed on a normalized T1 image. The left side of the picture is the left side of the brain. A, A significant gray-matter expansion was found in hMT/V5 on the right side. This area is virtually the same area as demonstrated previously (Draganski et al., 2004). The box plot shows relative gray-matter change in the peak voxel in the right hMT for all jugglers over the three time points (error bars indicate the SD, range, and the mean for each time point). B, C, Only the jugglers group, but not the controls, showed a significant gray-matter increase in the hippocampus on the left side (B) and the nucleus accumbens bilaterally (C). This increase of gray matter reversed when study participants were examined at time point 3 (after the weeks without practicing).

References

    1. Buonomano DV, Merzenich MM. Cortical plasticity: from synapses to maps. Annu Rev Neurosci. 1998;21:149–186.
    1. Colcombe SJ, Erickson KI, Raz N, Webb AG, Cohen NJ, McAuley E, Kramer AF. Aerobic fitness reduces brain tissue loss in aging humans. J Gerontol A Biol Sci Med Sci. 2003;58:176–180.
    1. 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;61:1166–1170.
    1. DeFelipe J. Brain plasticity and mental processes: Cajal again. Nat Rev Neurosci. 2006;7:811–817.
    1. Draganski B, Gaser C, Busch V, Schuierer G, Bogdahn U, May A. Neuroplasticity: Changes in grey matter induced by training. Nature. 2004;427:311–312.
    1. Draganski B, Moser T, Lummel N, Gänssbauer S, Bogdahn U, Haas F, May A. Decrease of thalamic gray matter following limb amputation. Neuroimage. 2006a;31:951–957.
    1. Draganski B, Gaser C, Kempermann G, Kuhn HG, Winkler J, Büchel C, May A. Temporal and spatial dynamics of brain structure changes during extensive learning. J Neurosci. 2006b;26:6314–6317.
    1. Elward K, Larson EB. Benefits of exercise for older adults. A review of existing evidence and current recommendations for the general population. Clin Geriatr Med. 1992;8:35–50.
    1. Eriksson PS, Perfilieva E, Björk-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH. Neurogenesis in the adult human hippocampus. Nat Med. 1998;4:1313–1317.
    1. Etgen T, Draganski B, Ilg C, Schröder M, Geisler P, Hajak G, Eisensehr I, Sander D, May A. Bilateral thalamic gray matter changes in patients with restless legs syndrome. Neuroimage. 2005;24:1242–1247.
    1. Flor H, Nikolajsen L, Staehelin Jensen T. Phantom limb pain: a case of maladaptive CNS plasticity? Nat Rev Neurosci. 2006;7:873–881.
    1. Gage FH. Neurogenesis in the adult brain. J Neurosci. 2002;22:612–613.
    1. Gaser C, Schlaug G. Brain structures differ between musicians and non-musicians. J Neurosci. 2003;23:9240–9245.
    1. Golestani N, Paus T, Zatorre RJ. Anatomical correlates of learning novel speech sounds. Neuron. 2002;35:997–1010.
    1. Good CD, Johnsrude IS, Ashburner J, Henson RN, Friston KJ, Frackowiak RS. A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage. 2001a;14:21–36.
    1. Good CD, Johnsrude I, Ashburner J, Henson RN, Friston KJ, Frackowiak RS. Cerebral asymmetry and the effects of sex and handedness on brain structure: a voxel-based morphometric analysis of 465 normal adult human brains. Neuroimage. 2001b;14:685–700.
    1. Guan J, Wade MG. The effect of aging on adaptive eye-hand coordination. J Gerontol B Psychol Sci Soc Sci. 2000;55:P151–P162.
    1. Haug H, Eggers R. Morphometry of the human cortex cerebri and corpus striatum during aging. Neurobiol Aging. 1991;12:336–338. discussion 352–355.
    1. Hedden T, Gabrieli JD. Insights into the ageing mind: a view from cognitive neuroscience. Nat Rev Neurosci. 2004;5:87–96.
    1. Ikemoto S, Panksepp J. The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretation with special reference to reward-seeking. Brain Res Brain Res Rev. 1999;31:6–41.
    1. Kauranen K, Vanharanta H. Influences of aging, gender, and handedness on motor performance of upper and lower extremities. Percept Mot Skills. 1996;82:515–525.
    1. Kempermann G, Kuhn HG, Gage FH. More hippocampal neurons in adult mice living in an enriched environment. Nature. 1997;386:493–495.
    1. Kempermann G, Gast D, Gage FH. Neuroplasticity in old age: sustained fivefold induction of hippocampal neurogenesis by long-term environmental enrichment. Ann Neurol. 2002;52:135–143.
    1. Knecht S, Henningsen H, Höhling C, Elbert T, Flor H, Pantev C, Taub E. Plasticity of plasticity? Changes in the pattern of perceptual correlates of reorganization after amputation. Brain. 1998;121:717–724.
    1. Labyt E, Szurhaj W, Bourriez JL, Cassim F, Defebvre L, Destée A, Guieu JD, Derambure P. Changes in oscillatory cortical activity related to a visuomotor task in young and elderly healthy subjects. Clin Neurophysiol. 2003;114:1153–1166.
    1. 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;97:4398–4403.
    1. Mahncke HW, Bronstone A, Merzenich MM. Brain plasticity and functional losses in the aged: scientific bases for a novel intervention. Prog Brain Res. 2006;157:81–109.
    1. May A, Gaser C. Magnetic resonance-based morphometry: a window into structural plasticity of the brain. Curr Opin Neurol. 2006;19:407–411.
    1. Moffat SD, Kennedy KM, Rodrigue KM, Raz N. Extrahippocampal contributions to age differences in human spatial navigation. Cereb Cortex. 2007;17:1274–1282.
    1. Mogenson GJ, Jones DL, Yim CY. From motivation to action: functional interface between the limbic system and the motor system. Prog Neurobiol. 1980;14:69–97.
    1. Mora F, Segovia G, Del Arco A. Aging, plasticity and environmental enrichment: structural changes and neurotransmitter dynamics in several areas of the brain. Brain Res Rev. 2007;55:78–88.
    1. 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;104:5638–5643.
    1. Resnick SM, Pham DL, Kraut MA, Zonderman AB, Davatzikos C. Longitudinal magnetic resonance imaging studies of older adults: a shrinking brain. J Neurosci. 2003;23:3295–3301.
    1. Rudisill ME, Toole T. Gender differences in motor performance of 50- to 79-year-old adults. Percept Mot Skills. 1993;77:939–947.
    1. Wagner AP, Schmoll H, Badan I, Platt D, Kessler C. Brain plasticity: to what extent do aged animals retain the capacity to coordinate gene activity in response to acute challenges. Exp Gerontol. 2000;35:1211–1227.
    1. Weiller C, Ramsay SC, Wise RJ, Friston KJ, Frackowiak RS. Individual patterns of functional reorganization in the human cerebral cortex after capsular infarction. Ann Neurol. 1993;33:181–189.

Source: PubMed

Sponsorit ja yhteistyökumppanit

Sairaudet

Huumeiden interventiot

3
Tilaa