Abstract
Hemispheric asymmetry reduction in older adults (HAROLD) has been reported in previous imaging studies that employed not only cognitive, but also motor tasks. However, whether age-related reductions in asymmetry of hemispheric activations affect the symmetry of motor behavior in older adults remains largely untested. We now examine the effect of aging on lateralization of motor adaptation and transfer by investigating adaptation to novel visuomotor transformations in both old and young age groups. We have previously reported substantial asymmetries in interlimb transfer of learning these transformations in young adults, and attributed these asymmetries in transfer to hemispheric lateralization for motor control, as detailed by our dynamic dominance hypothesis. Based on the HAROLD model, we reasoned that older adults should recruit more symmetrical hemispheric activity, and thus show more symmetrical transfer of adaptation across the arms. Half of the subjects in each age group first adapted to a rotated visual display with the left arm, then with the right arm; and the other half in the reversed order. Naïve performance with one arm and the same-arm performance following opposite arm adaptation were compared to determine the extent of transfer in each age group. Our results showed that interlimb transfer of initial direction information only occurred from the nondominant to dominant arm in young adults, whereas it occurred in both directions in older adults. Our findings clearly indicate substantially reduced asymmetry in visuomotor adaptation in older adults, and suggest that this reduced motor asymmetry might be related to diminished hemispheric lateralization for motor control.
Similar content being viewed by others
References
Anguera JA, Reuter-Lorenz PA, Willingham DT, Seidler RD (2011) Failure to engage spatial working memory contributes to age-related declines in visuomotor learning. J Cogn Neurosci 23:11–25
Bergerbest D, Gabrieli JD, Whitfield-Gabrieli S, Kim H, Stebbins GT, Bennett DA, Fleischman DA (2009) Age-associated reduction of asymmetry in prefrontal function and preservation of conceptual repetition priming. Neuroimage 45:237–246
Brown HD, Kosslyn SM (1993) Cerebral lateralization. Curr Opin Neurobiol 3:183–186
Buch ER, Young S, Contreras-Vidal JL (2003) Visuomotor adaptation in normal aging. Learn Mem 10:55–63
Cabeza R (2002) Hemispheric asymmetry reduction in older adults: the HAROLD model. Psychol Aging 17:85–100
Cabeza R, Anderson ND, Locantore JK, McIntosh AR (2002) Aging gracefully: compensatory brain activity in high-performing older adults. Neuroimage 17:1394–1402
Cabeza R, Daselaar SM, Dolcos F, Prince SE, Budde M, Nyberg L (2004) Task-independent and task-specific age effects on brain activity during working memory, visual attention and episodic retrieval. Cereb Cortex 14:364–375
Cerella J (1990) Aging and information-processing rate. In: Birren JE, Schaie KW (eds) Handbook of the psychology of aging, 3rd edn. Academic Press, New York, pp 201–221
Corballis MC (1991) Left brain, right brain. Science 251:575–576
Dassonville P, Zhu XH, Uurbil K, Kim SG, Ashe J (1997) Functional activation in motor cortex reflects the direction and the degree of handedness. Proc Natl Acad Sci USA 94:14015–14018
Dolcos F, Rice HJ, Cabeza R (2002) Hemispheric asymmetry and aging: right hemisphere decline or asymmetry reduction. Neurosci Biobehav Rev 26:819–825
Evans WJ (2010) Skeletal muscle loss: cachexia, sarcopenia, and inactivity. Am J Clin Nutr 91:1123S–1127S
Fjell AM, Walhovd KB (2010) Structural brain changes in aging: courses, causes and cognitive consequences. Rev Neurosci 21:187–221
Goodale MA (1990) Brain asymmetries in the control of reaching. In: Goodale MA (ed) Vision and action: the control of grasping. Ablex, Norwood, pp 14–32
Grabiner MD, Enoka RM (1995) Changes in movement capabilities with aging. Exerc Sport Sci Rev 23:65–104
Grady CL (2000) Functional brain imaging and age-related changes in cognition. Biol Psychol 54:259–281
Grady CL, Mcintosh AR, Horwitz B, Maisog JM, Ungerleider LG, Mentis MJ, Pietrini P, Schapiro MB, Haxby JV (1995) Age-related reductions in human recognition memory due to impaired encoding. Science 269:218–221
Green JJ (1986) Characteristics of aging human skeletal muscles. In: Sutton JR, Brock RM (eds) Sports medicine for the mature athlete. Benchmark Press, Indianapolis, pp 17–26
Heuer H, Hegele M (2008) Adaptation to visuomotor rotations in younger and older adults. Psychol Aging 23:190–202
Kenshalo DR (1977) Age changes in touch, vibration, temperature, kinesthesis, and pain sensitivity. In: Birren JE, Schaie KW (eds) Handbook of the psychology of aging. Van Nostrand Reinhold, New York, pp 562–579
Kim SG, Ashe J, Hendrich K, Ellermann JM, Merkle H, Ugurbil K, Georgopoulos AP (1993) Functional magnetic resonance imaging of motor cortex: hemispheric asymmetry and handedness. Science 261:615–617
Kutas M, Donchin E (1974) Studies of squeezing: handedness, responding hand, response force, and asymmetry of readiness potential. Science 186:545–548
Mattay VS, Fera F, Tessitore A, Hariri AR, Das S, Callicott JH, Weinberger DR (2002) Neurophysiological correlates of age-related changes in human motor function. Neurology 58:630–635
Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113
Przybyla A, Sainburg RL (2010) Non-dominant advantages for movement accuracy depend on task conditions. Program no. 293.11, Neuroscience meeting planner. Society for Neuroscience, San Diego, CA. Online
Reuter-Lorenz PA, Jonides J, Smith EE, Hartley A, Miller A, Marshuetz C, Koeppe RA (2000) Age differences in the frontal lateralization of verbal and spatial working memory revealed by PET. J Cogn Neurosci 12:174–187
Rowe JB, Siebner H, Filipovic SR, Cordivari C, Gerschlager W, Rothwell J, Frackowiak R (2006) Aging is associated with contrasting changes in local and distant cortical connectivity in the human motor system. Neuroimage 32:747–760
Rypma B, Prabhakaran V, Desmond JE, Gabrieli JD (2001) Age differences in prefrontal cortical activity in working memory. Psychol Aging 16:371–384
Sainburg RL (2002) Evidence for a dynamic dominance hypothesis of handedness. Exp Brain Res 142:241–258
Sainburg RL (2005) Handedness: differential specializations for control of trajectory and position. Exerc Sport Sci Rev 33:206–213
Sainburg RL, Wang J (2002) Interlimb transfer of visuomotor rotations: independence of direct and final end position information. Exp Brain Res 145:437–447
Schaefer SY, Haaland KY, Sainburg RL (2007) Ipsilesional motor deficits following stroke reflect hemispheric specializations for movement control. Brain 130:2146–2158
Schaefer SY, Haaland KY, and Sainburg RL (2009) Hemispheric specialization and functional impact of ipsilesional deficits in movement coordination and accuracy. Neuropsychologia 47:2953–2966. Erratum in: Neuropsychologia (2010) 48:1178–1180
Serrien DA, Ivry RB, Swinnen SP (2006) Dynamics of interhemispheric specialization and integration in the context of motor control. Nat Rev Neurosci 7:160–167
Tanji J, Okano K, Sato KC (1988) Neuronal activity in cortical motor areas related to ipsilateral, contralateral, and bilateral digit movements of the monkey. J Neurophysiol 60:325–343
Urbano A, Babiloni C, Onorati P, Babiloni F (1996) Human cortical activity related to unilateral movements. A high resolution EEG study. Neuroreport 8:203–206
Volkmann J, Schnitzler A, Witte OW, Freund H (1998) Handedness and asymmetry of hand representation in human motor cortex. J Neurophysiol 79:2149–2154
Wang J (2008) A dissociation between visual and motor workspace inhibits generalization of visuomotor adaptation across the limbs. Exp Brain Res 187:483–490
Wang J, Sainburg RL (2006a) Interlimb transfer of visuomotor rotations depends on handedness. Exp Brain Res 175:223–230
Wang J, Sainburg RL (2006b) The symmetry of interlimb transfer depends on workspace location. Exp Brain Res 170:464–471
Wang J, Sainburg RL (2007) The dominant and non-dominant arms are specialized for stabilizing different features of task performance. Exp Brain Res 178:565–570
Wang J, Sainburg RL (2009) Generalization of visuomotor learning between bilateral and unilateral conditions. J Neurophysiol 102:2790–2799
Ward NS, Frackowiak RS (2003) Age-related changes in the neural correlates of motor performance. Brain 126:873–888
Acknowledgments
This research was supported by the National Institutes of Health, National Institute for Child Health and Human Development RO1HD39311 and 1R01HD059783 to RS, K01HD050245 to JW; and Career Scientist Award from the Department of Veterans Affairs to KYH.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Wang, J., Przybyla, A., Wuebbenhorst, K. et al. Aging reduces asymmetries in interlimb transfer of visuomotor adaptation. Exp Brain Res 210, 283–290 (2011). https://doi.org/10.1007/s00221-011-2631-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-011-2631-1