Effects of aging on interjoint coordination during arm reaching
Silva, Marcus Vinicius da; Bagesteiro, Léia Bernardi
http://dx.doi.org/10.1590/2446-4740.05115
Res. Biomed. Eng., vol.32, n3, p.223-233, 2016
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Views: 872
Abstract
Introduction: Moving the arm towards an object is a complex task. Movements of the arm joints must be well coordinated in order to obtain a smooth and accurate hand trajectory. Most studies regarding reaching movements address young subjects. Coordination differences in the neural mechanism underlying motor control throughout the life stages is yet unknown. The understanding of these changes can lead to a better comprehension of neuromotor pathologies and therefore to more suitable therapies. Methods: Our purpose was to investigate interjoint coordination in three different aging groups (children, young, elderly). Kinematics and kinetics specific variables were analyzed focusing on defined parameters to get insight into arm coordination. Intersegmental dynamics was used to calculate shoulder and elbow torques assuming a 2-link segment model of the upper extremity (upper arm and forearm) with two friction-less joints (shoulder and elbow). A virtual reality environment was used to examine multidirectional planar reaching in three different directions (randomly presented). Results: Seven measures were computed to investigate group interlimb differences: shoulder and elbow muscle torques (peak and impulse), work performed by shoulder and elbow joints, maximum velocity, movement distance, distance error at final position, movement duration and acceleration duration. Our data analysis showed differences between movement performances for all analyzed variables, at all ages. Conclusion: We found that the intersegmental dynamics for the interlimb (left/right) comparisons were similar for the elderly and children groups as compared to the young. In addition, the coordination and control of motor tasks changes during life, becoming less effective in old age.
Keywords
Arm reaching, Kinetics, Motor coordination, Aging.
References
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Bagesteiro LB, Sainburg RL. Handedness: dominant arm advantages in control of limb dynamics. Journal of Neurophysiology. 2002; 88(5):2408-21. http://dx.doi.org/10.1152/jn.00901.2001. PMid:12424282.
Bagesteiro LB, Silva MV. Joints coordination during arm reaching. In: Associação Brasileira de Engenharia e Ciências Mecânica. COBEM 2011: Proceeedings of the 21st International Congress of Mechanical Engineering; 2011 Oct 24-28; Natal, RN, Brazil. Rio de Janeiro: ABCM; 2011. DVD.
Bagesteiro LB. Aging related responses to conflicting proprioceptive and visual information about initial position during reaching. Revista Brasileira de Engenharia Biomédica. 2013; 29(3):227-41. http://dx.doi.org/10.4322/rbeb.2013.029.
Berret B, Chiovetto E, Nori F, Pozzo T. Evidence for composite cost functions in arm movement planning: an inverse optimal control approach. PLoS Computational Biology. 2011; 7(10):e1002183. http://dx.doi.org/10.1371/journal.pcbi.1002183. PMid:22022242.
Danion F, Descoins M, Bootsma RJ. Aging affects the predictive control of grip force during object manipulation. Experimental Brain Research. 2007; 180(1):123-37. http://dx.doi.org/10.1007/s00221-006-0846-3. PMid:17279385.
Enoka RM, Christou EA, Hunter SK, Kornatz KW, Semmler JG, Taylor AM, Tracy BL. Mechanisms that contribute to differences in motor performance between young and old adults. Journal of Electromyography and Kinesiology. 2003; 13(1):1-12. http://dx.doi.org/10.1016/S1050-6411(02)00084-6. PMid:12488083.
Enoka RM. Neuromechanics of human movement. 2nd ed. Leeds: Human Kinetics; 2002.
Favilla M. Reaching movements in children: accuracy and reaction time development. Experimental Brain Research. 2006; 169(1):122-5. http://dx.doi.org/10.1007/s00221-005-0291-8. PMid:16369792.
Ferrel-Chapus C, Hay L, Olivier I, Bard C, Fleury M. Visuomanual coordination in childhood: adaptation to visual distortion. Experimental Brain Research. 2002; 144(4):506-17. http://dx.doi.org/10.1007/s00221-002-1064-2. PMid:12037635.
Francis KL, Spirduso WW. Age differences in the expression of manual asymmetry. Experimental Aging Research. 2000; 26(2):169-80. http://dx.doi.org/10.1080/036107300243632. PMid:10755223.
Gooderham SE, Bryden PJ. Does your dominant hand become less dominant with time? The effects of aging and task complexity on hand selection. Developmental Psychobiology. 2014; 56(3):537-46. http://dx.doi.org/10.1002/dev.21123. PMID: 23765799.
Graham KM, Moore KD, Cabel DW, Gribble PL, Cisek P, Scott SH. Kinematics and kinetics of multi-joint reaching in non- human primates. Journal of Neurophysiology. 2003; 89(5):2667-77. http://dx.doi.org/10.1152/jn.00742.2002. PMid:12612006.
Heineman KR, Middelburg KJ, Hadders-Algra M. Development of adaptive motor behaviour in typically developing infants. Acta Paediatrica. 2010; 99(4):618-24. http://dx.doi.org/10.1111/j.1651-2227.2009.01652.x. PMid:20050831.
Heuninckx S, Debaere F, Wenderoth N, Verschueren S, Swinnen SP. Ipsilateral coordination deficits and central processing requirements associated with coordination as a function of aging. The Journals of Gerontology. Series B, Psychological Sciences and Social Sciences. 2004; 59(5):225-32. http://dx.doi.org/10.1093/geronb/59.5.P225. PMid:15358795.
Holtrop JL, Loucks TM, Sosnoff JJ, Sutton BP. Investigating age-related changes in fine motor control across different effectors and the impact of white matter integrity. NeuroImage. 2014; 96:81-7. http://dx.doi.org/10.1016/j.neuroimage.2014.03.045. PMid:24657352.
Lambert J, Bard C. Acquisition of visuomanual skills and improvement of information processing capacities in 6 to 10 year old children performing a 2D pointing task. Neuroscience Letters. 2005; 377(1):1-6. http://dx.doi.org/10.1016/j.neulet.2004.11.058. PMid:15722176.
Lee G, Fradet L, Ketcham CJ, Dounskaia N. Efficient control of arm movements in advanced age. Experimental Brain Research. 2007; 177(1):78-94. http://dx.doi.org/10.1007/s00221-006-0648-7. PMid:16944112.
Linortner P, Jehna M, Johansen-Berg H, Matthews PM, Schmidt R, Fazekas F, Enzinger C. Aging associated changes in the motor control of ankle movements in the brain. Neurobiology of Aging. 2014; 35(10):2222-9. http://dx.doi.org/10.1016/j.neurobiolaging.2014.04.013. PMid:24836898.
Mistry M, Theodorou E, Schaal S, Kawato M. Optimal control of reaching includes kinematic constraints. Journal of Neurophysiology. 2013; 110(1):1-11. http://dx.doi.org/10.1152/jn.00794.2011. PMid:23554437.
Mutha PK, Haaland KY, Sainburg RL. Rethinking motor lateralization: Specialized but complementary mechanisms for motor control of each arm. PLoS One. 2013; 8(3):e58582. http://dx.doi.org/10.1371/journal.pone.0058582. PMid:23472210.
Oldfield RC. The assessment and analysis of handedness: the Edinburgh Inventory. Neuropsychologia. 1971; 9(1):97-113. http://dx.doi.org/10.1016/0028-3932(71)90067-4. PMid:5146491.
Olivier I, Hay L, Bard C, Fleury M. Age-related differences in the reaching and grasping coordination in children: unimanual and bimanual tasks. Experimental Brain Research. 2007; 179(1):17-27. http://dx.doi.org/10.1007/s00221-006-0762-6. PMid:17091289.
Paizis C, Papaxanthis C, Berret B, Pozzo T. Reaching beyond arm length in normal aging: adaptation of hand trajectory and dynamic equilibrium. Behavioral Neuroscience. 2008; 122(6):1361-70. http://dx.doi.org/10.1037/a0013280. PMid:19045955.
Pohl PS, Winstein CJ, Fisher BE. The locus of age-related movement slowing: sensory processing in continuous goal-directed aiming. The Journals of Gerontology. Series B, Psychological Sciences and Social Sciences. 1996; 51(2):94-102. http://dx.doi.org/10.1093/geronb/51B.2.P94. PMid:8785692.
Przybyla A, Haaland KY, Bagesteiro LB, Sainburg RL. Motor asymmetry reduction in older adults. Neuroscience Letters. 2011; 489(489):99-104. http://dx.doi.org/10.1016/j.neulet.2010.11.074. PMid:21144883.
Rival C, Olivier I, Ceyte H. Effects of temporal and/or spatial instructions on the speed-accuracy trade-off of pointing movements in children. Neuroscience Letters. 2003; 336(1):65-9. http://dx.doi.org/10.1016/S0304-3940(02)01246-6. PMid:12493603.
Sainburg RL, Kalakanis D. Differences in control of limb dynamics during dominant and nondominant arm reaching. Journal of Neurophysiology. 2000; 83(5):2661-75. PMid:10805666.
Sainburg RL, Schaefer SY. Interlimb differences in control of movement extent. Journal of Neurophysiology. 2004; 92(3):1374-83. http://dx.doi.org/10.1152/jn.00181.2004. PMid:15115793.
Sainburg RL. Evidence for a dynamic-dominance hypothesis of handedness. Experimental Brain Research. 2002; 142(2):241-58. http://dx.doi.org/10.1007/s00221-001-0913-8. PMid:11807578.
Schepens B, Willems PA, Cavagna GA, Heglund NC. Mechanical power and efficiency in running children. European Journal of Phycology. 2001; 442(1):107-16. PMid:11374057.
Schneiberg S, Sveistrup H, McFadyen B, McKinley P, Levin MF. The development of coordination for reach-to-grasp movements in children. Experimental Brain Research. 2002; 146(2):142-54. http://dx.doi.org/10.1007/s00221-002-1156-z. PMid:12195516.
Seidler RD, Bernard JA, Burutolu TB, Fling BW, Gordon MT, Gwin JT, Kwak Y, Lipps DB. Motor control and aging: Links to age-related brain structural, functional, and biochemical effects. Neuroscience and Biobehavioral Reviews. 2010; 34(5):721-33. http://dx.doi.org/10.1016/j.neubiorev.2009.10.005. PMid:19850077.
Semmler JG, Kornatz KW, Meyer FG, Enoka RM. Diminished task-related adjustments of common inputs to hand muscle motor neurons in older adults. Experimental Brain Research. 2006; 172(4):507-18. http://dx.doi.org/10.1007/s00221-006-0367-0. PMid:16489433.
Shadmehr R, Moussavi ZM. Spatial generalization from learning dynamics of reaching movements. The Journal of Neuroscience. 2000; 20(20):7807-15. PMid:11027245.
Sveistrup H, Schneiberg S, McKinley PA, McFadyen BJ, Levin MF. Head, arm and trunk coordination during reaching in children. Experimental Brain Research. 2008; 188(2):237-47. http://dx.doi.org/10.1007/s00221-008-1357-1. PMid:18392615.
Tutkuviene J, Schiefenhövel W. Laterality of handgrip strength: age- and physical training–related changes in Lithuanian schoolchildren and conscripts. Annals of the New York Academy of Sciences. 2013; 1288(1):124-34. http://dx.doi.org/10.1111/nyas.12126. PMid:23701486.
Wilson PH, Hyde C. The development of rapid online control inchildren aged 6-12 years: Reaching performance. Human Movement Science. 2013; 32:1138-50.
Winter DA. Biomechanics and motor control of human movement. New York: John Wiley and Sons; 2004.
Winter DA. Moments of force and mechanical power in jogging. Journal of Biomechanics. 1983; 16(1):91-7. http://dx.doi.org/10.1016/0021-9290(83)90050-7. PMid:6833314.
Yan JH. Effects of aging on linear and curvilinear aiming arm movements. Experimental Aging Research. 2000; 26(4):393-407. http://dx.doi.org/10.1080/036107300750015778. PMid:11091944.
Zelik KE, Kuo AD. Mechanical work as an indirect measure of subjective costs influencing human movement. PLoS One. 2012; 7(2):e31143. http://dx.doi.org/10.1371/journal.pone.0031143. PMid:22383998.
Bagesteiro LB, Sainburg RL. Handedness: dominant arm advantages in control of limb dynamics. Journal of Neurophysiology. 2002; 88(5):2408-21. http://dx.doi.org/10.1152/jn.00901.2001. PMid:12424282.
Bagesteiro LB, Silva MV. Joints coordination during arm reaching. In: Associação Brasileira de Engenharia e Ciências Mecânica. COBEM 2011: Proceeedings of the 21st International Congress of Mechanical Engineering; 2011 Oct 24-28; Natal, RN, Brazil. Rio de Janeiro: ABCM; 2011. DVD.
Bagesteiro LB. Aging related responses to conflicting proprioceptive and visual information about initial position during reaching. Revista Brasileira de Engenharia Biomédica. 2013; 29(3):227-41. http://dx.doi.org/10.4322/rbeb.2013.029.
Berret B, Chiovetto E, Nori F, Pozzo T. Evidence for composite cost functions in arm movement planning: an inverse optimal control approach. PLoS Computational Biology. 2011; 7(10):e1002183. http://dx.doi.org/10.1371/journal.pcbi.1002183. PMid:22022242.
Danion F, Descoins M, Bootsma RJ. Aging affects the predictive control of grip force during object manipulation. Experimental Brain Research. 2007; 180(1):123-37. http://dx.doi.org/10.1007/s00221-006-0846-3. PMid:17279385.
Enoka RM, Christou EA, Hunter SK, Kornatz KW, Semmler JG, Taylor AM, Tracy BL. Mechanisms that contribute to differences in motor performance between young and old adults. Journal of Electromyography and Kinesiology. 2003; 13(1):1-12. http://dx.doi.org/10.1016/S1050-6411(02)00084-6. PMid:12488083.
Enoka RM. Neuromechanics of human movement. 2nd ed. Leeds: Human Kinetics; 2002.
Favilla M. Reaching movements in children: accuracy and reaction time development. Experimental Brain Research. 2006; 169(1):122-5. http://dx.doi.org/10.1007/s00221-005-0291-8. PMid:16369792.
Ferrel-Chapus C, Hay L, Olivier I, Bard C, Fleury M. Visuomanual coordination in childhood: adaptation to visual distortion. Experimental Brain Research. 2002; 144(4):506-17. http://dx.doi.org/10.1007/s00221-002-1064-2. PMid:12037635.
Francis KL, Spirduso WW. Age differences in the expression of manual asymmetry. Experimental Aging Research. 2000; 26(2):169-80. http://dx.doi.org/10.1080/036107300243632. PMid:10755223.
Gooderham SE, Bryden PJ. Does your dominant hand become less dominant with time? The effects of aging and task complexity on hand selection. Developmental Psychobiology. 2014; 56(3):537-46. http://dx.doi.org/10.1002/dev.21123. PMID: 23765799.
Graham KM, Moore KD, Cabel DW, Gribble PL, Cisek P, Scott SH. Kinematics and kinetics of multi-joint reaching in non- human primates. Journal of Neurophysiology. 2003; 89(5):2667-77. http://dx.doi.org/10.1152/jn.00742.2002. PMid:12612006.
Heineman KR, Middelburg KJ, Hadders-Algra M. Development of adaptive motor behaviour in typically developing infants. Acta Paediatrica. 2010; 99(4):618-24. http://dx.doi.org/10.1111/j.1651-2227.2009.01652.x. PMid:20050831.
Heuninckx S, Debaere F, Wenderoth N, Verschueren S, Swinnen SP. Ipsilateral coordination deficits and central processing requirements associated with coordination as a function of aging. The Journals of Gerontology. Series B, Psychological Sciences and Social Sciences. 2004; 59(5):225-32. http://dx.doi.org/10.1093/geronb/59.5.P225. PMid:15358795.
Holtrop JL, Loucks TM, Sosnoff JJ, Sutton BP. Investigating age-related changes in fine motor control across different effectors and the impact of white matter integrity. NeuroImage. 2014; 96:81-7. http://dx.doi.org/10.1016/j.neuroimage.2014.03.045. PMid:24657352.
Lambert J, Bard C. Acquisition of visuomanual skills and improvement of information processing capacities in 6 to 10 year old children performing a 2D pointing task. Neuroscience Letters. 2005; 377(1):1-6. http://dx.doi.org/10.1016/j.neulet.2004.11.058. PMid:15722176.
Lee G, Fradet L, Ketcham CJ, Dounskaia N. Efficient control of arm movements in advanced age. Experimental Brain Research. 2007; 177(1):78-94. http://dx.doi.org/10.1007/s00221-006-0648-7. PMid:16944112.
Linortner P, Jehna M, Johansen-Berg H, Matthews PM, Schmidt R, Fazekas F, Enzinger C. Aging associated changes in the motor control of ankle movements in the brain. Neurobiology of Aging. 2014; 35(10):2222-9. http://dx.doi.org/10.1016/j.neurobiolaging.2014.04.013. PMid:24836898.
Mistry M, Theodorou E, Schaal S, Kawato M. Optimal control of reaching includes kinematic constraints. Journal of Neurophysiology. 2013; 110(1):1-11. http://dx.doi.org/10.1152/jn.00794.2011. PMid:23554437.
Mutha PK, Haaland KY, Sainburg RL. Rethinking motor lateralization: Specialized but complementary mechanisms for motor control of each arm. PLoS One. 2013; 8(3):e58582. http://dx.doi.org/10.1371/journal.pone.0058582. PMid:23472210.
Oldfield RC. The assessment and analysis of handedness: the Edinburgh Inventory. Neuropsychologia. 1971; 9(1):97-113. http://dx.doi.org/10.1016/0028-3932(71)90067-4. PMid:5146491.
Olivier I, Hay L, Bard C, Fleury M. Age-related differences in the reaching and grasping coordination in children: unimanual and bimanual tasks. Experimental Brain Research. 2007; 179(1):17-27. http://dx.doi.org/10.1007/s00221-006-0762-6. PMid:17091289.
Paizis C, Papaxanthis C, Berret B, Pozzo T. Reaching beyond arm length in normal aging: adaptation of hand trajectory and dynamic equilibrium. Behavioral Neuroscience. 2008; 122(6):1361-70. http://dx.doi.org/10.1037/a0013280. PMid:19045955.
Pohl PS, Winstein CJ, Fisher BE. The locus of age-related movement slowing: sensory processing in continuous goal-directed aiming. The Journals of Gerontology. Series B, Psychological Sciences and Social Sciences. 1996; 51(2):94-102. http://dx.doi.org/10.1093/geronb/51B.2.P94. PMid:8785692.
Przybyla A, Haaland KY, Bagesteiro LB, Sainburg RL. Motor asymmetry reduction in older adults. Neuroscience Letters. 2011; 489(489):99-104. http://dx.doi.org/10.1016/j.neulet.2010.11.074. PMid:21144883.
Rival C, Olivier I, Ceyte H. Effects of temporal and/or spatial instructions on the speed-accuracy trade-off of pointing movements in children. Neuroscience Letters. 2003; 336(1):65-9. http://dx.doi.org/10.1016/S0304-3940(02)01246-6. PMid:12493603.
Sainburg RL, Kalakanis D. Differences in control of limb dynamics during dominant and nondominant arm reaching. Journal of Neurophysiology. 2000; 83(5):2661-75. PMid:10805666.
Sainburg RL, Schaefer SY. Interlimb differences in control of movement extent. Journal of Neurophysiology. 2004; 92(3):1374-83. http://dx.doi.org/10.1152/jn.00181.2004. PMid:15115793.
Sainburg RL. Evidence for a dynamic-dominance hypothesis of handedness. Experimental Brain Research. 2002; 142(2):241-58. http://dx.doi.org/10.1007/s00221-001-0913-8. PMid:11807578.
Schepens B, Willems PA, Cavagna GA, Heglund NC. Mechanical power and efficiency in running children. European Journal of Phycology. 2001; 442(1):107-16. PMid:11374057.
Schneiberg S, Sveistrup H, McFadyen B, McKinley P, Levin MF. The development of coordination for reach-to-grasp movements in children. Experimental Brain Research. 2002; 146(2):142-54. http://dx.doi.org/10.1007/s00221-002-1156-z. PMid:12195516.
Seidler RD, Bernard JA, Burutolu TB, Fling BW, Gordon MT, Gwin JT, Kwak Y, Lipps DB. Motor control and aging: Links to age-related brain structural, functional, and biochemical effects. Neuroscience and Biobehavioral Reviews. 2010; 34(5):721-33. http://dx.doi.org/10.1016/j.neubiorev.2009.10.005. PMid:19850077.
Semmler JG, Kornatz KW, Meyer FG, Enoka RM. Diminished task-related adjustments of common inputs to hand muscle motor neurons in older adults. Experimental Brain Research. 2006; 172(4):507-18. http://dx.doi.org/10.1007/s00221-006-0367-0. PMid:16489433.
Shadmehr R, Moussavi ZM. Spatial generalization from learning dynamics of reaching movements. The Journal of Neuroscience. 2000; 20(20):7807-15. PMid:11027245.
Sveistrup H, Schneiberg S, McKinley PA, McFadyen BJ, Levin MF. Head, arm and trunk coordination during reaching in children. Experimental Brain Research. 2008; 188(2):237-47. http://dx.doi.org/10.1007/s00221-008-1357-1. PMid:18392615.
Tutkuviene J, Schiefenhövel W. Laterality of handgrip strength: age- and physical training–related changes in Lithuanian schoolchildren and conscripts. Annals of the New York Academy of Sciences. 2013; 1288(1):124-34. http://dx.doi.org/10.1111/nyas.12126. PMid:23701486.
Wilson PH, Hyde C. The development of rapid online control inchildren aged 6-12 years: Reaching performance. Human Movement Science. 2013; 32:1138-50.
Winter DA. Biomechanics and motor control of human movement. New York: John Wiley and Sons; 2004.
Winter DA. Moments of force and mechanical power in jogging. Journal of Biomechanics. 1983; 16(1):91-7. http://dx.doi.org/10.1016/0021-9290(83)90050-7. PMid:6833314.
Yan JH. Effects of aging on linear and curvilinear aiming arm movements. Experimental Aging Research. 2000; 26(4):393-407. http://dx.doi.org/10.1080/036107300750015778. PMid:11091944.
Zelik KE, Kuo AD. Mechanical work as an indirect measure of subjective costs influencing human movement. PLoS One. 2012; 7(2):e31143. http://dx.doi.org/10.1371/journal.pone.0031143. PMid:22383998.
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