Developmental improvements in dynamic control of fingertip forces last throughout childhood and into adolescence

Journal of Neurophysiology

Volumn 110, Issue 7, 2013, Pages 1583-1592

  Dayanidhi, Sudarshan ^a   Hedberg, Åsa ^b   Valero Cuevas, Francisco J ^a,c   Forssberg, Hans ^b  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^c University of Southern California   (United States)

Author keywords

Adolescence; Children; Development; Dexterity; Dynamic control; Fingertip forces

Indexed keywords

ADOLESCENCE; ADOLESCENT; ARTICLE; CHILD; CHILDHOOD; DEVELOPMENTAL STAGE; FEMALE; FINGER; FORCE; HUMAN; HUMAN EXPERIMENT; MALE; MATURATION; MOTOR PERFORMANCE; NEUROANATOMY; NORMAL HUMAN; PINCH STRENGTH; PRESCHOOL CHILD; PRIORITY JOURNAL; SCHOOL CHILD; SCORING SYSTEM;

ADOLESCENCE; CHILDREN; DEVELOPMENT; DEXTERITY; DYNAMIC CONTROL; FINGERTIP FORCES;

ADOLESCENT; ADOLESCENT DEVELOPMENT; CHILD; CHILD DEVELOPMENT; CHILD, PRESCHOOL; FEMALE; FINGERS; HUMANS; MALE; MOTOR SKILLS; PINCH STRENGTH;

EID: 84884171113     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00320.2013     Document Type: Article

References (57)

1. Armand J, Edgley SA, Lemon RN, Olivier E. Protracted postnatal development of corticospinal projections from the primary motor cortex to hand motoneurones in the macaque monkey. Exp Brain Res 101: 178-182, 1994.
2. Armand J, Olivier E, Edgley SA, Lemon RN. Postnatal development of corticospinal projections from motor cortex to the cervical enlargement in the macaque monkey. J Neurosci 17: 251-266, 1997.
3. Asato MR, Terwilliger R, Woo J, Luna B. White matter development in adolescence: a DTI study. Cereb Cortex 20: 2122-2131, 2010.
4. Bengtsson SL, Nagy Z, Skare S, Forsman L, Forssberg H, Ullen F. Extensive piano practicing has regionally specific effects on white matter development. Nat Neurosci 8: 1148-1150, 2005.
5. Birznieks I, Jenmalm P, Goodwin AW, Johansson RS. Encoding of direction of fingertip forces by human tactile afferents. J Neurosci 21: 8222-8237, 2001.
6. Bonnier B, Eliasson AC, Krumlinde-Sundholm L. Effects of constraintinduced movement therapy in adolescents with hemiplegic cerebral palsy: a day camp model. Scand J Occup Ther 13: 13-22, 2006.
7. Colby JB, Van Horn JD, Sowell ER. Quantitative in vivo evidence for broad regional gradients in the timing of white matter maturation during adolescence. Neuroimage 54: 25-31, 2011.
8. Dayanidhi S. Behavioral, Muscular and Dynamical Changes in Low Force Dexterous Manipulation during Development and Aging (PhD dissertation). Los Angeles, CA: University of Southern California, 2012.
9. Deutsch KM, Newell KM. Age differences in noise and variability of isometric force production. J Exp Child Psychol 80: 392-408, 2001.
10. Deutsch KM, Newell KM. Children's coordination of force output in a pinch grip task. Dev Psychobiol 41: 253-264, 2002.
11. Edin BB, Westling G, Johansson RS. Independent control of human fingertip forces at individual digits during precision lifting. J Physiol 450: 547-564, 1992.
12. Ehrsson HH, Fagergren E, Forssberg H. Differential fronto-parietal activation depending on force used in a precision grip task: an fMRI study. J Neurophysiol 85: 2613-2623, 2001.
13. Eliasson AC, Forssberg H, Hung YC, Gordon AM. Development of hand function and precision grip control in individuals with cerebral palsy: a 13-year follow-up study. Pediatrics 118: e1226-e1236, 2006.
14. Forssberg H, Eliasson AC, Kinoshita H, Johansson RS, Westling G. Development of human precision grip. I. Basic coordination of force. Exp Brain Res 85: 451-457, 1991.
15. Forssberg H, Eliasson AC, Kinoshita H, Westling G, Johansson RS. Development of human precision grip. IV. Tactile adaptation of isometric finger forces to the frictional condition. Exp Brain Res 104: 323-330, 1995.
16. Forssberg H, Kinoshita H, Eliasson AC, Johansson RS, Westling G, Gordon AM. Development of human precision grip. II. Anticipatory control of isometric forces targeted for object's weight. Exp Brain Res 90: 393-398, 1992.
17. Franklin DW, Wolpert DM. Computational mechanisms of sensorimotor control. Neuron 72: 425-442, 2011.
18. Giedd JN, Blumenthal J, Jeffries NO, Castellanos FX, Liu H, Zijdenbos A, Paus T, Evans AC, Rapoport JL. Brain development during childhood and adolescence: a longitudinal MRI study. Nat Neurosci 2: 861-863, 1999.
19. Gordon AM, Forssberg H, Johansson RS, Eliasson AC, Westling G. Development of human precision grip. III. Integration of visual size cues during the programming of isometric forces. Exp Brain Res 90: 399-403, 1992.
20. Gordon AM, Forssberg H, Johansson RS, Westling G. Visual size cues in the programming of manipulative forces during precision grip. Exp Brain Res 83: 477-482, 1991.
21. Gordon AM, Schneider JA, Chinnan A, Charles JR. Efficacy of a hand-arm bimanual intensive therapy (HABIT) in children with hemiplegic cerebral palsy: a randomized control trial. Dev Med Child Neurol 49: 830-838, 2007.
22. Häger-Ross C, Rösblad B. Norms for grip strength in children aged 4-16 years. Acta Paediatr 91: 617-625, 2002.
23. Häger-Ross C, Schieber MH. Quantifying the independence of human finger movements: comparisons of digits, hands, and movement frequencies. J Neurosci 20: 8542-8550, 2000.
24. Hirsch MW, Smale S, Devaney RL. Differential Equations, Dynamical Systems and an Introduction to Chaos. San Diego, CA: Academic/Elsevier, 2004.
25. Holmström L, de Manzano O, Vollmer B, Forsman L, Valero-Cuevas FJ, Ullen F, Forssberg H. Dissociation of brain areas associated with force production and stabilization during manipulation of unstable objects. Exp Brain Res 215: 359-367, 2011a.
26. Holmström L, Lennartsson F, Eliasson AC, Flodmark O, Clark C, Tedroff K, Forssberg H, Vollmer B. Diffusion MRI in corticofugal fibers correlates with hand function in unilateral cerebral palsy. Neurology 77: 775-783, 2011b.
27. Jebsen RH, Taylor N, Trieschmann RB, Trotter MJ, Howard LA. An objective and standardized test of hand function. Arch Phys Med Rehabil 50: 311-319, 1969.
28. Johansson RS, Flanagan JR. Coding and use of tactile signals from the fingertips in object manipulation tasks. Nat Rev Neurosci 10: 345-359, 2009.
29. Kuhtz-Buschbeck JP, Sundholm LK, Eliasson AC, Forssberg H. Quantitative assessment of mirror movements in children and adolescents with hemiplegic cerebral palsy. Dev Med Child Neurol 42: 728-736, 2000.
30. Lebel C, Beaulieu C. Longitudinal development of human brain wiring continues from childhood into adulthood. J Neurosci 31: 10937-10947, 2011.
31. Lebel C, Walker L, Leemans A, Phillips L, Beaulieu C. Microstructural maturation of the human brain from childhood to adulthood. Neuroimage 40: 1044-1055, 2008.
32. Lemon R, Sasaki S, Naito K, Yoshimura K, Isa T, Seki K, Pettersson LG, Alstermark B, Ohki Y. Cortico-motoneuronal system and dexterous finger movements. J Neurophysiol 92: 3601-3603, 2004a.
33. Lemon RN, Kirkwood PA, Maier MA, Nakajima K, Nathan P. Direct and indirect pathways for corticospinal control of upper limb motoneurons in the primate. Prog Brain Res 143: 263-279, 2004b.
34. Martin JH, Friel KM, Salimi I, Chakrabarty S. Activity-and use-dependent plasticity of the developing corticospinal system. Neurosci Biobehav Rev 31: 1125-1135, 2007.
35. Mathiowetz V, Rogers SL, Dowe-Keval M, Donahoe L, Rennells C. The Purdue Pegboard: norms for 14-to 19-year-olds. Am J Occup Ther 40: 174-179, 1986.
36. Moberg E. Objective methods for determining the functional value of sensibility in the hand. J Bone Joint Surg Br 40-B: 454-476, 1958.
37. Mosier KM, Lau C, Wang Y, Venkadesan M, Valero-Cuevas FJ. Controlling instabilities in manipulation requires specific cortical-striatal-cerebellar networks. J Neurophysiol 105: 1295-1305, 2011.
38. Muir RB, Lemon RN. Corticospinal neurons with a special role in precision grip. Brain Res 261: 312-316, 1983.
39. Müller K, Ebner B, Hömberg V. Maturation of fastest afferent and efferent central and peripheral pathways: no evidence for a constancy of central conduction delays. Neurosci Lett 166: 9-12, 1994.
40. Murray EA, Cermak SA, O'Brien V. The relationship between form and space perception, constructional abilities, and clumsiness in children. Am J Occup Ther 44: 623-628, 1990.
41. Murray RM, Sastry SS, Zexiang L. A Mathematical Introduction to Robotic Manipulation. Boca Raton, FL: CRC, 1994, p. 480.
42. Newell KM, Liu YT, Mayer-Kress G. Time scales in motor learning and development. Psychol Rev 108: 57-82, 2001.
43. Paus T, Zijdenbos A, Worsley K, Collins DL, Blumenthal J, Giedd JN, Rapoport JL, Evans AC. Structural maturation of neural pathways in children and adolescents: in vivo study. Science 283: 1908-1911, 1999.
44. Plautz EJ, Milliken GW, Nudo RJ. Effects of repetitive motor training on movement representations in adult squirrel monkeys: role of use versus learning. Neurobiol Learn Mem 74: 27-55, 2000.
45. Poole JL, Burtner PA, Torres TA, McMullen CK, Markham A, Marcum ML, Anderson JB, Qualls C. Measuring dexterity in children using the nine-hole peg test. J Hand Ther 18: 348-351, 2005.
46. Santos VJ. A Bayesian Approach to Biomechanical Modeling: A Treatise on the Human Thumb (PhD dissertation). Ithaca, NY: Cornell University, 2007.
47. Schieber MH, Santello M. Hand function: peripheral and central constraints on performance. J Appl Physiol 96: 2293-2300, 2004.
48. Schmithorst VJ, Holland SK, Dardzinski BJ. Developmental differences in white matter architecture between boys and girls. Hum Brain Mapp 29: 696-710, 2008.
49. Sowell ER, Thompson PM, Holmes CJ, Batth R, Jernigan TL, Toga AW. Localizing age-related changes in brain structure between childhood and adolescence using statistical parametric mapping. Neuroimage 9: 587-597, 1999a.
50. Sowell ER, Thompson PM, Holmes CJ, Jernigan TL, Toga AW. In vivo evidence for postadolescent brain maturation in frontal and striatal regions. Nat Neurosci 2: 859-860, 1999b.
51. Taylor N, Sand PL, Jebsen RH. Evaluation of hand function in children. Arch Phys Med Rehabil 54: 129-135, 1973.
52. Tiffin J, Asher EJ. The Purdue pegboard; norms and studies of reliability and validity. J Appl Psychol 32: 234-247, 1948.
53. Valero-Cuevas FJ, Smaby N, Venkadesan M, Peterson M, Wright T. The strength-dexterity test as a measure of dynamic pinch performance. J Biomech 36: 265-270, 2003.
54. Venkadesan M, Guckenheimer J, Valero-Cuevas FJ. Manipulating the edge of instability. J Biomech 40: 1653-1661, 2007.
55. Vollmer B, Holmström L, Forsman L, Krumlinde-Sundholm L, Valero-Cuevas FJ, Forssberg H, Ullén F. Evidence of validity in a new method for measurement of dexterity in children and adolescents. Dev Med Child Neurol 52: 948-954, 2010.
56. Wolpert DM, Diedrichsen J, Flanagan JR. Principles of sensorimotor learning. Nat Rev Neurosci 12: 739-751, 2011.
57. Zatsiorsky VM, Li ZM, Latash ML. Enslaving effects in multi-finger force production. Exp Brain Res 131: 187-195, 2000.