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Published in: Journal of NeuroEngineering and Rehabilitation 1/2017

Open Access 01-12-2017 | Research

Robot-aided developmental assessment of wrist proprioception in children

Authors: Francesca Marini, Valentina Squeri, Pietro Morasso, Claudio Campus, Jürgen Konczak, Lorenzo Masia

Published in: Journal of NeuroEngineering and Rehabilitation | Issue 1/2017

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Abstract

Background

Several neurodevelopmental disorders and brain injuries in children have been associated with proprioceptive dysfunction that will negatively affect their movement. Unfortunately, there is lack of reliable and objective clinical examination protocols and our current knowledge of how proprioception evolves in typically developing children is still sparse.

Methods

Using a robotic exoskeleton, we investigated proprioceptive acuity of the wrist in a group of 49 typically developing healthy children (8–15 years), and a group of 40 young adults. Without vision participants performed an ipsilateral wrist joint position matching task that required them to reproduce (match) a previously experienced target position. All three joint degrees-of-freedom of the wrist/hand complex were assessed. Accuracy and precision were evaluated as a measure of proprioceptive acuity. The cross-sectional data indicating the time course of development of acuity were then fitted by four models in order to determine which function best describes developmental changes in proprioception across age.

Results

First, the robot-aided assessment proved to be an easy to administer method for objectively measuring proprioceptive acuity in both children and adult populations. Second, proprioceptive acuity continued to develop throughout middle childhood and early adolescence, improving by more than 50% with respect to the youngest group. Adult levels of performance were reached approximately by the age of 12 years. An inverse-root function best described the development of proprioceptive acuity across the age groups. Third, wrist/forearm proprioception is anisotropic across the three DoFs with the Abduction/Adduction exhibiting a higher level of acuity than those of Flexion/extension and Pronation/Supination. This anisotropy did not change across development.

Conclusions

Proprioceptive development for the wrist continues well into early adolescence. Our normative data obtained trough this novel robot-aided assessment method provide a basis against which proprioceptive function of pediatric population can be compared. This may aid the design of more effective sensorimotor intervention programs.
Literature
1.
go back to reference Kusoffsky A, Wadell I, Nilsson BY. The relationship between sensory impairment and motor recovery in patients with hemiplegia. Scand J Rehabil Med. 1982; 14(1):27–32.PubMed Kusoffsky A, Wadell I, Nilsson BY. The relationship between sensory impairment and motor recovery in patients with hemiplegia. Scand J Rehabil Med. 1982; 14(1):27–32.PubMed
3.
go back to reference Cordo P, Carlton L, Bevan L, Carlton M, Kerr GK. Proprioceptive coordination of movement sequences: role of velocity and position information. J Neurophys. 1994; 71(5):1848–61. Cordo P, Carlton L, Bevan L, Carlton M, Kerr GK. Proprioceptive coordination of movement sequences: role of velocity and position information. J Neurophys. 1994; 71(5):1848–61.
4.
go back to reference Bard C, Fleury M, Teasdale N, Paillard J, Nougier V. Contribution of proprioception for calibrating and updating the motor space. Can J Physiol Pharmacol. 1995; 73(2):246–54. doi:10.1139/y95-035.CrossRefPubMed Bard C, Fleury M, Teasdale N, Paillard J, Nougier V. Contribution of proprioception for calibrating and updating the motor space. Can J Physiol Pharmacol. 1995; 73(2):246–54. doi:10.​1139/​y95-035.CrossRefPubMed
5.
go back to reference Sainburg RL, Ghilardi MF, Poizner H, Ghez C. Control of limb dynamics in normal subjects and patients without proprioception. J Neurophys. 1995; 73(2):820–35. Sainburg RL, Ghilardi MF, Poizner H, Ghez C. Control of limb dynamics in normal subjects and patients without proprioception. J Neurophys. 1995; 73(2):820–35.
6.
go back to reference Mussa-Ivaldi FA. Modular features of motor control and learning. Curr Opin Neurobiol. 1999; 9(6):713–7.CrossRefPubMed Mussa-Ivaldi FA. Modular features of motor control and learning. Curr Opin Neurobiol. 1999; 9(6):713–7.CrossRefPubMed
7.
go back to reference Mutsaarts M, Steenbergen B, Bekkering H. Anticipatory planning of movement sequences in hemiparetic cerebral palsy. Mot Control. 2005; 9(4):439–58.CrossRef Mutsaarts M, Steenbergen B, Bekkering H. Anticipatory planning of movement sequences in hemiparetic cerebral palsy. Mot Control. 2005; 9(4):439–58.CrossRef
10.
go back to reference Duque J, Thonnard JL, Vandermeeren Y, Sébire G, Cosnard G, Olivier E. Correlation between impaired dexterity and corticospinal tract dysgenesis in congenital hemiplegia. Brain. 2003; 126(Pt 3):732–47. doi:10.1093/brain/awg069.CrossRefPubMed Duque J, Thonnard JL, Vandermeeren Y, Sébire G, Cosnard G, Olivier E. Correlation between impaired dexterity and corticospinal tract dysgenesis in congenital hemiplegia. Brain. 2003; 126(Pt 3):732–47. doi:10.​1093/​brain/​awg069.CrossRefPubMed
12.
go back to reference Glencross DJ. Motor control and sensory-motor integration. Adv Psychol. 1995; 111:3–7.CrossRef Glencross DJ. Motor control and sensory-motor integration. Adv Psychol. 1995; 111:3–7.CrossRef
13.
go back to reference Goble DJ, Hurvitz EA, Brown SH. Deficits in the ability to use proprioceptive feedback in children with hemiplegic cerebral palsy. Int J Rehabil Res. Internationale Zeitschrift fur Rehabilitationsforschung. Revue internationale de recherches de readaptation. 2009; 32(3):267–9. 10.1097/MRR.0b013e32832a62d5.CrossRefPubMed Goble DJ, Hurvitz EA, Brown SH. Deficits in the ability to use proprioceptive feedback in children with hemiplegic cerebral palsy. Int J Rehabil Res. Internationale Zeitschrift fur Rehabilitationsforschung. Revue internationale de recherches de readaptation. 2009; 32(3):267–9. 10.​1097/​MRR.​0b013e32832a62d5​.CrossRefPubMed
15.
go back to reference Smyth MM, Mason UC. Use of proprioception in normal and clumsy children. Dev Med Child Neurol. 1998; 40(10):672–81.CrossRefPubMed Smyth MM, Mason UC. Use of proprioception in normal and clumsy children. Dev Med Child Neurol. 1998; 40(10):672–81.CrossRefPubMed
18.
20.
go back to reference Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 1971; 9(1):97–113.CrossRefPubMed Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 1971; 9(1):97–113.CrossRefPubMed
22.
23.
go back to reference Gay A, Harbst K, Kaufman KR, Hansen DK, Laskowski ER, Berger RA. New method of measuring wrist joint position sense avoiding cutaneous and visual inputs. J Neuroengineering Rehabil. 2010; 7:5. doi:10.1186/1743-0003-7-5.CrossRef Gay A, Harbst K, Kaufman KR, Hansen DK, Laskowski ER, Berger RA. New method of measuring wrist joint position sense avoiding cutaneous and visual inputs. J Neuroengineering Rehabil. 2010; 7:5. doi:10.​1186/​1743-0003-7-5.CrossRef
25.
go back to reference Schmidt RA, Lee T. Motor control and learning. Human kinetics. 1988. Schmidt RA, Lee T. Motor control and learning. Human kinetics. 1988.
26.
27.
go back to reference Bairstow PJ, Laszlo JI. Kinaesthetic sensitivity to passive movements and its relationship to motor development and motor control. Dev Med Child Neurol. 1981; 23(5):606–16.PubMed Bairstow PJ, Laszlo JI. Kinaesthetic sensitivity to passive movements and its relationship to motor development and motor control. Dev Med Child Neurol. 1981; 23(5):606–16.PubMed
28.
go back to reference 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 (New York). 1999; 283(5409):1908–11.CrossRef 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 (New York). 1999; 283(5409):1908–11.CrossRef
29.
go back to reference Sigmundsson H, Whiting HT, Loftesnes JM. Development of proprioceptive sensitivity. Exp Brain Res. 2000; 135(3):348–52.CrossRefPubMed Sigmundsson H, Whiting HT, Loftesnes JM. Development of proprioceptive sensitivity. Exp Brain Res. 2000; 135(3):348–52.CrossRefPubMed
31.
go back to reference Fry AF, Hale S. Relationships among processing speed, working memory, and fluid intelligence in children. Biological psychology. 2000; 54(1):1–34.CrossRefPubMed Fry AF, Hale S. Relationships among processing speed, working memory, and fluid intelligence in children. Biological psychology. 2000; 54(1):1–34.CrossRefPubMed
33.
go back to reference Hagert E. Proprioception of the wrist joint: a review of current concepts and possible implications on the rehabilitation of the wrist. J Hand Ther Off J Am Soc Hand Therapists; 23(1):2–1617. doi:10.1016/j.jht.2009.09.008. Hagert E. Proprioception of the wrist joint: a review of current concepts and possible implications on the rehabilitation of the wrist. J Hand Ther Off J Am Soc Hand Therapists; 23(1):2–1617. doi:10.​1016/​j.​jht.​2009.​09.​008.
36.
go back to reference Benes FM, Turtle M, Khan Y, Farol P. Myelination of a key relay zone in the hippocampal formation occurs in the human brain during childhood, adolescence, and adulthood. Arch Gen Psychiatr. 1994; 51(6):477–84.CrossRefPubMed Benes FM, Turtle M, Khan Y, Farol P. Myelination of a key relay zone in the hippocampal formation occurs in the human brain during childhood, adolescence, and adulthood. Arch Gen Psychiatr. 1994; 51(6):477–84.CrossRefPubMed
37.
go back to reference Black JE, Isaacs KR, Anderson BJ, Alcantara AA, Greenough WT. Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats. Proc Natl Acad Sci U S A. 1990; 87(14):5568–72.CrossRefPubMedPubMedCentral Black JE, Isaacs KR, Anderson BJ, Alcantara AA, Greenough WT. Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats. Proc Natl Acad Sci U S A. 1990; 87(14):5568–72.CrossRefPubMedPubMedCentral
39.
go back to reference Rogol AD, Clark PA, Roemmich JN. Growth and pubertal development in children and adolescents: effects of diet and physical activity. Am J Clin Nutr. 2000; 72(2 Suppl):521–8. Rogol AD, Clark PA, Roemmich JN. Growth and pubertal development in children and adolescents: effects of diet and physical activity. Am J Clin Nutr. 2000; 72(2 Suppl):521–8.
42.
go back to reference Gogtay N, Giedd JN, Lusk L, Hayashi KM, Greenstein D, Vaituzis AC, Nugent TF, Herman DH, Clasen LS, Toga AW, Rapoport JL, Thompson PM. Dynamic mapping of human cortical development during childhood through early adulthood. Proc Natl Acad Sci U S A. 2004; 101(21):8174–9. doi:10.1073/pnas.0402680101.CrossRefPubMedPubMedCentral Gogtay N, Giedd JN, Lusk L, Hayashi KM, Greenstein D, Vaituzis AC, Nugent TF, Herman DH, Clasen LS, Toga AW, Rapoport JL, Thompson PM. Dynamic mapping of human cortical development during childhood through early adulthood. Proc Natl Acad Sci U S A. 2004; 101(21):8174–9. doi:10.​1073/​pnas.​0402680101.CrossRefPubMedPubMedCentral
49.
go back to reference Hagert E, Forsgren S, Ljung BO. Differences in the presence of mechanoreceptors and nerve structures between wrist ligaments may imply differential roles in wrist stabilization. J Orthop Res Off Publ Orthop Res Soc. 2005; 23(4):757–63. doi:10.1016/j.orthres.2005.01.011.CrossRef Hagert E, Forsgren S, Ljung BO. Differences in the presence of mechanoreceptors and nerve structures between wrist ligaments may imply differential roles in wrist stabilization. J Orthop Res Off Publ Orthop Res Soc. 2005; 23(4):757–63. doi:10.​1016/​j.​orthres.​2005.​01.​011.CrossRef
53.
go back to reference Winward CE, Halligan PW, Wade DT. The Rivermead Assessment of Somatosensory Performance (RASP): standardization and reliability data. Clin Rehabil. 2002; 16(5):523–33.CrossRefPubMed Winward CE, Halligan PW, Wade DT. The Rivermead Assessment of Somatosensory Performance (RASP): standardization and reliability data. Clin Rehabil. 2002; 16(5):523–33.CrossRefPubMed
Metadata
Title
Robot-aided developmental assessment of wrist proprioception in children
Authors
Francesca Marini
Valentina Squeri
Pietro Morasso
Claudio Campus
Jürgen Konczak
Lorenzo Masia
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Journal of NeuroEngineering and Rehabilitation / Issue 1/2017
Electronic ISSN: 1743-0003
DOI
https://doi.org/10.1186/s12984-016-0215-9

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