The neural basis of central proprioceptive processing in older versus younger adults: An important sensory role for right putamen

Human Brain Mapping

Volumn 33, Issue 4, 2012, Pages 895-908

  Goble, Daniel J ^a,b   Coxon, James P ^a   Van Impe, Annouchka ^a   Geurts, Monique ^a   Van Hecke, Wim ^a   Sunaert, Stefan ^a   Wenderoth, Nicole ^a   Swinnen, Stephan P ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Aging; Basal ganglia; DTI; FMRI; Kinesthesis; Muscle spindle; Position sense; Proprioception

Indexed keywords

BIOLOGICAL MARKER;

ADULT; AGE; ANKLE; ARTICLE; BASAL GANGLION; BEHAVIOR; BRAIN CORTEX; BRAIN REGION; DIFFUSION TENSOR IMAGING; FOOT; FRACTIONAL ANISOTROPY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GROUPS BY AGE; HUMAN; MUSCLE EXCITATION; MUSCLE SPINDLE; NERVE CELL NETWORK; NORMAL HUMAN; PRIORITY JOURNAL; PROPRIOCEPTION; PUTAMEN; QUANTITATIVE ANALYSIS; SENSORY CORTEX; SOMATOSENSORY CORTEX; VIBRATION;

ADULT; AGED; AGED, 80 AND OVER; AGING; ANISOTROPY; ANKLE JOINT; BRAIN MAPPING; DIFFUSION TENSOR IMAGING; FEMALE; HUMANS; MALE; MIDDLE AGED; PHYSICAL STIMULATION; PROPRIOCEPTION; PUTAMEN; VIBRATION; YOUNG ADULT;

EID: 80755184439     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.21257     Document Type: Article

References (90)

1. Abe O, Yamasue H, Aoki S, Suga M, Yamada H, Kasai K, Masutani Y, Kato N, Kato N, Ohtomo K (2008): Aging in the CNS: Comparison of gray/white matter volume and diffusion tensor data. Neurobiol Aging 29: 102-116.
2. Adamovich SV, Berkinblit MB, Hening W, Sage J, Poizner H (2001): The interaction of visual and proprioceptive inputs in pointing to actual and remembered targets in Parkinson's disease. Neuroscience 104: 1027-1041.
3. Andersson JL, Hutton C, Ashburner J, Turner R, Friston K (2001): Modeling geometric deformations in EPI time series. Neuroimage 13: 903-919.
4. Beaulieu C (2002): The basis of anisotropic water diffusion in the nervous system-A technical review. NMR Biomed 15: 435-455.
5. Bhagat YA, Beaulieu C (2004): Diffusion anisotropy in subcortical white matter and cortical gray matter: Changes with aging and the role of CSF-suppression. J Magn Reson Imaging 20: 216-227.
6. Boska MD, Hasan KM, Kibuule D, Banerjee R, McIntyre E, Nelson JA, Hahn T, Gendelman HE, Mosley RL (2007): Quantitative diffusion tensor imaging detects dopaminergic neuronal degeneration in a murine model of Parkinson's disease. Neurobiol Dis 26: 590-596.
7. Brett M, Anton JL, Valabregue R, Poline JB (2002): Region of interest analysis using an SPM toolbox. In: 8th International Conference on Functional Mapping of the Human Brain, Sendai, Japan.
8. Chan LL, Rumpel H, Yap K, Lee E, Loo HV, Ho GL, Fook-Chong S, Yuen Y, Tan EK (2007): Case control study of diffusion tensor imaging in Parkinson's disease. J Neurol Neurosurg Psychiatry 78: 1383-1386.
9. Christensen MS, Lundbye-Jensen J, Geertsen SS, Petersen TH, Paulson OB, Nielsen JB (2007): Premotor cortex modulates somatosensory cortex during voluntary movements without proprioceptive feedback. Nat Neurosci 10: 417-419.
10. Corbetta M, Shulman GL (2002): Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3: 201-215.
11. Cordo P, Gurfinkel VS, Bevan L, Kerr GK (1995): Proprioceptive consequences of tendon vibration during movement. J Neurophysiol 74: 1675-1688.
12. Coxon JP, Goble DJ, Van IA, De VJ, Wenderoth N, Swinnen SP (2010): Reduced basal ganglia function when elderly switch between coordinated movement patterns. Cereb Cortex 20: 2368-2379.
13. Crutcher MD, DeLong MR (1984): Single cell studies of the primate putamen. I. Functional organization. Exp Brain Res 53: 233-243.
14. Daprati E, Sirigu A, Nico D (2010): Body and movement: Consciousness in the parietal lobes. Neuropsychologia 48: 756-762.
15. DeLong MR, Crutcher MD, Georgopoulos AP (1985): Primate globus pallidus and subthalamic nucleus: Functional organization. J Neurophysiol 53: 530-543.
16. Fjell AM, Walhovd KB, Fennema-Notestine C, McEvoy LK, Hagler DJ, Holland D, Brewer JB, Dale AM (2009): One-year brain atrophy evident in healthy aging. J Neurosci 29: 15223-15231.
17. Folstein MF, Folstein SE, McHugh PR (1975): "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12: 189-198.
18. Friston KJ, Holmes AP, Poline JB, Grasby PJ, Williams SC, Frackowiak RS, Turner R (1995): Analysis of fMRI time-series revisited. Neuroimage 2: 45-53.
19. Friston KJ, Rotshtein P, Geng JJ, Sterzer P, Henson RN (2006): A critique of functional localisers. Neuroimage 30: 1077-1087.
20. Goble DJ (2010): Proprioceptive acuity assessment via joint position matching: From basic science to general practice. Phys Ther 90: 1176-1184.
21. Goble DJ, Brown SH (2007): Task-dependent asymmetries in the utilization of proprioceptive feedback for goal-directed movement. Exp Brain Res 180: 693-704.
22. Goble DJ, Brown SH (2008a): The biological and behavioral basis of upper limb asymmetries in sensorimotor performance. Neurosci Biobehav Rev 32: 598-610.
23. Goble DJ, Brown SH (2008b): Upper limb asymmetries in the matching of proprioceptive versus visual targets. J Neurophysiol 99: 3063-3074.
24. Goble DJ, Brown SH (2009): Dynamic proprioceptive target matching behavior in the upper limb: Effects of speed, task difficulty and arm/hemisphere asymmetries. Behav Brain Res 200: 7-14.
25. Goble DJ, Brown SH (2010): Upper limb asymmetries in the perception of proprioceptively determined dynamic position sense. J Exp Psychol Hum Percept Perform 36: 768-775.
26. Goble DJ, Lewis CA, Hurvitz EA, Brown SH (2005): Development of upper limb proprioceptive accuracy in children and adolescents. Hum Mov Sci 24: 155-170.
27. Goble DJ, Lewis CA, Brown SH (2006): Upper limb asymmetries in the utilization of proprioceptive feedback. Exp Brain Res 168: 307-311.
28. Goble DJ, Coxon JP, Wenderoth N, Van IA, Swinnen SP (2009a): Proprioceptive sensibility in the elderly: Degeneration, functional consequences and plastic-adaptive processes. Neurosci Biobehav Rev 33: 271-278.
29. Goble DJ, Hurvitz EA, Brown SH (2009b): Deficits in the ability to use proprioceptive feedback in children with hemiplegic cerebral palsy. Int J Rehabil Res 32: 267-269.
30. Goble DJ, Noble BC, Brown SH (2009c): Proprioceptive target matching asymmetries in left-handed individuals. Exp Brain Res 197: 403-408.
31. Goble DJ, Coxon JP, Van IA, De VJ, Wenderoth N, Swinnen SP (2010): The neural control of bimanual movements in the elderly: Brain regions exhibiting age-related increases in activity, frequency-induced neural modulation, and task-specific compensatory recruitment. Hum Brain Mapp 31: 1281-1295.
32. Goodwin GM, McCloskey DI, Matthews PB (1972): Proprioceptive illusions induced by muscle vibration: Contribution by muscle spindles to perception? Science 175: 1382-1384.
33. Halligan PW, Marshall JC, Wade DT (1993): Three arms: A case study of supernumerary phantom limb after right hemisphere stroke. J Neurol Neurosurg Psychiatry 56: 159-166.
34. Hasan KM (2010): Simple linear regression model is misleading when used to analyze quantitative diffusion tensor imaging data that include young and old adults. AJNR Am J Neuroradiol 31: E80.
35. Henry F (1974): Variable and constant performance errors within a group of individuals. J Mot Behav 6: 149-154.
36. Heuninckx S, Wenderoth N, Debaere F, Peeters R, Swinnen SP (2005): Neural basis of aging: The penetration of cognition into action control. J Neurosci 25: 6787-6796.
37. Heuninckx S, Wenderoth N, Swinnen SP (2008): Systems neuroplasticity in the aging brain: Recruiting additional neural resources for successful motor performance in elderly persons. J Neurosci 28: 91-99.
38. Hurley MV, Rees J, Newham DJ (1998): Quadriceps function, proprioceptive acuity and functional performance in healthy young, middle-aged and elderly subjects. Age Ageing 27: 55-62.
39. Jones DK, Basser PJ (2004): "Squashing peanuts and smashing pumpkins": How noise distorts diffusion-weighted MR data. Magn Reson Med 52: 979-993.
40. Kaasinen V, Rinne JO (2002): Functional imaging studies of dopamine system and cognition in normal aging and Parkinson's disease. Neurosci Biobehav Rev 26: 785-793.
41. Kavounoudias A, Roll JP, Anton JL, Nazarian B, Roth M, Roll R (2008): Proprio-tactile integration for kinesthetic perception: An fMRI study. Neuropsychologia 46: 567-575.
42. Konczak J, Corcos DM, Horak F, Poizner H, Shapiro M, Tuite P, Volkmann J, Maschke M (2009): Proprioception and motor control in Parkinson's disease. J Mot Behav 41: 543-552.
43. Kunzle H (1975): Bilateral projections from precentral motor cortex to the putamen and other parts of the basal ganglia. An autoradiographic study in Macaca fascicularis. Brain Res 88: 195-209.
44. Kunzle H (1977): Projections from the primary somatosensory cortex to basal ganglia and thalamus in the monkey. Exp Brain Res 30: 481-492.
45. Lajoie Y, Teasdale N, Cole JD, Burnett M, Bard C, Fleury M, Forget R, Paillard J, Lamarre Y (1996): Gait of a deafferented subject without large myelinated sensory fibers below the neck. Neurology 47: 109-115.
46. Le Bihan D (2003): Looking into the functional architecture of the brain with diffusion MRI. Nat Rev Neurosci 4: 469-480.
47. LeBel C, Walker L, Leemans A, Phillips L, Beaulieu C (2008): Microstructural maturation of the human brain from childhood to adulthood. Neuroimage 40: 1044-1055.
48. Leemans A, Jones DK (2009): The B-matrix must be rotated when correcting for subject motion in DTI data. Magn Reson Med 61: 1336-1349.
49. Leemans A, Jeurissen B, Sijbers J, Jones DK (2009): ExploreDTI: A Graphical Toolbox for Processing, Analyzing, and Visualizing Diffusion MR Data. In: 17th Annual Meeting of Intl Soc Mag Reson Med, Hawaii, USA. p 3537.
50. Lehericy S, Ducros M, Krainik A, Francois C, Van de Moortele PF, Ugurbil K, Kim DS (2004): 3-D diffusion tensor axonal tracking shows distinct SMA and pre-SMA projections to the human striatum. Cereb Cortex 14: 1302-1309.
51. Lemon RN, van der Burg J (1979): Short-latency peripheral inputs to thalamic neurones projecting to the motor cortex in the monkey. Exp Brain Res 36: 445-462.
52. Lidsky TI, Manetto C, Schneider JS (1985): A consideration of sensory factors involved in motor functions of the basal ganglia. Brain Res 356: 133-146.
53. Liu JX, Eriksson PO, Thornell LE, Pedrosa-Domellof F (2005): Fiber content and myosin heavy chain composition of muscle spindles in aged human biceps brachii. J Histochem Cytochem 53: 445-454.
54. Maschke M, Gomez CM, Tuite PJ, Konczak J (2003): Dysfunction of the basal ganglia, but not the cerebellum, impairs kinaesthesia. Brain 126: 2312-2322.
55. McChesney JW, Woollacott MH (2000): The effect of age-related declines in proprioception and total knee replacement on postural control. J Gerontol A Biol Sci Med Sci 55: M658-M666.
56. Mima T, Sadato N, Yazawa S, Hanakawa T, Fukuyama H, Yonekura Y, Shibasaki H (1999): Brain structures related to active and passive finger movements in man. Brain 122 (Part 10): 1989-1997.
57. Miwa T, Miwa Y, Kanda K (1995): Dynamic and static sensitivities of muscle spindle primary endings in aged rats to ramp stretch. Neurosci Lett 201: 179-182.
58. Montant M, Romaiguere P, Roll JP (2009): A new vibrator to stimulate muscle proprioceptors in fMRI. Hum Brain Mapp 30: 990-997.
59. Naito E (2004): Sensing limb movements in the motor cortex: How humans sense limb movement. Neuroscientist 10: 73-82.
60. Naito E, Roland PE, Grefkes C, Choi HJ, Eickhoff S, Geyer S, Zilles K, Ehrsson HH (2005): Dominance of the right hemisphere and role of area 2 in human kinesthesia. J Neurophysiol 93: 1020-1034.
61. Naito E, Nakashima T, Kito T, Aramaki Y, Okada T, Sadato N (2007): Human limb-specific and non-limb-specific brain representations during kinesthetic illusory movements of the upper and lower extremities. Eur J Neurosci 25: 3476-3487.
62. Oldfield RC (1971): The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia 9: 97-113.
63. Pfefferbaum A, Adalsteinsson E, Rohlfing T, Sullivan EV (2010): Diffusion tensor imaging of deep gray matter brain structures: Effects of age and iron concentration. Neurobiol Aging 31: 482-493.
64. Phillips CG, Powell TP, Wiesendanger M (1971): Projection from low-threshold muscle afferents of hand and forearm to area 3a of baboon's cortex. J Physiol 217: 419-446.
65. Roll JP, Vedel JP (1982): Kinaesthetic role of muscle afferents in man, studied by tendon vibration and microneurography. Exp Brain Res 47: 177-190.
66. Roll JP, Vedel JP, Ribot E (1989): Alteration of proprioceptive messages induced by tendon vibration in man: A microneurographic study. Exp Brain Res 76: 213-222.
67. Romaiguere P, Anton JL, Roth M, Casini L, Roll JP (2003): Motor and parietal cortical areas both underlie kinaesthesia. Brain Res Cogn Brain Res 16: 74-82.
68. Rothwell JC, Traub MM, Day BL, Obeso JA, Thomas PK, Marsden CD (1982): Manual motor performance in a deafferented man. Brain 105 (Part 3): 515-542.
69. Sainburg RL, Ghilardi MF, Poizner H, Ghez C (1995): Control of limb dynamics in normal subjects and patients without proprioception. J Neurophysiol 73: 820-835.
70. Schoenbaum G, Roesch MR, Stalnaker TA, Takahashi YK (2009): A new perspective on the role of the orbitofrontal cortex in adaptive behaviour. Nat Rev Neurosci 10: 885-892.
71. Seidler RD, Bernard JA, Burutolu TB, Fling BW, Gordon MT, Gwin JT, Kwak Y, Lipps DB (2010): Motor control and aging: Links to age-related brain structural, functional, and biochemical effects. Neurosci Biobehav Rev 34: 721-733.
72. Snook L, Paulson LA, Roy D, Phillips L, Beaulieu C (2005): Diffusion tensor imaging of neurodevelopment in children and young adults. Neuroimage 26: 1164-1173.
73. Swash M, Fox KP (1972): The effect of age on human skeletal muscle. Studies of the morphology and innervation of muscle spindles. J Neurol Sci 16: 417-432.
74. Swinnen SP, Steyvers M, Van Den BL, Stelmach GE (2000): Motor learning and Parkinson's disease: Refinement of within-limb and between-limb coordination as a result of practice. Behav Brain Res 111: 45-59.
75. Talairach J, Tournaux P (1998): Co-planar Stereotaxic Atlas of the Human Brain. Stuttgart: Thieme.
76. Tanji J, Wise SP (1981): Submodality distribution in sensorimotor cortex of the unanesthetized monkey. J Neurophysiol 45: 467-481.
77. Vaillancourt DE, Spraker MB, Prodoehl J, Abraham I, Corcos DM, Zhou XJ, Comella CL, Little DM (2009): High-resolution diffusion tensor imaging in the substantia nigra of de novo Parkinson disease. Neurology 72: 1378-1384.
78. Van Hecke W, Leemans A, D'Agostino E, De BS, Vandervliet E, Parizel PM, Sijbers J (2007): Nonrigid coregistration of diffusion tensor images using a viscous fluid model and mutual information. IEEE Trans Med Imaging 26: 1598-1612.
79. Van Hecke W, Sijbers J, D'Agostino E, Maes F, De BS, Vandervliet E, Parizel PM, Leemans A (2008): On the construction of an inter-subject diffusion tensor magnetic resonance atlas of the healthy human brain. Neuroimage 43: 69-80.
80. Van Impe A, Coxon JP, Goble DJ, Wenderoth N, Swinnen SP (2009): Ipsilateral coordination at preferred rate: Effects of age, body side and task complexity. Neuroimage 47: 1854-1862.
81. Wang Q, Xu X, Zhang M (2010): Normal aging in the basal ganglia evaluated by eigenvalues of diffusion tensor imaging. AJNR Am J Neuroradiol 31: 516-520.
82. Ward NS, Frackowiak RS (2003): Age-related changes in the neural correlates of motor performance. Brain 126: 873-888.
83. Ward NS, Swayne OB, Newton JM (2008): Age-dependent changes in the neural correlates of force modulation: An fMRI study. Neurobiol Aging 29: 1434-1446.
84. Weiller C, Juptner M, Fellows S, Rijntjes M, Leonhardt G, Kiebel S, Muller S, Diener HC, Thilmann AF (1996): Brain representation of active and passive movements. Neuroimage 4: 105-110.
85. Wong YC, Kwan HC, MacKay WA, Murphy JT (1978): Spatial organization of precentral cortex in awake primates. I. Somatosensory inputs. J Neurophysiol 41: 1107-1119.
86. Wu T, Hallett M (2005): The influence of normal human ageing on automatic movements. J Physiol 562: 605-615.
87. Yoshikawa K, Nakata Y, Yamada K, Nakagawa M (2004): Early pathological changes in the parkinsonian brain demonstrated by diffusion tensor MRI. J Neurol Neurosurg Psychiatry 75: 481-484.
88. Zhang Y, Du AT, Hayasaka S, Jahng GH, Hlavin J, Zhan W, Weiner MW, Schuff N (2010): Patterns of age-related water diffusion changes in human brain by concordance and discordance analysis. Neurobiol Aging 31: 1991-2001.
89. Zia S, Cody F, O'Boyle D (2000): Joint position sense is impaired by Parkinson's disease. Ann Neurol 47: 218-228.
90. Zia S, Cody FW, O'Boyle DJ (2002): Identification of unilateral elbow-joint position is impaired by Parkinson's disease. Clin Anat 15: 23-31.