Brain activity during complex imagined gait tasks in Parkinson disease

Clinical Neurophysiology

Volumn 125, Issue 5, 2014, Pages 995-1005

  Peterson, Daniel S ^a   Pickett, Kristen A ^a,b   Duncan, Ryan P ^a   Perlmutter, Joel S ^a,b,c   Earhart, Gammon M ^a,b  

^a WASHINGTON UNIVERSITY   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

FMRI; Gait; Imagery; Parkinson disease

Indexed keywords

AGED; ARTICLE; BOLD SIGNAL; BRAIN FUNCTION; CEREBELLUM; CLINICAL ARTICLE; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GLOBUS PALLIDUS; HEAD MOVEMENT; HUMAN; IMAGERY; LOCOMOTION; MESENCEPHALON; NEUROLOGIC GAIT DISORDER; PARKINSON DISEASE; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; PUTAMEN; SUPPLEMENTARY MOTOR AREA; WALKING SPEED; ADULT; BETA RHYTHM; BRAIN REGION; COMPARATIVE STUDY; CORRELATION ANALYSIS; FUNCTIONAL NEUROIMAGING; GAIT; MOTOR ACTIVITY; MOTOR PERFORMANCE; NEUROPHYSIOLOGY; NUCLEAR MAGNETIC RESONANCE SCANNER; TASK PERFORMANCE; WALKING DIFFICULTY;

FMRI; GAIT; IMAGERY; PARKINSON DISEASE;

AGED; CEREBELLUM; GAIT; GAIT DISORDERS, NEUROLOGIC; GLOBUS PALLIDUS; HUMANS; IMAGINATION; LOCOMOTION; MAGNETIC RESONANCE IMAGING; MIDDLE AGED; MOTOR CORTEX; PARKINSON DISEASE; WALKING;

EID: 84897519137     PISSN: 13882457     EISSN: 18728952     Source Type: Journal    
DOI: 10.1016/j.clinph.2013.10.008     Document Type: Article

References (79)

1. Alexander G.E., DeLong M.R., Strick P.L. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 1986, 9:357-381.
2. Almeida Q.J., Frank J.S., Roy E.A., Jenkins M.E., Spaulding S., Patla A.E., et al. An evaluation of sensorimotor integration during locomotion toward a target in Parkinson's disease. Neuroscience 2005, 134:283-293.
3. Androulidakis A.G., Kuhn A.A., Chen C.C., Blomstedt P., Kempf F., Kupsch A., et al. Dopaminergic therapy promotes lateralized motor activity in the subthalamic area in Parkinson's disease. Brain 2007, 130:457-468.
4. Bakker M., De Lange F.P., Helmich R.C., Scheeringa R., Bloem B.R., Toni I. Cerebral correlates of motor imagery of normal and precision gait. Neuroimage 2008, 41:998-1010.
5. Brown P., Eusebio A. Paradoxes of functional neurosurgery: clues from basal ganglia recordings. Mov Disord 2008, 23:12-20. quiz 158.
6. Brown P., Mazzone P., Oliviero A., Altibrandi M.G., Pilato F., Tonali P.A., et al. Effects of stimulation of the subthalamic area on oscillatory pallidal activity in Parkinson's disease. Exp Neurol 2004, 188:480-490.
7. Brown P., Oliviero A., Mazzone P., Insola A., Tonali P., Di Lazzaro V. Dopamine dependency of oscillations between subthalamic nucleus and pallidum in Parkinson's disease. J Neurosci 2001, 21:1033-1038.
8. Bruck A., Aalto S., Nurmi E., Vahlberg T., Bergman J., Rinne J.O. Striatal subregional 6-[18F]fluoro-l-dopa uptake in early Parkinson's disease: a two-year follow-up study. Mov Disord 2006, 21:958-963.
9. Cassidy M., Mazzone P., Oliviero A., Insola A., Tonali P., Di Lazzaro V., et al. Movement-related changes in synchronization in the human basal ganglia. Brain 2002, 125:1235-1246.
10. Cremers J., D'Ostilio K., Stamatakis J., Delvaux V., Garraux G. Brain activation pattern related to gait disturbances in Parkinson's disease. Mov Disord 2012, 27:1498-1505.
11. Cremers J., Dessoullieres A., Garraux G. Hemispheric specialization during mental imagery of brisk walking. Hum Brain Mapp 2012, 33:873-882.
12. de Lange F.P., Hagoort P., Toni I. Neural topography and content of movement representations. J Cogn Neurosci 2005, 17:97-112.
13. DeArmond S., Fusco M., Maynard M. Structure of the human brain: a photographic atlas 1989, Oxford University Press, New York. 3rd ed.
14. Deiber M.P., Ibanez V., Honda M., Sadato N., Raman R., Hallett M. Cerebral processes related to visuomotor imagery and generation of simple finger movements studied with positron emission tomography. Neuroimage 1998, 7:73-85.
15. Foreman K.B., Addison O., Kim H.S., Dibble L.E. Testing balance and fall risk in persons with Parkinson disease, an argument for ecologically valid testing. Parkinson Relat Disord 2011, 17:166-171.
16. Fritz S., Lusardi M. White paper: "walking speed: the sixth vital sign". J Geriatr Phys Ther 2009, 32:46-49.
17. Glick S.D., Ross D.A., Hough L.B. Lateral asymmetry of neurotransmitters in human brain. Brain Res 1982, 234:53-63.
18. Godde B., Voelcker-Rehage C. More automation and less cognitive control of imagined walking movements in high- versus low-fit older adults. Front Aging Neurosci 2010, 2.
19. Goense J.B., Logothetis N.K. Neurophysiology of the BOLD fMRI signal in awake monkeys. Curr Biol 2008, 18:631-640.
20. Hackney M.E., Earhart G.M. Backward walking in Parkinson's disease. Mov Disord 2009, 24:218-223.
21. Hammond C., Bergman H., Brown P. Pathological synchronization in Parkinson's disease: networks, models and treatments. Trends Neurosci 2007, 30:357-364.
22. Hanakawa T., Katsumi Y., Fukuyama H., Honda M., Hayashi T., Kimura J., et al. Mechanisms underlying gait disturbance in Parkinson's disease: a single photon emission computed tomography study. Brain 1999, 122:1271-1282.
23. Hausdorff J.M., Cudkowicz M.E., Firtion R., Wei J.Y., Goldberger A.L. Gait variability and basal ganglia disorders: stride-to-stride variations of gait cycle timing in Parkinson's disease and Huntington's disease. Mov Disord 1998, 13:428-437.
24. Hirsch E.C., Graybiel A.M., Duyckaerts C., Javoy-Agid F. Neuronal loss in the pedunculopontine tegmental nucleus in Parkinson disease and in progressive supranuclear palsy. Proc Natl Acad Sci USA 1987, 84:5976-5980.
25. Horak F.B., Dimitrova D., Nutt J.G. Direction-specific postural instability in subjects with Parkinson's disease. Exp Neurol 2005, 193:504-521.
26. Hughes A.J., Daniel S.E., Kilford L., Lees A.J. Accuracy of clinical diagnosis of idiopathic Parkinson's disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 1992, 55:181-184.
27. Iansek R., Huxham F., McGinley J. The sequence effect and gait festination in Parkinson disease: contributors to freezing of gait?. Mov Disord 2006, 21:1419-1424.
28. Immisch I., Waldvogel D., van Gelderen P., Hallett M. The role of the medial wall and its anatomical variations for bimanual antiphase and in-phase movements. Neuroimage 2001, 14:674-684.
29. Jahanshahi M., Jenkins I.H., Brown R.G., Marsden C.D., Passingham R.E., Brooks D.J. Self-initiated versus externally triggered movements. I. An investigation using measurement of regional cerebral blood flow with PET and movement-related potentials in normal and Parkinson's disease subjects. Brain 1995, 118:913-933.
30. Jahn K., Deutschlander A., Stephan T., Kalla R., Hufner K., Wagner J., et al. Supraspinal locomotor control in quadrupeds and humans. Prog Brain Res 2008, 171:353-362.
31. Jahn K., Deutschlander A., Stephan T., Kalla R., Wiesmann M., Strupp M., et al. Imaging human supraspinal locomotor centers in brainstem and cerebellum. Neuroimage 2008, 39:786-792.
32. Jahn K., Deutschlander A., Stephan T., Strupp M., Wiesmann M., Brandt T. Brain activation patterns during imagined stance and locomotion in functional magnetic resonance imaging. Neuroimage 2004, 22:1722-1731.
33. Jahn K., Zwergal A. Imaging supraspinal locomotor control in balance disorders. Restor Neurol Neurosci 2010, 28:105-114.
34. Jeannerod M., Decety J. Mental motor imagery: a window into the representational stages of action. Curr Opin Neurobiol 1995, 5:727-732.
35. Karachi C., Grabli D., Bernard F.A., Tande D., Wattiez N., Belaid H., et al. Cholinergic mesencephalic neurons are involved in gait and postural disorders in Parkinson disease. J Clin Invest 2010, 120:2745-2754.
36. Karimi M., Golchin N., Tabbal S.D., Hershey T., Videen T.O., Wu J., et al. Subthalamic nucleus stimulation-induced regional blood flow responses correlate with improvement of motor signs in Parkinson disease. Brain 2008, 131:2710-2719.
37. Kish S.J., Shannak K., Hornykiewicz O. Uneven pattern of dopamine loss in the striatum of patients with idiopathic Parkinson's disease. Pathophysiologic and clinical implications. N Engl J Med 1988, 318:876-880.
38. Kooistra C.A., Heilman K.M. Motor dominance and lateral asymmetry of the globus pallidus. Neurology 1988, 38:388-390.
39. Kostic V.S., Agosta F., Pievani M., Stefanova E., Jecmenica-Lukic M., Scarale A., et al. Pattern of brain tissue loss associated with freezing of gait in Parkinson disease. Neurology 2012, 78:409-416.
40. Kuhn A.A., Doyle L., Pogosyan A., Yarrow K., Kupsch A., Schneider G.H., et al. Modulation of beta oscillations in the subthalamic area during motor imagery in Parkinson's disease. Brain 2006, 129:695-706.
41. Kuhn A.A., Kupsch A., Schneider G.H., Brown P. Reduction in subthalamic 8-35Hz oscillatory activity correlates with clinical improvement in Parkinson's disease. Eur J Neurosci 2006, 23:1956-1960.
42. la Fougere C., Zwergal A., Rominger A., Forster S., Fesl G., Dieterich M., et al. Real versus imagined locomotion: a [18F]-FDG PET-fMRI comparison. Neuroimage 2010, 50:1589-1598.
43. Logothetis N.K. The neural basis of the blood-oxygen-level-dependent functional magnetic resonance imaging signal. Philos Trans R Soc Lond B Biol Sci 2002, 357:1003-1037.
44. Logothetis N.K. What we can do and what we cannot do with fMRI. Nature 2008, 453:869-878.
45. Malouin F., Richards C.L., Jackson P.L., Dumas F., Doyon J. Brain activations during motor imagery of locomotor-related tasks: a PET study. Hum Brain Mapp 2003, 19:47-62.
46. Malouin F., Richards C.L., Jackson P.L., Lafleur M.F., Durand A., Doyon J. The kinesthetic and visual imagery questionnaire (KVIQ) for assessing motor imagery in persons with physical disabilities: a reliability and construct validity study. J Neurol Phys Ther 2007, 31:20-29.
47. Miyai I., Tanabe H.C., Sase I., Eda H., Oda I., Konishi I., et al. Cortical mapping of gait in humans: a near-infrared spectroscopic topography study. Neuroimage 2001, 14:1186-1192.
48. Mori S., Matsui T., Kuze B., Asanome M., Nakajima K., Matsuyama K. Stimulation of a restricted region in the midline cerebellar white matter evokes coordinated quadrupedal locomotion in the decerebrate cat. J Neurophysiol 1999, 82:290-300.
49. Morris M.E., Iansek R., Matyas T.A., Summers J.J. Stride length regulation in Parkinson's disease. Normalization strategies and underlying mechanisms. Brain 1996, 119:551-568.
50. Muslimovic D., Post B., Speelman J.D., Schmand B., de Haan R.J. Determinants of disability and quality of life in mild to moderate Parkinson disease. Neurology 2008, 70:2241-2247.
51. Nieuwboer A., Rochester L., Herman T., Vandenberghe W., Emil G.E., Thomaes T., et al. Reliability of the new freezing of gait questionnaire: agreement between patients with Parkinson's disease and their carers. Gait Posture 2009, 30:459-463.
52. Orlovsky G.N. Spontaneous and induced locomotion of the thalamic cat. Biophysics 1969, 14:1154-1162.
53. Pahapill P.A., Lozano A.M. The pedunculopontine nucleus and Parkinson's disease. Brain 2000, 123:1767-1783.
54. Palmer S.J., Li J., Wang Z.J., McKeown M.J. Joint amplitude and connectivity compensatory mechanisms in Parkinson's disease. Neuroscience 2010, 166:1110-1118.
55. Peterson D.S., Pickett K.A., Earhart G.M. Effects of levodopa on vivedness of motor imagery in Parkinson disease. J Parkinsons Dis 2012, 2:127-133.
56. Peterson D.S., Plotnik M., Hausdorff J.M., Earhart G.M. Evidence for a relationship between bilateral coordination during complex gait tasks and freezing of gait in Parkinson's disease. Parkinson Relat Disord 2012, 18:1022-1026.
57. Pickett K.A., Peterson D.S., Earhart G.M. Motor imagery of gait tasks in individuals with Parkinson disease. J Parkinsons Dis 2012, 2:19-22.
58. Playford E.D., Jenkins I.H., Passingham R.E., Nutt J., Frackowiak R.S., Brooks D.J. Impaired mesial frontal and putamen activation in Parkinson's disease: a positron emission tomography study. Ann Neurol 1992, 32:151-161.
59. Plotnik M., Giladi N., Hausdorff J.M. Bilateral coordination of walking and freezing of gait in Parkinson's disease. Eur J Neurosci 2008, 27:1999-2006.
60. Porro C.A., Francescato M.P., Cettolo V., Diamond M.E., Baraldi P., Zuiani C., et al. Primary motor and sensory cortex activation during motor performance and motor imagery: a functional magnetic resonance imaging study. J Neurosci 1996, 16:7688-7698.
61. Prodoehl J., Spraker M., Corcos D., Comella C., Vaillancourt D. Blood oxygenation level-dependent activation in basal ganglia nuclei relates to specific symptoms in de novo Parkinson's disease. Mov Disord 2010, 25:2035-2043.
62. Racette B.A., Rundle M., Parsian A., Perlmutter J.S. Evaluation of a screening questionnaire for genetic studies of Parkinson's disease. Am J Med Genet 1999, 88:539-543.
63. Schaafsma J.D., Balash Y., Gurevich T., Bartels A.L., Hausdorff J.M., Giladi N. Characterization of freezing of gait subtypes and the response of each to levodopa in Parkinson's disease. Eur J Neurol 2003, 10:391-398.
64. Schmid A., Duncan P.W., Studenski S., Lai S.M., Richards L., Perera S., et al. Improvements in speed-based gait classifications are meaningful. Stroke 2007, 38:2096-2100.
65. Schweder P.M., Hansen P.C., Green A.L., Quaghebeur G., Stein J., Aziz T.Z. Connectivity of the pedunculopontine nucleus in Parkinsonian freezing of gait. NeuroReport 2010, 21:914-916.
66. Shik M.L., Severin F.V., Orlovsky G.N. Control of walking and running by means of electrical stimulation of the mesencephalon. Electroencephalogr Clin Neurophysiol 1969, 26:549.
67. Snijders A.H., Leunissen I., Bakker M., Overeem S., Helmich R.C., Bloem B.R., et al. Gait-related cerebral alterations in patients with Parkinson's disease with freezing of gait. Brain 2011, 134:59-72.
68. Spildooren J., Vercruysse S., Desloovere K., Vandenberghe W., Kerckhofs E., Nieuwboer A. Freezing of gait in Parkinson's disease: the impact of dual-tasking and turning. Mov Disord 2010, 25:2563-2570.
69. Spraker M.B., Prodoehl J., Corcos D.M., Comella C.L., Vaillancourt D.E. Basal ganglia hypoactivity during grip force in drug naive Parkinson's disease. Hum Brain Mapp 2010, 31:1928-1941.
70. St.George R.J., Nutt J.G., Burchiel K.J., Horak F.B. A meta-regression of the long-term effects of deep brain stimulation on balance and gait in PD. Neurology 2010, 75:1292-1299.
71. Studenski S., Perera S., Patel K., Rosano C., Faulkner K., Inzitari M., et al. Gait speed and survival in older adults. JAMA 2011, 305:50-58.
72. Suzuki M., Miyai I., Ono T., Oda I., Konishi I., Kochiyama T., et al. Prefrontal and premotor cortices are involved in adapting walking and running speed on the treadmill: an optical imaging study. Neuroimage 2004, 23:1020-1026.
73. Talairach J., Tournoux P. Co-planar stereotaxic atlas of the human brain 1998, Thieme, New York.
74. Verghese J., Holtzer R., Lipton R.B., Wang C. Quantitative gait markers and incident fall risk in older adults. J Gerontol A Biol Sci Med Sci 2009, 64:896-901.
75. Wagner J., Stephan T., Kalla R., Bruckmann H., Strupp M., Brandt T., et al. Mind the bend: cerebral activations associated with mental imagery of walking along a curved path. Exp Brain Res 2008, 191:247-255.
76. Wai Y.Y., Wang J.J., Weng Y.H., Lin W.Y., Ma H.K., Ng S.H., et al. Cortical involvement in a gait-related imagery task: comparison between Parkinson's disease and normal aging. Parkinson Relat Disord 2012, 18:537-542.
77. Woosley T., Hanaway J., Gado M. The brain atlas: a visual guide to the human central nervous system 2008, John Wiley & Sons, Hoboken, New Jersey. 3rd ed.
78. Wu T., Wang L., Hallett M., Li K., Chan P. Neural correlates of bimanual anti-phase and in-phase movements in Parkinson's disease. Brain 2010, 133:2394-2409.
79. Zwergal A., Linn J., Xiong G., Brandt T., Strupp M., Jahn K. Aging of human supraspinal locomotor and postural control in fMRI. Neurobiol Aging 2012, 33:1073-1084.