Cerebral pathological and compensatory mechanisms in the premotor phase of leucine-rich repeat kinase 2 parkinsonism

Brain

Volumn 135, Issue 12, 2012, Pages 3687-3698

  Van Nuenen, Bart F L ^a,b   Helmich, Rick C ^a,b   Ferraye, Murielle ^b   Thaler, Avner ^c   Hendler, Talma ^c   Orr Urtreger, Avi ^c   Mirelman, Anat ^c   Bressman, Susan ^d   Marder, Karen S ^e   Giladi, Nir ^c   Van De Warrenburg, Bart P C ^a   Bloem, Bastiaan R ^a   Toni, Ivan ^b  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^c TEL AVIV SOURASKY MEDICAL CENTER   (Israel)

^d BETH ISRAEL MEDICAL CENTER   (United States)

^e Taub Institute for Research on Alzheimer's Disease and the Aging Brain and the Gertrude H Sergievsky Center   (United States)

Author keywords

compensation; functional MRI; motor imagery; Parkinon's disease; premotor LRRK2 parkinsonism

Indexed keywords

LEUCINE RICH REPEAT KINASE 2;

ADULT; ARTICLE; BIOMECHANICS; BODY POSTURE; BRAIN FUNCTION; CAUDATE NUCLEUS; CONTROLLED STUDY; DISEASE COURSE; EVOKED CORTICAL RESPONSE; EVOKED MUSCLE RESPONSE; EXTRASTRIATE BODY AREA; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GENE MUTATION; HAND MOVEMENT; HETEROZYGOTE; HUMAN; IMAGERY; LATENT PERIOD; MALE; MENTAL PERFORMANCE; MOTOR CONTROL; NEUROPATHOLOGY; NORMAL HUMAN; PARKINSONISM; PREMOTOR CORTEX; PRIORITY JOURNAL; RELATIVE;

EID: 84871755387     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/aws288     Document Type: Article

References (73)

1. Alcalay RN, Caccappolo E, Mejia-Santana H, Tang MX, Rosado L, Orbe Reilly M, et al. Cognitive performance of GBA mutation carriers with early-onset PD: the CORE-PD study. Neurology 2012; 78: 1434-40.
2. Alexander GE, DeLong MR, Strick PL. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 1986; 9: 357-81.
3. Ashburner J. A fast diffeomorphic image registration algorithm. Neuroimage 2007; 38: 95-113.
4. Ashburner J, Friston K. Multimodal image coregistration and partition-ing-a unified framework. Neuroimage 1997; 6: 209-17.
5. Astafiev SV, Stanley CM, Shulman GL, Corbetta M. Extrastriate body area in human occipital cortex responds to the performance of motor actions. Nat Neurosci 2004; 7: 542-8.
6. Baumer T, Pramstaller PP, Siebner HR, Schippling S, Hagenah J, Peller M, et al. Sensorimotor integration is abnormal in asymptomatic Parkin mutation carriers: a TMS study. Neurology 2007; 69: 1976-81.
7. Bezard E, Gross CE, Brotchie JM. Presymptomatic compensation in Parkinson's disease is not dopamine-mediated. Trends Neurosci 2003; 26: 215-21.
8. Binkofski F, Reetz K, Gaser C, Hilker R, Hagenah J, Hedrich K, et al. Morphometric fingerprint of asymptomatic Parkin and PINK1 mutation carriers in the basal ganglia. Neurology 2007; 69: 842-50.
9. Broussolle E, Lucking CB, Ginovart N, Pollak P, Remy P, Durr A. [18 F]-dopa PET study in patients with juvenile-onset PD and parkin gene mutations. Neurology 2000; 55: 877-9.
10. Brown RG, Marsden CD. Internal versus external cues and the control of attention in Parkinson's disease. Brain 1988; 111 (Pt 2): 323-45.
11. Bruggemann N, Hagenah J, Stanley K, Klein C, Wang C, Raymond D, et al. Substantia nigra hyperechogenicity with LRRK2 G2019S mutations. Mov Disord 2011; 26: 885-8.
12. Buhmann C, Binkofski F, Klein C, Buchel C, van Eimeren T, Erdmann C, et al. Motor reorganization in asymptomatic carriers of a single mutant Parkin allele: a human model for presymptomatic parkinsonism. Brain 2005; 128: 2281-90.
13. Cools R, D'Esposito M. Inverted-U-shaped dopamine actions on human working memory and cognitive control. Biol Psychiatry 2011; 69: e113-25.
14. de Lange FP, Hagoort P, Toni I. Neural topography and content of movement representations. J Cogn Neurosci 2005; 17: 97-112.
15. de Lange FP, Helmich RC, Toni I. Posture influences motor imagery: an fMRI study. Neuroimage 2006; 33: 609-17.
16. de Lange FP, Jensen O, Bauer M, Toni I. Interactions between posterior gamma and frontal alpha/beta oscillations during imagined actions. Front Hum Neurosci 2008a; 2: 7.
17. de Lange FP, Roelofs K, Toni I. Motor imagery: a window into the mechanisms and alterations of the motor system. Cortex 2008b; 44: 494-506.
18. Dominey P, Decety J, Broussolle E, Chazot G, Jeannerod M. Motor imagery of a lateralized sequential task is asymmetrically slowed in hemi-Parkinson's patients. Neuropsychologia 1995; 33: 727-41.
19. Downing PE, Jiang Y, Shuman M, Kanwisher N. A cortical area selective for visual processing of the human body. Science 2001; 293: 2470-3.
20. Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, et al. A new SPM toolbox for combining probabilistic cytoarchitec-tonic maps and functional imaging data. Neuroimage 2005; 25: 1325-35.
21. Escola L, Michelet T, Macia F, Guehl D, Bioulac B, Burbaud P. Disruption of information processing in the supplementary motor area of the MPTP-treated monkey: a clue to the pathophysiology of akinesia? Brain 2003; 126: 95-114.
22. Farrer MJ. Genetics of Parkinson disease: paradigm shifts and future prospects. Nat Rev Genet 2006; 7: 306-18.
23. Friston KJ, Ashburner J, Frith CD, Poline J-B, Heather JD, Frackowiak RS. Spatial registration and normalization of images. Hum Brain Mapp 1995; 3: 165-89.
24. Friston KJ, Buechel C, Fink GR, Morris J, Rolls E, Dolan RJ. Psychophysiological and modulatory interactions in neuroimaging. Neuroimage 1997; 6: 218-29.
25. Galter D, Westerlund M, Carmine A, Lindqvist E, Sydow O, Olson L. LRRK2 expression linked to dopamine-innervated areas. Ann Neurol 2006; 59: 714-19.
26. Gibb WR, Lees AJ. A comparison of clinical and pathological features of young-and old-onset Parkinson's disease. Neurology 1988; 38: 1402-6.
27. Goldman-Rakic PS, Muly EC 3rd, Williams GV. D(1) receptors in pre-frontal cells and circuits. Brain Res 2000; 31: 295-301.
28. Good CD, Johnsrude IS, Ashburner J, Henson RN, Friston KJ, Frackowiak RS. A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage 2001; 14: 21-36.
29. Hagenah JM, Becker B, Bruggemann N, Djarmati A, Lohmann K, Sprenger A, et al. Transcranial sonography findings in a large family with homozygous and heterozygous PINK1 mutations. J Neurol Neurosurg Psychiatry 2008; 79: 1071-4.
30. Hagenah JM, Konig IR, Becker B, Hilker R, Kasten M, Hedrich K, et al. Substantia nigra hyperechogenicity correlates with clinical status and number of Parkin mutated alleles. J Neurol 2007; 254: 1407-13.
31. Haslinger B, Erhard P, Kampfe N, Boecker H, Rummeny E, Schwaiger M, et al. Event-related functional magnetic resonance imaging in Parkinson's disease before and after levodopa. Brain 2001; 124: 558-70.
32. Helmich RC, Aarts E, de Lange FP, Bloem BR, Toni I. Increased dependence of action selection on recent motor history in Parkinson's disease. J Neurosci 2009; 29: 6105-13.
33. Helmich RC, Bloem BR, Toni I. Motor imagery evokes increased somato-sensory activity in Parkinson's disease patients with tremor. Hum Brain Mapp 2012; 33: 1763-79.
34. Helmich RC, de Lange FP, Bloem BR, Toni I. Cerebral compensation during motor imagery in Parkinson's disease. Neuropsychologia 2007; 45: 2201-15.
35. Hilker R, Klein C, Ghaemi M, Kis B, Strotmann T, Ozelius LJ, et al. Positron emission tomographic analysis of the nigrostriatal dopamin-ergic system in familial parkinsonism associated with mutations in the parkin gene. Ann Neurol 2001; 49: 367-76.
36. Johnson SH, Rotte M, Grafton ST, Hinrichs H, Gazzaniga MS, Heinze HJ. Selective activation of a parietofrontal circuit during implicitly imagined prehension. Neuroimage 2002; 17: 1693-704.
37. Khan NL, Brooks DJ, Pavese N, Sweeney MG, Wood NW, Lees AJ, et al. Progression of nigrostriatal dysfunction in a parkin kindred: an [18F]dopa PET and clinical study. Brain 2002a; 125: 2248-56.
38. Khan NL, Jain S, Lynch JM, Pavese N, Abou-Sleiman P, Holton JL, et al. Mutations in the gene LRRK2 encoding dardarin (PARK8) cause familial Parkinson's disease: clinical, pathological, olfactory and functional imaging and genetic data. Brain 2005a; 128: 2786-96.
39. Khan NL, Scherfler C, Graham E, Bhatia KP, Quinn N, Lees AJ, et al. Dopaminergic dysfunction in unrelated, asymptomatic carriers of a single parkin mutation. Neurology 2005b; 64: 134-6.
40. Khan NL, Valente EM, Bentivoglio AR, Wood NW, Albanese A, Brooks DJ, et al. Clinical and subclinical dopaminergic dysfunction in PARK6-linked parkinsonism: an 18F-dopa PET study. Ann Neurol 2002b; 52: 849-53.
41. Kish SJ, 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: 876-80.
42. Kühn S, Keizer A, Rombouts SA, Hommel B. The functional and neural mechanism of action preparation: roles of EBA and FFA in voluntary action control. J Cogn Neurosci 2011; 23: 214-20.
43. Lin CH, Tsai PI, Wu RM, Chien CT. LRRK2 Parkinson's disease: from animal models to cellular mechanisms. Rev Neurosci 2011; 22: 411-18.
44. Lund TE, Norgaard MD, Rostrup E, Rowe JB, Paulson OB. Motion or activity: their role in intra-and inter-subject variation in fMRI. Neuroimage 2005; 26: 960-4.
45. Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH. An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 2003; 19: 1233-9.
46. Marklund P, Larsson A, Elgh E, Linder J, Riklund KA, Forsgren L, et al. Temporal dynamics of basal ganglia under-recruitment in Parkinson's disease: transient caudate abnormalities during updating of working memory. Brain 2009; 132: 336-46.
47. Mayka MA, Corcos DM, Leurgans SE, Vaillancourt DE. Three-dimensional locations and boundaries of motor and premotor cortices as defined by functional brain imaging: a meta-analysis. Neuroimage 2006; 31: 1453-74.
48. Mounayar S, Boulet S, Tande D, Jan C, Pessiglione M, Hirsch EC, et al. A new model to study compensatory mechanisms in MPTP-treated monkeys exhibiting recovery. Brain 2007; 130: 2898-914.
49. Orr-Urtreger A, Shifrin C, Rozovski U, Rosner S, Bercovich D, Gurevich T, et al. The LRRK2 G2019S mutation in Ashkenazi Jews with Parkinson disease: is there a gender effect? Neurology 2007; 69: 1595-602.
50. Palop JJ, Chin J, Mucke L. A network dysfunction perspective on neu-rodegenerative diseases. Nature 2006; 443: 768-73.
51. Parsons LM. Imagined spatial transformations of one's hands and feet. Cogn Psychol 1987; 19: 178-241.
52. Parsons LM. Temporal and kinematic properties of motor behavior reflected in mentally simulated action. J Exp Psychol Hum Percept Perform 1994; 20: 709-30.
53. Parsons LM, Fox PT, Downs JH, Glass T, Hirsch TB, Martin CC, et al. Use of implicit motor imagery for visual shape discrimination as revealed by PET. Nature 1995; 375: 54-8.
54. Pessiglione M, Guehl D, Agid Y, Hirsch EC, Feger J, Tremblay L. Impairment of context-adapted movement selection in a primate model of pre-symptomatic Parkinson's disease. Brain 2003; 126: 1392-408.
55. Picard N, Strick PL. Imaging the premotor areas. Curr Opin Neurobiol 2001; 11: 663-72.
56. Poulopoulos M, Levy OA, Alcalay RN. The neuropathology of genetic Parkinson's disease. Mov Disord 2012; 27: 831-42.
57. Price CJ, Friston KJ. Scanning patients with tasks they can perform. Hum Brain Mapp 1999; 8: 102-8.
58. Reetz K, Gaser C, Klein C, Hagenah J, Buchel C, Gottschalk S, et al. Structural findings in the basal ganglia in genetically determined and idiopathic Parkinson's disease. Mov Disord 2009; 24: 99-103.
59. Reetz K, Tadic V, Kasten M, Bruggemann N, Schmidt A, Hagenah J, et al. Structural imaging in the presymptomatic stage of genetically determined parkinsonism. Neurobiol Dis 2010; 39: 402-8.
60. Sabatini U, Boulanouar K, Fabre N, Martin F, Carel C, Colonnese C, et al. Cortical motor reorganization in akinetic patients with Parkinson's disease: a functional MRI study. Brain 2000; 123 (Pt 2): 394-403.
61. Samuel M, Ceballos-Baumann AO, Blin J, Uema T, Boecker H, Passingham RE, et al. Evidence for lateral premotor and parietal over-activity in Parkinson's disease during sequential and bimanual movements. A PET study. Brain 1997; 120 (Pt 6): 963-76.
62. Saunders-Pullman R, Hagenah J, Dhawan V, Stanley K, Pastores G, Sathe S, et al. Gaucher disease ascertained through a Parkinson's center: imaging and clinical characterization. Mov Disord 2010; 25: 1364-72.
63. Schweitzer KJ, Brussel T, Leitner P, Kruger R, Bauer P, Woitalla D, et al. Transcranial ultrasound in different monogenetic subtypes of Parkinson's disease. J Neurol 2007; 254: 613-16.
64. Shenton JT, Schwoebel J, Coslett HB. Mental motor imagery and the body schema: evidence for proprioceptive dominance. Neurosci Lett 2004; 370: 19-24.
65. Thaler A, Mirelman A, Gurevich T, Simon E, Orr-Urtreger A, Marder K, et al. Lower cognitive performance in healthy G2019S LRRK2 mutation carriers. Neurology 2012; 79: 1027-32.
66. Tomassini V, Jbabdi S, Klein JC, Behrens TE, Pozzilli C, Matthews PM, et al. Diffusion-weighted imaging tractography-based parcellation of the human lateral premotor cortex identifies dorsal and ventral sub-regions with anatomical and functional specializations. J Neurosci 2007; 38: 10259-69.
67. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 2002; 15: 273-89.
68. van Nuenen BF, Helmich RC, Buenen N, van de Warrenburg BP, Bloem BR, Toni I. Compensatory activity in the extrastriate body area of Parkinson's disease patients. J Neurosci 2012; 32: 9546-53.
69. van Nuenen BF, van Eimeren T, van der Vegt JP, Buhmann C, Klein C, Bloem BR, et al. Mapping preclinical compensation in Parkinson's disease: an imaging genomics approach. Mov Disord 2009a; 24 (Suppl 2): S703-10.
70. van Nuenen BF, Weiss MM, Bloem BR, Reetz K, van Eimeren T, Lohmann K, et al. Heterozygous carriers of a Parkin or PINK1 mutation share a common functional endophenotype. Neurology 2009b; 72: 1041-7.
71. Walter U, Klein C, Hilker R, Benecke R, Pramstaller PP, Dressler D. Brain parenchyma sonography detects preclinical parkinsonism. Mov Disord 2004; 19: 1445-9.
72. Wu T, Hallett M. A functional MRI study of automatic movements in patients with Parkinson's disease. Brain 2005; 128: 2250-9.
73. Zimmermann M, Meulenbroek RG, de Lange FP. Motor planning is facilitated by adopting an action's goal posture: an fMRI study. Cereb Cortex 2012; 22: 122-31.