Impaired sequence learning in dystonia mutation carriers: A genotypic effect

Brain

Volumn 134, Issue 5, 2011, Pages 1416-1427

  Carbon, Maren ^a   Argyelan, Miklos ^a   Ghilardi, Maria Felice ^b   Mattis, Paul ^a   Dhawan, Vijay ^a   Bressman, Susan ^c   Eidelberg, David ^a  

^a FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b CITY UNIVERSITY OF NEW YORK MEDICAL SCHOOL   (United States)

^c BETH ISRAEL MEDICAL CENTER   (United States)

Author keywords

cerebellum; DYT1 dystonia; DYT6 dystonia; PET; sequence learning

Indexed keywords

BACLOFEN; BRAIN PROTEIN; DOPAMINE 2 RECEPTOR; DYT1 PROTEIN; DYT6 PROTEIN; LEVODOPA; PREGABALIN; PROFENAMINE; RACLOPRIDE C 11; TOPIRAMATE; TRIHEXYPHENIDYL; UNCLASSIFIED DRUG; ZONISAMIDE;

ADULT; AGED; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; CORRELATIONAL STUDY; DIFFUSION TENSOR IMAGING; DYSTONIA; GENOTYPE; HETEROZYGOTE; HUMAN; MOTOR SEQUENCE LEARNING DEFICIT; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PROTEIN BINDING; PSYCHOMOTOR DISORDER; SEQUENCE ALIGNMENT; SPINOCEREBELLAR TRACT; TRACTOGRAPHY;

ADULT; APOPTOSIS REGULATORY PROTEINS; BRAIN MAPPING; CEREBELLUM; DNA-BINDING PROTEINS; DYSTONIA; FEMALE; GENOTYPE; HUMANS; LEARNING DISORDERS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; MOLECULAR CHAPERONES; MOTOR ACTIVITY; MUTATION; NEUROPSYCHOLOGICAL TESTS; NUCLEAR PROTEINS; PHOTIC STIMULATION; POSITRON-EMISSION TOMOGRAPHY; SERIAL LEARNING; STATISTICS AS TOPIC;

EID: 79957458673     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awr060     Document Type: Article

References (58)

1. Akkal D, Dum RP, Strick PL. Supplementary motor area and presupplementary motor area: Targets of basal ganglia and cerebellar output. J Neurosci 2007; 27: 10659-73. (Pubitemid 47535859)
2. Argyelan M, Carbon M, Ghilardi MF, Feigin A, Mattis P, Tang C, et al. Dopaminergic suppression of brain deactivation responses during sequence learning. J Neurosci 2008; 28: 10687-95.
3. Argyelan M, Carbon M, Niethammer M, Ulug AM, Voss HU, Bressman SB, et al. Cerebellothalamocortical connectivity regulates penetrance in dystonia. J Neurosci 2009; 29: 9740-7.
4. Asanuma K, Ma Y, Okulski J, Dhawan V, Chaly T, Carbon M, et al. Decreased striatal D2 receptor binding in non-manifesting carriers of the DYT1 dystonia mutation. Neurology 2005; 64: 347-9.
5. Aso K, Hanakawa T, Aso T, Fukuyama H. Cerebro-cerebellar interactions underlying temporal information processing. J Cogn Neurosci 2010; 22: 2913-25.
6. Badgaiyan RD, Fischman AJ. Alpert non-manifesting. Striatal dopamine release in sequential learning. Neuroimage 2007; 38: 549-56. (Pubitemid 47539910)
7. Bapi RS, Miyapuram KP, Graydon FX, Doya K. fMRI investigation of cortical and subcortical networks in the learning of abstract and effector-specific representations of motor sequences. Neuroimage 2006; 32: 714-27. (Pubitemid 44149156)
8. Bostan AC, Dum RP, Strick PL. The basal ganglia communicate with the cerebellum. Proc Natl Acad Sci USA 2010; 107: 8452-6.
9. Breakefield XO, Blood AJ, Li Y, Hallett M, Hanson PI, Standaert DG. The pathophysiological basis of dystonias. Nat Rev Neurosci 2008; 9: 222-34. (Pubitemid 351272666)
10. Bressman S. Genetics of dystonia. J Neural Transm Suppl 2006; 489-95. (Pubitemid 44622242)
11. Carbon M, Argyelan M, Habeck C, Ghilardi MF, Fitzpatrick T, Dhawan V, et al. Increased sensorimotor network activity in DYT1 dystonia: A functional imaging study. Brain 2010; 133: 690-700.
12. Carbon M, Eidelberg D. Modulation of regional brain function by deep brain stimulation: studies with positron emission tomography. Curr Opin Neurol 2002; 15: 451-5. (Pubitemid 34828122)
13. Carbon M, Eidelberg D. Abnormal structure-function relationships in hereditary dystonia. Neuroscience 2009; 164: 220-9.
14. Carbon M, Ghilardi MF, Argyelan M, Dhawan V, Bressman SB, Eidelberg D. Increased cerebellar activation during sequence learning in DYT1 carriers: An equiperformance study. Brain 2008; 131: 146-54.
15. Carbon M, Ghilardi MF, Feigin A, Fukuda M, Silvestri G, Mentis MJ, et al. Learning networks in health and Parkinson's disease: Reproducibility and treatment effects. Hum Brain Mapp 2003; 19: 197-211. (Pubitemid 36736662)
16. Carbon M, Ma Y, Barnes A, Dhawan V, Chaly T, Ghilardi MF, et al. Caudate nucleus: Influence of dopaminergic input on sequence learning and brain activation in Parkinsonism. Neuroimage 2004a; 21: 1497-507. (Pubitemid 38446574)
17. Carbon M, Niethammer M, Peng S, Raymond D, Dhawan V, Chaly T, et al. Abnormal striatal and thalamic dopamine neurotransmission: Genotype-related features of dystonia. Neurology 2009; 72: 2097-103.
18. Carbon M, Su S, Dhawan V, Raymond D, Bressman S, Eidelberg D. Regional metabolism in primary torsion dystonia: Effects of penetrance and genotype. Neurology 2004b; 62: 1384-90. (Pubitemid 38526053)
19. Carbon M, Trost M, Ghilardi MF, Eidelberg D. Abnormal brain networks in primary torsion dystonia. Adv Neurol 2004c; 94: 155-61.
20. Clower DM, West RA, Lynch JC, Strick PL. The inferior parietal lobule is the target of output from the superior colliculus, hippocampus, and cerebellum. J Neurosci 2001; 21: 6283-91. (Pubitemid 32737759)
21. Daskalakis ZJ, Paradiso GO, Christensen BK, Fitzgerald PB, Gunraj C, Chen R. Exploring the connectivity between the cerebellum and motor cortex in humans. J Physiol 2004; 557: 689-700. (Pubitemid 38807403)
22. Doyon J. Motor sequence learning and movement disorders. Curr Opin Neurol 2008; 21: 478-83.
23. Doyon J, Benali H. Reorganization and plasticity in the adult brain during learning of motor skills. Curr Opin Neurobiol 2005; 15: 161-7. (Pubitemid 41569264)
24. Doyon J, Owen AM, Petrides M, Sziklas V, Evans AC. Functional anatomy of visuomotor skill learning in human subjects examined with positron emission tomography. Eur J Neurosci 1996; 8: 637-48. (Pubitemid 26114609)
25. Doyon J, Song AW, Karni A, Lalonde F, Adams MM, Ungerleider LG. Experience-dependent changes in cerebellar contributions to motor sequence learning. Proc Natl Acad Sci USA 2002; 99: 1017-22. (Pubitemid 34106628)
26. Eckart MT, Huelse-Matia MC, McDonald RS, Schwarting RK. 6-Hydroxydopamine lesions in the rat neostriatum impair sequential learning in a serial reaction time task. Neurotoxicity Research 2010; 17: 287-98.
27. Eidelberg D, Moeller JR, Antonini A, Kazumata K, Nakamura T, Dhawan V, et al. Functional brain networks in DYT1 dystonia. Ann Neurol 1998; 44: 303-12. (Pubitemid 28421433)
28. Feigin A, Tang C, Ma Y, Mattis P, Zgaljardic D, Guttman M, et al. Thalamic metabolism and symptom onset in preclinical Huntington's disease. Brain 2007; 130: 2858-67. (Pubitemid 350033965)
29. Ferrieri RA, Alexoff DL, Schlyer DJ, Wolf AP. Remote processing, delivery and injection of H2[15O] produced from a N2/H2 gas target using a simple and compact apparatus. Appl Radiat Isot 1994; 45: 1149-54.
30. Fiorio M, Gambarin M, Valente EM, Liberini P, Loi M, Cossu G, et al. Defective temporal processing of sensory stimuli in DYT1 mutation carriers: A new endophenotype of dystonia? Brain 2007; 130: 134-42. (Pubitemid 46026229)
31. Forstmann BU, Dutilh G, Brown S, Neumann J, von Cramon DY, Ridderinkhof KR, et al. Striatum and pre-supplementary motor area facilitate decision-making under time pressure. Proc Natl Acad Sci USA 2008; 105: 17538-42.
32. Frima N, Rome SM, Grunewald RA. The effect of fatigue on abnormal vibration induced illusion of movement in idiopathic focal dystonia. J Neurol Neurosurg Psychiatry 2003; 74: 1154-6.
33. Friston KJ, Stephan KE, Lund TE, Morcom A, Kiebel S. Mixed-effects and fMRI studies. Neuroimage 2005; 24: 244-52. (Pubitemid 39611045)
34. Fuchs T, Gavarini S, Saunders-Pullman R, Raymond D, Ehrlich ME, Bressman SB, et al. Mutations in the THAP1 gene are responsible for DYT6 primary torsion dystonia. Nat Genet 2009; 41: 286-8.
35. Ghilardi MF, Carbon M, Silvestri G, Dhawan V, Tagliati M, Bressman S, et al. Impaired sequence learning in carriers of the DYT1 dystonia mutation. Ann Neurol 2003; 54: 102-9. (Pubitemid 36764986)
36. Ghilardi M, Ghez C, Dhawan V, Moeller J, Mentis M, Nakamura T, et al. Patterns of regional brain activation associated with different forms of motor learning. Brain Res 2000; 871: 127-45. (Pubitemid 30406877)
37. Hallett M. Physiology of dystonia. Adv Neurol 1998; 78: 11-8.
38. Ikeda A, Yazawa S, Kunieda T, Ohara S, Terada K, Mikuni N, et al. Cognitive motor control in human pre-supplementary motor area studied by subdural recording of discrimination/selection-related potentials. Brain 1999; 122: 915-31. (Pubitemid 29219265)
39. Jung J, Jerbi K, Ossandon T, Ryvlin P, Isnard J, Bertrand O, et al. Brain responses to success and failure: Direct recordings from human cerebral cortex. Hum Brain Mapp 2010; 31: 1217-32.
40. Karabanov A, Cervenka S, de Manzano O, Forssberg H, Farde L, Ullen F. Dopamine D2 receptor density in the limbic striatum is related to implicit but not explicit movement sequence learning. Proc Natl Acad Sci USA 2010; 107: 7574-9.
41. Kriegeskorte N, Lindquist MA, Nichols TE, Poldrack RA, Vul E. Everything you never wanted to know about circular analysis, but were afraid to ask. J Cereb Blood Flow Metab 2010; 30: 1551-7.
42. Kriegeskorte N, Simmons WK, Bellgowan PS, Baker CI. Circular analysis in systems neuroscience: The dangers of double dipping. Nat Neurosci 2009; 12: 535-40.
43. Kwak Y, Muller ML, Bohnen NI, Dayalu P, Seidler RD. Effect of dopaminergic medications on the time course of explicit motor sequence learning in Parkinson's disease. J Neurophysiol 2010; 103: 942-9.
44. Leggio MG, Molinari M, Neri P, Graziano A, Mandolesi L, Petrosini L. Representation of actions in rats: The role of cerebellum in learning spatial performances by observation. Proc Natl Acad Sci USA 2000; 97: 2320-5. (Pubitemid 30134067)
45. Luppino G, Matelli M, Camarda R, Rizzolatti G. Corticocortical connections of area F3 (supplementary motor area-proper) and area F6 (pre-supplementary motor area) in the macaque monkey. J Comp Neurol 1993; 338: 114-40. (Pubitemid 23337260)
46. Matsumoto N, Hanakawa T, Maki S, Graybiel AM, Kimura M. Role of [corrected] nigrostriatal dopamine system in learning to perform sequential motor tasks in a predictive manner. J Neurophysiol 1999; 82: 978-98. (Pubitemid 29387869)
47. Molinari M, Filippini V, Leggio MG. Neuronal plasticity of interrelated cerebellar and cortical networks. Neuroscience 2002; 111: 863-70. (Pubitemid 34603253)
48. Nachev P, Kennard C, Husain M. Functional role of the supplementary and pre-supplementary motor areas. Nat Rev Neurosci 2008; 9: 856-69.
49. Nakamura T, Ghilardi MF, Mentis M, Dhawan V, Fukuda M, Hacking A, et al. Functional networks in motor sequence learning: Abnormal topographies in Parkinson's disease. Hum Brain Mapp 2001; 12: 42-60. (Pubitemid 32048356)
50. O'Reilly JX, Mesulam MM, Nobre AC. The cerebellum predicts the timing of perceptual events. J Neurosci 2008; 28: 2252-60. (Pubitemid 351317632)
51. Penhune VB, Doyon J. Cerebellum and M1 interaction during early learning of timed motor sequences. Neuroimage 2005; 26: 801-12. (Pubitemid 40825023)
52. Saunders-Pullman R, Raymond D, Senthil G, Kramer P, Ohmann E, Deligtisch A, et al. Narrowing the DYT6 dystonia region and evidence for locus heterogeneity in the Amish-Mennonites. Am J Med Genet A 2007; 143A: 2098-105.
53. Steele CJ, Penhune VB. Specific increases within global decreases: A functional magnetic resonance imaging investigation of five days of motor sequence learning. J Neurosci 2010; 30: 8332-41.
54. Thyrion C, Roll JP. Perceptual integration of illusory and imagined kinesthetic images. J Neurosci 2009; 29: 8483-92.
55. Torriero S, Oliveri M, Koch G, Lo Gerfo E, Salerno S, Ferlazzo F, et al. Changes in Cerebello-motor Connectivity during Procedural Learning by Actual Execution and Observation. J Cogn Neurosci 2010; 23: 338-48.
56. Trost M, Carbon M, Edwards C, Ma Y, Raymond D, Mentis MJ, et al. Primary dystonia: Is abnormal functional brain architecture linked to genotype? Ann Neurol 2002; 52: 853-6. (Pubitemid 35403200)
57. van Gaal S, Ridderinkhof KR, Scholte HS, Lamme VA. Unconscious activation of the prefrontal no-go network. J Neurosci 2010; 30: 4143-50.
58. Vul E, Harris C, Winkielman P, Pashler H. Puzzlingly high correlations in fMRI studies of emotion, personality, and social cognition. Perspect Psychol Sci 2009; 4: 274-90.