Improved sequence learning with subthalamic nucleus deep brain stimulation: Evidence for treatment-specific network modulation

Journal of Neuroscience

Volumn 32, Issue 8, 2012, Pages 2804-2813

  Mure, Hideo ^a   Tang, Chris C ^a   Argyelan, Miklos ^a   Ghilardi, Maria Felice ^b   Kaplitt, Michael G ^c   Dhawan, Vijay ^a   Eidelberg, David ^a  

^a FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

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

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LEVODOPA;

ADULT; ARTICLE; BRAIN BLOOD FLOW; BRAIN DEPTH STIMULATION; CEREBELLUM; COMPARATIVE STUDY; CONTROLLED STUDY; EVOKED MUSCLE RESPONSE; FEMALE; HUMAN; HUMAN EXPERIMENT; LEARNING; MALE; MOTOR PERFORMANCE; MOTOR SEQUENCE LEARNING; NEUROMODULATION; ORBITAL CORTEX; PARAHIPPOCAMPAL GYRUS; PARKINSON DISEASE; POSITRON EMISSION TOMOGRAPHY; PREMOTOR CORTEX; PRIORITY JOURNAL; SUBTHALAMIC NUCLEUS; SUPPLEMENTARY MOTOR AREA; UNIFIED PARKINSON DISEASE RATING SCALE;

AGED; ANALYSIS OF VARIANCE; BRAIN MAPPING; CEREBROVASCULAR CIRCULATION; DEEP BRAIN STIMULATION; FEMALE; HUMANS; LEARNING DISORDERS; MALE; MENTAL RECALL; MIDDLE AGED; MODELS, BIOLOGICAL; NEURAL PATHWAYS; NEUROPSYCHOLOGICAL TESTS; PARKINSON DISEASE; POSITRON-EMISSION TOMOGRAPHY; REACTION TIME; SERIAL LEARNING; SEVERITY OF ILLNESS INDEX; SUBTHALAMIC NUCLEUS;

EID: 84857326642     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4331-11.2012     Document Type: Article

References (55)

1. Aarsland D, Brønnick K, Larsen JP, Tysnes OB, Alves G (2009) Cognitive impairment in incident, untreated Parkinson disease: the Norwegian ParkWest study. Neurology 72:1121-1126.
2. Aarsland D, Bronnick K, Williams-Gray C, Weintraub D, Marder K, Kulisevsky J, Burn D, Barone P, Pagonabarraga J, Allcock L, Santangelo G, Foltynie T, Janvin C, Larsen JP, Barker RA, Emre M (2010) Mild cognitive impairment in Parkinson disease: a multicenter pooled analysis. Neurology 75:1062-1069.
3. Argyelan M, Carbon M, Ghilardi MF, Feigin A, Mattis P, Tang C, Dhawan V, Eidelberg D (2008) Dopaminergic suppression of brain deactivation responses during sequence learning. J Neurosci 28:10687-10695.
4. Asanuma K, Tang C, Ma Y, Dhawan V, Mattis P, Edwards C, Kaplitt MG, Feigin A, Eidelberg D (2006) Network modulation in the treatment of Parkinson's disease. Brain 129:2667-2678.
5. Baudrexel S, Witte T, Seifried C, von Wegner F, Beissner F, Klein JC, Steinmetz H, Deichmann R, Roeper J, Hilker R (2011) Resting state fMRI reveals increased subthalamic nucleus-motor cortex connectivity in Parkinson's disease. Neuroimage 55:1728-1738.
6. Beck A (1987) Beck Depression Inventory: Manual. San Antonio, TX: Psychological Corporation.
7. Benedict RH, Schretlen D, Groninger L, Brandt J (1998) Hopkins Verbal Learning Test-revised: normative data and analysis of interform and test-retest reliability. Clin Neuropsychol 12:43-55.
8. Benton A, Hamsher K, Varyney N, Spreen O (1983) Contributions to neuropsychological assessment. New York: Oxford UP.
9. Blair JR, Spreen O (1989) Predicting premorbid IQ: a revision of the National Adult Reading Test. Clin Neuropsychol 3:129-136.
10. Brandt J (1991) The Hopkins Verbal Learning Test: development of a new verbal memory rest with six alternate forms. Clin Neuropsychol 5:125-142.
11. Carbon M, Eidelberg D (2002) Modulation of regional brain function by deep brain stimulation: studies with positron emission tomography. Curr Opin Neurol 15:451-455.
12. Carbon M, Eidelberg D (2006) Functional imaging of sequence learning in Parkinson's disease. J Neurol Sci 248:72-77.
13. Carbon M, Ghilardi MF, Feigin A, Fukuda M, Silvestri G, Mentis MJ, Ghez C, Moeller JR, Eidelberg D (2003) Learning networks in health and Parkinson's disease: reproducibility and treatment effects. Hum Brain Mapp 19:197-211.
14. Carbon M, Argyelan M, Habeck C, Ghilardi MF, Fitzpatrick T, Dhawan V, Pourfar M, Bressman SB, Eidelberg D (2010a) Increased sensorimotor network activity in DYT1 dystonia: a functional imaging study. Brain 133:690-700.
15. Carbon M, Reetz K, Ghilardi MF, Dhawan V, Eidelberg D (2010b) Early Parkinson's disease: longitudinal changes in brain activity during sequence learning. Neurobiol Dis 37:455-460.
16. Cools R, Altamirano L, D'Esposito M (2006) Reversal learning in Parkinson's disease depends on medication status and outcome valence. Neuropsychologia 44:1663-1673.
17. Dejean C, Gross CE, Bioulac B, Boraud T (2008) Dynamic changes in the cortex-basal ganglia network after dopamine depletion in the rat. J Neurophysiol 100:385-396.
18. Doyon J (2008) Motor sequence learning and movement disorders. Curr Opin Neurol 21:478-483.
19. Doyon J, Bellec P, Amsel R, Penhune V, Monchi O, Carrier J, Lehéricy S, Benali H (2009) Contributions of the basal ganglia and functionally related brain structures to motor learning. Behav Brain Res 199:61-75.
20. Efron B, Tibshirani RJ (1994) An Introduction to the Bootstap. New York: CRC.
21. Eidelberg D (2009) Metabolic brain networks in neurodegenerative disorders: a functional imaging approach. Trends Neurosci 32:548-557.
22. Fahn S, Elton, RL, Members of the UPDRS Development Committee (1987) Unified Parkinson's Disease Rating Scale. In: Recent developments in Parkinson's disease (Fahn S, Marsden DM, Goldstein M, Calne DB, eds), pp 153-163. New York: MacMillan.
23. Feigin A, Ghilardi MF, Carbon M, Edwards C, Fukuda M, Dhawan V, Margouleff C, Ghez C, Eidelberg D (2003) Effects of levodopa on motor sequence learning in Parkinson's disease. Neurology 60:1744-1749.
24. Feigin A, Ghilardi MF, Huang C, Ma Y, Carbon M, Guttman M, Paulsen JS, Ghez CP, Eidelberg D (2006) Preclinical Huntington's disease: compensatory brain responses during learning. Ann Neurol 59:53-59.
25. Frank MJ, Claus ED (2006) Anatomy of a decision: striato-orbitofrontal interactions in reinforcement learning, decision making, and reversal. Psychol Rev 113:300-326.
26. Fukuda M, Ghilardi MF, Carbon M, Dhawan V, Ma Y, Feigin A, Mentis MJ, Ghez C, Eidelberg D (2002) Pallidal stimulation for parkinsonism: improved brain activation during sequence learning. Ann Neurol 52:144-152.
27. Ghilardi MF, Eidelberg D, Silvestri G, Ghez C (2003) The differential effect of PD and normal aging on early explicit sequence learning. Neurology 60:1313-1319.
28. Ghilardi MF, Feigin AS, Battaglia F, Silvestri G, Mattis P, Eidelberg D, Di Rocco A (2007) L-Dopa infusion does not improve explicit sequence learning in Parkinson's disease. Parkinsonism Relat Disord 13:146-151.
29. Ghilardi MF, Moisello C, Silvestri G, Ghez C, Krakauer JW (2009) Learning of a sequential motor skill comprises explicit and implicit components that consolidate differently. J Neurophysiol 101:2218-2229.
30. Ghilardi M, Ghez C, Dhawan V, Moeller J, Mentis M, Nakamura T, Antonini A, Eidelberg D (2000) Patterns of regional brain activation associated with different forms of motor learning. Brain Res 871:127-145.
31. Gradinaru V, Mogri M, Thompson KR, Henderson JM, Deisseroth K (2009) Optical deconstruction of parkinsonian neural circuitry. Science 324:354-359.
32. Habeck C, Stern Y (2010) Multivariate data analysis for neuroimaging data: overview and application to Alzheimer's disease. Cell Biochem Biophys 58:53-67.
33. Habeck C, Krakauer JW, Ghez C, Sackeim HA, Eidelberg D, Stern Y, Moeller JR (2005) A new approach to spatial covariance modeling of functional brain imaging data: ordinal trend analysis. Neural Comput 17:1602-1645.
34. Hauser RA, Holford NH (2002) Quantitative description of loss of clinical benefit following withdrawal of levodopa-carbidopa and bromocriptine in early Parkinson's disease. Mov Disord 17:961-968.
35. Hirano S, Asanuma K, Ma Y, Tang C, Feigin A, Dhawan V, Carbon M, Eidelberg D (2008) Dissociation of metabolic and neurovascular responses to levodopa in the treatment of Parkinson's disease. J Neurosci 28:4201-4209.
36. Huang C, Tang C, Feigin A, Lesser M, Ma Y, Pourfar M, Dhawan V, Eidelberg D (2007) Changes in network activity with the progression of Parkinson's disease. Brain 130:1834-1846.
37. Kehagia AA, Barker RA, Robbins TW (2010) Neuropsychological and clinical heterogeneity of cognitive impairment and dementia in patients with Parkinson's disease. Lancet Neurol 9:1200-1213.
38. Levin BE, Katzen HL (2005) Early cognitive changes and nondementing behavioral abnormalities in Parkinson's disease. Adv Neurol 96:84-94.
39. Lin TP, Carbon M, Tang C, Mogilner AY, Sterio D, Beric A, Dhawan V, Eidelberg D (2008) Metabolic correlates of subthalamic nucleus activity in Parkinson's disease. Brain 131:1373-1380.
40. Mattis PJ, Tang CC, Ma Y, Dhawan V, Eidelberg D (2011) Networks correlates of the cognitive response to levodopa in Parkinson's disease. Neurology 77:858-865.
41. Moeller J, HabeckC (2006) Reciprocal benefits of mass-univariate and multivariate modeling in brain mapping: applications to event-related functional MRI, H215O-, and FDG PET. Int J Biomed Imaging 2006:1-13.
42. Mure H, Hirano S, Tang CC, Isaias IU, Antonini A, Ma Y, Dhawan V, Eidelberg D (2011) Parkinson's disease tremor-related metabolic network: characterization, progression, and treatment effects. Neuroimage 54:1244-1253.
43. Nachev P, Kennard C, Husain M (2008) Functional role of the supplementary and pre-supplementary motor areas. Nat Rev Neurosci 9:856-869.
44. Nakamura T, Ghilardi MF, Mentis M, Dhawan V, Fukuda M, Hacking A, Moeller JR, Ghez C, Eidelberg D (2001) Functional networks in motor sequence learning: abnormal topographies in Parkinson's disease. Hum Brain Mapp 12:42-60.
45. Nelson HE (1982) The National Adult Reading Test (NART): Test Manual. Windsor, UK: NFER-Nelson.
46. Orban P, Peigneux P, Lungu O, Albouy G, Breton E, Laberenne F, Benali H, Maquet P, Doyon J (2010) The multifaceted nature of the relationship between performance and brain activity in motor sequence learning. Neuroimage 49:694-702.
47. Parsons TD, Rogers SA, Braaten AJ, Woods SP, Tröster AI (2006) Cognitive sequelae of subthalamic nucleus deep brain stimulation in Parkinson's disease: a meta-analysis. Lancet Neurol 5:578-588.
48. Schmahmann JD, Doyon J, Toga AW, Petrides M, Evans AC (2000) MRI atlas of the human cerebellum. San Diego: Academic.
49. Schretlen D (1989) Brief test of attention. Odessa, FL: Psychological Assessment Resources.
50. Smith A (1982) Symbol Digit Modalities Test (SDMT) Manual (revised). Los Angeles: Western Psychological Services.
51. Spetsieris PG, Eidelberg D (2011) Scaled subprofile modeling of resting state imaging data in Parkinson's disease: methodological issues. Neuroimage 54:2899-2914.
52. Tang CC, Poston KL, Dhawan V, Eidelberg D (2010) Abnormalities in metabolic network activity precede the onset of motor symptoms in Parkinson's disease. J Neurosci 30:1049-1056.
53. Wilkinson L, Khan Z, Jahanshahi M (2009) The role of the basal ganglia and its cortical connections in sequence learning: evidence from implicit and explicit sequence learning in Parkinson's disease. Neuropsychologia 47:2564-2573.
54. Williams AE, Arzola GM, Strutt AM, Simpson R, Jankovic J, York MK (2011) Cognitive outcome and reliable change indices two years following bilateral subthalamic nucleus deep brain stimulation. Parkinsonism Relat Disord 17:321-327.
55. Williams-Gray CH, Foltynie T, Brayne CE, Robbins TW, Barker RA (2007) Evolution of cognitive dysfunction in an incident Parkinson's disease cohort. Brain 130:1787-1798.