Subthalamic nucleus stimulation influences expression and suppression of impulsive behaviour in Parkinson's disease

Brain

Volumn 133, Issue 12, 2010, Pages 3611-3624

  Wylie, Scott A ^a   Richard Ridderinkhof, K ^b   Elias, William J ^c   Frysinger, Robert C ^c   Bashore, Theodore R ^d   Downs, Kara E ^a   Van Wouwe, Nelleke C ^e   Van Den Wildenberg, Wery P M ^b  

^a UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c UNIVERSITY OF VIRGINIA   (United States)

^d UNIVERSITY OF NORTHERN COLORADO   (United States)

^e LEIDEN UNIVERSITY   (Netherlands)

Author keywords

Deep brain stimulation; Impulsivity; Parkinson's disease; Response inhibition; Subthalamic nucleus

Indexed keywords

DOPAMINE; DOPAMINE RECEPTOR STIMULATING AGENT;

ADULT; ARTICLE; BRAIN DEPTH STIMULATION; BRAIN NERVE CELL; CLINICAL ARTICLE; CONFLICT; CONTROLLED STUDY; ELECTRODE; FEMALE; HUMAN; IMPULSIVENESS; MALE; PARKINSON DISEASE; PRIORITY JOURNAL; REACTION TIME; SUBTHALAMIC NUCLEUS; TASK PERFORMANCE;

EID: 79951862422     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awq239     Document Type: Article

References (69)

1. Albin RL, Young A, Penny JB. The functional anatomy of basal ganglia disorders. Trends Neurosci 1989; 12: 366-75. (Pubitemid 19238787)
2. Aron AR, Behrens TE, Smith S, Frank MJ, Poldrack RA. Triangulating a cognitive control network using diffusion-weighted magnetic resonance Imaging (MRI) and functional MRI. J Neurosci 2007; 27: 3743-52. (Pubitemid 46557676)
3. Aron AR, Fletcher PC, Bullmore ET, Sahaklan BJ, Robbins TW. Stop signal inhibition disrupted by damage to right inferior frontal gyrus in humans. Nat Neurosci 2003; 6: 115-6. (Pubitemid 36182778)
4. Aron AR, Poldrack RA. Cortical and subcortical contributions to stop signal response inhibition: role of the subthalamic nucleus. J Neurosci 2006; 26: 2424-33. (Pubitemid 44699002)
5. Ballanger B, van Eimeren T, Moro E, Lozano AM, Hamani C, Boulinguez P, et al. Stimulation of the subthalamic nucleus and impulsivity: Release your horses. Ann Neurol 2009; 66: 817-24.
6. Bergman H, Wichmann T, Karmon B, DeLong M. The primate subthalamic nucleus. II. Neuronal activity in the MPTP model of parkinsonism. J Neurophysiol 1994; 72: 507-20. (Pubitemid 24273560)
7. Blandini F, Nappi G, Tassorelli C, Martignoni E. Functional changes of the basal ganglia circuitry in Parkinson's disease. Prog Neurobiol 2000; 62: 63-88. (Pubitemid 30252017)
8. Bub DN, Masson MEJ, Lalonde CE. Cognitive control in children: stroop interference and suppression of word reading. Psychol Sci 2006; 17: 351-57.
9. Burle B, Possamaï CA, Vidal F, Bonnet M, Hasbroucq T. Executive control in the Simon effect: an electromyographic and distributional analysis. Psychol Res 2002; 66: 324-36.
10. Campbell MC, Karimi M, Weaver PM, Wu J, Perantie DC, Golchin NA, et al. Neural correlates of STN DBS-induced cognitive variability in Parkinson disease. Neuropsychologia 2008; 47: 3162-9.
11. Ceravolo R, Fronsini D, Rossi C, Bonuccelli U. Impulse control disorders in Parkinson's disease: definition, epidemiology, risk factors, neurobiology and management. Parkinsonism Relat Disord 2009; 15: 111-5.
12. Cope MT, Georgiou N, Bradshaw JL, lansek R, Phillips JG. Simon effect and attention in Parkinson's disease: a comparison with Huntington's disease and Tourette's syndrome. J Clin Exp Neuropsychol 1996; 18: 276-90. (Pubitemid 26199418)
13. Davelaar EJ. A computational study of conflict-monitoring at two levels of processing: reaction time distributional analyses and hemodynamic responses. Brain Res 2008; 1202: 109-19. (Pubitemid 351389310)
14. De Jong R, Liang CC, Lauber E. Conditional and unconditional automaticity: a dual-process model of effects of spatial stimulus-response correspondence. J Exp Psychol Hum Percept Perform 1994; 20: 731-50.
15. DeLong MR. Primate models of movement disorders of basal ganglia origin. Trends Neurosci 1990; 13: 281-5. (Pubitemid 20193459)
16. Desbonnet L, Temel Y, Visser-Vandewalle V, Blokland A, Hornikx V, Steinbusch HW. Premature responding following bilateral stimulation of the rat subthalamic nucleus is amplitude and frequency dependent. Brain Res 2004; 1008: 198-204. (Pubitemid 38624050)
17. Eagle D, Baunez C, Hutcheson DM, Lehmann O, Shah AP, Robbins TW. Stop-signal reaction-time task performance: role of prefrontal cortex and subthalamic nucleus. Cereb Cortex 2008; 18: 178-88. (Pubitemid 350233064)
18. Eagle DM, Baunez C. Is there an inhibitory-response-control system in the rat? Evidence from anatomical and pharmacological studies of behavioral inhibition. Neurosci Biobehav Rev 2010; 34: 50-72.
19. Elias WJ, Fu KM, Frysinger RC. Cortical and subcortical brain shift during stereotactic procedures. J Neurosurg 2007; 107: 983-8. (Pubitemid 350255213)
20. Fielding J, Georgiou-Karistianis N, Bradshaw J, Millist L, White O. No sequence dependent modulation of the Simon effect in Parkinson's disease. Brain Res Cogn Brain Res 2005; 25: 251-60. (Pubitemid 41278502)
21. Folstein MF, Folstein SE, McHugh PR. Mini-mental state. J Psychiatric Res 1975; 12: 189-98.
22. Forstmann BU, Jahfari S, Scholte HS, Wolfensteller U, van den Wildenberg WPM, Ridderinkhof KR. Function and structure of the right inferior frontal cortex predict individual differences in response inhibition: a model-based approach. J Neurosci 2008a; 28: 9790-6.
23. Forstmann BU, van den Wildenberg WPM, Ridderinkhof KR. Neural mechansims, temporal dynamics, and individual differences in interference control. J Cogn Neurosci 2008b; 20: 1854-65.
24. Forstmann BU, Dutlilh G, Brown S, Neumann J, von Cramon DY, Ridderinkhof KR, et al. Striatum and pre-SMA facilitate decision-making under time pressure. Proc Natl Acad Sci 2008c; 105: 17538-42.
25. Frank MJ. Hold your horses: a dynamic computational role for the subthalamic nucleus in decision making. Neural Netw 2006; 19: 1120-36. (Pubitemid 44466333)
26. Frank MJ, Samanta J, Moustafa AA, Sherman SJ. Hold your horses: impulsivity, deep brain stimulation, and medication in Parkinsonism. Science 2007; 318: 1309-12. (Pubitemid 350172897)
27. Gauggel S, Rieger M, Feghoff TA. Inhibition of ongoing responses in patients with Parkinson's disease. J Neurol Neurosurg Psychiatry 2004; 75: 539-44. (Pubitemid 38406648)
28. Haaxma CA, Bloem BR, Borm GF, Horstink M. Comparison of a timed motor test battery to the unified Parkinson's disease rating scale-III in Parkinson's disease. Mov Dis 2008; 23: 1707-17.
29. Hershey T, Revilla FJ, Wernle A, Schneider Gibson P, Dowling JL, Perlmutter JS. Stimulation of STN impairs aspects of cognitive control on PD. Neurol 2004; 62: 1110-4. (Pubitemid 38456504)
30. Hoehn MM, Yahr MD. Parkinsonism: onset, progression, and mortality. Neurol 1967; 17: 427-42.
31. Hristova A, Lyons K, Troster Al, Pahwa R, Wilkinson SB, Koller WC. Effect and time course of deep brain stimulation of the globus pallidus and subthalamus on motor features of Parkinson's disease. Clin Neuropharm 2000; 23: 208-11.
32. Jahanshahi M, Ardouin CM, Brown RG, Rothwell JC, Obeso J, Albanese A, et al. The Impact of deep brain stimulation on executive function in Parkinson's disease. Brain 2000; 123: 1142-54. (Pubitemid 30312106)
33. Komblum S, Hasbroucq T, Osman A. Dimensional overlap: cognitive basis for stimulus-response compatibility- a model and taxonomy. Psychol Rev 1990; 97: 253-70.
34. Krack P, Batir A, van Blercom N, Chabardes S, Fraix V, Ardouin C, et al. Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson's disease. N Engl J Med 2003; 349: 1925-34. (Pubitemid 37409709)
35. Kropotov JD, Etlinger S. Selection of actions in the basal ganglia-thalamocortical circuits: review and model. Int J Psychophysiol 1999; 31: 197-217. (Pubitemid 29083434)
36. Limousin P, Pollak P, Benazzouz A, Hoffmann D, Le Bas JF, Broussolle E, et al. Effect of parkinsonian signs and symptoms of bilateral subthalamic nucleus stimulation. Lancet 1995; 345: 91-5.
37. Liu Y, Postupna N, Falkenberg J, Anderson ME. High refrequency deep brain stimulation: what are the therapeutic mechanisms? Neurosci Biobehav Rev 2008; 32: 343-51.
38. Lopiano L, Torre E, Benedetti F, Bergamasco B, Perozzo P, Pollo A, et al. Temporal changes in movement time during the switch of the stimulators in parkinson's disease patients treated by subthalamic nucleus stimulation. Eur Neurol 2003; 50: 94-9. (Pubitemid 37116970)
39. Mink JW. The basal ganglia: Focused selection an inhibition of competing motor programs. Prog Neurobiol 1996; 50: 381-425. (Pubitemid 27028538)
40. Montgomery EB Jr, Gale JT. Mechanisms of action of deep brain stimulation (DBS). Neurosci Biobehav Rev 2008; 32: 388-407. (Pubitemid 351181336)
41. Müller T, Schäfer S, Kuhn W, Przuntek H. Correlation between tapping and inserting of pegs in Parkinson's disease. Can J Neurol Sci 2000; 27: 311-5.
42. Nambu A, Tokuno H, Takada M. Functional significance of the cortico-subthalamo-pallidal "hyper-direct" pathway. Neurosci Res 2002; 43: 111-7.
43. Parsons TD, Rogers SA, Braaten AJ, Woods SP, Tröster Al. Cognitive sequelae of subthalamic nucleus deep brain stimulation in Parkinson's disease: a meta-analysis. Lancet Neurol 2006; 5: 578-88. (Pubitemid 43867425)
44. Pattij T, Vanderschuren LJ. The neuropharmacology of impulsive behaviour. Trends Pharmacol Sci. 2008; 29: 192-9.
45. Phillips JM, Brown VJ. Anticipatory errors after unilateral lesions of the subthalamic nucleus in the rat: evidence for a failure of response inhibition. Beh Neurosci 2000; 114: 150-7. (Pubitemid 30131594)
46. Praamstra P, Plat EM. Failed suppression of direct visuomotor activation in Parkinson's disease. J Cogn Neurosci 2001; 13: 31-43. (Pubitemid 32121494)
47. Radloff LS. The CES-D scale: a self report depression scale for research in the general population. Appl Psychol Meas 1977; 1: 385-401.
48. Ray NJ, Jenkinson N, Brittain J, Holland P, Joint C, Nandi D, et al. The role of the subthalamic nucleus in response inhibition: evidence from deep brain stimulation for Parkinson's disease. Neuropsychologia 2009; 47: 2828-34.
49. Redgrave P, Prescott TJ, Gurney K. The basal ganglia: a vertebrate solution to the selection problem? Neuroscience 1999; 89: 1009-23.
50. Ridderinkhof KR. Activation and suppression in conflict tasks: empirical clarification through distributional analyses. In: Prinz W, Hommel, editors. Common mechanisms in perception and action, attention & performance. Vol. XIX. Oxford: Oxford University Press; 2002. p. 495-519.
51. Ridderinkhof KR, Scheres A, Oosterlaan J, Sergeant JA. Delta plots in the study of individual differences: new tools reveal response inhibition deficits in AD/HD that are eliminated by methylphenidate treatment. J Abnorm Psych 2005; 114: 197-215. (Pubitemid 40663761)
52. Ridderinkhof KR, van den Wildenberg WPM, Wijnen J, Burle B. Response inhibition in conflict tasks is revealed in delta plots. In: Posner MI, editor. Cognitive neuroscience of attention. New York: Guilford Press; 2004. p. 369-77.
53. Schmiedt-Fehr C, Schwendemann G, Herrmann M, Basar-Eroglu C. Parkinson's disease and age-related alterations in brain oscillations during a Simon task. Neuroreport 2007; 18: 277-81.
54. Simon JR. Reactions toward the source of stimulation. J Exp Psychol 1969; 81: 174-6.
55. Smeding HM, Goudriaan AE, Foncke EM, Schuurman PR, Speelman JD, Schmand B. Pathological gambling after bilateral subthalamic nucleus stimulation in Parkinson disease. J Neurol Neurosurg Psychiatry 2007; 78: 517-9. (Pubitemid 46662902)
56. Thobois S, Hotton GR, Pinto S, Wilkinson L, Limousin-Dowsey P, Brooks DJ, et al. STN stimulation alters pallidal-frontal coupling during response selection under competition. J Cereb Blood Flow Metab 2007; 27: 1173-84. (Pubitemid 46808707)
57. Verbruggen F, Logan GD. Response inhibition in the stop-signal paradigm. Trends Cogn Sci. 2008; 12: 418-24.
58. van den Wildenberg WPM, Burle B, Vidal F, van der Molen MW, Ridderinkhof KR, Hasbroucq T. Mechanisms and dynamics of cortical motor inhibition in the stop-signal paradigm: A TMS study. J Cogn Neurosci 2010; 22: 225-39.
59. van den Wildenberg WPM, van Boxtel GJM, van der Molen MW, Bosch DA, Speelman JD, Brunia CHM. Stimulation of the subthalamic region facilitates the selection and inhibition of motor responses in Parkinson's disease. J Cogn Neurosci 2006; 18: 626-36. (Pubitemid 43763862)
60. Voon V, Kubu C, Krack P, Houeto JL, Troster Al. Deep brain stimulation: neuropsychological and neuropsychiatric issues. Move Dis 2006; 21: S305-26.
61. Weintraub D, Siderowf AD, Potenza MN, Goveas J, Morales KH, Duda JE, et al. Association of dopamine agonist use with impulse control disorders in Parkinson's disease. Arch Neurol 2006; 63: 969-73. (Pubitemid 44036299)
62. Wijnen JG, Ridderinkhof KR. Response inhibition in motor and oculomotor conflict tasks: different mechanisms, different dynamics? Brain Cogn 2007; 63: 260-70. (Pubitemid 46367409)
63. Williams D, Kühn A, Kupsch A, Tijssen M, van Bruggen G, Speelman H, et al. The relationship between oscillatory activity and motor reaction time in the parkinsonian subthalamic nucleus. Eur J Neurosci 2005; 21: 249-58. (Pubitemid 40193893)
64. Winstanley CA, Baunez C, Theobald DE, Robbins TW. Lesions to the subthalamic nucleus decrease impulsive choice but impair autoshapingin rats: the importance of the basal ganglia in Pavlovian conditioning and impulse control. Eur J Neurosci 2005; 21: 3107-16. (Pubitemid 40917073)
65. Witt K, Pulkowski U, Herzog J, Lorenz D, Hamel W, Deuschl G, et al. Deep brain stimulation of the subthalamic nucleus improves cognitive flexibility but impairs response inhibition in Parkinson disease. Arch Neurol 2004; 61: 697-700. (Pubitemid 38637686)
66. Wylie SA, Ridderinkhof KR, Bashore TR, van den Wildenberg WPM. The effect of Parkinson's disease on the dynamics of online and proactive cognitive control during action selection. J Cogn Neurosci 2010; 22: 2058-73.
67. Wylie SA, van den Wildenberg WPM, Ridderinkhof KR, Bashore TR, Powell VD, Manning CA, et al. The effect of Parkinson's disease on interference control during action selection. Neuropsychology 2009a; 47: 145-57.
68. Wylie SA, van den Wildenberg WPM, Ridderinkhof KR, Bashore TR, Powell VD, Manning CA, et al. The effect of speed-accuracy strategy on response interference control in Parkinson's disease. Neuropsychologia 2009b; 47: 1844-53.
69. Wylie SA, Ridderinkhof KR, Eckerle MK, Manning CA. Inefficient response inhibition in individuals with mild cognitive impairment. Neuropsychologia 2007; 45: 1408-19. (Pubitemid 46097001)