Subthalamic nucleus deep brain stimulation induces impulsive action when patients with Parkinson's disease act under speed pressure

Inês Pote, Mariam Torkamani, Zinovia-Maria Kefalopoulou, Ludvic Zrinzo, Patricia Limousin-Dowsey, Thomas Foltynie, Maarten Speekenbrink, Marjan Jahanshahi, Inês Pote, Mariam Torkamani, Zinovia-Maria Kefalopoulou, Ludvic Zrinzo, Patricia Limousin-Dowsey, Thomas Foltynie, Maarten Speekenbrink, Marjan Jahanshahi

Abstract

The subthalamic nucleus (STN) is proposed to modulate response thresholds and speed-accuracy trade-offs. In situations of conflict, the STN is considered to raise response thresholds, allowing time for the accumulation of information to occur before a response is selected. Conversely, speed pressure is thought to reduce the activity of the STN and lower response thresholds, resulting in fast, errorful responses. In Parkinson's disease (PD), subthalamic nucleus deep brain stimulation (STN-DBS) reduces the activity of the nucleus and improves motor symptoms. We predicted that the combined effects of STN stimulation and speed pressure would lower STN activity and lead to fast, errorful responses, hence resulting in impulsive action. We used the motion discrimination 'moving-dots' task to assess speed-accuracy trade-offs, under both speed and accuracy instructions. We assessed 12 patients with PD and bilateral STN-DBS and 12 age-matched healthy controls. Participants completed the task twice, and the patients completed it once with STN-DBS on and once with STN-DBS off, with order counterbalanced. We found that STN stimulation was associated with significantly faster reaction times but more errors under speed instructions. Application of the drift diffusion model showed that stimulation resulted in lower response thresholds when acting under speed pressure. These findings support the involvement of the STN in the modulation of speed-accuracy trade-offs and establish for the first time that speed pressure alone, even in the absence of conflict, can result in STN stimulation inducing impulsive action in PD.

Keywords: Deep brain stimulation; Impulsivity; Parkinson’s disease; Response threshold; Speed–accuracy trade-off; Subthalamic nucleus.

Figures

Fig. 1
Fig. 1
Sequence of stimulus and feedback presentation on the screen for the moving-dots task during: a the accuracy trials and b the speed trials
Fig. 2
Fig. 2
Mean RT (ms) as a function of STN-DBS on or off for patients with Parkinson’s disease, and Time of assessment (Time 1 = first, Time 2 = second assessment) for the healthy controls; asterisk denotes significant differences
Fig. 3
Fig. 3
Mean RT (ms) for a patients with Parkinson’s disease with STN-DBS on or off and b healthy controls for Time 1 (first) and Time 2 (second) assessments, under both speed and accuracy instructions; asterisk denotes significant differences
Fig. 4
Fig. 4
Mean percentage error (PE%) a for patients with Parkinson’s disease and healthy controls, under speed versus accuracy instructions, and b as a function of STN-DBS/Time, under speed versus accuracy instructions; asterisk denotes significant differences
Fig. 5
Fig. 5
Mean response thresholds for a patients with Parkinson’s disease with STN-DBS on or off (DBS on, DBS off), and b healthy controls at the two assessments (Time 1 = first, Time 2 = second), under speed versus accuracy instructions
Fig. 6
Fig. 6
Mean non-decision time for patients with Parkinson’s disease with deep brain stimulation on versus off (DBS on, DBS off) and healthy controls for the Time 1 versus Time 2 assessments (Time 1 = first, Time 2 = second); asterisk denotes significant differences

References

    1. Afsharpour S. Topographical projections of the cerebral cortex to the subthalamic nucleus. J Comp Neurol. 1985;236(1):14–28. doi: 10.1002/cne.902360103.
    1. 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;27:3743–3752. doi: 10.1523/JNEUROSCI.0519-07.2007.
    1. 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(6):817–824. doi: 10.1002/ana.21795.
    1. Beck AT, Steer RA, Brown GK, editors. Manual for the Beck Depression Inventory-II. San Antonio: Psychological Corporation; 1996.
    1. Bogacz R, Turner R. Cortico-striatal connections predict control over speed and accuracy in perceptual decision-making. PNAS. 2010;107(36):15916–15920. doi: 10.1073/pnas.1004932107.
    1. Bogacz R, Wagenmakers E, Forstmann BU, Nieuwenhuis S. The neural basis of the speed–accuracy tradeoff. Trends Neurosci. 2009;33(1):10–16. doi: 10.1016/j.tins.2009.09.002.
    1. Britten KH, Shadlen MN, Newsome WT, Movshon JA. The analysis of visual motion: a comparison of neuronal and psychophysical performance. J Neurosci. 1992;12:4745–4765.
    1. Brown SD, Heathcote AJ. The simplest complete model of choice reaction time: linear ballistic accumulation. Cogn Psychol. 2008;57:153–178. doi: 10.1016/j.cogpsych.2007.12.002.
    1. Castrioto A, L’Hommée E, Moro E, Krack P. Mood and behavioural effects of subthalamic stimulation in Parkinson’s disease. Lancet Neurol. 2014;13(3):287–305. doi: 10.1016/S1474-4422(13)70294-1.
    1. Cavanagh JF, Wiecki TV, Cohen MX, Figueroa CM, Samanta J, Sherman SJ, et al. Subthalamic nucleus stimulation reverses mediofrontal influence over decision threshold. Nat Neurosci. 2011;14(11):1462–1469. doi: 10.1038/nn.2925.
    1. Cavanagh JF, Sanguinetti JL, Allen JJ, Sherman SJ, Frank MJ. the subthalamic nucleus contributes to post-error slowing. J Cogn Neurosci. 2014;26(11):2637–2644. doi: 10.1162/jocn_a_00659.
    1. Dalley JW, Roiser JP. Dopamine, serotonin and impulsivity. Neuroscience. 2012;215:42–58. doi: 10.1016/j.neuroscience.2012.03.065.
    1. Dalley JW, Everitt BJ, Robbins TW. Impulsivity, compulsivity, and top-down cognitive control. Neuron. 2011;69(4):680–694. doi: 10.1016/j.neuron.2011.01.020.
    1. Deuschl D, Schade-Brittinger C, Krack P, Volkmann J, Schäfer H, Bötzel K, et al. A randomized trial of deep-brain stimulation for Parkinson’s disease. N Engl J Med. 2006;355:896–908. doi: 10.1056/NEJMoa060281.
    1. Dickman SJ, Meyer DE. Impulsivity and speed–accuracy tradeoffs in information processing. J Pers Soc Psychol. 1988;54:274–290. doi: 10.1037/0022-3514.54.2.274.
    1. Djamshidian A, O’Sullivana SS, Foltynie T, Aviles-Olmos T, Limousin P, Noyce A, et al. Dopamine agonists rather than deep brain stimulation cause reflection impulsivity in Parkinson’s disease. J Parkinson’s Dis. 2013;3:139–144.
    1. Domenech P, Dreher JC. Decision threshold modulation in the human brain. J Neurosci. 2010;30(43):14305–14317. doi: 10.1523/JNEUROSCI.2371-10.2010.
    1. Evenden JL. Varieties of impulsivity. Psychopharmacology. 1999;146:348–361. doi: 10.1007/PL00005481.
    1. Fitts PM. Cognitive aspects of information processing: III. Set for speed versus accuracy. J Exp Psychol. 1966;71:849–857. doi: 10.1037/h0023232.
    1. Follett KA, Weaver FM, Stern M, Hur K, Harris CL, Luo P, et al. Pallidal versus subthalamic deep-brain stimulation for Parkinson’s disease. N Engl J Med. 2010;362(22):2077–2091. doi: 10.1056/NEJMoa0907083.
    1. Folstein MF, Folstein SE, McHugh PR. “Mini-mental state”: a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 1975;12(3):189–198. doi: 10.1016/0022-3956(75)90026-6.
    1. Forstmann BU, Dutilh 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 USA. 2008;105:17538–17542. doi: 10.1073/pnas.0805903105.
    1. Forstmann BU, Anwander A, Schäfer A, Neumann J, Brown S, Wagenmakers EJ, et al. Cortico-striatal connections predict control over speed and accuracy in perceptual decision making. Proc Natl Acad Sci USA. 2010;107(36):15916–15920. doi: 10.1073/pnas.1004932107.
    1. Frank MJ. Hold your horses: a dynamic computational role for the subthalamic nucleus in decision-making. Neural Netw. 2006;19:1120–1136. doi: 10.1016/j.neunet.2006.03.006.
    1. Frank MJ, Samanta J, Moustafa AA, Sherman SJ. Hold your horses: impulsivity, deep brain stimulation, and medication in Parkinsonism. Science. 2007;318:1309–1312. doi: 10.1126/science.1146157.
    1. Goetz CG, Fahn S, Martinez-Martin P, Poewe W, Sampaio C, Stebbins GT, et al. Movement disorder society-sponsored revision of the unified Parkinson’s disease rating scale (MDS-UPDRS): process, format, and clinimetric testing plan. Mov Disord. 2007;22:41–47. doi: 10.1002/mds.21198.
    1. Grasman RP, Wagenmakers EJ, van der Maas HL. On the mean and variance of response times under the diffusion model with an application to parameter estimation. J Math Psychol. 2009;53:55–68. doi: 10.1016/j.jmp.2009.01.006.
    1. Green N, Biele GP, Heekeren HR. Changes in neural connectivity underlie decision threshold modulation for reward maximization. J Neurosci. 2012;32(43):14942–14950. doi: 10.1523/JNEUROSCI.0573-12.2012.
    1. Green N, Bogacz R, Huebl J, Beyer AK, Kühn AA, Heekeren HR. Reduction of influence of task difficulty on perceptual decision making by STN deep brain stimulation. Curr Biol. 2013;23:1681–1684. doi: 10.1016/j.cub.2013.07.001.
    1. Hack N, Akbar U, Thompson-Avila A, Fayad SM, Hastings EM, Moro E, Nestor K, Ward H, York M, Okun MS. Impulsive and compulsive behaviors in Parkinson Study Group (PSG) centers performing deep brain stimulation surgery. J Parkinsons Dis. 2014;4(4):591–598.
    1. Hälbig TD, Tse W, Frisina PG, Baker BR, Hollander E, Shapiro H, et al. Subthalamic deep brain stimulation and impulse control in Parkinson’s disease. Eur J Neurol. 2009;16:493–497. doi: 10.1111/j.1468-1331.2008.02509.x.
    1. Hälbig TD, Tse W, Frisina PG, Baker BR, Hollander E, Shapiro H, Tagliati M, Koller WC, Olanow CW. Subthalamic deep brain stimulation and impulse control in Parkinson’s disease. Eur J Neurol. 2009;16(4):493–497. doi: 10.1111/j.1468-1331.2008.02509.x.
    1. Heekeren HR, Marrett S, Ruff DA, Bandettini PA, Ungerleider LG. Involvement of human left dorsolateral prefrontal cortex in perceptual decision making is independent of response modality. Proc Natl Acad Sci USA. 2006;103(26):10023–10028. doi: 10.1073/pnas.0603949103.
    1. Hershey T, Revilla FJ, Wernle A, Gibson PS, Dowling JL, Perlmutter JS. Stimulation of STN impairs aspects of cognitive control in Parkinson’s disease. Neurology. 2004;62(7):1110–1114. doi: 10.1212/01.WNL.0000118202.19098.10.
    1. Hershey T, Campbell MC, Videen TO, Lugar HM, Weaver PM, Hartlein J, et al. Mapping Go–No–Go performance within the subthalamic nucleus region. Brain. 2010;133(12):3625–3634. doi: 10.1093/brain/awq256.
    1. Hoehn M, Yahr M. Parkinsonism: onset, progression and mortality. J Neurol. 1967;17(5):427–442. doi: 10.1212/WNL.17.5.427.
    1. Huang Y, Georgiev D, Foltynie T, Limousin P, Speekenbrink M, Jahanshahi M. Different effects of dopaminergic medication on perceptual decision-making in Parkinson’s disease as a function of task difficulty and speed–accuracy instructions. Neuropsychologia. 2015;75:577–587. doi: 10.1016/j.neuropsychologia.2015.07.012.
    1. Ivanoff J, Branning P, Marois R. fMRI evidence for a dual process account of the speed–accuracy tradeoff in decision-making. PLoS One. 2008;3(7):e2635–e2648. doi: 10.1371/journal.pone.0002635.
    1. Jahanshahi M. Effects of deep brain stimulation of the subthalamic nucleus on inhibitory and executive control over prepotent responses in Parkinson’s disease. Front Syst Neurosci. 2013;7(118):1–20.
    1. Jahanshahi M, Ardouin CMA, 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;123:1142–1154. doi: 10.1093/brain/123.6.1142.
    1. Jahanshahi M, Obeso I, Baunez C, Alegre M, Krack P. Parkinson’s disease, the subthalamic nucleus, inhibition, and impulsivity. Mov Disord. 2015;30(2):128–140. doi: 10.1002/mds.26049.
    1. L’Hommée E, Klinger H, Thobois S, Schmitt E, Ardouin C, Bichon A, et al. Subthalamic stimulation in Parkinson’s disease: restoring the balance of motivated behaviours. Brain. 2012;135(5):1463–1477. doi: 10.1093/brain/aws078.
    1. Lim SY, O’Sullivan SS, Kotschet K, et al. Dopamine dysregulation syndrome, impulse control disorders and punding after deep brain stimulation surgery for Parkinson’s disease. J Clin Neurosci. 2009;16(9):1148–1152. doi: 10.1016/j.jocn.2008.12.010.
    1. Mansfield EL, Karayanidis F, Jamadar S, Heathcote A, Forstmann BU. Adjustments of response threshold during task switching: a model-based functional magnetic resonance imaging study. J Neurosci. 2011;31(41):14688–14692. doi: 10.1523/JNEUROSCI.2390-11.2011.
    1. McIntyre CC, Savasta M, Kerkerian-Le GL, Vitek JL. Uncovering the mechanism(s) of action of deep brain stimulation: activation, inhibition, or both. Clin Neurophysiol. 2004;115(6):1239–1248. doi: 10.1016/j.clinph.2003.12.024.
    1. Moran A, Stein E, Tischler H, Bar-Gad I. Decoupling neuronal oscillations during subthalamic nucleus stimulation in the parkinsonian primate. Neurobiol Dis. 2012;45:583–590. doi: 10.1016/j.nbd.2011.09.016.
    1. Moum SJ, Price CC, Limotai N, Oyama G, Ward H, Jacobson C, Foote KD, Okun MS. Effects of STN and GPi deep brain stimulation on impulse control disorders and dopamine dysregulation syndrome. PLoS One. 2012;7(1):e29768. doi: 10.1371/journal.pone.0029768.
    1. Mulder MJ, Wagenmakers E-J, Ratcliff R, Boekel W, Forstmann BU. Bias in the brain: a diffusion model analysis of prior probability and potential payoff. J Neurosci. 2012;32:2335–2343. doi: 10.1523/JNEUROSCI.4156-11.2012.
    1. Nambu A, Tokuno H, Inase M, Takada M. Corticosubthalamic input zones from forelimb representations of the dorsal and ventral divisions of the premotor cortex in the macaque monkey: comparison with the input zones from the primary motor cortex and the supplementary motor area. Neurosci Lett. 1997;239(1):13–16. doi: 10.1016/S0304-3940(97)00877-X.
    1. Obeso I, Wilkinson L, Rodríguez-Oroz MC, Obeso JA, Jahanshahi M. Bilateral stimulation of the subthalamic nucleus has differential effects on reactive and proactive inhibition and conflict-induced slowing in Parkinson’s disease. Exp Brain Res. 2013;226(3):451–462. doi: 10.1007/s00221-013-3457-9.
    1. Oyama G, Shimo Y, Natori S, Nakajima M, Ishii H, Arai H, et al. Acute effects of bilateral subthalamic stimulation on decision-making in Parkinson’s disease. Parkinsonism Relat Disord. 2011;17:189–193. doi: 10.1016/j.parkreldis.2010.12.004.
    1. Parent A, Hazrati LN. Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop. Brain Res Brain Res Rev. 1995;20:91–127. doi: 10.1016/0165-0173(94)00007-C.
    1. Parsons TD, Rogers SA, Braaten AJ, Woods SP, Troster AI. Cognitive sequelae of subthalamic nucleus deep brain stimulation in Parkinson’s disease: a meta-analysis. Lancet Neurol. 2006;5:578–588. doi: 10.1016/S1474-4422(06)70475-6.
    1. Plessow F, Fischer R, Volkmann J, Schubert T. Subthalamic deep brain stimulation restores automatic response activation and increases susceptibility to impulsive behavior in patients with Parkinson’s disease. Brain Cogn. 2014;87:16–21. doi: 10.1016/j.bandc.2014.02.009.
    1. Ratcliff R. A theory of memory retrieval. Psychol Rev. 1978;83:59–108. doi: 10.1037/0033-295X.85.2.59.
    1. Ratcliff R, McKoon G. The diffusion decision model: theory and data for two-choice decision tasks. Neural Comput. 2008;20(4):873–922. doi: 10.1162/neco.2008.12-06-420.
    1. 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(13):2828–2834. doi: 10.1016/j.neuropsychologia.2009.06.011.
    1. Soulas T, Gurruchaga JM, Palfi S, Cesaro P, Nguyen JP, Fenelon G. Attempted and completed suicides after subthalamic nucleus stimulation for Parkinson disease. J Neurology Neurosurg Psychiatr. 2008;79(8):952–954. doi: 10.1136/jnnp.2007.130583.
    1. Standage D, Blohm G, Dorris MC. On the neural implementation of the speed–accuracy trade-off. Front Neurosci. 2014;8(236):1–19.
    1. Starkstein SE, Mayberg HS, Preziosi TJ, Andrezejewski P, Leiguarda R, Robinson RG. Reliability, validity, and clinical correlates of apathy in Parkinson’s disease. J Neuropsychiatry Clin Neurosci. 1992;4(2):134–139. doi: 10.1176/jnp.4.2.134.
    1. Thobois S, Ardouin C, L’Hommée E, Klinger H, Lagrange C, Xie J, et al. Non-motor dopamine withdrawal syndrome after surgery for Parkinson’s disease: predictors and underlying mesolimbic denervation. Brain. 2010;133(4):1111–1127. doi: 10.1093/brain/awq032.
    1. Torta DM, Vizzari V, Castelli L, Zibetti M, Lanotte M, Lopiano L, et al. Impulsivities and Parkinson’s disease: delay aversion is not worsened by deep brain stimulation of the subthalamic nucleus. PLoS One. 2012;7:e43261. doi: 10.1371/journal.pone.0043261.
    1. van Maanen L, Brown SD, Eichele T, Wagenmakers EJ, Ho T, Serences J, Forstmann BU. Neural correlates of trial-to-trial fluctuations in response caution. J Neurosci. 2011;31(48):17488–17495. doi: 10.1523/JNEUROSCI.2924-11.2011.
    1. van Veen V, Krug MK, Carter CS. The neural and computational basis of controlled speed–accuracy tradeoff during task performance. J Cogn Neurosci. 2008;20(11):1952–1965. doi: 10.1162/jocn.2008.20146.
    1. Vickers D. Evidence for an accumulator model of psychophysical discrimination. Ergonomics. 1970;13:37–58. doi: 10.1080/00140137008931117.
    1. Volkmann J, Daniels C, Witt K. Neuropsychiatric effects of subthalamic neurostimulation in Parkinson disease. Nat Rev Neurol. 2010;6(9):487–498.
    1. Voon V, Krack P, Lang AE, Lozano AM, Dujardin K, Schüpbach M, et al. A multicentre study on suicide outcomes following subthalamic stimulation for Parkinson’s disease. Brain. 2008;131:2720–2728. doi: 10.1093/brain/awn214.
    1. Voss A, Voss J. Fast-dm: a free program for efficient diffusion model analysis. Behav Res Methods. 2007;39(4):767–775. doi: 10.3758/BF03192967.
    1. Weaver FM, Follett K, Stern M, Hur K, Harris C, Marks WJ, Jr, et al. Bilateral deep brain stimulation vs. best medical therapy for patients with advanced Parkinson disease: a randomized controlled trial. JAMA. 2009;301(1):63–73. doi: 10.1001/jama.2008.929.
    1. Whitmer D, de Solages C, Hill B, Yu H, Henderson JM, Bronte- Stewart H. High frequency deep brain stimulation attenuates sub-thalamic and cortical rhythms in Parkinson’s disease. Front Hum Neurosci. 2012;6:155. doi: 10.3389/fnhum.2012.00155.
    1. Wickelgren W. Speed–accuracy tradeoff and information-processing dynamics. Acta Psychol. 1977;41:67–85. doi: 10.1016/0001-6918(77)90012-9.
    1. Williams A, Gill S, Varma T, Jenkinson C, Quinn N, Mitchell R, et al. Deep brain stimulation plus best medical therapy versus best medical therapy alone for advanced Parkinson’s disease (PD SURG trial): a randomised, open-label trial. Lancet Neurol. 2010;9(6):581–591. doi: 10.1016/S1474-4422(10)70093-4.
    1. Williams IA, Wilkinson L, Limousin P, Jahanshahi M. Load-dependent interference of deep brain stimulation of the subthalamic nucleus with switching from automatic to controlled processing during random number generation in Parkinson’s disease. J Parkinsons Dis. 2015;5(2):321–331. doi: 10.3233/JPD-140355.
    1. 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. doi: 10.1001/archneur.61.5.697.
    1. Woodworth RS. The accuracy of voluntary movement. Psychol Rev. 1899;3:1–114.
    1. Wylie SA, Ridderinkhof KR, Elias WJ, Frysinger RC, Bashore TR, Downs KE, et al. Subthalamic nucleus stimulation influences expression and suppression of impulsive behaviour in Parkinson’s disease. Brain. 2010;133(12):3611–3624. doi: 10.1093/brain/awq239.

Source: PubMed

Sponsoren und Mitarbeiter

Krankheiten

Drogeninterventionen

3
Abonnieren