BRAIN STIMULATION: Basic, Translational, and Clinical Research in Neuromodulation
Volume 3, Issue 3 , Pages 170-176 , July 2010

Continuous theta burst stimulation of right dorsolateral prefrontal cortex induces changes in impulsivity level

  • Sang Soo Cho

      Affiliations

    • PET Imaging Centre, Centre for Addiction and Mental Health, University of Toronto, Toronto, Canada
  • ,
  • Ji Hyun Ko

      Affiliations

    • PET Imaging Centre, Centre for Addiction and Mental Health, University of Toronto, Toronto, Canada
  • ,
  • Giovanna Pellecchia

      Affiliations

    • PET Imaging Centre, Centre for Addiction and Mental Health, University of Toronto, Toronto, Canada
    • Toronto Western Research Institute and Hospital, University Health Network, University of Toronto, Toronto, Canada
  • ,
  • Thilo Van Eimeren

      Affiliations

    • PET Imaging Centre, Centre for Addiction and Mental Health, University of Toronto, Toronto, Canada
    • Toronto Western Research Institute and Hospital, University Health Network, University of Toronto, Toronto, Canada
  • ,
  • Roberto Cilia

      Affiliations

    • PET Imaging Centre, Centre for Addiction and Mental Health, University of Toronto, Toronto, Canada
    • Toronto Western Research Institute and Hospital, University Health Network, University of Toronto, Toronto, Canada
  • ,
  • Antonio P. Strafella

      Affiliations

    • PET Imaging Centre, Centre for Addiction and Mental Health, University of Toronto, Toronto, Canada
    • Toronto Western Research Institute and Hospital, University Health Network, University of Toronto, Toronto, Canada
    • Corresponding Author InformationCorrespondence: Antonio P. Strafella, MD, PhD, FRCPC, Toronto Western Hospital and Institute CAMH-PET Imaging Centre, University of Toronto, 399 Bathurst Street, Toronto, ON, M5T 2S8 Canada.

Received 6 May 2009 ,Revised 8 September 2009 ,Accepted 7 October 2009.

References 

  1. Kirby KN, Petry NM. Heroin and cocaine abusers have higher discount rates for delayed rewards than alcoholics or non-drug-using controls. Addiction. 2004;99(4):461–471
  2. Barkley R, Edwards G, Laneri M, Fletcher K, Metevia L. Executive functioning, temporal discounting, and sense of time in adolescents with attention deWcit hyperactivity disorder (ADHD) and oppositional deWant disorder (ODD). J Abnorm Child Psychol. 2001;29:541–556
  3. Alessi SM, Petry NM. Pathological gambling severity is associated with impulsivity in a delay discounting procedure. Behav Processes. 2003;64(3):345–354
  4. Bechara A, Damasio AR, Damasio H, Anderson SW. Insensitivity to future consequences following damage to human prefrontal cortex. Cognition. 1994;50:7–12
  5. Ainslie G. Specious reward: a behavioral theory of impulsiveness and impulse control. Psychol Bull. 1975;82:463–494
  6. Dixon MR, Jacobs EA, Sanders S, et al. Impulsivity, self-control, and delay discounting in persons with acquired brain injury. Behav Intervent. 2005;20:101–120
  7. Kalenscher T, Windmann S, Diekamp B, et al. Single units in the pigeon brain integrate reward amount and time-to-reward in an impulsive choice task. Curr Biol. 2005;15(7):594–602
  8. Garavan H, Ross TJ, Stein EA. Right hemispheric dominance of inhibitory control: an event-related functional MRI study. Proc Natl Acad Sci U S A. 1999;96:8301–8306
  9. Aron AR, Fletcher PC, Bullmore ET, Sahakian BJ, Robbins TW. Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans. Nat Neurosci. 2003;6:115–116
  10. Conway MA, Fthenaki A. Disruption of inhibitory control of memory following lesions to the frontal and temporal lobes. Cortex. 2003;39:667–686
  11. Fleck MS, Daselaar SM, Dobbins IG, Cabeza R. Role of prefrontal and anterior cingulate regions in decision-making processes shared by memory and nonmemory tasks. Cereb Cortex. 2006;6(11):1623–1630
  12. van't Wout M, Kahn RS, Sanfey AG, Aleman A. Repetitive transcranial magnetic stimulation over the right dorsolateral prefrontal cortex affects strategic decision-making. Neuroreport. 2005;16(16):1849–1852
  13. Fecteau S, Knoch D, Fregni F, et al. Diminishing risk-taking behavior by modulating activity in the prefrontal cortex: a direct current stimulation study. J Neurosci. 2007;727(46):12500–12505
  14. Knoch D, Gianotti LR, Pascual-Leone A, et al. Disruption of right prefrontal cortex by low-frequency repetitive transcranial magnetic stimulation induces risk-taking behavior. J Neurosci. 2006;26:6469–6472
  15. Knoch D, Pascual-Leone A, Meyer K, Treyer V, Fehr E. Diminishing reciprocal fairness by disrupting the right prefrontal cortex. Science. 2006;314:829–832
  16. Di Lazzaro V, Pilato F, Saturno E, et al. Theta-burst repetitive transcranial magnetic stimulation suppresses specific excitatory circuits in the human motor cortex. J Physiol. 2005;565(Pt 3):945–950
  17. Huang YZ, Edwards MJ, Rounis E, Bhatia KP, Rothwell JC. Theta burst stimulation of the human motor cortex. Neuron. 2005;45(2):201–206
  18. Hubl D, Nyffeler T, Wurtz P, et al. Time course of blood oxygenation level-dependent signal response after theta burst transcranial magnetic stimulation of the frontal eye field. Neuroscience. 2008;151(3):921–928
  19. Ko JH, Monchi O, Ptito A, et al. Theta burst stimulation-induced inhibition of dorsolateral prefrontal cortex reveals hemispheric asymmetry in striatal dopamine release during a set-shifting task—a TMS– [11C]raclopride PET study. Eur J Neurosci. 2008;28:2147–2155
  20. Vallesi A, Shallice T, Walsh V. Role of the prefrontal cortex in the foreperiod effect: TMS evidence for dual mechanisms in temporal preparation. Cereb Cortex. 2007;17:466–474
  21. Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 1971;9(1):97–113
  22. Talairach J, Tournoux P. Co-planar stereotactic atlas of the human brain: 3-dimensional proportional system: an approach to cerebral imaging. New York: Thieme; 1988;
  23. Paus T. Imaging the brain before, during, and after transcranial magnetic stimulation. Neuropsychologia. 1999;37(2):219–224
  24. Strafella AP, Paus T, Barrett J, Dagher A. Repetitive transcranial magnetic stimulation of the human prefrontal cortex induces dopamine release in the caudate nucleus. J Neurosci. 2001;21(15):1–4
  25. Collins DL, Neelin P, Peters TM, Evans AC. Automatic 3D intersubjectregistration of MR volumetric data in standardized Talairach space. J Comput Assist Tomogr. 1994;18(2):192–205
  26. Kirby K, Petry N, Bickel W. Heroin addicts have higher discount rates for delayed rewards than non-drug-using controls. J Exp Psychol Gen. 1999;128:78–87
  27. Mitchell SH. Measures of impulsivity in cigarette smokers and non-smokers. Psychopharmacology. 1999;146:455–464
  28. Richards JB, Zhang L, Mitchell SH, De Wit H. Delay or probability discounting in a model of impulsive behavior: effect of alcohol. J Exp Anal Behav. 1999;71:121–143
  29. de Wit H, Enggasser JL, Richards JB. Acute administration of d-amphetamine decreases impulsivity in healthy volunteers. Neuropsychopharmacology. 2002;27(5):813–825
  30. Monterosso JR, Ainslie G, Xu J, et al. Frontoparietal cortical activity of methamphetamine-dependent and comparison subjects performing a delay discounting task. Hum Brain Mapp. 2007;28(5):383–393
  31. Johnson MW, Bickel WK. Within-subject comparison of real and hypothetical money rewards in delay discounting. J Exp Anal Behav. 2002;77:129–146
  32. Madden GJ, Begotka AM, Raiff BR, Kastern LL. Delay discounting of real and hypothetical rewards. Exp Clin Psychopharmacol. 2003;11:139–145
  33. Aron AR, Robbins TW, Poldrack RA. Inhibition and the right inferior frontal cortex. Trends Cogn Sci. 2004;8(4):170–177
  34. Conway MA, Fthenaki A. Disruption of inhibitory control of memory following lesions to the frontal and temporal lobes. Cortex. 2003;39(4-5):667–686
  35. Damasio AR. The Somatic marker hypothesis and the possible functions of the prefrontal cortex. Philos Trans R Soc Lond B Biol Sci. 1996;351:1413–1420
  36. Kringelbach ML. The human orbitofrontal cortex: linking reward to hedonic experience. Nat Rev Neurosci. 2005;6:691–702
  37. Petrides M, Pandya DN. Dorsolateral prefrontal cortex: comparative cytoarchitectonic analysis in the human and the macaque brain and corticocortical connection patterns. Eur J Neurosci. 1999;11(3):1011–1036
  38. Knoch D, Treyer V, Regard M, et al. Lateralized and frequency-dependent effects of prefrontal rTMS on regional cerebral blood flow. Neuroimage. 2006;31(2):641–648
  39. Wittmann M, Paulus MP. Decision making, impulsivity and time perception. Trends Cogn Sci. 2008;12(1):7–12
  40. Harrington DL, Haaland KY, Knight RT. Cortical networks underlying mechanisms of time perception. J Neurosci. 1998;18(3):1085–1095
  41. Rao SM, Mayer AR, Harrington DL. The evolution of brain activation during temporal processing. Nat Neurosci. 2001;4:317–323
  42. Koch G, Oliveri M, Carlesimo GA, Caltagirone C. Selective deficit of time perception in a patient with right prefrontal cortex lesion. Neurology. 2002;59(10):1658–1659
  43. Koch G, Oliveri M, Torriero S, Caltagirone C. Underestimation of time perception after repetitive transcranial magnetic stimulation. Neurology. 2003;60(11):1844–1846
  44. Reynolds B, Schiffbauer R. Measuring state changes in human delay discounting: an experiential discounting task. Behav Processes. 2004;67:343–356
  45. Berlin HA, Rolls ET. Time perception, impulsivity, emotionality, and personality in self-harming borderline personality disorder patients. J Personal Disord. 2004;18:358–378
  46. Wittmann M, Leland DS, Paulus MP. Time and decision making: differential contribution of the posterior insular cortex and the striatum during a delay discounting task. Exp Brain Res. 2007;179:643–653
  47. Koch G, Costa A, Brusa L, et al. Impaired reproduction of second but not millisecond time intervals in Parkinson's disease. Neuropsychologia. 2008;46(5):1305–1313
  48. Cardinal RN, Robbins TW, Everitt BJ. The effects of d-amphetamine, chlordiazepoxide, alpha-flupenthixol and behavioral manipulations on choice of signaled and unsignaled delayed reinforcement in rats. Psychopharmacology. 2000;152:362–375
  49. Tanaka SC, Doya K, Okada G, et al. Prediction of immediate and future rewards differentially recruits cortico-basal ganglia loops. Nat Neurosci. 2004;7(8):887–893
  50. Tanaka SC, Samejima K, Okada G, et al. Brain mechanism of reward prediction under predictable and unpredictable environmental dynamics. Neural Netw. 2006;19(8):1233–1241
  51. Franca M, Koch G, Mochizuki H, et al. Effects of theta burst stimulation protocols on phosphene threshold. Clin Neurophysiol. 2006;117(8):1808–1813
  52. Wilkinson L, Teo JT, Obeso I, et al. The contribution of primary motor cortex is essential for probabilistic implicit sequence learning: evidence from theta burst magnetic stimulation [published ahead of print March 20 2009]. J Cogn Neurosci. doi: 10.1162
  53. Voss M, Bays PM, Rothwell JC, et al. An improvement in perception of self-generated tactile stimuli following theta-burst stimulation of primary motor cortex. Neuropsychologia. 2007;45(12):2712–2717
  54. Fierro B, Brighina F, Vitello G, et al. Modulatory effects of low- and high-frequency repetitive transcranial magnetic stimulation on visual cortex of healthy subjects undergoing light deprivation. J Physiol. 2005;565(Pt2):659–665
  55. Ziemann U, Corwell B, Cohen LG. Modulation of plasticity in human motor cortex after forearm ischemic nerve block. J Neurosci. 1998;18(3):1115–1123
  56. Enomoto H, Ugawa Y, Hanajima R, et al. Decreased sensory cortical excitability after 1 Hz rTMS over the ipsilateral primary motor cortex. Clin Neurophysiol. 2001;112:2154–2158
  57. Pascual-Leone A, Valls-Sole J, Wassermann EM, Hallett M. Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. Brain. 1994;117:847–858

 This work was funded by the Canadian Institutes of Health Research to A.P.S. (MOP-64423). S.S.C. was supported by the Korea Research Foundation Grant funded by the Korean Government (MOEHRD, Basic Research Promotion Fund) (KRF-2007-359-E00014).

PII: S1935-861X(09)00106-5

doi: 10.1016/j.brs.2009.10.002

BRAIN STIMULATION: Basic, Translational, and Clinical Research in Neuromodulation
Volume 3, Issue 3 , Pages 170-176 , July 2010