Prefrontal transcranial direct current stimulation alters activation and connectivity in cortical and subcortical reward systems: A tDCS-fMRI study

Human Brain Mapping

Volumn 35, Issue 8, 2014, Pages 3673-3686

  Weber, Matthew J ^a   Messing, Samuel B ^a   Rao, Hengyi ^a   Detre, John A ^a   Thompson Schill, Sharon L ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Balloon Analog Risk Task; FMRI; Network analysis; Resting state connectivity; TDCS

Indexed keywords

ADULT; ANTERIOR CINGULATE; ARTICLE; BALLOON ANALOG RISK TASK; BOLD SIGNAL; CONNECTOME; CONTROLLED STUDY; ECHO PLANAR IMAGING; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HUMAN; HUMAN EXPERIMENT; MALE; MIDDLE FRONTAL GYRUS; NEUROLOGIC EXAMINATION; NORMAL HUMAN; ORBITAL CORTEX; PRIORITY JOURNAL; SUBCORTEX; TRANSCRANIAL DIRECT CURRENT STIMULATION; BLOOD; BRAIN; BRAIN CIRCULATION; BRAIN MAPPING; NERVE TRACT; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PREFRONTAL CORTEX; PROCEDURES; REST; REWARD; YOUNG ADULT;

OXYGEN;

ADULT; BRAIN; BRAIN MAPPING; CEREBROVASCULAR CIRCULATION; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; NEURAL PATHWAYS; NEUROPSYCHOLOGICAL TESTS; OXYGEN; PREFRONTAL CORTEX; REST; REWARD; TRANSCRANIAL DIRECT CURRENT STIMULATION; YOUNG ADULT;

EID: 84903946459     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.22429     Document Type: Article

References (85)

1. Achard S, Salvador R, Whitcher B, Suckling J, Bullmore E (2006): A resilient, low-frequency, small-world human brain functional network with highly connected association cortical hubs. J Neurosci 26:63-72.
2. Aguirre GK, Detre JA, Zarahn E, Alsop DC (2002): Experimental design and the relative sensitivity of BOLD and perfusion fMRI. Neuroimage 15:488-500.
3. Antal A, Polanía R, Schmidt-Samoa C, Dechent P, Paulus W (2011): Transcranial direct current stimulation over the primary motor cortex during fMRI. Neuroimage 55:590-596.
4. Antal A, Kovács G, Chaieb L, Cziraki C, Paulus W, Greenlee MW (2012): Cathodal stimulation of human MT+ leads to elevated fMRI signal: A tDCS-fMRI study. Restor Neurol Neurosci 30:255-263.
5. Avants BB, Tustison NJ, Song G, Cook PA, Klein A, Gee JC (2010): A reproducible evaluation of ANTs similarity metric performance in brain image registration. Neuroimage 54:2033-2044.
6. Baudewig J, Nitsche MA, Paulus W, Frahm J (2001): Regional modulation of BOLD MRI responses to human sensorimotor activation by transcranial direct current stimulation. Magn Reson Med 45:196-201.
7. Bonacich P (1972): Factoring and weighting approaches to clique identification. J Math Sociol 2:113-120.
8. Bonacich P (2007): Some unique properties of eigenvector centrality. Soc Netw 29:555-564.
9. Botvinick MM, Cohen JD, Carter CS (2004): Conflict monitoring and anterior cingulate cortex: An update. Trends Cogn Sci 8:539-546.
10. Brand M, Labudda K, Markowitsch HJ (2006): Neuropsychological correlates of decision-making in ambiguous and risky situations. Neural Netw 19:1266-1276.
11. Camus M, Halelamien N, Plassmann H, Shimojo S, O'Doherty J, Camerer C, Rangel A (2009): Repetitive transcranial magnetic stimulation over the right dorsolateral prefrontal cortex decreases valuations during food choices. Eur J Neurosci 30:1980-1988.
12. Carter CS, van Veen V (2007): Anterior cingulate and conflict detection: An update of theory and data. Cogn Affect Behav Neurosci 7:367-379.
13. Chen Y, Wang DJ, Detre JA (2011): Test-retest reliability of arterial spin labeling with common labeling strategies. J Magn Reson Imaging 33:940-949.
14. Clark L, Manes F, Antoun N, Sahakian BJ, Robbins TW (2003): The contributions of lesion laterality and lesion volume to decision-making impairment following frontal lobe damage. Neuropsychologia 41:1474-1483.
15. Cohen J, Cohen P (1983): Applied Multiple Regression/Correlation Analysis for the Behavioral Sciences. Hillsdale, NJ: Erlbaum.
16. Cox RW (1996): AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 29:162-173.
17. Croxson PL, Walton ME, OReilly JX, Behrens TEJ, Rushworth MFS (2009): Effort-based cost-benefit valuation and the human brain. J Neurosci 29:4531-4541.
18. Csardi G, Nepusz T (2006): The igraph software package for complex network research. Int J Complex Syst 1695, 1-9.
19. Dai W, Garcia D, de Bazelaire C, Alsop DC (2008): Continuous flow-driven inversion for arterial spin labeling using pulsed radio frequency and gradient fields. Magn Reson Med 60:1488-1497.
20. Delgado MR, Schotter A, Ozbay EY, Phelps EA (2008): Understanding overbidding: using the neural circuitry of reward to design economic auctions. Science 321:1849-1852.
21. Detre JA, Alsop DC (1999): Perfusion magnetic resonance imaging with continuous arterial spin labeling: methods and clinical applications in the central nervous system. Eur J Radiol 30:115-124.
22. Detre JA, Rao H, Wang DJJ, Chen YF, Wang Z (2012): Applications of arterial spin labeled MRI in the brain. J Magn Reson Imaging 35:1026-1037.
23. Egan MF, Goldberg TE, Kolachana BS, Callicott JH, Mazzanti CM, Straub RE, Goldman D, Weinberger DR (2001): Effect of COMT Val108/158 Met genotype on frontal lobe function and risk for schizophrenia. Proc Natl Acad Sci USA 98:6917-6922.
24. Fecteau S, Pascual-Leone A, Zald DH, Liguori P, Théoret H, Boggio PS, Fregni F (2007a): Activation of prefrontal cortex by transcranial direct current stimulation reduces appetite for risk during ambiguous decision making. J Neurosci 27:6212-6218.
25. Fecteau S, Knoch D, Fregni F, Sultani N, Boggio P, Pascual-Leone A (2007b): Diminishing risk-taking behavior by modulating activity in the prefrontal cortex: A direct current stimulation study. J Neurosci 27:12500-12505.
26. Fellows LK, Farah MJ (2005): Different underlying impairments in decision-making following ventromedial and dorsolateral frontal lobe damage in humans. Cereb Cortex 15:58-63.
27. Fishbein DH, Eldreth DL, Hyde C, Matochik JA, London ED, Contoreggi C, Kurian V, Kimes AS, Breeden A, Grant S (2005): Risky decision making and the anterior cingulate cortex in abstinent drug abusers and nonusers. Cognit Brain Res 23:119-136.
28. Fukunaga R, Brown JW, Bogg T (2012): Decision making in the Balloon Analogue Risk Task (BART): Anterior cingulate cortex signals loss aversion but not the infrequency of risky choices. Cogn Affect Behav Neurosci 12:479-490.
29. Gläscher J, Adolphs R, Damasio H, Bechara A, Rudrauf D, Calamia M, Paul LK, Tranel D (2012): Lesion mapping of cognitive control and value-based decision making in the prefrontal cortex. Proc Natl Acad Sci USA 109:14681-14686.
30. Gonzalez C, Dana J, Koshino H, Just M (2005): The framing effect and risky decisions: Examining cognitive functions with fMRI. J Econ Psychol 26:1-20.
31. Hassani OK, Cromwell HC, Schultz W (2001): Influence of expectation of different rewards on behavior-related neuronal activity in the striatum. J Neurophysiol 85:2477-2489.
32. Holland R, Leff AP, Josephs O, Galea JM, Desikan M, Price CJ, Rothwell JC, Crinion J (2011): Speech facilitation by left inferior frontal cortex stimulation. Curr Biol 21:1403-1407.
33. Jang SH, Ahn SH, Byun WM, Kim CS, Lee MY, Kwon YH (2009): The effect of transcranial direct current stimulation on the cortical activation by motor task in the human brain: An fMRI study. Neurosci Lett 460:117.
34. Kawagoe R, Takikawa Y, Hikosaka O (1998): Expectation of reward modulates cognitive signals in the basal ganglia. Nat Neurosci 1:411-416.
35. Kawagoe R, Takikawa Y, Hikosaka O (2004): Reward-predicting activity of dopamine and caudate neurons-A possible mechanism of motivational control of saccadic eye movement. J Neurophysiol 91:1013-1024.
36. Keeser D, Meindl T, Bor J, Palm U, Pogarell O, Mulert C, Brunelin J, Moller HJ, Reiser M, Padberg F (2011): Prefrontal transcranial direct current stimulation changes connectivity of resting-state networks during fMRI. J Neurosci 31:15284-15293.
37. Kennerley SW, Walton ME, Behrens TEJ, Buckley MJ, Rushworth MFS (2006): Optimal decision making and the anterior cingulate cortex. Nat Neurosci 9:940-947.
38. Kim JN, Shadlen MN (1999): Neural correlates of a decision in the dorsolateral prefrontal cortex of a macaque. Nat Neurosci 2:176-185.
39. Knoch D, Gianotti LRR, Pascual-Leone A, Treyer V, Regard M, Hohmann M, Brugger P (2006): Disruption of right prefrontal cortex by low-frequency repetitive transcranial magnetic stimulation induces risk-taking behavior. J Neurosci 26:6469-6472.
40. Kriegeskorte N, Simmons WK, Bellgowan PS, Baker CI (2009): Circular analysis in systems neuroscience: the dangers of double dipping. Nat Neurosci 12:535-540.
41. Kwon YH, Ko MH, Ahn SH, Kim YH, Song JC, Lee CH, Chang MC, Jang SH (2008): Primary motor cortex activation by transcranial direct current stimulation in the human brain. Neurosci Lett 435:56-59.
42. Lang N, Siebner HR, Ward NS, Lee L, Nitsche MA, Paulus W, Rothwell JC, Lemon RN, Frackowiak RS (2005): How does transcranial DC stimulation of the primary motor cortex alter regional neuronal activity in the human brain? Eur J Neurosci 22:495-504.
43. Lejuez CW, Read JP, Kahler CW, Richards JB, Ramsey SE, Stuart GL, Strong DR, Brown RA (2002): Evaluation of a behavioral measure of risk taking: the Balloon Analogue Risk Task (BART). J Exp Psychol 8:75-84.
44. Liang X, Wang J, Yan C, Shu N, Xu K, Gong G, He Y (2012): Effects of different correlation metrics and preprocessing factors on small-world brain functional networks: A resting-state functional MRI study. PLoS One 7:e32766.
45. Liu Y, Liang M, Zhou Y, He Y, Hao Y, Song M, Yu C, Liu H, Liu Z, Jiang T (2008): Disrupted small-world networks in schizophrenia. Brain 131:945-961.
46. Manes F, Sahakian B, Clark L, Rogers R, Antoun N, Aitken M, Robbins T (2002): Decision-making processes following damage to the prefrontal cortex. Brain 125:624-639.
47. Marco-Pallarés J, Nager W, Krämer UM, Cunillera T, Càmara E, Cucurell D, Schüle R, Schöls L, Rodriguez-Fornells A, Münte TF (2010): Neurophysiological markers of novelty processing are modulated by COMT and DRD4 genotypes. Neuroimage 53:962-969.
48. McDannald MA, Lucantonio F, Burke KA, Niv Y, Schoenbaum G (2011): Ventral striatum and orbitofrontal cortex are both required for model-based, but not model-free, reinforcement learning. J Neurosci 31:2700-2705.
49. Merzagora AC, Foffani G, Panyavin I, Mordillo-Mateos L, Aguilar J, Onaral B, Oliviero A (2010): Prefrontal hemodynamic changes produced by anodal direct current stimulation. Neuroimage 49:2304-2310.
50. Nair DG, Renga V, Lindenberg R, Zhu L, Schlaug G (2011): Optimizing recovery potential through simultaneous occupational therapy and non-invasive brain-stimulation using tDCS. Restor Neurol Neurosci 29:411-420.
51. Nitsche MA, Paulus W (2001): Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology 57:1899-1901.
52. Nitsche MA, Nitsche MS, Klein CC, Tergau F, Rothwell JC, Paulus W (2003): Level of action of cathodal DC polarisation induced inhibition of the human motor cortex. Clin Neurophysiol 114:600-604.
53. Paulus MP, Rogalsky C, Simmons A, Feinstein JS, Stein MB (2003): Increased activation in the right insula during risk-taking decision making is related to harm avoidance and neuroticism. Neuroimage 19:1439-1448.
54. Peña-Gómez C, Sala-Lonch R, Junqué C, Clemente IC, Vidal D, Bargalló N, Falcón C, Valls-Solé J, Pascual-Leone A, Bartrés-Faz D (2012): Modulation of large-scale brain networks by transcranial direct current stimulation evidenced by resting-state functional MRI. Brain Stimul 5:252-263.
55. Pereira JB, Junqué C, Bartrés-Faz D, Martí MJ, Sala-Llonch R, Compta Y, Falcón C, Vendrell P, Pascual-Leone A, Valls-Solé J, Tolosa E (2012): Modulation of verbal fluency networks by transcranial direct current stimulation (tDCS) in Parkinson's disease. Brain Stimul 6:16-24.
56. Polanía R, Paulus W, Antal A, Nitsche MA (2011a): Introducing graph theory to track for neuroplastic alterations in the resting human brain: A transcranial direct current stimulation study. Neuroimage 54:2287-2296.
57. Polanía R, Nitsche MA, Paulus W (2011b): Modulating functional connectivity patterns and topological functional organization of the human brain with transcranial direct current stimulation. Hum Brain Mapp 32:1236-1249.
58. Polanía R, Paulus W, Nitsche MA (2011c): Modulating cortico-striatal and thalamo-cortical functional connectivity with transcranial direct current stimulation. Hum Brain Mapp 33:2499-2508.
59. Rangel A, Camerer C, Montague PR (2008): A framework for studying the neurobiology of value-based decision making. Nat Rev Neurosci 9:545-556.
60. Rao H, Korczykowski M, Pluta J, Hoang A, Detre JA (2008): Neural correlates of voluntary and involuntary risk taking in the human brain: An fMRI study of the Balloon Analog Risk Task (BART). Neuroimage 42:902-910.
61. Rao H, Mamikonyan E, Detre JA, Siderowf AD, Stern MB, Potenza MN, Weintraub D (2010): Decreased ventral striatal activity with impulse control disorders in Parkinson's disease. Mov Disord 25:1660-1669.
62. Rogers RD, Owen AM, Middleton HC, Williams EJ, Pickard JD, Sahakian BJ, Robbins TW (1999): Choosing between small, likely rewards and large, unlikely rewards activates inferior and orbital prefrontal cortex. J Neurosci 19:9029-9038.
63. Rushworth MFS, Buckley MJ, Behrens TEJ, Walton ME, Bannerman DM (2007): Functional organization of the medial frontal cortex. Curr Opin Neurobiol 17:220-227.
64. Rushworth MFS, Noonan MP, Boorman ED, Walton ME, Behrens TE (2011): Frontal cortex and reward-guided learning and decision making. Neuron 70:1054-1069.
65. Schoenbaum G, Esber GR (2010): How do you (estimate you will) like them apples? Integration as a defining trait of orbitofrontal function. Curr Opin Neurobiol 20:205-211.
66. Schoenbaum G, Roesch MR, Stalnaker TA (2006): Orbitofrontal cortex, decision-making and drug addiction. Trends Neurosci 29:116-124.
67. Schonberg T, Fox CR, Mumford JA, Congdon E, Trepel C, Poldrack RA (2012): Decreasing ventromedial prefrontal cortex activity during sequential risk-taking: An fMRI investigation of the balloon analog risk task. Front Neurosci 6:80.
68. Supekar K, Menon V, Rubin D, Musen M, Greicius MD (2008): Network analysis of intrinsic functional brain connectivity in Alzheimer's disease. PLoS Comput Biol 4:e1000100.
69. Takahashi YK, Roesch MR, Wilson RC, Toreson K, O'Donnell P, Niv Y, Schoenbaum G (2011): Expectancy-related changes in firing of dopamine neurons depend on orbitofrontal cortex. Nat Neurosci 14:1590-1597.
70. Tanaka SC, Doya K, Okada G, Ueda K, Okamoto Y, Yamawaki S (2004): Prediction of immediate and future rewards differentially recruits cortico-basal ganglia loops. Nat Neurosci 7:887-893.
71. Taylor SF, Welsh RC, Wager TD, Phan KL, Fitzgerald KD, Gehring WJ (2004): A functional neuroimaging study of motivation and executive function. Neuroimage 21:1045-1054.
72. Trepel C, Fox CR, Poldrack RA (2005): Prospect theory on the brain? Toward a cognitive neuroscience of decision under risk. Cogn Brain Res 23:34-50.
73. Venkatraman V, Payne JW, Bettman JR, Luce MF, Huettel SA (2009): Separate neural mechanisms underlie choices and strategic preferences in risky decision making. Neuron 62:593-600.
74. Vul E, Harris C, Winkielman P, Pashler H (2009): Puzzlingly high correlations in fMRI studies of emotion, personality, and social cognition. Perspect Psychol Sci 4:274-290.
75. Wallis JD, Miller EK (2003): Neuronal activity in primate dorsolateral and orbital prefrontal cortex during performance of a reward preference task. Eur J Neurosci 18:2069-2081.
76. Walton ME, Bannerman DM, Alterescu K, Rushworth MF (2003): Functional specialization within medial frontal cortex of the anterior cingulate for evaluating effort-based decisions. J Neurosci 23:6475-6479.
77. Walton ME, Bannerman DM, Rushworth MF (2002): The role of rat medial frontal cortex in effort-based decision making. J Neurosci 22:10996-11003.
78. Walton ME, Croxson PL, Behrens TE, Kennerley SW, Rushworth MF (2007): Adaptive decision making and value in the anterior cingulate cortex. Neuroimage 36(Suppl 2):T142-T154.
79. Walton ME, Kennerley SW, Bannerman DM, Phillips PEM, Rushworth MF (2006): Behavioral and neural analyses of effort-related decision making. Neural Netw 19:1302-1314.
80. Wang J, Alsop DC, Song HK, Maldjian JA, Tang K, Salvucci AE, Detre JA (2003): Arterial transit time imaging with flow encoding arterial spin tagging (FEAST). Magn Reson Med 50:599-607.
81. Weber BJ, Huettel SA (2008): The neural substrates of probabilistic and intertemporal decision making. Brain Res 1234:104-15.
82. Wu WC, Fernandez-Seara M, Detre JA, Wehrli FW, Wang J (2007): A theoretical and experimental investigation of the tagging efficiency of pseudocontinuous arterial spin labeling. Magn Reson Med 58:1020-1027.
83. Yin HH, Ostlund SB, Knowlton BJ, Balleine BW (2005): The role of the dorsomedial striatum in instrumental conditioning. Eur J Neurosci 22:513-523.
84. Zhang Y, Brady M, Smith S (2001): Segmentation of brain MR images through a hidden Markov random field model and the expectation maximization algorithm. IEEE Trans Med Imaging 20:45-57.
85. Zheng X, Alsop DC, Schlaug G (2011): Effects of transcranial direct current stimulation (tDCS) on human regional cerebral blood flow. Neuroimage 58:26-33.