Noninvasive remote activation of the ventral midbrain by transcranial direct current stimulation of prefrontal cortex

Translational Psychiatry

Volumn 3, Issue , 2013, Pages

  Chib, V S ^a   Yun, K ^a   Takahashi, H ^b,c   Shimojo, S ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Brain stimulation; Midbrain; Preference; Prefrontal cortex; Transcranial direct current stimulation (tDCS)

Indexed keywords

ADULT; ARTICLE; BRAIN DEPTH STIMULATION; BRAIN REGION; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN EXPERIMENT; MALE; MESENCEPHALON; NERVE CELL; NON INVASIVE PROCEDURE; NORMAL HUMAN; TRANSCRANIAL DIRECT CURRENT STIMULATION; VENTROMEDIAL PREFRONTAL CORTEX; ADOLESCENT; ELECTROSTIMULATION THERAPY; FUNCTIONAL NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; PHOTOSTIMULATION; PHYSIOLOGY; PREFRONTAL CORTEX; PROCEDURES; YOUNG ADULT; METHODOLOGY;

ADOLESCENT; ADULT; ELECTRIC STIMULATION THERAPY; FEMALE; FUNCTIONAL NEUROIMAGING; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MESENCEPHALON; PHOTIC STIMULATION; PREFRONTAL CORTEX; YOUNG ADULT;

EID: 84879900445     PISSN: None     EISSN: 21583188     Source Type: Journal    
DOI: 10.1038/tp.2013.44     Document Type: Article

References (73)

1. Hedreen JC, Delong MR. Organization of striatopallidal, striatonigal, and nigrostriatal projections in the Macaque. J Comp Neurol 1991; 304: 569-595.
2. Lynd-Balta E, Haber SN. The organization of midbrain projections to the striatum in the primate: sensorimotor-related striatum vs. ventral striatum. Neuroscience 1994; 59: 635-640.
3. Lidow MS, Goldman-Rakic PS, Gallager DW, Rakic P. Distribution of dopaminergic receptors in the primate cerebral cortex: quantitative autoradiographic analysis using [3H] raclopride, [3H] spiperone and [3H]sch23390. Neuroscience 1991; 40: 657-671.
4. Williams SM, Goldman-Rakic PS. Characterization of the dopaminergic innervation of the primate frontal cortex using a dopamine-specific antibody. Cerebral Cortex 1993; 3: 199-222. (Pubitemid 23184929)
5. Goldman-Rakic PS, Bergson C, Krimer LS, Lidow MS, Williams SM, Williams GV. Three primate mesocortical dopamine system. In: Bloom FE, Bjorklund A, Hokfelt T (eds). Handbook of Chemical Neuroanatomy vol. 15 (Elsevier: Amsterdam, The Netherlands, 1999).
6. Lewis DA. The catechoaminergic innervation of primate prefrontal cortex. J Neural Transm Suppl 1992; 36: 179-200.
7. Goto Y, Grace AA. The dopamine system and the pathophysiology of schizophrenia: a basic science perspective. Int Rev Neurobiol 2007; 78: 41-68.
8. Murray GK, Corlett PR, Clark L, Pessiglione M, Blackwell AD, Honey G et al. Substantia nigra/ventral tegmental reward prediction error disruption in psychosis. Mol Psychiatry 2008; 13: 239 267-276.
9. Lisman JE, Coyle JT, Green RW, Javitt DC, Benes FM, Heckers S et al. Circuit-based framework for understanding neurotransmitter and risk gene interactions in schizophrenia. Trends Neurosci 2008; 31: 234-242.
10. Schott BH, Niehaus L, Wittmann BC, Schutze H, Seidenbecher CI, Heinze HJ et al. Ageing and early-stage Parkinson's disease affect separable neural mechanisms of mesolimbic reward processing. Brain 2007; 130Pt 9: 2412-2424. (Pubitemid 47327626)
11. Carlsson M, Carlsson A. Interactions between glutamatergic and monoaminergic systems within the basal ganglia-implications for schizophrenia and Parkinson's disease. Trends Neurosci 1990; 13: 272-276. (Pubitemid 20193457)
12. Vingerhoets FJG, Villemure J-G, Temperli P, Pollo C, Pralong E, Ghika J. Subthalamic DBS replaces levodopa in Parkinson's disease. Neurology 2002; 58: 396-401. (Pubitemid 34150913)
13. Miyamoto S, Miyake N, Jarskog LF, Fleischhaker WW, Lieberman JA. Pharmacological treatment of schizophrenia: a critical review of the pharmacology and clinical effects of current and future therapeutic agents. Mol Psychiatry 2012; 17: 1206-1227.
14. Mayberg HS, Lozano AM, Voon V, McNeaely HE, Seminowicz D, Clement H et al. Deep brain stimulation for treatment-resistant depression. Neuron 2005; 45: 651-660. (Pubitemid 40320700)
15. George MS, Aston-Jones G. Noninvasive techniques for probing neurocircuitry and treating illness: vagus nerve stimulation (VNS), transcranial magnetic stimulation (TMS) and transcranial direct current stimulation (tDCS). Neuropsychopharmacology 2009; 35: 301-316.
16. Nitsche MA, Cohen LG, Wassermann EM, Priori A, Lang N, Antal A et al. Transcranial direct current stimulation: state of the art. Brain Stimul 2008; 1: 206-223.
17. Reis J, Schambra HM, Cohen LG, Buch ER, Fritsch B, Zarahn E et al. Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation. Proc Natl Acad Sci USA 2009; 106: 1590-1595.
18. George MS, Padberg F, Schlaepfer TE, O'Reardon JP, Fitzgerald PB, Nahas ZH et al. Controversy: Repetitive transcranial magnetic stimulation or transcranial direct current stimulation shows efficacy in treating psychiatric diseases (depression, mania, schizophrenia, obsessive-complusive disorder, panic, posttraumatic stress disorder). Brain Stimul 2009; 2: 14-21.
19. Alonso-Alonso M, Fregni F, Pascual-Leone A. Brain stimulation in poststroke rehabilitation. Cerebrovasc Dis 2007; 24(Suppl 1): 157-166. (Pubitemid 350035863)
20. Knoch D, Gianotti LRR, Pascual-Leone A, Treyer V, Regard M, Hohmann M et al. Disruption of right prefrontal cortex by low-frequency repetitive transcrnial magnetic stimulation induces risk-taking behavior. J Neurosci 2006; 26: 6469-6472. (Pubitemid 44318327)
21. Pascual-Leone A, Walsh V. Fast backprojections from the motion to the primary visual area necessary for visual awareness. Science 2001; 292: 510-512. (Pubitemid 32335955)
22. Kanai R, Bahrami B, Roylance R, Rees G. Human parietal cortex structure predicts individual differences in perceptual rivalry. Curr Biol 2011; 20: 1626-1630.
23. Nowak DA, Grefkes C, Ameli M, Fing GR. Interhemispheric competition after stroke: brain stimulation to enhance recovery of function of the affected hand. Nerorehabil Neural Repair 2009; 23: 641-656.
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: 1-4.
25. Polania R, Paulus W, Nitsche MA. Modulating cortico-striatal and thalamo-cortical functional connectivity with transcranial direct current stimulation. Human Brain Mapp 2011; 33: 2499-2508.
26. van Schouwenburg M, O'Shea J, Mars R, Rushworth M, Cools R. Controlling human striatal cognitive function via the frontal cortex. J Neurosci 2012; 32: 5631-5637.
27. Takano Y, Yokawa T, Masuda A, Niimi J, Tanaka S, Hironaka N. A rat model for measuring the effectiveness of transcranial direct current stimulation using fMRI. Neurosci Lett 2011; 491: 40-43.
28. Frankel WG, Laruelle M, Haber SN. Prefrontal cortical projections to the midbrain in primates: evidence for a sparse connection. Neuropsychopharmacology 2006; 31: 1627-1636. (Pubitemid 44106694)
29. An X, Bandler R, ngur D, Price JL. Prefrontal cortical projections to longitudinal columns in midbrain periaqueductal gray in macaque monkeys. J Comp Neurol 1998; 401: 455-479. (Pubitemid 28509880)
30. Ongur D, An X, Price JL. Prefrontal cortical projections to the hypothalamus in macaque monkeys. J Comp Neurol 1998; 401: 480-505. (Pubitemid 28509881)
31. Carr DB, Sesack SR. Projections from the rat prefrontal cortex to the ventral tegmental area: target specificity in the synaptic associations with mesoaccumbens and mesocortical neurons. J Neurosci, 2000; 20(10): 3864-3873. (Pubitemid 30266247)
32. Sesack SR, Carr DB, Omelchenko N, Pinto A. Anatomical substrates for glutamatedopamine interactions: evidence for specificity of connections and extrasynaptic actions. Ann N Y Acad Sci 2003; 1003: 36-52. (Pubitemid 38083044)
33. Haber SN, Knuston B. The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 2010; 35: 4-26.
34. Haber SN, Lynd E, Klein C, Groenewegen HJ. Topographic organization of the ventral striatal efferent projections in teh rheseus monkey: an anterograde tracing study. J Comp Neurol 1990; 293: 282-298. (Pubitemid 20085870)
35. Parent M, Levesque M, Parent A. The pallidofugal projection system in primates: evidence for neurons branching ipsilaterally and contralaterally to the thalamus and brainstem. J Chem Neuroanat 1999; 16: 153-165. (Pubitemid 29261753)
36. Gao M, Liu C, Yang S, Jin G, Bunney BS, Shi W. Functional coupling between the prefrontal cortex and dopamine neurons in the ventral tegmental area. J Neurosci 2007; 27: 5414-5421. (Pubitemid 46790172)
37. Ballard IC, Murty VP, Carter RM, MacInnes JJ, Huettel SA. Dorsolateral prefrontal cortex drives mesolimbic dopaminergic regions to initiate motivated behavior. J Neurosci 2011; 31: 10340-10346.
38. Gariano RF, Groves PM. Burst firing induced in midbrain dopamine neurons by stimulation of the medial prefrontal and anterior cingulate cortices. Brain Res 1988; 462: 194-198.
39. Murase S, Grenhoff J, Chouvet G, Gonon FG, Svensson TH. Prefrontal cortex regulates burst firing and transmitter release in rat mesolimbic dopamine neurons studied in vivo. Neurosci Lett 1993; 157: 53-56. (Pubitemid 23213054)
40. Au-Young SM, Shen H, Yang CR. Medial prefrontal cortical output neurons to the ventral tegmental area (VTA) and their responses to burst-patterned stimulation of the VTA: neuroanatomical and in vivo electrophysiological analyses. Synapse 1999; 34: 245-255. (Pubitemid 29523131)
41. Tzschentke TM, Schmidt WJ. Functional relationship among medial prefrontal cortex, nucleus accumbens, and ventral tegmental area in locomotion and reward. Crit Rev Neurobiol 2000; 14: 131-142. (Pubitemid 32756782)
42. Meyer-Lindenberg A, Miletich RS, Kohn PD, Esposito G, Carson RE, Quarantelli M et al. Reduced prefrontal activity predicts exaggerated striatal dopaminergic function in schizophrenia. Nat Neurosci 2002; 5: 267-271. (Pubitemid 34171141)
43. Bertolino A, Breier A, Callicott JH, Adler C, Mattay VS, Shapiro M et al. The relationship between dorsolateral prefrontal neuronal N-acetylaspartate and evoked release of striatal dopamine in schizophrenia. Neuropsychopharmacology 2000; 22: 125-132. (Pubitemid 30016014)
44. Pycock CJ, Kerwin RW, Carter CJ. Effect of lesion of cortical dopamine terminals on subcortical dopamine receptors in rats. Nature 1990; 286: 74-76.
45. Baumgartner T, Knoch D, Hotz P, Eisenegger C, Fehr E. Dorsolateral and ventromedial prefrontal cortex orchestrate normative choice. Nat Neurosci 14: 1468-1474.
46. Figner B, Knoch D, Johnson EJ, Krosch AR, Lisanby SH, Fehr E et al. Lateral prefrontal cortex and self-control in intertemporal choice. Nat Neurosci. 13: 538-539.
47. Hare TA, Camerer CF, Rangel A. Self-control in decision-making involves modulation of the vmPFC valuation system. Science 2009; 324: 646-648.
48. Archer RP, Cash TF. Physical attractiveness and maladjustment among psychiatric inpatients. J Soc Clin Psychol 1985; 3: 170-180.
49. Noles SW, Cash TF, Winstead BA. Body image, physical attractiveness, and depression. J Consult and Clin Psychol 1985; 53: 88-94. (Pubitemid 15096163)
50. Gaebel W, Wolwer W. Facial expression and emotional face recognition in schizophrenia and depression. Eur Arch Psychiatry Clin Neurosci 1992; 242: 46-52.
51. Sprengelmeyera R, Young AW, Mahna K, Schroedera U, Woitallaa D, Büttnera T et al. Facial expression recognition in people with medicated and unmedicated Parkinson's disease. Neuropsychologia 2003; 41: 1047-1057. (Pubitemid 36349396)
52. Deichmann R, Gottfried JA, Hutton C, Turner R. Optimized EPI for fMRI studies of the orbitofrontal cortex. Neuroimage 2003; 19(2 Pt 1): 430-441. (Pubitemid 39665693)
53. Nitsche MA, Doemkes S, Karakose T, Antal A, Lievetanz D, Lang N et al. Shaping the effects of transcranial direct current stimulation of the human motor cortex. J Neurophysiol 2007; 97: 3109-3117. (Pubitemid 46557737)
54. Fregni F, Boggio PS, Nitsche MA, Bermpohl F, Antal A, Feredoes E et al. Anodal transcranial direct current stimulation of prefrontal cortex enhances working memory. Exp Brain Res 2005; 166:: 23-30. (Pubitemid 41451033)
55. Gerloff C, Corwell B, Chen R, Hallett M, Cohen LG. Stimulation over the human supplementary motor area interferes with the organization of futuer elements in complex motor sequences. Brain 1997; 120: 1587-1602. (Pubitemid 27389226)
56. Rossi S, Cappa SF, Babiloni C, Pasqualetti P, Miniussi C, Carducci F et al. Prefrontal cortex in long-term memory: an 'interference' approach using magnetic stimulation. Nat Neurosci 2001; 4: 948-952. (Pubitemid 32801600)
57. Boggio PS, Khoury LP, Martins DC, Martins OE, Macedo ECd, Fregni F. Temporal cortex direct current stimulation enhances performance on a visual recognition working memory task in Alzheimer disease. J Neurol Neurosurg Psychiatry 2009; 80: 444-447.
58. Herwig U, Satrapi P, Schonfeldt-Lecuona C. Using the international 10-20 EEG system for position of transcranial magnetic stimulation. Brain Topogr 2003; 16: 95-99. (Pubitemid 38045059)
59. O'Doherty JP. Reward representations and reward-related learning in the human brain: insights from neuroimaging. Curr Opin Neurobiol 2004; 14: 769-776. (Pubitemid 39576211)
60. O'Doherty J, Winston J, Critchley H, Perrett D, Burt DM, Dolan RJ. Beauty in a smile: the role of medial orbitofrontal cortex in facial attractiveness. Neuropsychologia 2003; 41: 147-155. (Pubitemid 35379692)
61. Gitelman D, Penny W, Ashburner J, Friston K. Modeling regional and psychophysiologic interactions in fMRI: the importance of hemodynamic deconvolution. Neuroimage 2003; 19: 200-207. (Pubitemid 36627392)
62. Winston JS, O'Doherty J, Kilner JM, Perrett D, Dolan RJ. Brain systems for assessing facial attractiveness. Neuropsychologia 2007; 45: 195-206. (Pubitemid 44821235)
63. Aharon I, Etcoff N, Ariely D, Chabris CF, O'Connor E, Breiter HC. Beautiful faces have variable reward value: fMRI and behavioral evidence. Neuron 2001; 32: 537-551. (Pubitemid 33082052)
64. Bray S, O'Doherty J. Neural coding of reward-prediction error signals during classical conditioning with attractive faces. J Neurophysiol 2007; 97, p 3036-3045. (Pubitemid 46557731)
65. D'Ardenne K, McClure SM, Nystrom LE, Cohen JD. BOLD responses reflecting dopaminergic signals in the human ventral tegmental area. Science 2008; 319: 1264-1267. (Pubitemid 351323026)
66. O'Doherty JP, Buchanan TW, Seymour B, Dolan RJ. Predictive neural coding of reward preference involves dissociable responses in human ventral midbrain and ventral striatum. Neuron 2006; 49: 157-166. (Pubitemid 43017193)
67. Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A. Neurophysiological investigation of the basis of the fMRI signal. Nature 2001; 412: 150-157. (Pubitemid 32674704)
68. Karreman M, Moghaddam B. The prefrontal cortex regulates the basal release of dopamine in the limbic system: An effect mediated by ventral tegmental area. J Neurochem 1996; 66: 589-598. (Pubitemid 26036693)
69. Doherty MD, Gratton A. Effects of medial prefrontal cortical injections of GABA receptor agonists and atongonists on the local and nucleus accumbens dopamine response to stress. Synapse 1999; 32: 288-300. (Pubitemid 29222642)
70. Márquez-Ruiza J, Leal-Campanarioa R, Sánchez-Campusanoa R, Molaee-Ardekanib B, Wendling F, Mirandad PC et al. Transcranial direct-current stimulation modulates synaptic mechanisms involved in associative learning in behaving rabbits. Proc Natl Acad Sci USA 2012; 109: 6710-6715.
71. Stagg CJ, Nitsche MA. Physiological basis of transcranial direct current stimulation. Neuroscientist 2011; 17: 37-53.
72. Stagg CJ, Best JG, Stephenson MC, O'Shea J, Wylezinska M, Kincses ZT et al. Polaritysensative modulation of cortical neurostransmitters by transcranial stimulation. J Neurosci 2009; 29: 5202-5206.
73. Krain AL, Wilson AM, Arbuckle R, Castellanos FX, Milham MP. Distinct neural mechanisms of risk and ambiguity: a meta-analysis of decision-making. Neuroimage 2006; 32: 477-484.