Efficacy of transcranial magnetic stimulation targets for depression is related to intrinsic functional connectivity with the subgenual cingulate

Biological Psychiatry

Volumn 72, Issue 7, 2012, Pages 595-603

  Fox, Michael D ^a,b   Buckner, Randy L ^a,b,c   White, Matthew P ^d   Greicius, Michael D ^d   Pascual Leone, Alvaro ^b,e  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c HARVARD UNIVERSITY   (United States)

^d STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e University Institute affiliated with the Autonomous University of Barcelona   (Spain)

Author keywords

Depression; dorsolateral prefrontal cortex; intrinsic connectivity; MRI; resting state functional connectivity; subgenual; TMS; transcranial magnetic stimulation

Indexed keywords

ADULT; ANTIDEPRESSANT ACTIVITY; ARTICLE; BOLD SIGNAL; BRAIN REGION; CINGULATE GYRUS; CLINICAL ARTICLE; CLINICAL EFFECTIVENESS; CONTROLLED STUDY; CORRELATION ANALYSIS; DEPRESSION; ELECTROENCEPHALOGRAM; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HAMILTON SCALE; HUMAN; LIMBIC SYSTEM; MAJOR DEPRESSION; MALE; PREFRONTAL CORTEX; PRIORITY JOURNAL; TRANSCRANIAL MAGNETIC STIMULATION;

ADULT; BRAIN MAPPING; DEPRESSIVE DISORDER, MAJOR; FEMALE; FUNCTIONAL LATERALITY; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; LINEAR MODELS; MAGNETIC RESONANCE IMAGING; MALE; NERVE NET; OXYGEN; PREFRONTAL CORTEX; PSYCHIATRIC STATUS RATING SCALES; TRANSCRANIAL MAGNETIC STIMULATION; YOUNG ADULT;

EID: 84866032645     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2012.04.028     Document Type: Article

References (73)

1. T. Wagner, A. Valero-Cabre, A. Pascual-Leone Noninvasive human brain stimulation Annu Rev Biomed Eng 9 2007 527 565
2. M. Kobayashi, A. Pascual-Leone Transcranial magnetic stimulation in neurology Lancet Neurol 2 2003 145 156
3. M. Hallett Transcranial magnetic stimulation: A primer Neuron 55 2007 187 199
4. A. Valero-Cabre, B.R. Payne, J. Rushmore, S.G. Lomber, A. Pascual-Leone Impact of repetitive transcranial magnetic stimulation of the parietal cortex on metabolic brain activity: A 14C-2DG tracing study in the cat Exp Brain Res 163 2005 1 12
5. A. Valero-Cabre, B.R. Payne, A. Pascual-Leone Opposite impact on 14C-2-deoxyglucose brain metabolism following patterns of high and low frequency repetitive transcranial magnetic stimulation in the posterior parietal cortex Exp Brain Res 176 2007 603 615
6. H.R. Siebner, T.O. Bergmann, S. Bestmann, M. Massimini, H. Johansen-Berg, H. Mochizuki Consensus paper: Combining transcranial stimulation with neuroimaging Brain Stimul 2 2009 58 80
7. C.C. Ruff, J. Driver, S. Bestmann Combining TMS and fMRI: From 'virtual lesions' to functional-network accounts of cognition Cortex 45 2009 1043 1049
8. F. Ferreri, P. Pasqualetti, S. Maatta, D. Ponzo, F. Ferrarelli, G. Tononi Human brain connectivity during single and paired pulse transcranial magnetic stimulation Neuroimage 54 2011 90 201
9. S.H. Lisanby, R.H. Belmaker Animal models of the mechanisms of action of repetitive transcranial magnetic stimulation (RTMS): Comparisons with electroconvulsive shock (ECS) Depress Anxiety 12 2000 178 187
10. M.D. Fox, M.A. Halko, M.C. Eldaief, A. Pascual-Leone Measuring and manipulating brain connectivity with resting state functional connectivity magnetic resonance imaging (fcMRI) and transcranial magnetic stimulation (TMS) [published online ahead of print March 19] Neuroimage 2012
11. J.P. O'Reardon, H.B. Solvason, P.G. Janicak, S. Sampson, K.E. Isenberg, Z. Nahas Efficacy and safety of transcranial magnetic stimulation in the acute treatment of major depression: A multisite randomized controlled trial Biol Psychiatry 62 2007 1208 1216
12. F. Padberg, M.S. George Repetitive transcranial magnetic stimulation of the prefrontal cortex in depression Exp Neurol 219 2009 2 13
13. M.S. George, E.M. Wassermann, W.A. Williams, A. Callahan, T.A. Ketter, P. Basser Daily repetitive transcranial magnetic stimulation (rTMS) improves mood in depression Neuroreport 6 1995 1853 1856
14. A. Pascual-Leone, B. Rubio, F. Pallardo, M.D. Catala Rapid-rate transcranial magnetic stimulation of left dorsolateral prefrontal cortex in drug-resistant depression Lancet 348 1996 233 237
15. H.S. Mayberg Defining the neural circuitry of depression: Toward a new nosology with therapeutic implications Biol Psychiatry 61 2007 729 730
16. W.C. Drevets, J. Savitz, M. Trimble The subgenual anterior cingulate cortex in mood disorders CNS Spectr 13 2008 663 681
17. H.S. Mayberg, A.M. Lozano, V. Voon, H.E. McNeely, D. Seminowicz, C. Hamani Deep brain stimulation for treatment-resistant depression Neuron 45 2005 651 660
18. H.S. Mayberg Targeted electrode-based modulation of neural circuits for depression J Clin Invest 119 2009 717 725
19. M.S. George, E.M. Wassermann, T.A. Kimbrell, J.T. Little, W.E. Williams, A.L. Danielson Mood improvement following daily left prefrontal repetitive transcranial magnetic stimulation in patients with depression: A placebo-controlled crossover trial Am J Psychiatry 154 1997 1752 1756
20. M.S. George, L.E. Stallings, A.M. Speer, Z. Nahas, K.M. Spicer, D.J. Vincent Prefrontal repetitive transcranial magnetic stimulation (rTMS) changes relative perfusion locally and remotely Hum Psychopharmacol 14 1999 161 170
21. T.A. Kimbrell, R.T. Dunn, M.S. George, A.L. Danielson, M.W. Willis, J.D. Repella Left prefrontal-repetitive transcranial magnetic stimulation (rTMS) and regional cerebral glucose metabolism in normal volunteers Psychiatry Res 115 2002 101 113
22. K. Narushima, L.M. McCormick, T. Yamada, R.W. Thatcher, R.G. Robinson Subgenual cingulate theta activity predicts treatment response of repetitive transcranial magnetic stimulation in participants with vascular depression J Neuropsychiatry Clin Neurosci 22 2010 75 84
23. S. Kito, K. Fujita, Y. Koga Regional cerebral blood flow changes after low-frequency transcranial magnetic stimulation of the right dorsolateral prefrontal cortex in treatment-resistant depression Neuropsychobiology 58 2008 29 36
24. S. Kito, T. Hasegawa, Y. Koga Neuroanatomical correlates of therapeutic efficacy of low-frequency right prefrontal transcranial magnetic stimulation in treatment-resistant depression Psychiatry Clin Neurosci 65 2011 175 182
25. T. Paus, M.A. Castro-Alamancos, M. Petrides Cortico-cortical connectivity of the human mid-dorsolateral frontal cortex and its modulation by repetitive transcranial magnetic stimulation Eur J Neurosci 14 2001 1405 1411
26. X. Li, Z. Nahas, F.A. Kozel, B. Anderson, D.E. Bohning, M.S. George Acute left prefrontal transcranial magnetic stimulation in depressed patients is associated with immediately increased activity in prefrontal cortical as well as subcortical regions Biol Psychiatry 55 2004 882 890
27. C.C. Teneback, Z. Nahas, A.M. Speer, M. Molloy, L.E. Stallings, K.M. Spicer Changes in prefrontal cortex and paralimbic activity in depression following two weeks of daily left prefrontal TMS J Neuropsychiatry Clin Neurosci 11 1999 426
28. Z. Nahas, M. Lomarev, D.R. Roberts, A. Shastri, J.P. Lorberbaum, C. Teneback Unilateral left prefrontal transcranial magnetic stimulation (TMS) produces intensity-dependent bilateral effects as measured by interleaved BOLD fMRI Biol Psychiatry 50 2001 712 720
29. A.M. Speer, T.A. Kimbrell, E.M. Wassermann, J. D Repella, M.W. Willis, P. Herscovitch, R.M. Post Opposite effects of high and low frequency rTMS on regional brain activity in depressed patients Biol Psychiatry 48 2000 1133 1141
30. F.M. Mottaghy, C.E. Keller, M. Gangitano, J. Ly, M. Thall, J.A. Parker, A. Pascual-Leone Correlation of cerebral blood flow and treatment effects of repetitive transcranial magnetic stimulation in depressed patients Psychiatry Res 115 2002 1 14
31. C. Eisenegger, V. Treyer, E. Fehr, D. Knoch Time-course of "off-line" prefrontal rTMS effects-a PET study Neuroimage 42 2008 379 384
32. D. Knoch, V. Treyer, M. Regard, R.M. Muri, A. Buck, B. Weber Lateralized and frequency-dependent effects of prefrontal rTMS on regional cerebral blood flow Neuroimage 31 2006 641 648
33. A.M. Speer, M.W. Willis, P. Herscovitch, M. Daube-Witherspoon, J.R. Shelton, B.E. Benson Intensity-dependent regional cerebral blood flow during 1-Hz repetitive transcranial magnetic stimulation (rTMS) in healthy volunteers studied with H215O positron emission tomography: II Effects of prefrontal cortex rTMS Biol Psychiatry 54 2003 826 832
34. F. Ferrarelli, H.M. Haraldsson, T.E. Barnhart, A.D. Roberts, T.R. Oakes, M. Massimini A [17F]-fluoromethane PET/TMS study of effective connectivity Brain Res Bull 64 2004 103 113
35. P.B. Fitzgerald, K. Hoy, S. McQueen, J.J. Maller, S. Herring, R. Segrave A randomized trial of rTMS targeted with MRI based neuro-navigation in treatment-resistant depression Neuropsychopharmacology 34 2009 1255 1262
36. T. Herbsman, D. Avery, D. Ramsey, P. Holtzheimer, C. Wadjik, F. Hardaway More lateral and anterior prefrontal coil location is associated with better repetitive transcranial magnetic stimulation antidepressant response Biol Psychiatry 66 2009 509 515
37. U. Herwig, F. Padberg, J. Unger, M. Spitzer, C. Schonfeldt-Lecuona Transcranial magnetic stimulation in therapy studies: Examination of the reliability of "standard" coil positioning by neuronavigation Biol Psychiatry 50 2001 58 61
38. R. Ahdab, S.S. Ayache, P. Brugières, C. Goujon, J.-P. Lefaucheur Comparison of "standard" and "navigated" procedures of TMS coil positioning over motor, premotor and prefrontal targets in patients with chronic pain and depression Neurophysiol Clin 40 2010 27 36
39. M.S. George, E.M. Wassermann, W.A. Williams, J. Steppel, A. Pascual-Leone, P. Basser Changes in mood and hormone levels after rapid-rate transcranial magnetic stimulation (rTMS) of the prefrontal cortex J Neuropsychiatry Clin Neurosci 8 1996 172 180
40. U. Herwig, P. Satrapi, C. Schonfeldt-Lecuona Using the international 10-20 EEG system for positioning of transcranial magnetic stimulation Brain Topogr 16 2003 95 99
41. P.M. Rusjan, M.S. Barr, F. Farzan, T. Arenovich, J.J. Maller, P.B. Fitzgerald, Z.J. Daskalakis Optimal transcranial magnetic stimulation coil placement for targeting the dorsolateral prefrontal cortex using novel magnetic resonance image-guided neuronavigation Hum Brain Mapp 31 2010 1643 1652
42. M.-L. Paillère Martinot, A. Galinowski, D. Ringuenet, T. Gallarda, J.-P. Lefaucheur, F. Bellivier Influence of prefrontal target region on the efficacy of repetitive transcranial magnetic stimulation in patients with medication-resistant depression: A [(18)F]-fluorodeoxyglucose PET and MRI study Int J Neuropsychopharmacol 13 2010 45 59
43. U. Herwig, Y. Lampe, F.D. Juengling, A. Wunderlich, H. Walter, M. Spitzer, C. Schönfeldt-Lecuona Add-on rTMS for treatment of depression: A pilot study using stereotaxic coil-navigation according to PET data J Psychiatr Res 37 2003 267 275
44. M. Garcia-Toro, J. Salva, J. Daumal, J. Andres, M. Romera, O. Lafau High (20-Hz) and low (1-Hz) frequency transcranial magnetic stimulation as adjuvant treatment in medication-resistant depression Psychiatry Res 146 2006 53 57
45. B. Biswal, F. Yetkin, V. Haughton, J. Hyde Functional connectivity in the motor cortex of resting human brain using echo-planar MRI Magn Reson Med 34 1995 537 541
46. M.D. Fox, M.E. Raichle Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging Nat Rev Neurosci 8 2007 700 711
47. K.R. Van Dijk, T. Hedden, A. Venkataraman, K.C. Evans, S.W. Lazar, R.L. Buckner Intrinsic functional connectivity as a tool for human connectomics: Theory, properties, and optimization J Neurophysiol 103 2010 297 321
48. M.D. Fox, A.Z. Snyder, J.L. Vincent, M. Corbetta, D.C. Van Essen, M.E. Raichle The human brain is intrinsically organized into dynamic, anticorrelated functional networks Proc Natl Acad Sci U S A 102 2005 9673 9678
49. J. Wu, M.S. Buchsbaum, J.C. Gillin, C. Tang, S. Cadwell, M. Wiegand Prediction of antidepressant effects of sleep deprivation by metabolic rates in the ventral anterior cingulate and medial prefrontal cortex Am J Psychiatry 156 1999 1149 1158
50. H.S. Mayberg, S.K. Brannan, J.L. Tekell, J.A. Silva, R.K. Mahurin, S. McGinnis, P.A. Jerabek Regional metabolic effects of fluoxetine in major depression: Serial changes and relationship to clinical response Biol Psychiatry 48 2000 830 843
51. W.C. Drevets, W. Bogers, M.E. Raichle Functional anatomical correlates of antidepressant drug treatment assessed using PET measures of regional glucose metabolism Eur Neuropsychopharmacol 12 2002 527 544
52. Z. Nahas, C. Teneback, J.H. Chae, Q. Mu, C. Molnar, F.A. Kozel Serial vagus nerve stimulation functional MRI in treatment-resistant depression Neuropsychopharmacology 32 2007 1649 1660
53. S.S. Cho, A.P. Strafella rTMS of the left dorsolateral prefrontal cortex modulates dopamine release in the ipsilateral anterior cingulate cortex and orbitofrontal cortex PloS One 4 2009 e6725
54. G. Rajkowska, P.S. Goldman-Rakic Cytoarchitectonic definition of prefrontal areas in the normal human cortex: II Variability in locations of areas 9 and 46 and relationship to the Talairach Coordinate System Cereb Cortex 5 1995 323 337
55. D.J. Schutter, D.M. Laman, J. van Honk, A.C. Vergouwen, G.F. Koerselman Partial clinical response to 2 weeks of 2 Hz repetitive transcranial magnetic stimulation to the right parietal cortex in depression Int J Neuropsychopharmacol 12 2009 643 650
56. D.J. Schutter, J. van Honk A framework for targeting alternative brain regions with repetitive transcranial magnetic stimulation in the treatment of depression J Psychiatry Neurosci 30 2005 91 97
57. M.D. Greicius, B.H. Flores, V. Menon, G.H. Glover, H.B. Solvason, H. Kenna Resting-state functional connectivity in major depression: Abnormally increased contributions from subgenual cingulate cortex and thalamus Biol Psychiatry 62 2007 429 437
58. M. Koenigs, J. Grafman The functional neuroanatomy of depression: Distinct roles for ventromedial and dorsolateral prefrontal cortex Behav Brain Res 201 2009 239 243
59. P.B. Fitzgerald, T.J. Oxley, A.R. Laird, J. Kulkarni, G.F. Egan, Z.J. Daskalakis An analysis of functional neuroimaging studies of dorsolateral prefrontal cortical activity in depression Psychiatry Res 148 2006 33 45
60. J.D. Steele, J. Currie, S.M. Lawrie, I. Reid Prefrontal cortical functional abnormality in major depressive disorder: A stereotactic meta-analysis J Affect Disord 101 2007 1 11
61. P.B. Fitzgerald, A.R. Laird, J. Maller, Z.J. Daskalakis A meta-analytic study of changes in brain activation in depression Hum Brain Mapp 29 2008 683 695
62. M. Koenigs, E.D. Huey, M. Calamia, V. Raymont, D. Tranel, J. Grafman Distinct regions of prefrontal cortex mediate resistance and vulnerability to depression J Neurosci 28 2008 12341 12348
63. T. Paus, J. Barrett Transcranial magnetic stimulation (TMS) of the human frontal cortex: Implications for repetitive TMS treatment of depression J Psychiatry Neurosci 29 2004 268 279
64. K. Murphy, R.M. Birn, D.A. Handwerker, T.B. Jones, P.A. Bandettini The impact of global signal regression on resting state correlations: Are anti-correlated networks introduced? Neuroimage 44 2009 893 905
65. M.D. Fox, D. Zhang, A.Z. Snyder, M.E. Raichle The global signal and observed anticorrelated resting state brain networks J Neurophysiol 101 2009 3270 3283
66. J.S. Anderson, T.J. Druzgal, M. Lopez-Larson, E.-K. Jeong, K. Desai, D. Yurgelun-Todd Network anticorrelations, global regression, and phase-shifted soft tissue correction Hum Brain Mapp 32 2011 919 934
67. X.J. Chai, A.N. Castanon, D. Ongur, S. Whitfield-Gabrieli Anticorrelations in resting state networks without global signal regression Neuroimage 59 2012 1420 1428
68. M. Petrides, D.N. Pandya Dorsolateral prefrontal cortex: Comparative cytoarchitectonic analysis in the human and the macaque brain and corticocortical connection patterns Eur J Neurosci 11 1999 1011 1036
69. B.A. Vogt, D.N. Pandya Cingulate cortex of the rhesus monkey: II Cortical afferents J Comp Neurol 262 1987 271 289
70. D. Sridharan, D.J. Levitin, V. Menon A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks Proc Natl Acad Sci U S A 105 2008 12569 12574
71. H.J. Groenewegen, Y. Galis-de Graaf, W.J. Smeets Integration and segregation of limbic cortico-striatal loops at the thalamic level: An experimental tracing study in rats J Chem Neuroanat 16 1999 167 185
72. D.C. Van Essen, D.L. Dierker Surface-based and probabilistic atlases of primate cerebral cortex Neuron 56 2007 209 225
73. C. Hamani, J.N. Nobrega, A.M. Lozano Deep brain stimulation in clinical practice and in animal models Clin Pharmacol Ther 88 2010 559 562