Prefrontal Cortex Stimulation Enhances Fear Extinction Memory in Humans

Biological Psychiatry

Volumn 84, Issue 2, 2018, Pages 129-137

  Raij, Tommi ^a,b   Nummenmaa, Aapo ^a,b   Marin, Marie France ^b,c   Porter, Daria ^c   Furtak, Sharon ^c   Setsompop, Kawin ^a,b   Milad, Mohammed R ^b,c  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Connectivity; Cortical map; Diffusion tensor imaging; Fear conditioning; Fear extinction; TMS; Transcranial magnetic stimulation

Indexed keywords

ARTICLE; CONDITIONED REFLEX; CONDITIONING; CONTROLLED STUDY; DEVICES; DIFFUSION WEIGHTED IMAGING; ELECTRIC FIELD; ELECTRODERMAL RESPONSE; FEAR; FRONTAL CORTEX; HUMAN; HUMAN EXPERIMENT; INFRALIMBIC CORTEX; MEMORY; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PREFRONTAL CORTEX; PRIORITY JOURNAL; RECALL; TRACTOGRAPHY; TRANSCRANIAL MAGNETIC STIMULATION; VENTROMEDIAL PREFRONTAL CORTEX; WHITE MATTER; ANIMAL; PHYSIOLOGY; RAT; REGRESSION ANALYSIS; REINFORCEMENT;

ANIMALS; CONDITIONING, CLASSICAL; EXTINCTION, PSYCHOLOGICAL; FEAR; HUMANS; MAGNETIC RESONANCE IMAGING; MENTAL RECALL; PREFRONTAL CORTEX; RATS; REGRESSION ANALYSIS; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 85038968807     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2017.10.022     Document Type: Article

References (70)

1. Milad, M., Quirk, G., Fear extinction as a model for translational neuroscience: Ten years of progress. Annu Rev Psychol 63 (2012), 129–151.
2. Milad, M., Rauch, S., Pitman, R., Quirk, G., Fear extinction in rats: Implications for human brain imaging and anxiety disorders. Biol Psychol 73 (2006), 61–71.
3. Graham, B., Milad, M., The study of fear extinction: Implications for anxiety disorders. Am J Psychiatry 168 (2011), 1255–1265.
4. Smith, N., Doran, J., Sippel, L., Harpaz-Rotem, I., Fear extinction and memory reconsolidation as critical components in behavioral treatment for posttraumatic stress disorder and potential augmentation of these processes. Neurosci Lett 649 (2017), 170–175.
5. Bowers, M., Ressler, K., An overview of translationally informed treatments for posttraumatic stress disorder: Animal models of Pavlovian fear conditioning to human clinical trials. Biol Psychiatry 78 (2015), E15–E27.
6. Vervliet, B., Craske, M., Hermans, D., Fear extinction and relapse: State of the art. Annu Rev Clin Psychol 9 (2013), 215–248.
7. Foa, E., Prolonged exposure therapy: past, present, and future. Depress Anxiety 28 (2011), 1043–1047.
8. Foa, E., McLean, C., The efficacy of exposure therapy for anxiety-related disorders and its underlying mechanisms: The case of OCD and PTSD. Annu Rev Clin Psychol 12 (2016), 1–28.
9. Dejean, C., Courtin, J., Rozeske, R., Bonnet, M., Dousset, V., Michelet, T., et al. Neuronal circuits for fear expression and recovery: Recent advances and potential therapeutic strategies. Biol Psychiatry 78 (2015), 298–306.
10. Quirk, G., Mueller, D., Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 33 (2008), 56–72.
11. Milad, M., Quirk, G., Neurons in medial prefrontal cortex signal memory for fear extinction. Nature 420 (2002), 70–74.
12. Milad, M., Vidal-Gonzalez, I., Quirk, G., Electrical stimulation of medial prefrontal cortex reduces conditioned fear in a temporally specific manner. Behav Neurosci 118 (2004), 389–394.
13. Vidal-Gonzalez, I., Vidal-Gonzalez, B., Rauch, S., Quirk, G., Microstimulation reveals opposing influences of prelimbic and infralimbic cortex on the expression of conditioned fear. Learn Mem 13 (2006), 728–733.
14. Kim, H., Cho, H., Augustine, G., Han, J., Selective control of fear expression by optogenetic manipulation of infralimbic cortex after extinction. Neuropsychopharmacology 41 (2016), 1261–1273.
15. Do-Monte, F., Manzano-Nieves, G., Quiñones-Laracuente, K., Ramos-Medina, L., Quirk, G., Revisiting the role of infralimbic cortex in fear extinction with optogenetics. J Neurosci 35 (2015), 3607–3615.
16. Quirk, G., Likhtik, E., Pelletier, J., Pare, D., Stimulation of medial prefrontal cortex decreases the responsiveness of central amygdala output neurons. J Neurosci 23 (2003), 8800–8807.
17. Herry, C., Ciocchi, S., Senn, V., Demmou, L., Muller, C., Luthi, A., Switching on and off fear by distinct neuronal circuits. Nature 454 (2008), 600–606.
18. Kawasaki, H., Kaufman, O., Damasio, H., Damasio, A., Granner, M., Bakken, H., et al. Single-neuron responses to emotional visual stimuli recorded in human ventral prefrontal cortex. Nat Neurosci 4 (2001), 15–16.
19. Milad, M., Pitman, R., Ellis, C., Gold, A., Shin, L., Lasko, N., et al. Neurobiological basis of failure to recall extinction memory in posttraumatic stress disorder. Biol Psychiatry 66 (2009), 1075–1082.
20. Milad, M., Furtak, S., Greenberg, J., Keshaviah, A., Im, J., Falkenstein, M., et al. Deficits in conditioned fear extinction in obsessive-compulsive disorder and neurobiological changes in the fear circuit. JAMA Psychiatry 70 (2013), 608–618.
21. Holt, D., Coombs, G., Zeidan, M., Goff, D., Milad, M., Failure of neural responses to safety cues in schizophrenia. Arch Gen Psychiatry 69 (2012), 893–903.
22. Garfinkel, S., Abelson, J., King, A., Sripada, R., Wang, X., Gaines, L., et al. Impaired contextual modulation of memories in PTSD: An fMRI and psychophysiological study of extinction retention and fear renewal. J Neurosci 34 (2014), 13435–13443.
23. Marin, M., Song, H., VanElzakker, M., Staples-Bradley, L., Linnman, C., Pace-Schott, E., et al. Association of resting metabolism in the fear neural network with extinction recall activations and clinical measures in trauma-exposed individuals. Am J Psychiatry 173 (2016), 930–938.
24. Marin, M., Zsido, R., Song, H., Lasko, N., Killgore, W., Rauch, S., et al. Skin conductance responses and neural activations during fear conditioning and extinction recall across anxiety disorders. JAMA Psychiatry 74 (2017), 622–631.
25. Barker, A., Jalinous, R., Freeston, I., Non-invasive magnetic stimulation of human motor cortex. Lancet 1 (1985), 1106–1107.
26. Diana, M., Raij, T., Melis, M., Nummenmaa, A., Leggio, L., Bonci, A., Rehabilitating the addicted brain with transcranial magnetic stimulation. Nat Rev Neurosci 18 (2017), 685–693.
27. Milad, M., Orr, S., Pitman, R., Rauch, S., Context modulation of memory for fear extinction in humans. Psychophysiology 42 (2005), 456–464.
28. Milad, M., Quirk, G., Pitman, R., Orr, S., Fischl, B., Rauch, S., A role for the human dorsal anterior cingulate cortex in fear expression. Biol Psychiatry 62 (2007), 1191–1194.
29. Linnman, C., Zeidan, M., Furtak, S., Pitman, R., Quirk, G., Milad, M., Resting amygdala and medial prefrontal metabolism predicts functional activation of the fear extinction circuit. Am J Psychiatry 169 (2012), 415–423.
30. Zeidan, M., Lebron-Milad, K., Thompson-Hollands, J., Im, J., Dougherty, D., Holt, D., et al. Test-retest reliability during fear acquisition and fear extinction in humans. CNS Neurosci Ther 18 (2011), 313–317.
31. Gramfort, A., Luessi, M., Larson, E., Engemann, D., Strohmeier, D., Brodbeck, C., et al. MNE software for processing MEG and EEG data. Neuroimage 86 (2014), 446–460.
32. Setsompop, K., Cohen-Adad, J., Gagoski, B., Raij, T., Yendiki, A., Keil, B., et al. Improving diffusion MRI using simultaneous multi-slice echo planar imaging. Neuroimage 63 (2012), 569–580.
33. Friston, K., Buechel, C., Fink, G., Morris, J., Rolls, E., Dolan, R., Psychophysiological and modulatory interactions in neuroimaging. Neuroimage 6 (1997), 218–229.
34. Milad, M., Wright, C., Orr, S., Pitman, R., Quirk, G., Rauch, S., Recall of fear extinction in humans activates the ventromedial prefrontal cortex and hippocampus in concert. Biol Psychiatry 62 (2007), 446–454.
35. Nummenmaa, A., Stenroos, M., Ilmoniemi, R., Okada, Y., Hämäläinen, M., Raij, T., Comparison of spherical and anatomically realistic boundary element head models for transcranial magnetic stimulation navigation. Clin Neurophysiol 124 (2013), 1995–2007.
36. Stenroos, M., Mäntynen, V., Nenonen, J., A Matlab library for solving quasi-static volume conduction problems using the boundary element method. Comput Methods Programs Biomed 88 (2007), 256–263.
37. Postelnicu, G., Zollei, L., Fischl, B., Combined volumetric and surface registration. IEEE Trans Med Imaging 28 (2009), 508–522.
38. Ahveninen, J., Huang, S., Nummenmaa, A., Belliveau, J., Hung, A., Jaaskelainen, I., et al. Evidence for distinct human auditory cortex regions for sound location versus identity processing. Nature Comm, 4, 2013, 2585.
39. Fischl, B., Sereno, M., Tootell, R., Dale, A., High-resolution inter-subject averaging and a coordinate system for the cortical surface. Hum Brain Mapp 8 (1999), 272–284.
40. Behrens, T., Woolrich, M., Jenkinson, M., Johansen-Berg, H., Nunes, R., Clare, S., et al. Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magn Reson Med 50 (2003), 1077–1088.
41. Chen, R., Classen, J., Gerloff, C., Celnik, P., Wassermann, E., Hallett, M., et al. Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology 48 (1997), 1398–1403.
42. Pascual-Leone, A., Valls-Sole, J., Wassermann, E., Hallett, M., Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. Brain 117 (1994), 847–858.
43. Guhn, A., Dresler, T., Andreatta, M., Müller, L., Hahn, T., Tupak, S., et al. Medial prefrontal cortex stimulation modulates the processing of conditioned fear. Front Behav Neurosci, 8, 2014, 44.
44. Stehberg, J., Levy, D., Zangen, A., Impairment of aversive memory reconsolidation by localized intracranial electrical stimulation. Eur J Neurosci 29 (2009), 964–969.
45. Baek, K., Chae, J., Jeong, J., The effect of repetitive transcranial magnetic stimulation on fear extinction in rats. Neuroscience 200 (2012), 159–165.
46. Schiller, D., Monfils, M., Raio, C., Johnson, D., Ledoux, J., Phelps, E., Preventing the return of fear in humans using reconsolidation update mechanisms. Nature 463 (2010), 49–53.
47. Rodriguez-Romaguera, J., Do-Monte, F., Tanimura, Y., Quirk, G., Haber, S., Enhancement of fear extinction with deep brain stimulation: Evidence for medial orbitofrontal involvement. Neuropsychopharmacology 40 (2015), 1726–1733.
48. Burgos-Robles, A., Kimchi, E., Izadmehr, E., Porzenheim, M., Ramos-Guasp, W., Nieh, E., et al. Amygdala inputs to prefrontal cortex guide behavior amid conflicting cues of reward and punishment. Nat Neurosci 20 (2017), 824–835.
49. Baeken, C., De Raedt, R., Neurobiological mechanisms of repetitive transcranial magnetic stimulation on the underlying neurocircuitry in unipolar depression. Dialogues Clin Neurosci 13 (2011), 139–145.
50. O'Shea, J., Johansen-Berg, H., Trief, D., Göbel, S., Rushworth, M., Functionally specific reorganization in human premotor cortex. Neuron 54 (2007), 479–490.
51. Chen, A., Oathes, D., Chang, C., Bradley, T., Zhou, Z., Williams, L., et al. Causal interactions between fronto-parietal central executive and default-mode networks in humans. Proc Natl Acad Sci U S A 110 (2013), 19944–19949.
52. Nummenmaa, A., McNab, J., Savadjiev, P., Okada, Y., Hämäläinen, M., Wang, R., et al. Targeting of white matter tracts with transcranial magnetic stimulation. Brain Stimul 7 (2014), 80–84.
53. Sack, A., Kadosh, R., Schuhmann, T., Moerel, M., Walsh, V., Goebel, R., Optimizing functional accuracy of TMS in cognitive studies: A comparison of methods. J Cogn Neurosci 21 (2009), 207–221.
54. Fox, M., Liu, H., Pascual-Leone, A., Identification of reproducible individualized targets for treatment of depression with TMS based on intrinsic connectivity. Neuroimage 66 (2013), 151–160.
55. Herry, C., Johansen, J., Encoding of fear learning and memory in distributed neuronal circuits. Nat Neurosci 17 (2014), 1644–1654.
56. Asthana, M., Nueckel, K., Mühlberger, A., Neueder, D., Polak, T., Domschke, K., et al. Effects of transcranial direct current stimulation on consolidation of fear memory. Front Psychiatry, 4, 2013, 107.
57. van't Wout, M., Mariano, T., Garnaat, S., Reddy, M., Rasmussen, S., Greenberg, B., Can transcranial direct current stimulation augment extinction of conditioned fear?. Brain Stimul 9 (2016), 529–536.
58. van't Wout, M., Longo, S., Reddy, M., Philip, N., Bowker, M., Greenberg, B., Transcranial direct current stimulation may modulate extinction memory in posttraumatic stress disorder. Brain Behav, 7, 2017, e00681.
59. Mungee, A., Burger, M., Bajbouj, M., No effect of cathodal transcranial direct current stimulation on fear memory in healthy human subjects. Brain Sci, 6, 2016, E55.
60. Mungee, A., Kazzer, P., Feeser, M., Nitsche, M., Schiller, D., Bajbouj, M., Transcranial direct current stimulation of the prefrontal cortex: A means to modulate fear memories. Neuroreport 25 (2014), 480–484.
61. Herrmann, M., Katzorke, A., Busch, Y., Gromer, D., Polak, T., Pauli, P., et al. Medial prefrontal cortex stimulation accelerates therapy response of exposure therapy in acrophobia. Brain Stimul 10 (2017), 291–297.
62. Grisaru, N., Amir, M., Cohen, H., Kaplan, Z., Effect of transcranial magnetic stimulation in posttraumatic stress disorder: A preliminary study. Biol Psychiatry 44 (1998), 52–55.
63. Cohen, H., Kaplan, Z., Kotler, M., Kouperman, I., Moisa, R., Grisaru, N., Repetitive transcranial magnetic stimulation of the right dorsolateral prefrontal cortex in posttraumatic stress disorder: A double-blind, placebo-controlled study. Am J Psychiatry 161 (2004), 515–524.
64. Boggio, P., Rocha, M., Oliveira, M., Fecteau, S., Cohen, R., Campanhã C., et al. Noninvasive brain stimulation with high-frequency and low-intensity repetitive transcranial magnetic stimulation treatment for posttraumatic stress disorder. J Clin Psychiatry 71 (2010), 992–999.
65. Watts, B., Landon, B., Groft, A., Young-Xu, Y., A sham controlled study of repetitive transcranial magnetic stimulation for posttraumatic stress disorder. Brain Stimul 5 (2012), 38–43.
66. Nam, D., Pae, C., Chae, J., Low-frequency, repetitive transcranial magnetic stimulation for the treatment of patients with posttraumatic stress disorder: A double-blind, sham-controlled study. Clin Psychopharmacol Neurosci 11 (2013), 96–102.
67. Osuch, E., Benson, B., Luckenbaugh, D., Geraci, M., Post, R., McCann, U., Repetitive TMS combined with exposure therapy for PTSD: A preliminary study. J Anxiety Disord 23 (2009), 54–59.
68. Isserles, M., Shalev, A., Roth, Y., Peri, T., Kutz, I., Zlotnick, E., et al. Effectiveness of deep transcranial magnetic stimulation combined with a brief exposure procedure in post-traumatic stress disorder—a pilot study. Brain Stimul 6 (2013), 377–383.
69. Clark, C., Cole, J., Winter, C., Williams, K., Grammer, G., A review of transcranial magnetic stimulation as a treatment for post-traumatic stress disorder. Curr Psychiatry Rep, 17, 2015, 83.
70. Do-Monte, F., Quiñones-Laracuente, K., Quirk, G., A temporal shift in the circuits mediating retrieval of fear memory. Nature 519 (2015), 460–463.