Low-frequency stimulation depresses the primate anterior-cingulate-cortex and prevents spontaneous recovery of aversive memories

Journal of Neuroscience

Volumn 32, Issue 25, 2012, Pages 8589-8597

  Klavir, Oded ^a   Genud Gabai, Rotem ^a   Paz Dr , Rony ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANTERIOR CINGULATE; ARTICLE; AUDITORY STIMULATION; AVERSIVE MEMORY; BEHAVIOR; CONDITIONING; ELECTROSTIMULATION; EVOKED RESPONSE; FEAR; LONG TERM DEPRESSION; LOW FREQUENCY STIMULATION; MACACA FASCICULARIS; MALE; MEMORY; NERVE CELL PLASTICITY; NERVE EXCITABILITY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; SINGLE UNIT ACTIVITY; SPIKE; TRAINING; VISUAL STIMULATION;

ACOUSTIC STIMULATION; ANIMALS; ANTICIPATION, PSYCHOLOGICAL; BLINKING; CEREBRAL CORTEX; CONDITIONING, CLASSICAL; ELECTRIC STIMULATION; ELECTRODES, IMPLANTED; EVOKED POTENTIALS; EXTINCTION, PSYCHOLOGICAL; GYRUS CINGULI; MACACA FASCICULARIS; MAGNETIC RESONANCE IMAGING; MALE; MEMBRANE POTENTIALS; MEMORY; PHOTIC STIMULATION; REINFORCEMENT (PSYCHOLOGY);

EID: 84862891791     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.6481-11.2012     Document Type: Article

References (76)

1. Alvarez RP, Johnson L, Grillon C (2007) Contextual-specificity of short-delay extinction in humans: renewal of fear-potentiated startle in a virtual environment. Learn Mem 14:247-253.
2. Amano T, Unal CT, Paré D (2010) Synaptic correlates of fear extinction in the amygdala. Nat Neurosci 13:489-494.
3. Bar-Gad I, Elias S, Vaadia E, Bergman H (2004) Complex locking rather than complete cessation of neuronal activity in the globus pallidus of a 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-treated primate in response to pallidal microstimulation. J Neurosci 24:7410-7419.
4. Blum S, Hebert AE, Dash PK (2006) A role for the prefrontal cortex in recall of recent and remote memories. Neuroreport 17:341-344.
5. Bouton ME (1993) Context, time, and memory retrieval in the interference paradigms of Pavlovian learning. Psychol Bull 114:80-99.
6. Bouton ME (2006) Learning and behavior: a contemporary synthesis. Sunderland, MA: Sinauer.
7. Bremner JD, Vermetten E, Schmahl C, Vaccarino V, Vythilingam M, Afzal N, Grillon C, Charney DS (2005) Positron emission tomographic imaging of neural correlates of a fear acquisition and extinction paradigm in women with childhood sexual-abuse-related post-traumatic stress disorder. Psychol Med 35:791-806.
8. Bryden DW, Johnson EE, Tobia SC, Kashtelyan V, Roesch MR (2011) Attention for learning signals in anterior cingulate cortex. J Neurosci 31:18266-18274.
9. Corcoran KA, Quirk GJ (2007) Activity in prelimbic cortex is necessary for the expression of learned, but not innate, fears. J Neurosci 27:840-844.
10. Delgado MR, Olsson A, Phelps EA (2006) Extending animal models of fear conditioning to humans. Biol Psychol 73:39-48.
11. Dudai Y (2009) Predicting not to predict too much: how the cellular machinery of memory anticipates the uncertain future. Philos Trans R Soc Lond B Biol Sci 364:1255-1262.
12. Dudek SM, Bear MF (1992) Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. Proc Natl Acad Sci U S A 89:4363-4367.
13. Dunsmoor JE, Bandettini PA, Knight DC (2007) Impact of continuous versus intermittent CS-UCS pairing on human brain activation during Pavlovian fear conditioning. Behav Neurosci 121:635-642.
14. Dunsmoor JE, Prince SE, Murty VP, Kragel PA, LaBar KS (2011) Neurobehavioral mechanisms of human fear generalization. Neuroimage 55:1878-1888.
15. Duvarci S, Popa D, Paré D (2011) Central amygdala activity during fear conditioning. J Neurosci 31:289-294.
16. Foa EB (2006) Psychosocial therapy for posttraumatic stress disorder. J Clin Psychiatry 67 [Suppl 2]:40-45.
17. Ghashghaei HT, Hilgetag CC, Barbas H (2007) Sequence of information processing for emotions based on the anatomic dialogue between prefrontal cortex and amygdala. Neuroimage 34:905-923.
18. Goosens KA, Maren S (2004) NMDA receptors are essential for the acquisition, but not expression, of conditional fear and associative spike firing in the lateral amygdala. Eur J Neurosci 20:537-548.
19. Gubellini P, Salin P, Kerkerian-Le Goff L, Baunez C (2009) Deep brain stimulation in neurological diseases and experimental models: from molecule to complex behavior. Progress in neurobiology 89:79-123.
20. Hashimoto T, Elder CM, Okun MS, Patrick SK, Vitek JL (2003) Stimulation of the subthalamic nucleus changes the firing pattern of pallidal neurons. J Neurosci 23:1916-1923.
21. Hayden BY, Heilbronner SR, Pearson JM, Platt ML (2011) Surprise signals in anterior cingulate cortex: neuronal encoding of unsigned reward prediction errors driving adjustment in behavior. J Neurosci 31:4178-4187.
22. Herry C, Garcia R (2002) Prefrontal cortex long-term potentiation, but not long-term depression, is associated with the maintenance of extinction of learned fear in mice. J Neurosci 22:577-583.
23. Herry C, Ciocchi S, Senn V, Demmou L, Müller C, Lüthi A (2008) Switching on and off fear by distinct neuronal circuits. Nature 454:600-606.
24. Hugues S, Garcia R (2007) Reorganization of learning-associated prefrontal synaptic plasticity between the recall of recent and remote fear extinction memory. Learning and Memory 14:520-524.
25. Jovanovic T, Norrholm SD, Blanding NQ, Davis M, Duncan E, Bradley B, Ressler KJ (2010) Impaired fear inhibition is a biomarker of PTSD but not depression. Depress Anxiety 27:244-251.
26. Kim J, Lee S, Park K, Hong I, Song B, Son G, Park H, Kim WR, Park E, Choe HK, Kim H, Lee C, Sun W, Kim K, Shin KS, Choi S (2007) Amygdala depotentiation and fear extinction. Proc Natl Acad Sci U S A 104: 20955-20960.
27. Kirkwood A, Dudek SM, Gold JT, Aizenman CD, Bear MF (1993) Common forms of synaptic plasticity in the hippocampus and neocortex in vitro. Science 260:1518-1521.
28. Laurent V, Westbrook RF (2009) Inactivation of the infralimbic but not the prelimbic cortex impairs consolidation and retrieval of fear extinction. Learn Mem 16:520-529.
29. LeDoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23:155-184.
30. Liberzon I, Taylor SF, Amdur R, Jung TD, Chamberlain KR, Minoshima S, Koeppe RA, Fig LM (1999) Brain activation in PTSD in response to trauma-related stimuli. Biol Psychiatry 45:817-826.
31. Likhtik E, Pelletier JG, Paz R, Paré D (2005) Prefrontal control of the amygdala. J Neurosci 25:7429-7437.
32. Lissek S, Rabin S, Heller RE, Lukenbaugh D, Geraci M, Pine DS, Grillon C (2010) Overgeneralization of conditioned fear as a pathogenic marker of panic disorder. Am J Psychiatry 167:47-55.
33. Malenka RC (1994) Synaptic plasticity in the hippocampus: LTP and LTD. Cell 78:535-538.
34. Maren S, Chang CH (2006) Recent fear is resistant to extinction. Proc Natl Acad Sci U S A 103:18020-18025.
35. Maren S, Quirk GJ (2004) Neuronal signalling of fear memory. Nat Rev Neurosci 5:844-852.
36. Maroun M (2006) Stress reverses plasticity in the pathway projecting from the ventromedial prefrontal cortex to the basolateral amygdala. Eur J Neurosci 24:2917-2922.
37. Martin RF, Bowden DM (2000) Primate brain maps: structure of the macaque brain. Amsterdam: Elsevier Science.
38. Maurice N, Thierry AM, Glowinski J, Deniau JM (2003) Spontaneous and evoked activity of substantia nigra pars reticulata neurons during high-frequency stimulation of the subthalamic nucleus. J Neurosci 23:9929-9936.
39. McDonald AJ (1998) Cortical pathways to the mammalian amygdala. Prog Neurobiol 55:257-332.
40. McIntyre CC, Savasta M, Kerkerian-Le Goff L, Vitek JL (2004) Uncovering the mechanism(s) of action of deep brain stimulation: activation, inhibition, or both. Clin Neurophysiol 115:1239-1248.
41. Milad MR, Quirk GJ (2002) Neurons in medial prefrontal cortex signal memory for fear extinction. Nature 420:70-74.
42. Milad MR, Rauch SL, Pitman RK, Quirk GJ (2006) Fear extinction in rats: implications for human brain imaging and anxiety disorders. Biol Psychol 73:61-71.
43. Milad MR, Quirk GJ, Pitman RK, Orr SP, Fischl B, Rauch SL (2007) A role for the human dorsal anterior cingulate cortex in fear expression. Biol Psychiatry 62:1191-1194.
44. Milad MR, Pitman RK, Ellis CB, Gold AL, Shin LM, Lasko NB, Zeidan MA, Handwerger K, Orr SP, Rauch SL (2009) Neurobiological basis of failure to recall extinction memory in posttraumatic stress disorder. Biol Psychiatry 66:1075-1082.
45. Mockett B, Coussens C, Abraham WC (2002) NMDA receptor-mediated metaplasticity during the induction of long-term depression by low-frequency stimulation. Eur J Neurosci 15:1819-1826.
46. Monfils MH, Cowansage KK, Klann E, LeDoux JE (2009) Extinction-reconsolidation boundaries: key to persistent attenuation of fear memories. Science 324:951-955.
47. Myers KM, Davis M (2007) Mechanisms of fear extinction. Mol Psychiatry 12:120-150.
48. Myers KM, Ressler KJ, Davis M (2006) Different mechanisms of fear extinction dependent on length of time since fear acquisition. Learn Mem 13:216-223.
49. Nader K, Hardt O (2009) A single standard for memory: the case for reconsolidation. Nat Rev Neurosci 10:224-234.
50. Norrholm SD, Vervliet B, Jovanovic T, Boshoven W, Myers KM, Davis M, Rothbaum B, Duncan EJ (2008) Timing of extinction relative to acquisition: A parametric analysis of fear extinction in humans. Behav Neurosci 122:1016-1030.
51. Pannu Hayes J, Labar KS, Petty CM, McCarthy G, Morey RA (2009) Alterations in the neural circuitry for emotion and attention associated with posttraumatic stress symptomatology. Psychiatry Res 172:7-15.
52. Pape HC, Pare D (2010) Plastic synaptic networks of the amygdala for the 'acquisition, expression, and extinction of conditioned fear. Physiol Rev 90:419-463.
53. Pascual-Leone A, Tormos JM, Keenan J, Tarazona F, Cañete C, Catalá MD (1998) Study and modulation of human cortical excitability with transcranial magnetic stimulation. J Clin Neurophysiol 15:333-343.
54. Paton JJ, Belova MA, Morrison SE, Salzman CD (2006) The primate amygdala represents the positive and negative value of visual stimuli during learning. Nature 439:865-870.
55. Pavlov I (1927) Conditioned reflexes. London: Oxford UP.
56. Phelps EA, Delgado MR, Nearing KI, LeDoux JE (2004) Extinction learning in humans: role of the amygdala and vmPFC. Neuron 43:897-905.
57. Quirk GJ, Paré D, Richardson R, Herry C, Monfils MH, Schiller D, Vicentic A (2010) Erasing fear memories with extinction training. J Neurosci 30:14993-14997.
58. Rescorla RA (2004) Spontaneous recovery varies inversely with the training-extinction interval. Learn Behav 32:401-408.
59. Resnik J, Sobel N, Paz R (2011) Auditory aversive learning increases discrimination thresholds. Nat Neurosci 14:791-796.
60. Robbins SJ (1990) Mechanisms underlying spontaneous recovery in autoshaping. J Exp Psychol: Animal Behav Proc 16:235-249.
61. Rushworth MF, Behrens TE (2008) Choice, uncertainty and value in prefrontal and cingulate cortex. Nat Neurosci 11:389-397.
62. Sagi D (2011) Perceptual learning in vision research. Vision Res 51:1552-1566.
63. Saleem K, Logothetis N (2007) A combined MRI and histology atlas of the rhesus monkey brain. London: Elsevier.
64. Schiller D, Cain CK, Curley NG, Schwartz JS, Stern SA, Ledoux JE, Phelps EA (2008) Evidence for recovery of fear following immediate extinction in rats and humans. Learn Mem 15:394-402.
65. Seidemann E, Arieli A, Grinvald A, Slovin H (2002) Dynamics of depolarization and hyperpolarization in the frontal cortex and saccade goal. Science 295:862-865.
66. Shin LM, Bush G, Milad MR, Lasko NB, Brohawn KH, Hughes KC, Macklin ML, Gold AL, Karpf RD, Orr SP, Rauch SL, Pitman RK (2011) Exaggerated activation of dorsal anterior cingulate cortex during cognitive interference: a monozygotic twin study of posttraumatic stress disorder. Am J Psychiatry 168:979-985.
67. Sierra-Mercado D, Padilla-Coreano N, Quirk GJ (2011) Dissociable roles of prelimbic and infralimbic cortices, ventral hippocampus, and basolateral amygdala in the expression and extinction of conditioned fear. Neuropsychopharmacology 36:529-538.
68. Stefanacci L, Amaral DG (2002) Some observations on cortical inputs to the macaque monkey amygdala: an anterograde tracing study. J Comp Neurol 451:301-323.
69. Straube T, Glauer M, Dilger S, Mentzel HJ, Miltner WH (2006) Effects of cognitive-behavioral therapy on brain activation in specific phobia. Neuroimage 29:125-135.
70. Vervliet B, Vansteenwegen D, Eelen P (2006) Generalization gradients for acquisition and extinction in human contingency learning. Exp Psychol 53:132-142.
71. Vervliet B, Kindt M, Vansteenwegen D, Hermans D (2010) Fear generalization in humans: impact of prior non-fearful experiences. Behav Res Ther 48:1078-1084.
72. Vidal-Gonzalez I, Vidal-Gonzalez B, Rauch SL, Quirk GJ (2006) Microstimulation reveals opposing influences of prelimbic and infralimbic cortex on the expression of conditioned fear. Learn Mem 13:728-733.
73. Wang SJ, Gean PW (1999) Long-term depression of excitatory synaptic transmission in the rat amygdala. J Neurosci 19:10656-10663.
74. Wichmann T, Delong MR (2006) Deep brain stimulation for neurologic and neuropsychiatric disorders. Neuron 52:197-204.
75. Woods AM, Bouton ME (2008) Immediate extinction causes a less durable loss of performance than delayed extinction following either fear or appetitive conditioning. Learn Mem 15:909-920.
76. Yehuda R, LeDoux J (2007) Response variation following trauma: a translational neuroscience approach to understanding PTSD. Neuron 56:19-32.