Memory consolidation of fear conditioning: Bi-stable amygdala connectivity with dorsal anterior cingulate and medial prefrontal cortex

Social Cognitive and Affective Neuroscience

Volumn 9, Issue 11, 2014, Pages 1730-1737

  Feng, Pan ^a   Feng, Tingyong ^a,b   Chen, Zhencai ^a   Lei, Xu ^a  

^a SOUTHWEST UNIVERSITY   (China)

^b BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

Author keywords

Amygdala; Fear memory consolidation; Functional connectivity; Resting state fMRI

Indexed keywords

OXYGEN;

AMYGDALOID NUCLEUS; ANXIETY; BLOOD; BRAIN MAPPING; CINGULATE GYRUS; CONDITIONED REFLEX; DIAGNOSIS; FEAR; FEMALE; HUMAN; IMAGE PROCESSING; INDIVIDUALITY; MALE; MEMORY; NERVE TRACT; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PHYSIOLOGY; PREFRONTAL CORTEX; REST; TIME; VASCULARIZATION; YOUNG ADULT;

AMYGDALA; ANXIETY; BRAIN MAPPING; CONDITIONING, CLASSICAL; FEAR; FEMALE; GYRUS CINGULI; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; INDIVIDUALITY; MAGNETIC RESONANCE IMAGING; MALE; MEMORY; NEURAL PATHWAYS; OXYGEN; PREFRONTAL CORTEX; REST; TIME FACTORS; YOUNG ADULT;

EID: 84928662507     PISSN: 17495016     EISSN: 17495024     Source Type: Journal    
DOI: 10.1093/scan/nst170     Document Type: Article

References (83)

1. Admon, R., Lubin, G., Stern, O., et al. (2009). Human vulnerability to stress depends on amygdala's predisposition and hippocampal plasticity. Proceedings of the National Academy of Sciences United States of America, 106(33), 14120-5.
2. Adolphs, R., Tranel, D., Hamann, S., et al. (1999). Recognition of facial emotion in nine individuals with bilateral amygdala damage. Neuropsychologia, 37(10), 1111-7.
3. Albert, J., López-Martín, S., Tapia, M., Montoya, D., Carretié, L. (2011). The role of the anterior cingulate cortex in emotional response inhibition. Human Brain Mapping, 33(9), 2147-60.
4. Albert, N.B., Robertson, E.M., Miall, R.C. (2009). The resting human brain and motor learning. Current Biology, 19(12), 1023.
5. Armony, J.L., LeDoux, J.E. (1997). How the brain processes emotional information. Annals of the New York Academy of Sciences, 821(1), 259-70.
6. Augustine, J.R. (1996). Circuitry and functional aspects of the insular lobe in primates including humans. Brain Research Reviews, 22(3), 229-44.
7. Biswal, B., Zerrin Yetkin, F., Haughton, V.M., Hyde, J.S. (1995). Functional connectivity in the motor cortex of resting human brain using echo-planar mri. Magnetic Resonance in Medicine, 34(4), 537-541.
8. Buckner, R.L., Vincent, J.L. (2007). Unrest at rest: default activity and spontaneous network correlations. Neuroimage, 37(4), 1091-96.
9. Cowell, R.A., Bussey, T.J., Saksida, L.M. (2010). Components of recognition memory: Dissociable cognitive processes or just differences in representational complexity? Hippocampus, 20(11), 1245-62.
10. Craig, A. (2009). How do you feel-now? The anterior insula and human awareness. Nature Reviews Neuroscience, 10(1), 59-70.
11. Critchley, H.D. (2005). Neural mechanisms of autonomic, affective, and cognitive integration. The Journal of Comparative Neurology, 493(1), 154-66.
12. Daselaar, S., Huijbers, W., de Jonge, M., Goltstein, P., Pennartz, C. (2010). Experiencedependent alterations in conscious resting state activity following perceptuomotor learning. Neurobiology of Learning and Memory, 93(3), 422-7.
13. Delgado, M.R., Li, J., Schiller, D., Phelps, E.A. (2008a). The role of the striatum in aversive learning and aversive prediction errors. Philosophical Transactions of the Royal Society B: Biological Sciences, 363(1511), 3787-800.
14. Delgado, M.R., Nearing, K.I., LeDoux, J.E., Phelps, E.A. (2008b). Neural circuitry underlying the regulation of conditioned fear and its relation to extinction. Neuron, 59(5), 829-38.
15. Dunsmoor, J.E., Prince, S.E., Murty, V.P., Kragel, P.A., LaBar, K.S. (2011). Neurobehavioral mechanisms of human fear generalization. Neuroimage, 55(4), 1878-88.
16. Fox, M.D., Snyder, A.Z., Vincent, J.L., Corbetta, M., Van Essen, D.C., Raichle, M.E. (2005). The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proceedings of the National Academy of Sciences of the United States of America, 102(27), 9673.
17. Frankland, P.W., Bontempi, B. (2005). The organization of recent and remote memories. Nature Reviews Neuroscience, 6(2), 119-30.
18. Friston, K., Buechel, C., Fink, G., Morris, J., Rolls, E., Dolan, R. (1997). Psychophysiological and modulatory interactions in neuroimaging. Neuroimage, 6(3), 218-29.
19. Friston, K.J., Holmes, A.P., Worsley, K.J., Poline, J.P., Frith, C.D., Frackowiak, R.S.J. (1994). Statistical parametric maps in functional imaging: a general linear approach. Human Brain Mapping, 2(4), 189-210.
20. Ghashghaei, H., Hilgetag, C., Barbas, H. (2007). Sequence of information processing for emotions based on the anatomic dialogue between prefrontal cortex and amygdala. Neuroimage, 34(3), 905-23.
21. Greicius, M.D., Krasnow, B., Reiss, A.L., Menon, V. (2003). Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proceedings of the National Academy of Sciences, 100(1), 253.
22. Hartley, C.A., Fischl, B., Phelps, E.A. (2011). Brain structure correlates of individual differences in the acquisition and inhibition of conditioned fear. Cerebral Cortex, 21(9), 1954-62.
23. Indovina, I., Robbins, T.W., Núñez-Elizalde, A.O., Dunn, B.D., Bishop, S.J. (2011). Fearconditioning mechanisms associated with trait vulnerability to anxiety in humans. Neuron, 69(3), 563-71.
24. Kalisch, R., Korenfeld, E., Stephan, K.E., Weiskopf, N., Seymour, B., Dolan, R.J. (2006). Context-dependent human extinction memory is mediated by a ventromedial prefrontal and hippocampal network. The Journal of Neuroscience, 26(37), 9503-11.
25. Kim, M.J., Gee, D.G., Loucks, R.A., Davis, F.C., Whalen, P.J. (2011). Anxiety dissociates dorsal and ventral medial prefrontal cortex functional connectivity with the amygdala at rest. Cerebral Cortex, 21(7), 1667-73.
26. Kim, M.J., Whalen, P.J. (2009). The structural integrity of an amygdala-prefrontal pathway predicts trait anxiety. The Journal of Neuroscience, 29(37), 11614-8.
27. LaBar, K.S., Cabeza, R. (2006). Cognitive neuroscience of emotional memory. Nature Reviews Neuroscience, 7(1), 54-64.
28. Lang, P.J., Bradley, M.M., Cuthbert, B.N. (1999). International Affective Picture System (IAPS): Technical Manual and Affective Ratings. Gainesville, FL: The Center for Research in Psychophysiology, University of Florida.
29. Lang, S., Kroll, A., Lipinski, S.J., et al. (2009). Context conditioning and extinction in humans: differential contribution of the hippocampus, amygdala and prefrontal cortex. European Journal of Neuroscience, 29(4), 823-32.
30. Lanius, R.A., Williamson, P.C., Hopper, J., et al. (2003). Recall of emotional states in posttraumatic stress disorder: an fMRI investigation. Biological Psychiatry, 53(3), 204-10.
31. LeDoux, J.E. (2003). Synaptic self: How our Brains Become Who We are. USA: Penguin Group.
32. LeDoux, J., Bemporad, J.R. (1997). The emotional brain. Journal of the American Academy of Psychoanalysis, 25(3), 525-8.
33. Lei, X., Ostwald, D., Hu, J., et al. (2011). Multimodal Functional Network Connectivity: An EEG-fMRI Fusion in Network Space. PloS One, 6(9), e24642.
34. Liang, Z., King, J., Zhang, N. (2011). Uncovering intrinsic connectional architecture of functional networks in awake rat brain. The Journal of Neuroscience, 31(10), 3776-83.
35. Likhtik, E., Pelletier, J.G., Paz, R., Paré, D. (2005). Prefrontal control of the amygdala. The Journal of Neuroscience, 25(32), 7429-37.
36. Linnman, C., Zeidan, M.A., Furtak, S.C., Pitman, R.K., Quirk, G.J., Milad, M.R. (2012). Resting amygdala and medial prefrontal metabolism predicts functional activation of the fear extinction circuit. American Journal of Psychiatry, 169(4), 415-23.
37. Linnman, C., Zeidan, M.A., Pitman, R.K., Milad, M.R. (2011). Resting cerebral metabolism correlates with skin conductance and functional brain activation during fear conditioning. Biological Psychology, 89(2), 450-9.
38. Lowe, M., Mock, B., Sorenson, J. (1998). Functional connectivity in single and multislice echoplanar imaging using resting-state fluctuations. Neuroimage, 7(2), 119-32.
39. Milad, M.R., Quinn, B.T., Pitman, R.K., Orr, S.P., Fischl, B., Rauch, S.L. (2005). Thickness of ventromedial prefrontal cortex in humans is correlated with extinction memory. Proceedings of the National Academy of Sciences of the United States of America, 102(30), 10706.
40. Milad, M.R., Quirk, G.J. (2002). Neurons in medial prefrontal cortex signal memory for fear extinction. Nature, 420(6911), 70-74.
41. Milad, M.R., Quirk, G.J., Pitman, R.K., Orr, S.P., Fischl, B., Rauch, S.L. (2007a). A role for the human dorsal anterior cingulate cortex in fear expression. Biological Psychiatry, 62(10), 1191-4.
42. Milad, M.R., Wright, C.I., Orr, S.P., Pitman, R.K., Quirk, G.J., Rauch, S.L. (2007b). Recall of fear extinction in humans activates the ventromedial prefrontal cortex and hippocampus in concert. Biological Psychiatry, 62(5), 446-54.
43. Monfils, M.H., Cowansage, K.K., Klann, E., LeDoux, J.E. (2009). Extinction-reconsolidation boundaries: key to persistent attenuation of fear memories. Science, 324(5929), 951-5.
44. Morgan, M.A., LeDoux, J.E. (1995). Differential contribution of dorsal and ventral medial prefrontal cortex to the acquisition and extinction of conditioned fear in rats. Behavioral Neuroscience, 109(4), 681.
45. Öngür, D., Price, J. (2000). The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cerebral Cortex, 10(3), 206-19.
46. Pessoa, L., Adolphs, R. (2010). Emotion processing and the amygdala: from a'low road'to'many roads' of evaluating biological significance. Nature Reviews Neuroscience, 11(11), 773-83.
47. Phan, K.L., Wager, T., Taylor, S.F., Liberzon, I. (2002). Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI. Neuroimage, 16(2), 331-48.
48. Phelps, E.A. (2004). Human emotion and memory: interactions of the amygdala and hippocampal complex. Current Opinion in Neurobiology, 14(2), 198-202.
49. Phelps, E.A., Delgado, M.R., Nearing, K.I., LeDoux, J.E. (2004). Extinction learning in humans: role of the amygdala and vmPFC. Neuron, 43(6), 897-905.
50. Phelps, E.A., LeDoux, J.E. (2005). Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron, 48(2), 175-87.
51. Price, J.L., Drevets, W.C. (2009). Neurocircuitry of mood disorders. Neuropsychopharmacology, 35(1), 192-216.
52. Quirk, G.J. (2002). Memory for extinction of conditioned fear is long-lasting and persists following spontaneous recovery. Learning and Memory, 9(6), 402-7.
53. Quirk, G.J., Beer, J.S. (2006). Prefrontal involvement in the regulation of emotion: convergence of rat and human studies. Current Opinion in Neurobiology, 16(6), 723-7.
54. Quirk, G.J., Garcia, R., Gonz lez-Lima, F. (2006). Prefrontal mechanisms in extinction of conditioned fear. Biological Psychiatry, 60(4), 337-43.
55. Quirk, G.J., Milad, M.R. (2010). Neuroscience: Editing out fear. Nature, 463(7277), 36-7.
56. Radley, J., Sisti, H., Hao, J., et al. (2004). Chronic behavioral stress induces apical dendritic reorganization in pyramidal neurons of the medial prefrontal cortex. Neuroscience, 125(1), 1-6.
57. Raichle, M.E. (2006). The brain's dark energy. Science, 314(5803), 1249.
58. Raichle, M.E., Gusnard, D.A. (2005). Intrinsic brain activity sets the stage for expression of motivated behavior. The Journal of Comparative Neurology, 493(1), 167-76.
59. Raichle, M.E., MacLeod, A.M., Snyder, A.Z., Powers, W.J., Gusnard, D.A., Shulman, G.L. (2001). A default mode of brain function. Proceedings of the National Academy of Sciences United States of America, 98(2), 676.
60. Roy, A.K., Shehzad, Z., Margulies, D.S., et al. (2009). Functional connectivity of the human amygdala using resting state fMRI. Neuroimage, 45(2), 614-26.
61. Royer, S., Pare, D. (2002). Bidirectional synaptic plasticity in intercalated amygdala neurons and the extinction of conditioned fear responses. Neuroscience, 115(2), 455.
62. Schiller, D., Monfils, M.H., Raio, C.M., Johnson, D.C., LeDoux, J.E., Phelps, E.A. (2009). Preventing the return of fear in humans using reconsolidation update mechanisms. Nature, 463(7277), 49-53.
63. Schoenbaum, G., Chiba, A.A., Gallagher, M. (2000). Changes in functional connectivity in orbitofrontal cortex and basolateral amygdala during learning and reversal training. The Journal of neuroscience, 20(13), 5179-89.
64. Schultz, D.H., Balderston, N.L., Helmstetter, F.J. (2012). Resting-state connectivity of the amygdala is altered following Pavlovian fear conditioning. Frontiers in Human Neuroscience, 6, 242.
65. Seeley, W.W., Menon, V., Schatzberg, A.F., et al. (2007). Dissociable intrinsic connectivity networks for salience processing and executive control. The Journal of neuroscience, 27(9), 2349-56.
66. Shin, L.M., Wright, C.I., Cannistraro, P.A., et al. (2005). A functional magnetic resonance imaging study of amygdala and medial prefrontal cortex responses to overtly presented fearful faces in posttraumatic stress disorder. Archives of General Psychiatry, 62(3), 273.
67. Song, X.W., Dong, Z.Y., Long, X.Y., et al. (2011). REST: a toolkit for resting-state functional magnetic resonance imaging data processing. PLoS One, 6(9), e25031.
68. Spielberger, C.D., Gorsuch, R.L., Lushene, R., Vagg, P.R., Jacobs, G.A. (1983). Manual for the State-Trait Anxiety Inventory. Palo Alto, CA: Consulting Psychologists Press.
69. Squire, L.R., Wixted, J.T. (2011). The cognitive neuroscience of human memory since HM. Annual review of neuroscience, 34, 259-88.
70. Sripada, R.K., King, A.P., Garfinkel, S.N., Wang, X., Sripada, C.S., Welsh, R.C., Liberzon, I. (2012). Altered resting-state amygdala functional connectivity in men with posttraumatic stress disorder. Journal of Psychiatry and Neuroscience: JPN, 37(4), 241.
71. Steiger, J.H. (2005). Comparing correlations: Pattern hypothesis tests between and/or within independent samples. In: Maydeu-Olivares, A., McArdle, J.J., editors. Contemporary Psychometrics: A festschrift for Roderick P. McDonald. Mahwah, NJ, US: Lawrence Erlbaum Associates, Inc, pp. 377-414.
72. Stevens, W.D., Buckner, R.L., Schacter, D.L. (2010). Correlated low-frequency BOLD fluctuations in the resting human brain are modulated by recent experience in categorypreferential visual regions. Cerebral Cortex, 20(8), 1997-2006.
73. Tambini, A., Ketz, N., Davachi, L. (2010). Enhanced brain correlations during rest are related to memory for recent experiences. Neuron, 65(2), 280-90.
74. Van Marle, H.J., Hermans, E.J., Qin, S., Fernández, G. (2010). Enhanced resting-state connectivity of amygdala in the immediate aftermath of acute psychological stress. Neuroimage, 53(1), 348-54.
75. Vertes, R.P. (2004). Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse, 51(1), 32-58.
76. Vyas, A., Mitra, R., Rao, B.S.S., Chattarji, S. (2002). Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. The Journal of Neuroscience, 22(15), 6810-8.
77. Wang, D.-Y., Han, X.-J., Li, S.-F., et al. (2012). Effects of apolipoprotein E genotype on the off-line memory consolidation. PLoS One, 7(12), e51617.
78. Whalen, P.J., Shin, L.M., McInerney, S.C., Fischer, H., Wright, C.I., Rauch, S.L. (2001). A functional MRI study of human amygdala responses to facial expressions of fear versus anger. Emotion, 1(1), 70.
79. Xue, Y.X., Luo, Y.X., Wu, P., et al. (2012). A memory retrieval-extinction procedure to prevent drug craving and relapse. Science, 336(6078), 241-5.
80. Yan, C.G., Zang, Y.F. (2010). DPARSF: a MATLAB toolbox for "pipeline" data analysis of resting-state fMRI. Frontiers in systems neuroscience, 4, 13.
81. Yehuda, R., LeDoux, J. (2007). Response variation following trauma: a translational neuroscience approach to understanding PTSD. Neuron, 56(1), 19-32.
82. Zang, Y.F., He, Y., Zhu, C.Z., et al. (2007). Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI. Brain and Development, 29(2), 83-91.
83. Zhu, C.-Z., Zang, Y.-F., Cao, Q.-J., et al. (2008). Fisher discriminative analysis of restingstate brain function for attention-deficit/hyperactivity disorder. Neuroimage, 40(1), 110-20.