Inhibition of fear by learned safety signals: A mini-symposium review

Journal of Neuroscience

Volumn 32, Issue 41, 2012, Pages 14118-14124

  Christianson, John P ^a   Fernando, Anushka B P ^b   Kazama, Andy M ^c   Jovanovic, Tanja ^d   Ostroff, Linnaea E ^e   Sangha, Susan ^f  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c EMORY UNIVERSITY   (United States)

^d EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e NEW YORK UNIVERSITY   (United States)

^f UNIVERSITY OF CALIFORNIA SAN FRANCISCO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; ASSOCIATION; BASAL AMYGDALA; CENTRAL NUCLEUS (AMYGDALA); CONDITIONING; DISCRIMINATION LEARNING; FEAR; HUMAN; INSULA; LATERAL AMYGDALA; LEARNING; NERVE CELL NETWORK; NONHUMAN; PRIORITY JOURNAL; SAFETY LEARNING; SYNAPSE; VENTROMEDIAL PREFRONTAL CORTEX;

ANIMALS; CONDITIONING (PSYCHOLOGY); FEAR; HUMANS; INHIBITION (PSYCHOLOGY); LEARNING; NERVE NET; REINFORCEMENT (PSYCHOLOGY); SAFETY;

EID: 84867240742     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3340-12.2012     Document Type: Article

References (80)

1. Amano T, Unal CT, Paré D (2010) Synaptic correlates of fear extinction in the amygdala. Nat Neurosci 13:489-494. CrossRef Medline
2. Barbas H (2007) Flow of information for emotions through temporal and orbitofrontal pathways. J Anat 211:237-249. CrossRef Medline
3. Belova MA, Paton JJ, Morrison SE, Salzman CD (2007) Expectation modulates neural responses to pleasant and aversive stimuli in primate amygdala. Neuron 55:970-984. CrossRef Medline
4. Bouton ME (2004) Context and behavioral processes in extinction. Learn Mem 11:485-494. CrossRef Medline
5. Christianson JP, Benison AM, Jennings J, Sandsmark EK, Amat J, Kaufman RD, Baratta MV, Paul ED, Campeau S, Watkins LR, Barth DS, Maier SF (2008) The sensory insular cortex mediates the stress-buffering effects of safety signals but not behavioral control. J Neurosci 28:13703-13711. CrossRef Medline
6. Christianson JP, Jennings JH, Ragole T, Flyer JG, Benison AM, Barth DS, Watkins LR, Maier SF (2011) Safety signals mitigate the consequences of uncontrollable stress via a circuit involving the sensory insular cortex and bed nucleus of the stria terminalis. Biol Psychiatry 70:458-464. CrossRef Medline
7. Corbo V, Clément MH, Armony JL, Pruessner JC, Brunet A (2005) Size versus shape differences: contrasting voxel-based and volumetric analyses of the anterior cingulate cortex in individuals with acute posttraumatic stress disorder. Biol Psychiatry 58:119-124. CrossRef Medline
8. Dickinson A, Dearing MF (1979) Appetitive-aversive interactions and inhibitory processes. In: Mechanism of learning and motivation (Dickinson A, Boakes RA, eds.). Hillsdale, NJ: Lawrence Erlbaum Associates.
9. Dickinson A, Pearce JM (1977) Inhibitory interactions between appetitive and aversive stimuli. Psychol Bull 84:690-711. CrossRef
10. Dinsmoor JA (2001) Stimuli inevitably generated by behavior that avoids electric shock are inherently reinforcing. J Exp Anal Behav 75:311-333. CrossRef Medline
11. Dong S, Allen JA, Farrell M, Roth BL (2010) A chemical-genetic approach for precise spatio-temporal control of cellular signaling. Mol Biosyst 6:1376-1380. CrossRef Medline
12. Ehrlich I, Humeau Y, Grenier F, Ciocchi S, Herry C, Lüthi A (2009) Amygdala inhibitory circuits and the control of fear memory. Neuron 62:757-771. CrossRef Medline
13. Etkin A, Wager TD (2007) Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. Am J Psychiatry 164:1476-1488. CrossRef Medline
14. Falls WA, Davis M (1995) Lesions of the central nucleus of the amygdala block conditioned excitation, but not conditioned inhibition of fear as measured with the fear-potentiated startle effect. Behav Neurosci 109: 379-387. CrossRef Medline
15. Falls WA, Bakken KT, Heldt SA (1997) Lesions of the perirhinal cortex interfere with conditioned excitation but not with conditioned inhibition of fear. Behav Neurosci 111:476-486. CrossRef Medline
16. Gewirtz JC, Falls WA, Davis M (1997) Normal conditioned inhibition and extinction of freezing and fear-potentiated startle following electrolytic lesions of medical prefrontal cortex in rats. Behav Neurosci 111:712-726. CrossRef Medline
17. Glavis-Bloom CK, Kazama AM, Bachevalier J (2008) Paradoxical functional facilitationin rhesus macaques with neonatal hippocampal lesions on two stimulus-reward association tasks. Soc Neurosci Abstr 34:791.1.
18. Gray JA (1987) The psychology of fear and stress, Ed 2. Cambridge, UK: Cambridge UP.
19. Hammond LJ (1967) A traditional demonstration of the properties of Pav-lovian inhibition using differential CER. Psychon Sci 9:65-66.
20. Heldt SA, Falls WA (2006) Posttraining lesions of the auditory thalamus, but not cortex, disrupt the inhibition of fear conditioned to an auditory stimulus. Eur J Neurosci 23:765-779. CrossRef Medline
21. Heldt SA, Coover GD, Falls WA (2002) Posttraining but not pretraining lesions of the hippocampus interfere with feature-negative discrimination of fear-potentiated startle. Hippocampus 12:774-786. CrossRef Medline
22. Hughes KC, Shin LM (2011) Functional neuroimaging studies of post-traumatic stress disorder. Expert Rev Neurother 11:275-285. CrossRef Medline
23. Josselyn SA, Falls WA, Gewirtz JC, Pistell P, Davis M (2005) The nucleus accumbens is not critically involved in mediating the effects of a safety signal on behavior. Neuropsychopharmacology 30:17-26. CrossRef Medline
24. Jovanovic T, Keyes M, Fiallos A, Myers KM, Davis M, Duncan EJ (2005) Fear potentiation and fear inhibition in a human fear-potentiated startle paradigm. Biol Psychiatry 57:1559-1564. CrossRef Medline
25. Jovanovic T, Norrholm SD, Fennell JE, Keyes M, Fiallos AM, Myers KM, Davis M, Duncan EJ (2009) Posttraumatic stress disorder may be associated with impaired fear inhibition: relation to symptom severity. Psychiatry Res 167:151-160. CrossRef Medline
26. 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. CrossRef Medline
27. Jovanovic T, Kazama A, Bachevalier J, Davis M (2012a) Impaired safety signal learning may be a biomarker of PTSD. Neuropharmacology 62: 695-704. CrossRef Medline
28. Jovanovic T, Sakoman AJ, Kozarić-Kovačić D, Meštrović AH, Duncan EJ, Davis M, Norrholm SD (2012b) Acute stress disorder versus chronic posttraumatic stress disorder: inhibition offear as a function of time since trauma. Depress Anxiety. Advance online publication. doi: 10.1002/da.21991.
29. Kazama AM, Heuer E, Davis M, Bachevalier J (2012) Effects of neonatal amygdala lesions on fear learning, conditioned inhibition, and extinction in adult macaques. Behav Neurosci 126:392-403. CrossRef Medline
30. Kim JJ, Jung MW (2006) Neural circuits and mechanisms involved in Pav-lovian fear conditioning: a critical review. Neurosci Biobehav Rev 30: 188-202. CrossRef Medline
31. Konorski J (1948) Conditioned reflexes and neuron organization. Cambridge, UK: Cambridge UP.
32. Konorski J (1967) Integrative activity of the brain. Chicago: University of Chicago.
33. Koob GF (1992) Drugs of abuse: anatomy, pharmacology and function of reward pathways. Trends Pharmacol Sci 13:177-184. CrossRef Medline
34. Maier SF, Grahn RE, Kalman BA, Sutton LC, Wiertelak EP, Watkins LR (1993) The role of the amygdala and dorsal raphe nucleus in mediating the behavioral consequences of inescapable shock. Behav Neurosci 107: 377-388. CrossRef Medline
35. Matsumoto M, Hikosaka O (2009) Two types of dopamine neuron distinctly convey positive and negative motivational signals. Nature 459: 837-841. CrossRef Medline
36. McDonald AJ, Shammah-Lagnado SJ, Shi C, Davis M (1999) Cortical affer-ents to the extended amygdala. Ann N Y Acad Sci 877:309-338. CrossRef Medline
37. McNally GP, Johansen JP, Blair HT (2011) Placing prediction into the fear circuit. Trends Neurosci 34:283-292. CrossRef Medline
38. Milad MR, Quirk GJ (2002) Neurons in medial prefrontal cortex signal memory for fear extinction. Nature 420:70-74. CrossRef Medline
39. Milad MR, Pitman RK, Ellis CB, Gold AL, Shin LM, Lasko NB, Zeidan MA, Handwerger K, Orr SP, Rauch SL (2009) Neurobiological basisoffailure to recall extinction memory in posttraumatic stress disorder. Biol Psychiatry 66:1075-1082. CrossRef Medline
40. Miller RR, Spear NS (Eds.) (1985) Information processing in animals: conditioned inhibition. Hillsdale, NJ: Erlbaum.
41. Mineka S, Cook M, Miller S (1984) Fear conditioned with escapable and inescapable shock: effects of a feedback stimulus. J Exp Psychol Anim Behav Process 10:307-323. CrossRef
42. Murray EA, Izquierdo A (2007) Orbitofrontal cortex and amygdala contributions to affect and action in primates. Ann N YAcadSci 1121:273-296. CrossRef Medline
43. Myers KM, Davis M (2004) AX+, BX-discrimination learning in the fear-potentiated startle paradigm: possible relevance to inhibitory fear learning in extinction. Learn Mem 11:464-475. CrossRef Medline
44. Nieuwenhuys R (2012) The insular cortex: a review. Prog Brain Res 195: 123-163. CrossRef Medline
45. Ongür D, Price JL (2000) The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb Cortex 10:206-219. CrossRef Medline
46. Ostroff LE, Cain CK, Bedont J, Monfils MH, Ledoux JE (2010) Fear and safety learning differentially affect synapse size and dendritic translation in the lateral amygdala. Proc Natl Acad Sci USA 107:9418-9423. CrossRef Medline
47. Ostroff LE, Cain CK, Jindal N, Dar N, Ledoux JE (2012) Stability of presynaptic vesicle pools and changes in synapse morphology in the amygdala following fear learning in adult rats. J Comp Neurol 520:295-314. CrossRef Medline
48. Paulus MP, Stein MB (2006) An insular view of anxiety. Biol Psychiatry 60:383-387. CrossRef Medline
49. Pavlov IP (1927) Conditioned reflexes. London: Oxford UP.
50. Pollak DD, Monje FJ, Zuckerman L, Denny CA, Drew MR, Kandel ER (2008) An animal model of a behavioral intervention for depression. Neuron 60:149-161. CrossRef Medline
51. Pollak DD, Monje FJ, Lubec G (2010a) The learned safety paradigm as a mouse model for neuropsychiatric research. Nat Protoc 5:954-962. CrossRef Medline
52. Pollak DD, Rogan MT, Egner T, Perez DL, Yanagihara TK, Hirsch J (2010b) A translational bridge between mouse and human models of learned safety. Ann Med 42:115-122. CrossRef Medline
53. Price JL (2007) Definition of the orbital cortex in relation to specific connections with limbic and visceral structures and other cortical regions. AnnNYAcadSci 1121:54-71. CrossRef Medline
54. Rauch SL, Shin LM, Phelps EA (2006) Neurocircuitry models of posttraumatic stress disorder and extinction: human neuroimaging research-past, present, and future. Biol Psychiatry 60:376-382. CrossRef Medline
55. Rescorla RA (1969a) Establishment of a positive reinforcer through contrast with shock. J Comp Physiol Psychol 67:260-263. CrossRef Medline
56. Rescorla RA (1969b) Pavlovian conditioned inhibition. Psychol Bull 72:77-94. CrossRef
57. Rodgers KM, Benison AM, Klein A, Barth DS (2008) Auditory, somatosensory, and multisensory insular cortex in the rat. Cereb Cortex 18: 2941-2951. CrossRef Medline
58. Rogan MT, Staubli UV, LeDoux JE (1997) Fear conditioning induces associative long-term potentiation in the amygdala. Nature 390:604-607. CrossRef Medline
59. Rogan MT, Leon KS, Perez DL, Kandel ER (2005) Distinct neural signatures for safety and danger in the amygdala and striatum of the mouse. Neuron 46:309-320. CrossRef Medline
60. Roper G, Rachman S, Hodgson R (1973) An experiment on obsessional checking. Behav Res Ther 11:271-277. CrossRef Medline
61. Sah P, Faber ES, Lopez De Armentia M, Power J (2003) The amygdaloid complex: anatomy and physiology. Physiol Rev 83:803-834. CrossRef Medline
62. Schoenbaum G, Chiba AA, Gallagher M (1998) Orbitofrontal cortex and basolateral amygdala encode expected outcomes during learning. Nat Neurosci 1:155-159. CrossRef Medline
63. Schoenbaum G, Setlow B, Saddoris MP, Gallagher M (2003) Encoding predicted outcome and acquired value in orbitofrontal cortex during cue sampling depends upon input from basolateral amygdala. Neuron 39: 855-867. CrossRef Medline
64. Schuff N, Zhang Y, Zhan W, Lenoci M, Ching C, Boreta L, Mueller SG, Wang Z, Marmar CR, Weiner MW, Neylan TC (2011) Patterns of altered cortical perfusion and diminished subcortical integrity in posttraumatic stress disorder: an MRI study. Neuroimage 54:S62-S68. CrossRef Medline
65. SchultzW, Dickinson A (2000) Neuronal coding of prediction errors. Annu Rev Neurosci 23:473-500. CrossRef Medline
66. Soltysik S, Zielinski K (1962) Conditioned inhibition of the avoidance reflex. Acta Biol Exp (Warsz) 22:157-167.
67. Tanimoto H, Heisenberg M, Gerber B (2004) Event timing turns punishment to reward. Nature 430:983. CrossRef Medline
68. Tronson NC, Corcoran KA, Jovasevic V, Radulovic J (2012) Fear conditioning and extinction: emotional states encoded by distinct signaling pathways. Trends Neurosci 35:145-155. CrossRef Medline
69. Tye KM, Prakash R, Kim SY, Fenno LE, Grosenick L, Zarabi H, Thompson KR, Gradinaru V, Ramakrishnan C, Deisseroth K (2011) Amygdala circuitry mediating reversible and bidirectional control of anxiety. Nature 471:358-362. CrossRef Medline
70. Waddell J, Heldt S, Falls WA (2003) Posttraining lesion of the superior col-liculus interferes with feature-negative discrimination of fear-potentiated startle. Behav Brain Res 142:115-124. CrossRef Medline
71. Walasek G, Wesierska M, Zielinski K (1995) Conditioning of fear and conditioning of safety in rats. Acta Neurobiol Exp 55:121-132.
72. Watkins LR, Wiertelak EP, McGorry M, Martinez J, Schwartz B, Sisk D, Maier SF (1998) Neurocircuitry of conditioned inhibition of analgesia: effects of amygdala, dorsal raphe, ventral medullary, and spinal cord lesions on antianalgesia in the rat. Behav Neurosci 112:360-378. CrossRef Medline
73. Weisman RG, Litner JS (1969a) The course of Pavlovian excitation and inhibition of fear in rats. J Comp Physiol Psychol 69:667-672. CrossRef Medline
74. Weisman RG, Litner JS (1969b) Positive conditioned reinforcement of Sid-man avoidance behavior in rats. J Comp Physiol Psychol 68:597-603. CrossRef
75. Weisman RG, Litner JS (1971) Role of the intertrial interval in Pavlovian differential conditioning of fear in rats. J Comp Physiol Psychol 74:211-218. CrossRef Medline
76. Weisman RG, Denny MR, Platt SA, Zerbolio DJ Jr (1966) Facilitation of extinction by a stimulus associated with long nonshock confinement periods. J Comp Physiol Psychol 62:26-30. CrossRef Medline
77. Weiss JM (1971) Effects of coping behavior with and without a feedback signal on stress pathology in rats. J Comp Physiol Psychol 77:22-30. CrossRef Medline
78. Wiertelak EP, Maier SF, Watkins LR (1992) Cholecystokinin antianalgesia: safety cues abolish morphine analgesia. Science 256:830-833. CrossRef Medline
79. Winslow JT, Noble PL, Davis M (2008) AX+/BX- discrimination learning in the fear-potentiated startle paradigm in monkeys. Learn Mem 15:63-66. CrossRef Medline
80. Wolfensteller U, Ruge H (2012) Frontostriatal mechanisms in instruction-based learning as a hallmark of flexible goal-directed behavior. Front Psychol 3:192. Medline