Renewal of conditioned fear in a novel context is associated with hippocampal activation and connectivity

Social Cognitive and Affective Neuroscience

Volumn 11, Issue 9, 2016, Pages 1411-1421

  Hermann, A ^a   Stark, R ^a   Milad, M R ^b   Merz, C J ^c,d  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c RUHR UNIVERSITY BOCHUM   (Germany)

^d UNIVERSITY OF TRIER   (Germany)

Author keywords

Amygdala; Extinction; Fear conditioning; fMRI; Hippocampus

Indexed keywords

OXYGEN;

ADULT; ASSOCIATION; BLOOD; CONDITIONING; ELECTRODERMAL RESPONSE; FEAR; HIPPOCAMPUS; HUMAN; MALE; NERVE TRACT; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; REINFORCEMENT; YOUNG ADULT;

ADULT; CONDITIONING (PSYCHOLOGY); CUES; EXTINCTION, PSYCHOLOGICAL; FEAR; GALVANIC SKIN RESPONSE; HIPPOCAMPUS; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; NEURAL PATHWAYS; OXYGEN; YOUNG ADULT;

EID: 84987673724     PISSN: 17495016     EISSN: 17495024     Source Type: Journal    
DOI: 10.1093/scan/nsw047     Document Type: Article

References (36)

1. Augustine, J.R. (1996). Circuitry and functional aspects of the insular lobe in primates including humans. Brain Research Reviews 22, 229-44.
2. Balooch, S.B., Neumann, D.L., Boschen, M.J. (2012). Extinction treatment in multiple contexts attenuates ABC renewal in humans. Behaviour Research and Therapy 50, 604-9.
3. Boschen, M.J., Neumann, D.L., Waters, A.M. (2009). Relapse of successfully treated anxiety and fear: theoretical issues and recommendations for clinical practice. Australian and New Zealand Journal of Psychiatry 43, 89-100.
4. Bouton, M.E. (1994). Conditioning, remembering, and forgetting. Journal of Experimental Psychology. Animal Behavior Processes 20, 219-31.
5. Bouton, M.E. (2002). Context, ambiguity, and unlearning: Sources of relapse after behavioral extinction. Biological Psychiatry 52, 976-86.
6. Bouton, M.E. (2004). Context and behavioral processes in extinction. Learning and Memory 11, 485-94.
7. Diekhof, E.K., Geier, K., Falkai, P., Gruber, O. (2011). Fear is only as deep as the mind allows: a coordinate-based meta-analysis of neuroimaging studies on the regulation of negative affect. NeuroImage 58, 275-85.
8. Effting, M., Kindt, M. (2007). Contextual control of human fear associations in a renewal paradigm. Behaviour Research and Therapy 45, 2002-18.
9. El-Gaby, M., Shipton, O.A., Paulsen, O. (2015). Synaptic plasticity and memory: new insights from hippocampal left-right asymmetries. Neuroscientist 21, 490-502.
10. Graham, B.M., Milad, M.R. (2011). The study of fear extinction: implications for anxiety disorders. The American Journal of Psychiatry 168, 1255-65.
11. Ishihara, S. (1990) Ishihara's Tests for color-Blindness, 38 plate edn. Tokyo/Kyoto: Kanehara, Shuppan Co. Ltd.
12. 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, 9503-11.
13. Kessler, R.C., Berglund, P., Demler, O., Jin, R., Merikangas, K.R., Walters, E.E. (2005). Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the national comorbidity survey replication. Archives of General Psychiatry 62, 593-602.
14. Knapska, E., Macias, M., Mikosz, M., et al. (2012). Functional anatomy of neural circuits regulating fear and extinction. Proceedings of the National Academy of Sciences of the United States of America 109, 17093-8.
15. Lebron-Milad, K., Milad, M.R. (2012). Sex differences, gonadal hormones and the fear extinction network: implications for anxiety disorders. Biology of Mood and Anxiety Disorders 2, 3.
16. Maren, S., Phan, K.L., Liberzon, I. (2013). The contextual brain: implications for fear conditioning, extinction and psychopathology. Nature Reviews Neuroscience 14, 417-28.
17. Milad, M.R., Pitman, R.K., Ellis, C.B., et al. (2009). Neurobiological basis of failure to recall extinction memory in posttraumatic stress disorder. Biological Psychiatry 66, 1075-82.
18. Milad, M.R., Quirk, G.J. (2012). Fear extinction as a model for translational neuroscience: ten years of progress. Annual Review of Psychology 63, 129-51.
19. Milad, M.R., Wright, C.I., Orr, S.P., Pitman, R.K., Quirk, G.J., Rauch, S.L. (2007). Recall of fear extinction in humans activates the ventromedial prefrontal cortex and hippocampus in concert. Biological Psychiatry 62, 446-54.
20. Mineka, S., Zinbarg, R. (2006). A contemporary learning theory perspective on the etiology of anxiety disorders-it's not what you thought it was. American Psychologist 61, 10-26.
21. Neumann, D.L., Kitlertsirivatana, E. (2010). Exposure to a novel context after extinction causes a renewal of extinguished conditioned responses: Implications for the treatment of fear. Behaviour Research and Therapy 48, 565-70.
22. Neumann, D.L., Longbottom, P.L. (2008). The renewal of extinguished conditioned fear with fear-relevant and fear- irrelevant stimuli by a context change after extinction. Behaviour Research and Therapy 46, 188-206
23. Oldfield, R.C. (1971). The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia 9, 97-113.
24. Orsini, C.A., Kim, J.H., Knapska, E., Maren, S. (2011). Hippocampal and prefrontal projections to the basal amygdala mediate contextual regulation of fear after extinction. The Journal of Neuroscience 31, 17269-77.
25. Orsini, C.A., Maren, S. (2012). Neural and cellular mechanisms of fear and extinction memory formation. Neuroscience and Biobehavioral Reviews 36, 1773-802.
26. 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, 897-905.
27. Phillips, M.L., Drevets, W.C., Rauch, S.L., Lane, R. (2003). Neurobiology of emotion perception I: the neural basis of normal emotion perception. Biological Psychiatry 54, 504-14.
28. Quirk, G.J., Likhtik, E., Pelletier, J.G., Paré, D. (2003). Stimulation of medial prefrontal cortex decreases the responsiveness of central amygdala output neurons. The Journal of Neuroscience 23, 8800-7.
29. Quirk, G.J., Mueller, D. (2008). Neural mechanisms of extinction learning and retrieval. Neuropharmacology 33, 56-72.
30. Rougemont-Bücking, A., Linnman, C., Zeffiro, T.A., et al. (2011). Altered processing of contextual information during fear extinction in PTSD: an fMRI study. CNS Neuroscience & Therapeutics 17, 227-36.
31. Shipton, O.A., El-Gaby, M., Apergis-Schoute, J., et al. (2014). Leftright dissociation of hippocampal memory processes in mice. Proceedings of the National Academy of Sciences of the United States of America 111, 15238-43.
32. Strange, B.A., Witter, M.P., Lein, E.S., Moser, E.I. (2014). Functional organization of the hippocampal longitudinal axis. Nature Reviews. Neuroscience 15, 655-69.
33. van Ast, V.A., Vervliet, B., Kindt, M. (2012). Contextual control over expression of fear is affected by cortisol. Frontiers in Behavioral Neuroscience 6, 67.
34. Vervliet, B., Baeyens, F., van den Bergh, O., Hermans, D. (2013). Extinction, generalization, and return of fear: A critical review of renewal research in humans. Biological Psychology 92, 51-8.
35. Walter, B. (2002) Marina: an easy to use tool for the creation of masks for region of interest analyses. Proceedings of the 9th International Conference on Functional Mapping of the Human Brain, available on CD-Rom in NeuroImage, 19 (2).
36. Zeidan, M.A., Igoe, S.A., Linnman, C., et al. (2011). Estradiol modulates medial prefrontal cortex and amygdala activity during fear extinction in women and female rats. Biological Psychiatry 70, 920-7.