Paradoxical enhancement of fear expression and extinction deficits in mice resilient to social defeat

Behavioural Brain Research

Volumn 256, Issue , 2013, Pages 580-590

  Meduri, Jeremy D ^a   Farnbauch, Laure A ^a   Jasnow, Aaron M ^a  

^a KENT STATE UNIVERSITY   (United States)

Author keywords

Behavioral flexibility; Fear learning; Resilience; Social avoidance; Susceptibility

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; CONTROLLED STUDY; COPING BEHAVIOR; DEPRESSION; FEAR; LONG TERM EXPOSURE; MALE; MOUSE; NONHUMAN; PHENOTYPIC VARIATION; PRIORITY JOURNAL; REINFORCEMENT; SOCIAL INTERACTION; SOCIAL STRESS; STATE DEPENDENT LEARNING;

BEHAVIORAL FLEXIBILITY; FEAR LEARNING; RESILIENCE; SOCIAL AVOIDANCE; SUSCEPTIBILITY;

ANIMALS; BEHAVIOR, ANIMAL; EXTINCTION, PSYCHOLOGICAL; FEAR; MALE; MICE; MICE, INBRED C57BL; RESILIENCE, PSYCHOLOGICAL; SOCIAL BEHAVIOR; SOCIAL DOMINANCE; STRESS, PSYCHOLOGICAL;

EID: 84884687248     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2013.09.009     Document Type: Article

References (72)

1. Charuvastra A., Charuvastra A., Cloitre M., Cloitre M. Social Bonds and Posttraumatic Stress Disorder. Annu Rev Psychol 2008, 59:301-328.
2. Jasnow A., Cooper M., Huhman K. N-methyl--aspartate receptors in the amygdala are necessary for the acquisition and expression of conditioned defeat. Neuroscience 2004, 123:625-634.
3. Malatynska E., Knapp R.J. Dominant-submissive behavior as models of mania and depression. Neurosci Biobehav Rev 2005, 29:715-737.
4. Day D.E., Cooper M.A., Markham C.M., Huhman K.L. NR2B subunit of the NMDA receptor in the basolateral amygdala is necessary for the acquisition of conditioned defeat in Syrian hamsters. Behav Brain Res 2011, 217:55-59.
5. Jasnow A., Huhman K. Activation of GABA(A) receptors in the amygdala blocks the acquisition and expression of conditioned defeat in Syrian hamsters. Brain Res 2001, 920:142-150.
6. Jasnow A.M., Shi C., Israel J.E., Davis M., Huhman K.L. Memory of social defeat is facilitated by cAMP response element-binding protein overexpression in the amygdala. Behav Neurosci 2005, 119:1125-1130.
7. Huhman K., Solomon M., Janicki M., Harmon A., Lin S., Jasnow A. Conditioned defeat in male and female Syrian hamsters. Horm Behav 2003, 44:293-299.
8. Avgustinovich D.F., Kovalenko I.L., Kudryavtseva N.N. A model of anxious depression: persistence of behavioral pathology. Neurosci Behav Physiol 2005, 35:917-924.
9. Huhman K.L. Social conflict models: can they inform us about human psychopathology?. Horm Behav 2006, 50:640-646.
10. Jasnow A.M., Davis M., Huhman K.L. Involvement of central amygdalar and bed nucleus of the stria terminalis corticotropin-releasing factor in behavioral responses to social defeat. Behav Neurosci 2004, 118:1052-1061.
11. Huhman K.L., Solomon M.B., Janicki M., Harmon A.C., Lin S.M., Israel J.E., et al. Conditioned defeat in male and female Syrian hamsters. Horm Behav 2003, 44:293-299.
12. Rothbaum B.O., Davis M. Applying learning principles to the treatment of post-trauma reactions. Ann NY Acad Sci 2003, 1008:112-121.
13. Ressler K.J., Rothbaum B.O., Tannenbaum L., Anderson P., Graap K., Zimand E., et al. Cognitive enhancers as adjuncts to psychotherapy: use of D-cycloserine in phobic individuals to facilitate extinction of fear. Arch Gen Psychiatry 2004, 61:1136-1144.
14. Meyer E.M., Long V., Fanselow M.S., Spigelman I. Stress Increases Voluntary Alcohol Intake, but Does not Alter Established Drinking Habits in a Rat Model of Posttraumatic Stress Disorder. Alcohol Clin Exp Res 2012, 37:566-574.
15. Corley M.J., Caruso M.J., Takahashi L.K. Stress-induced enhancement of fear conditioning and sensitization facilitates extinction-resistant and habituation-resistant fear behaviors in a novel animal model of posttraumatic stress disorder. Physiol Behav 2012, 105:408-416.
16. Sauerhöfer E., Pamplona F.A., Bedenk B., Moll G.H., Dawirs R.R., Hörsten von S., et al. Generalization of contextual fear depends on associative rather than non-associative memory components. Behav Brain Res 2012, 233:483-493.
17. Knox D., George S.A., Fitzpatrick C.J., Rabinak C.A., Maren S., Liberzon I. Single prolonged stress disrupts retention of extinguished fear in rats. Learn Mem 2012, 19:43-49.
18. Mirshekar M., Abrari K., Goudarzi I., Rashidy-Pour A. Systemic administrations of β-estradiol alleviate both conditioned and sensitized fear responses in an ovariectomized rat model of post-traumatic stress disorder. Neurobiol Learn Mem 2013, 102:12-19.
19. Cordero M.I., Venero C., Kruyt N.D., Sandi C. Prior exposure to a single stress session facilitates subsequent contextual fear conditioning in rats. Horm Behav 2003, 44:338-345.
20. Rau V., DeCola J.P., Fanselow M.S. Stress-induced enhancement of fear learning: An animal model of posttraumatic stress disorder. Neurosci Biobehav Rev 2005, 29:1207-1223.
21. Rau V., Fanselow M.S. Exposure to a stressor produces a long lasting enhancement of fear learning in rats. Stress 2009, 12:125-133.
22. Goswami S., Cascardi M., Rodriguez-Sierra O.E., Duvarci S., Pare D. Impact of predatory threat on fear extinction in Lewis rats. Learn Memory 2010, 17:494-501.
23. Barik J., Marti F., Morel C., Fernandez S.P., Lanteri C., Godeheu G., et al. Chronic Stress Triggers Social Aversion via Glucocorticoid Receptor in Dopaminoceptive Neurons. Science (New York, NY) 2013, 339:332-335.
24. Yu T., Guo M., Garza J., Rendon S., Sun X.-L., Zhang W., et al. Cognitive and neural correlates of depression-like behaviour in socially defeated mice: an animal model of depression with cognitive dysfunction. Int J Neuropsychopharm 2010, 14:303-317.
25. Dubreucq S., Kambire S., Conforzi M., Metna-Laurent M., Cannich A., Soria-Gomez E., et al. Cannabinoid type 1 receptors located on single-minded 1-expressing neurons control emotional behaviors. Neuroscience 2012, 204:230-244.
26. Narayanan V., Heiming R.S., Jansen F., Lesting J., Sachser N., Pape H.-C., et al. Social Defeat: Impact on Fear Extinction and Amygdala-Prefrontal Cortical Theta Synchrony in 5-HTT Deficient Mice. PLoS ONE 2011, 6:e22600.
27. Wood S.K., Walker H.E., Valentino R.J., Bhatnagar S. Individual Differences in Reactivity to Social Stress Predict Susceptibility and Resilience to a Depressive Phenotype: Role of Corticotropin-Releasing Factor. Endocrinology 2010, 151:1795-1805.
28. Couch Y., Anthony D.C., Dolgov O., Revischin A., Festoff B., Santos A.I., et al. Microglial activation, increased TNF and SERT expression in the prefrontal cortex define stress-altered behaviour in mice susceptible to anhedonia. Brain Behav Immun 2013, 29:136-146.
29. Farley S., Dumas S. Mestikawy El SGiros B. Increased expression of the Vesicular Glutamate Transporter-1 (VGLUT1) in the prefrontal cortex correlates with differential vulnerability to chronic stress in various mouse strains: Effects of fluoxetine and MK-801. Neuropharmacology 2012, 62:503-517.
30. Kanarik M., Alttoa A., Matrov D., Kõiv K., Sharp T., Panksepp J., et al. Brain responses to chronic social defeat stress: Effects on regional oxidative metabolism as a function of a hedonic trait, and gene expression in susceptible and resilient rats. Eur Neuropsychopharmacol 2011, 21:92-107.
31. Krishnan V., Han M.-H., Graham D.L., Berton O., Renthal W., Russo S.J., et al. Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell 2007, 131:391-404.
32. Espallergues J., Teegarden S.L., Veerakumar A., Boulden J., Challis C., Jochems J., et al. HDAC6 Regulates Glucocorticoid Receptor Signaling in Serotonin Pathways with Critical Impact on Stress Resilience. J Neurosci 2012, 32:4400-4416.
33. Elliott E., Ezra-Nevo G., Regev L., Neufeld-Cohen A., Chen A. Resilience to social stress coincides with functional DNA methylation of the Crf gene in adult mice. Nature Neurosci 2010, 13:1351-1353.
34. Lutter M., Sakata I., Osborne-Lawrence S., Rovinsky S., Anderson J., Jung S., et al. The orexigenic hormone ghrelin defends against depressive symptoms of chronic stress. Nature Neurosci 2008, 11:752-753.
35. Berton O., McClung C.A., Dileone R.J., Krishnan V., Renthal W., Russo S.J., et al. Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 2006, 311:864-868.
36. Krishnan V., Han M., Mazei-Robison M., Iniguez S., Ables J., Vialou V., et al. AKT signaling within the ventral tegmental area regulates cellular and behavioral responses to stressful stimuli. Biol Psychiatry 2008, 64:691-700.
37. Russo S.J., Murrough J.W., Han M.-H., Charney D.S., Nestler E.J. Neurobiology of resilience. Nature Neurosci 2012, 15:1475-1484.
38. Golden S.A., Covington H.E., Berton O., Russo S.J. A standardized protocol for repeated social defeat stress in mice. Nat Protoc 2011, 6:1183-1191.
39. Vorhees C.V., Williams M.T. Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat Protoc 2006, 1:848-858.
40. Bonanno G.A. Loss, trauma, and human resilience: have we underestimated the human capacity to thrive after extremely aversive events?. Am Psychol 2004, 59:20-28.
41. Coifman K.G., Bonanno G.A., Rafaeli E. Affect dynamics, bereavement and resilience to loss. J Happiness Stud 2006, 8:371-392.
42. Bonanno G.A. Resilience in the Face of Potential Trauma. Current Directions in Psychol Sci 2005, 14:135-138.
43. Yehuda R. Developing an Agenda for Translational Studies of Resilience and Vulnerability Following Trauma Exposure. Ann NY Acad Sci 2006, 1071:379-396.
44. Waugh C.E., Thompson R.J., Gotlib I.H. Flexible emotional responsiveness in trait resilience. Emotion 2011, 11:1059-1067.
45. Covington H.E., Lobo M.K., Maze I., Vialou V., Hyman J.M., Zaman S., et al. Antidepressant effect of optogenetic stimulation of the medial prefrontal cortex. J Neurosci 2010, 30:16082-16090.
46. Nikulina E.M., Lacagnina M.J., Fanous S., Wang J., Hammer R.P. Intermittent social defeat stress enhances mesocorticolimbic δFosB/BDNF co-expression and persistently activates corticotegmental neurons: implication for vulnerability to psychostimulants. Neuroscience 2012, 212:38-48.
47. Bonanno G.A., Papa A., Lalande K., Westphal M., Coifman K. The Importance of Being Flexible. Psychol Sci 2004, 15:482-487.
48. Quirk G.J., Mueller D. Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 2008, 33:56-72.
49. Izquierdo A. Brief Uncontrollable Stress Causes Dendritic Retraction in Infralimbic Cortex and Resistance to Fear Extinction in Mice. J Neurosci 2006, 26:5733-5738.
50. Akirav I., Maroun M. The role of the medial prefrontal cortex-amygdala circuit in stress effects on the extinction of fear. Neural Plast 2007, 2007:30873.
51. Kollack-Walker S., Watson S.J., Akil H. Social stress in hamsters: defeat activates specific neurocircuits within the brain. J Neurosci 1997, 17:8842-8855.
52. Morrison K.E., Curry D.W., Cooper M.A. Social status alters defeat-induced neural activation in Syrian hamsters. Neuroscience 2012, 210:168-178.
53. Sierra-Mercado D., Padilla-Coreano N., Quirk G.J. Dissociable Roles of Prelimbic and Infralimbic Cortices, Ventral Hippocampus, and Basolateral Amygdala in the Expression and Extinction of Conditioned Fear. Neuropsychopharmacology 2010, 36:529-538.
54. Lebron K. Delayed Recall of Fear Extinction in Rats With Lesions of Ventral Medial Prefrontal Cortex. Learn Memory 2004, 11:544-548.
55. Mueller D., Porter J., Quirk G. Noradrenergic Signaling in Infralimbic Cortex Increases Cell Excitability and Strengthens Memory for Fear Extinction. J Neurosci 2008, 28:369-375.
56. Cerqueira J.J., Pêgo J.M., Taipa R., Bessa J.M., Almeida O.F.X., Sousa N. Morphological correlates of corticosteroid-induced changes in prefrontal cortex-dependent behaviors. J Neurosci 2005, 25:7792-7800.
57. Cerqueira J.J., Taipa R., Uylings H.B.M., Almeida O.F.X., Sousa N. Specific configuration of dendritic degeneration in pyramidal neurons of the medial prefrontal cortex induced by differing corticosteroid regimens. Cerebral Cortex 2007, 17:1998-2006.
58. Cerqueira J.J., Mailliet F., Almeida O.F.X., Jay T.M., Sousa N. The prefrontal cortex as a key target of the maladaptive response to stress. J Neurosci 2007, 27:2781-2787.
59. Liston C., Miller M.M., Goldwater D.S., Radley J.J., Rocher A.B., Hof P.R., et al. Stress-induced alterations in prefrontal cortical dendritic morphology predict selective impairments in perceptual attentional set-shifting. J Neurosci 2006, 26:7870-7874.
60. Rudebeck P.H., Walton M.E., Millette B.H.P., Shirley E., Rushworth M.F.S., Bannerman D.M. Distinct contributions of frontal areas to emotion and social behaviour in the rat. Eur J Neurosci 2007, 26:2315-2326.
61. Schoenbaum G., Roesch M.R., Stalnaker T.A., Takahashi Y.K. A new perspective on the role of the orbitofrontal cortex in adaptive behaviour. Nature Rev Neurosci 2010, 10:885.
62. Milad M.R., RAUCH S.L. The Role of the Orbitofrontal Cortex in Anxiety Disorders. Ann NY Acad Sci 2007, 1121:546-561.
63. Bush D.E.A., Sotres-Bayon F., LeDoux J.E. Individual differences in fear: isolating fear reactivity and fear recovery phenotypes. J Trauma Stress 2007, 20:413-422.
64. Galatzer-Levy I.R., Bonanno G.A., Bush D.E.A., LeDoux J.E. Heterogeneity in threat extinction learning: substantive and methodological considerations for identifying individual difference in response to stress. Front Behav Neurosci 2013, 7.
65. McEwen B.S., Stress, Adaptation, Disease: Allostasis, Allostatic Load. Ann NY Acad Sci 2006, 840:33-44.
66. Sterling P, Eyer J. Allostasis: a new paradigm to explain arousal pathology. In: editors. Handbook of Life Stress, Cognition and Health, John Wiley & Sons; n.d., 629-49.
67. Karatsoreos I.N., McEwen B.S. Psychobiological allostasis: resistance, resilience and vulnerability. Trend Cogn Sci 2011, 15:576-584.
68. Mahan A.L., Ressler K.J. Fear conditioning, synaptic plasticity and the amygdala: implications for posttraumatic stress disorder. Trends Neurosci 2012, 35:24-35.
69. Quirk G.J., Garcia R., González-Lima F. Prefrontal mechanisms in extinction of conditioned fear. Biol Psychiatry 2006, 60:337-343.
70. Jovanovic T., Kazama A., Bachevalier J., Davis M. Impaired safety signal learning may be a biomarker of PTSD. Neuropharmacology 2011, 1-10.
71. Jovanovic T., Norrholm S.D., Blanding N.Q., Phifer J.E., Weiss T., Davis M., et al. Fear potentiation is associated with hypothalamic-pituitary-adrenal axis function in PTSD. Psychoneuroendocrinology 2010, 35:846-857.
72. Milad M.R., Orr S.P., Lasko N.B., Chang Y., Rauch S.L., Pitman R.K. Presence and acquired origin of reduced recall for fear extinction in PTSD: Results of a twin study. J Psychiatr Res 2008, 42:515-520.