Traits of fear resistance and susceptibility in an advanced intercross line

European Journal of Neuroscience

Volumn 38, Issue 9, 2013, Pages 3314-3324

  Mcguire, Jennifer L ^a   Bergstrom, Hadley C ^a,b   Parker, Clarissa C ^c   Le, Thien ^a,b   Morgan, Maria ^a   Tang, Haiying ^a   Selwyn, Reed G ^a   Silva, Afonso C ^d   Choi, Kwang ^a,b   Ursano, Robert J ^a,b   Palmer, Abraham A ^c   Johnson, Luke R ^a,b,e  

^a Uniformed Services University of the Health Sciences   (United States)

^b Center for the Study of Traumatic Stress (CSTS)   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

^d NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^e QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

Author keywords

AIL; Fear conditioning; Fear generalisation; Hippocampus; HPA axis; Manganese enhanced MRI

Indexed keywords

CORTICOTROPIN RELEASING FACTOR RECEPTOR 1; GLUCOCORTICOID RECEPTOR; MANGANESE; MINERALOCORTICOID RECEPTOR;

ADVANCED INTERCROSS LINE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; BREEDING; CONTROLLED STUDY; ELECTROENCEPHALOGRAPHY; ENDOPHENOTYPE; FEAR; FEMALE; GENE EXPRESSION PROFILING; GENE FREQUENCY; GENETIC PREDISPOSITION; GENETIC TRAIT; GENETIC VARIABILITY; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMAGE ENHANCEMENT; LEARNING; MALE; MEMORY; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS;

AIL; FEAR CONDITIONING; FEAR GENERALISATION; HIPPOCAMPUS; HPA AXIS; MANGANESE-ENHANCED MRI;

ANIMALS; CONDITIONING, CLASSICAL; CORTICOSTERONE; CORTICOTROPIN-RELEASING HORMONE; FEAR; GENERALIZATION (PSYCHOLOGY); HYPOTHALAMO-HYPOPHYSEAL SYSTEM; INBREEDING; MICE; MICE, INBRED C57BL; PHENOTYPE; PITUITARY-ADRENAL SYSTEM; QUANTITATIVE TRAIT, HERITABLE; RECEPTORS, CORTICOTROPIN-RELEASING HORMONE; RECEPTORS, MINERALOCORTICOID; RETENTION (PSYCHOLOGY); RNA, MESSENGER;

EID: 84887195059     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12337     Document Type: Article

References (80)

1. Amstadter, A., Nugent, N. & Koenen, K. (2009) Genetics of PTSD: fear conditioning as a model for future research. Psychiat. Ann., 39, 358-367.
2. Baker, D., West, S., Nicholson, W., Ekhator, N., Kaskow, J., Hill, K., Bruce, A., Orth, D. & Geracioti, T.D. (1999) Serial CSF corticotropin-releasing hormone levels and adrenocortical activity in combat veterans with posttraumatic stress disorder. Am. J. Psychiat., 156, 585-588.
3. Baker, D., Ekhator, N., Kaskow, J., Dashevsky, B., Horn, P., Bedarnik, L. & Geracioti, T. (2005) Higher basal serial CSF cortisol in combat veterans with posttraumatic stress disorder. Am. J. Psychiat., 162, 992-994.
4. Belknap, J., Richards, S., O'Toole, L., Helms, M. & Phillips, T. (1997) Short-term selective breeding as a tool for QTL mapping: ethanol preference drinking in mice. Behav. Genet., 27, 55-65.
5. Berger, S., Wolfer, D.P., Selbach, O., Alter, H., Erdmann, G., Reichardt, H.M., Cheplova, A.N., Welzl, H., Haas, H.L., Lipp, H.-P. & Schutz, G. (2006) Loss of the limbic mineralocorticoid receptor impairs behavioral plasticity. Proc. Natl. Acad. Sci. USA, 103, 195-200.
6. Blanchard, R.J. & Blanchard, D.C. (1969a) Crouching as an index of fear. J. Comp. Physiol. Psych., 67, 370-375.
7. Blanchard, R.J. & Blanchard, D.C. (1969b) Passive and active reactions to fear-eliciting stimuli. J. Comp. Physiol. Psych., 68, 129-135.
8. Brinks, V., Berger, S., Gass, P., de Kloet, E.R. & Oitzl, M.S. (2009) Mineralocorticoid receptors in control of emotional arousal and fear memory. Horm. Behav., 56, 232-238.
9. Britton, J., Lissek, S., Grillon, C., Norcross, B. & Pine, D. (2011) Development of anxiety: the role of threat appraisal and fear learning. Depress. Anxiety, 28, 5-17.
10. Daumas, S., Halley, H., Frances, B. & Lassalle, J. (2005) Encoding, consolidation, and retrieval of contextual memory: differential involvement of dorsal CA3 and CA1 hippocampal subregions. Learn. Memory, 4, 375-383.
11. Delgado, M., Olsson, A. & Phelps, E. (2006) Extending animal models of fear conditioning to humans. Biol. Psychiat., 73, 39-48.
12. Derijk, R., de Kloet, E., Zitman, F.G. & van Leeuwen, N. (2011) Mineralocorticoid receptor gene variants as determinants of HPA-axis regulation and behavior. Endocrin. Dev., 20, 137-148.
13. Drapeau, P. & Nachshen, D.A. (1984) Manganese fluxes and manganese-dependent neurotransmitter release in presynaptic nerve endings isolated from rat brain. J. Physiol., 348, 493-510.
14. Dunsmoor, J., Mitroff, S. & LaBar, K. (2009) Generalization of conditioned fear along a dimension of increasing fear intensity. Learn. Memory, 16, 460-469.
15. Elzinga, B. & Bremner, J. (2002) Are substrates of memory the final common pathway in posttraumatic stress disorder (PTSD)? J. Affect. Disorders, 70, 1-17.
16. Fanselow, M. (1980) Conditioned and unconditioned components of post-shock freezing. Pavlovian J. Biol. Sci., 15, 177-182.
17. Felmingham, K.L., Bryant, R.A. & Gordon, E. (2003) Processing angry and neutral faces in post-traumatic stress disorder: an event-related potentials study. NeuroReport, 14, 77-780.
18. Franklin, K. & Paxinos, G. (2008) The Mouse Brain in Stereotaxic Coordinates. Academic Press, New York.
19. Gillespie, C., Phifer, J.E., Bradley, B. & Ressler, K.J. (2009) Risk and resilience: genetic and environmental influences on development of the stress response. Depress. Anxiety, 26, 984-992.
20. Gold, P. & Chrousos, G. (2002) Organization of the stress system and its dysregulation in melancholic and atypical depression: high vs low CRH/NE states. Mol. Psychiatr., 7, 254-275.
21. Grillon, C., Pine, D., Baas, J., Lawley, M., Ellis, V. & Charney, D. (2006) Cortisol and DHEA-S are associated with startle potentiation during aversive conditioning in humans. Psychopharmacology, 186, 434-441.
22. Guthrie, R. & Bryant, R. (2006) Extinction learning before trauma and subsequent posttraumatic stress. Psychosom. Med., 68, 307-311.
23. Hall, C. (1938) The inheritance of emotionality. Sigma Xi Q., 26, 17-28.
24. Han, F., Ozawa, H., Matsuda, K. & Kawata, M. (2005) Colocalization of mineralocorticoid receptor and glucocorticoid receptor in the hippocampus and hypothalamus. Neurosci. Res., 51, 371-381.
25. Hankir, M.K., Parkinson, J.R., Bloom, S.R. & Bell, J.D. (2012) The effects of glutamate receptor agonists and antagonists on mouse hypothalamic and hippocampal neuronal activity shown through manganese enhanced MRI. NeuroImage, 59, 968-978.
26. Harris, A., Holmes, M., de Kloet, E., Chapman, K. & Seckl, J. (2012) Mineralocorticoid and glucocorticoid receptor balance in control of HPA-axis and behaviour. Psychoneuroendocrino., 38, 648-658.
27. Hettema, J., Annas, P., Neale, M., Kendler, K. & Fredrikson, M. (2003) A twin study of the genetics of fear conditioning. Arch. Gen. Psychiat., 60, 702-708.
28. Indovina, I., Robbins, T.W., Nunez-Elizalde, A.O., Dunn, B.D. & Bishop, S.J. (2011) Fear-conditioning mechanisms associated with trait vulnerability to anxiety in humans. Neuron, 69, 563-571.
29. Johansen, J.P., Cain, C.K., Ostroff, L.E. & LeDoux, J.E. (2011) Molecular mechanisms of fear learning and memory. Cell, 147, 509-524.
30. Johnson, L.R. & Ledoux, J.E. (2004) The anatomy of fear: microcircuits of the lateral amygdala. In Gorman, J.M. (Ed.), Fear and Anxiety: The Benefits of Translational Research. American Psychiatric Publishing, Arlington, VA, pp. 227-250.
31. Johnson, L., McGuire, J., Lazarus, R. & Palmer, A. (2012) Pavlovian fear memory circuits and phenotype models of PTSD. Neuropharmacology, 62, 638-646.
32. Jovanovic, T., Kazama, A., Bachevalier, J. & Davis, M. (2012) Impaired safety signal learning may be a biomarker of PTSD. Neuropharmacology, 62, 695-704.
33. Kalin, N. & Takahashi, L. (1990) Fear-motivated behavior induced by prior shock experience is mediated by corticotrophin-releasing hormone systems. Brain Res., 509, 80-84.
34. Kalin, N., Shelton, S., Rickman, M. & Davidson, R. (1998) Individual differences in freezing and cortisol in infant and mother rhesus monkeys. Behav. Neurosci., 112, 251-255.
35. Kaouane, N., Porte, Y., Vallee, M., Brayda-Bruno, L., Mons, N., Calandreau, L., Marighetto, A., Piazza, P.V. & Desmedt, A. (2012) Glucocorticoids can induce PTSD-like memory impairments in mice. Science, 335, 1510-1513.
36. Klaassens, E.R., Giltay, E.J., Cuijpers, P., van Veen, T. & Zitman, F.G. (2012) Adulthood trauma and HPA-axis functioning in healthy subjects and PTSD patients: a meta-analysis. Psychoneuroendocrino., 37, 317-331.
37. de Kloet, E., Vreugdenhil, E., Oitzl, M. & Joels, M. (1998) Brain corticosteroid receptor balance in health and disease. Endocr. Rev., 19, 269-301.
38. Koretsky, A.P. (2004) New developments in magnetic resonance imaging of the brain. NeuroRx, 1, 155-164.
39. Koretsky, A.P. (2012) Is there a path beyond BOLD? Molecular imaging of brain function. NeuroImage, 62, 1208-1215.
40. Kovacs, K. & Mezey, E. (1987) Dexamethasone inhibits corticotropin-releasing factor expression in the rat paraventricular nucleus. Neuroendocrinology, 46, 365-368.
41. LeDoux, J.E. (2000) Emotion circuits in the brain. Annu. Rev. Neurosci., 23, 155-184.
42. Lee, I. & Kesner, R. (2004) Differential contributions of the dorsal hippocampal subregions to memory acquisition and retrieval in contextual fear conditioning. Hippocampus, 14, 301-310.
43. Lissek, S., Powers, A., McClure, E., Phelps, E., Woldehawariat, G., Grillon, C. & Pine, D. (2005) Classical fear conditioning in the anxiety disorders: a meta analysis. Behav. Res. Ther., 43, 1391-1424.
44. Lissek, S., Rabin, S., Heller, R., Lukenbaugh, D., Geraci, M., Pine, D. & Grillon, C. (2010) Overgeneralization of fear as a pathogenic marker of panic disorder. Am. J. Psychiat., 167, 47-55.
45. Lok, A., Mocking, R., Ruhe, H., Visser, I., Koeter, M., Assies, J., Bockting, C., Olff, M. & Schene, A. (2012) Longitudinal hypothalamic-pituitary-adrenal axis trait and state effects in recurrent depression. Psychoneuroendocrino., 37, 892-901.
46. Mahan, A. & Ressler, K. (2012) Fear conditioning, synaptic plasticity and the amygdala: implications for posttraumatic stress disorder. Trends Neurosci., 35, 24-35.
47. Maren, S. & Quirk, G. (2004) Neuronal signaling of fear and memory. Neuroscience, 5, 844-852.
48. Merz, C., Stark, R., Vaitl, D., Tabbert, K. & Wolf, O. (2012) Stress hormones are associated with the neuronal correlates of instructed fear conditioning. Biol. Psychiat., 92, 82-89.
49. Mok, S.I., Munasinghe, J.P. & Scott Young, W. (2011) Infusion-based manganese-enhanced MRI: a new imaging technique to visualize the mouse brain. Brain Struct. Funct., 217, 107-114.
50. Nemeroff, C., Widerlov, E., Bissette, G., Walleus, H., Karlsson, I., Eklund, K., Kilts, C., Loosen, P. & Vale, W. (1984) Elevated concentrations of CSF corticotripin-releasing factor-like immunoreactivity in depressed patients. Science, 226, 1342-1345.
51. Nemeroff, C., Owens, M., Bissette, G., Andorn, A. & Stanley, M. (1988) Reduced corticotropin releasing factor binding sites in the frontal cortex of suicide victims. Arch. Gen. Psychiat., 45, 577-589.
52. Nissen, C., Holz, J., Blechert, J., Feige, B., Riemann, D., Voderholzer, U. & Normann, C. (2010) Learning as a model for neural plasticity in major depression. Biol. Psychiat., 68, 544-553.
53. Norrholm, S.D., Jovanovic, T., Olin, I.W., Sands, L.A., Karapanou, I., Bradley, B. & Ressler, K.J. (2011) Fear extinction in traumatized civilians with posttraumatic stress disorder: relation to symptom severity. Biol. Psychiat., 69, 556-563.
54. Orr, S., Metzger, L., Lasko, N., Macklin, M., Peri, T. & Pitman, R. (2000) De novo conditioning in trauma-exposed individuals with and without posttraumatic stress disorder. J. Abnorm. Psychol., 109, 290-298.
55. Orr, S., Lasko, N., Macklin, M., Pineles, S., Chan, Y. & Pitman, R. (2012) Predicting post-trauma stress symptoms from pre-trauma psychophysiologic reactivity, personality traits, and measures of psychopathology. Biol. Mood Anxiety Disord., 2, 1-12.
56. Pape, H.C. & Pare, D. (2010) Plastic synaptic networks of the amygdala for the acquisition, expression, and extinction of conditioned fear. Physiol. Rev., 90, 419-463.
57. Parker, C. & Palmer, A. (2011) Dark matter: are mice the solution to missing heretibility? Front. Genet., 2, 1-7.
58. Parker, C., Sokoloff, G., Cheng, R. & Palmer, A. (2012) Genome-wide association for fear conditioning in an advanced intercross mouse line. Behav. Genet., 42, 437-448.
59. Peri, T., Ben-Shakhar, G., Orr, S. & Shalev, A. (2000) Psychophysiologic assessment of aversive conditioning in posttraumatic stress disorder. Biol. Psychiat., 47, 512-519.
60. Pineles, S., Rasmusson, A., Yehuda, R., Lasko, N., Macklin, M., Pitman, R. & Orr, S. (2012) Predicting emotional responses to potentially traumatic events from pre-exposure waking cortisol levels: a longitudinal study of police and firefighters. Anxiety Stress Copin., 26, 241-253.
61. Ponder, C.A., Kliethermes, M.R., Drew, M.R., Muller, J., Das, K., Risbrough, V.B., Crabbe, J.C., Gilliam, T.C. & Palmer, A.A. (2007) Selection for contextual fear conditioning affects anxiety-like behaviors and gene expression. Genes Brain Behav., 6, 736-749.
62. Qi, X.-R., Kamphuis, W., Wang, S., Wang, Q., Lucassen, P., Zhou, J.-N. & Swaab, D. (2012) Aberrent stress hormone receptor balance in the human prefrontal cortex and hypothalamic paraventricular nucleus of depressed patients. Psychoneuroendocrino., 38, 863-870.
63. Ratka, A., Sutanto, W., Bloemers, M. & de Kloet, E. (1989) On the role of brain mineralocorticoid (type I) and glucocorticoid (type II) receptors in neuroendocrine regulation. Neuroendocrinology, 50, 117-123.
64. 2+/calmodulin-dependent protein kinase II at lateral amygdala synapses. J. Neurosci., 24, 3281-3288.
65. Rodrigues, S., LeDoux, J. & Sapolsky, R. (2009) The influence of stress hormones on fear circuitry. Annu. Rev. Neurosci., 32, 289-313.
66. Schmidt, M., Deussing, J., Oitzl, M., Ohl, F., Levine, S., Wurst, W., Holsboer, F., Muller, M. & de Kloet, E. (2006) Differential disinhibition of the neonatal hypothalamic-pituitary-adrenal axis in brain-specific CRH receptor 1-knockout mice. Eur. J. Neurosci., 24, 2291-2298.
67. Shin, L. & Handwerger, K. (2009) Is posttraumatic stress disorder a stress-induced fear circuitry disorder? J. Trauma. Stress, 22, 409-415.
68. Silva, A.C. & Bock, N.A. (2008) Manganese-enhanced MRI: an exceptional tool in translational neuroimaging. Schizophrenia Bull., 34, 595-604.
69. Silva, A.C., Lee, J.H., Aoki, I. & Koretsky, A.P. (2004) Manganese-enhanced magnetic resonance imaging (MEMRI): methodological and practical considerations. NMR Biomed., 17, 532-543.
70. Sled, J.G., Zijdenbos, A.P. & Evans, A.C. (1998) A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE T. Med. Imaging, 17, 87-97.
71. Sripada, R., King, A., Garfinkel, S., Wang, X., Sripanda, C., Welsh, R. & Liberzon, I. (2012) Altered resting-state amygdala functional connectivity in men with posttraumatic stress disorder. J. Psychiatr. Neurosci., 37, 241-249.
72. Thompson, B., Erickson, K., Schulkin, J. & Rosen, J.B. (2004) Corticosterone facilitates retention of contextually conditioned fear and increases CRH mRNA expression in the amygdala. Behav. Brain Res., 149, 209-215.
73. Tryon, W. (1999) A bidirectional associative memory explanation of posttraumatic stress disorder. Clin. Psychol. Rev., 19, 789-818.
74. Veer, I., Beckman, C., van Tol, M., Ferrarini, L., Milles, J., Veltman, D., Aleman, A., van Buchem, M.A., van der Wee, N. & Rombouts, S. (2010) Whole brain resting-state analysis reveals decreased functional connectivity in major depression. Front. Syst. Neurosci., 4, 1-10.
75. Veer, I., Oei, N., Spinhoven, P., van Buchem, M., Elzinga, B. & Rombouts, S. (2012) Endogenous cortisol is associated with functional connectivity between the amygdala and prefrontal cortex. Psychoneuroendocrino., 37, 1039-1047.
76. Wang, S.H., de Oliveira Alvares, L. & Nader, K. (2009) Cellular and systems mechanisms of memory strength as a constraint on auditory fear reconsolidation. Nat. Neurosci., 12, 905-912.
77. Wasserman, D., Wasserman, J. & Sokolowski, M. (2010) Genetics of HPA-axis, depression and suicidality. Eur. Psychiat., 25, 278-280.
78. Wichers, M., Myin-Germeys, I., Jacobs, N., Kenis, G., Derom, C., Vlietinck, R., Delespaul, P., Mengelers, R., Peeters, F., Nicolson, N. & Van Os, J. (2008) Susceptibility to depression expressed as alterations in cortisol day curve: a cross-twin, cross-trait study. Psychosom. Med., 70, 314-318.
79. Zheng, Q., Johnson, K. & Erway, L. (1999) Assessment of hearing in 80 inbred strains of mice by ABR threshold analysis. Hearing Res., 130, 94-107.
80. Zhou, M., Bakker, E., Velzing, E., Berger, S., Oitzl, M.S., Joels, M. & Krugers, H. (2010) Both mineralocorticoid and glucocorticoid receptors regulate emotional memory in mice. Neurobiol. Learn. Mem., 94, 530-537.