Impaired Pavlovian fear extinction is a common phenotype across genetic lineages of the 129 inbred mouse strain

Genes, Brain and Behavior

Volumn 8, Issue 8, 2009, Pages 744-752

  Camp, M ^a   Norcross, M ^a   Whittle, N ^b   Feyder, M ^a   D'Hanis, W ^c   Yilmazer Hanke, D ^b,d   Singewald, N ^b   Holmes, A ^a  

^a NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

^b INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^c OTTO VON GUERICKE UNIVERSITY   (Germany)

^d UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

Amygdala; Anxiety; Behavior; Gene; Genetics; Incubation; Prefrontal cortex; PTSD; Rodent; Sensitization

Indexed keywords

129 MOUSE; AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; C57BL 6 MOUSE; CONDITIONING; CONTROLLED STUDY; EVOKED RESPONSE; FEAR; GENETIC LINE; HABITUATION; MALE; MOUSE; NONHUMAN; PHENOTYPE; PREFRONTAL CORTEX; PRIORITY JOURNAL; REINFORCEMENT; SPECIES DIFFERENCE; STRAIN DIFFERENCE; STRAIN IDENTIFICATION;

ACOUSTIC STIMULATION; ANIMALS; AVOIDANCE LEARNING; BRAIN CHEMISTRY; CONDITIONING (PSYCHOLOGY); EXTINCTION, PSYCHOLOGICAL; FEAR; GENETIC VARIATION; GENOME; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED STRAINS; NEUROPSYCHOLOGICAL TESTS; PHENOTYPE; SPECIES SPECIFICITY;

RODENTIA;

EID: 70449396805     PISSN: 16011848     EISSN: 1601183X     Source Type: Journal    
DOI: 10.1111/j.1601-183X.2009.00519.x     Document Type: Article

References (47)

1. Adams, D.J., Dermitzakis, E.T., Cox, T., Smith, J., Davies, R., Banerjee, R., Bonfield, J., Mullikin, J.C., Chung, Y.J., Rogers, J. & Bradley, A. (2005) Complex haplotypes, copy number polymorphisms and coding variation in two recently divergent mouse strains. Nat Genet 37, 532 536.
2. Balogh, S.A. & Wehner, J.M. (2003) Inbred mouse strain differences in the establishment of long-term fear memory. Behav Brain Res 140, 97 106.
3. Blanchard, R.J. & Blanchard, D.C. (1969) Crouching as an index of fear. J Comp Physiol Psychol 67, 370 375.
4. Bolivar, V.J., Pooler, O. & Flaherty, L. (2001) Inbred strain variation in contextual and cued fear conditioning behavior. Mamm Genome 12, 651 656.
5. Bothe, G.W., Bolivar, V.J., Vedder, M.J. & Geistfeld, J.G. (2004) Genetic and behavioral differences among five inbred mouse strains commonly used in the production of transgenic and knockout mice. Genes Brain Behav 3, 149 157.
6. Bothe, G.W., Bolivar, V.J., Vedder, M.J. & Geistfeld, J.G. (2005) Behavioral differences among fourteen inbred mouse strains commonly used as disease models. Comp Med 55, 326 334.
7. Cain, C.K., Blouin, A.M. & Barad, M. (2003) Temporally massed CS presentations generate more fear extinction than spaced presentations. J Exp Psychol Anim Behav Process 29, 323 333.
8. Cook, M.N., Bolivar, V.J., McFadyen, M.P. & Flaherty, L. (2002) Behavioral differences among 129 substrains: implications for knockout and transgenic mice. Behav Neurosci 116, 600 611.
9. Crawley, J.N., Belknap, J.K., Collins, A., Crabbe, J.C., Frankel, W., Henderson, N., Hitzemann, R.J., Maxson, S.C., Miner, L.L., Silva, A.J., Wehner, J.M., Wynshaw-Boris, A. & Paylor, R. (1997) Behavioral phenotypes of inbred mouse strains: implications and recommendations for molecular studies. Psychopharmacology (Berl) 132, 107 124.
10. Crusio, W.E., Goldowitz, D., Holmes, A. & Wolfer, D. (2008) Standards for the publication of mouse mutant studies. Genes Brain Behav 8, 1 4.
11. Cryan, J.F. & Holmes, A. (2005) The ascent of mouse: advances in modelling human depression and anxiety. Nat Rev Drug Discov 4, 775 790.
12. Evans, M.J. & Kaufman, M.H. (1981) Establishment in culture of pluripotential cells from mouse embryos. Nature 292, 154 156.
13. Eysenck, H.J. (1968) A theory of the incubation of anxiety-fear responses. Behav Res Ther 6, 309 321.
14. Festing, M.F., Simpson, E.M., Davisson, M.T. & Mobraaten, L.E. (1999) Revised nomenclature for strain 129 mice. Mamm Genome 10, 836.
15. Hefner, K. & Holmes, A. (2007) Ontogeny of fear-, anxiety- and depression-related behavior across adolescence in C57BL/6J mice. Behav Brain Res 176, 210 215.
16. Hefner, K., Whittle, N., Juhasz, J., Norcross, M., Karlsson, R.M., Saksida, L.M., Bussey, T.J., Singewald, N. & Holmes, A. (2008) Impaired fear extinction learning and cortico-amygdala circuit abnormalities in a common genetic mouse strain. J Neurosci 28, 8074 8085.
17. Herry, C. & Mons, N. (2004) Resistance to extinction is associated with impaired immediate early gene induction in medial prefrontal cortex and amygdala. Eur J Neurosci 20, 781 790.
18. Holmes, A. & Wellman, C.L. (2009) Stress-induced prefrontal reorganization and executive dysfunction in rodents. Neurosci Biobehav Rev 33, 773 783.
19. Holmes, A., Wrenn, C.C., Harris, A.P., Thayer, K.E. & Crawley, J.N. (2002) Behavioral profiles of inbred strains on novel olfactory, spatial and emotional tests for reference memory in mice. Genes Brain Behav 1, 55 69.
20. Holt, D.J., Lebron-Milad, K., Milad, M.R., Rauch, S.L., Pitman, R.K., Orr, S.P., Cassidy, B.S., Walsh, J.P. & Goff, D.C. (2008) Extinction memory is impaired in schizophrenia. BiolPsychiatry 65, 455 463.
21. Hymowitz, N. (1973) Comparisons between variable-interval and fixed-interval schedules of electric shock delivery. J Exp Anal Behav 19, 101 111.
22. Kamprath, K., Marsicano, G., Tang, J., Monory, K., Bisogno, T., Di Marzo, V., Lutz, B. & Wotjak, C.T. (2006) Cannabinoid CB1 receptor mediates fear extinction via habituation-like processes. J Neurosci 26, 6677 6686.
23. Kamprath, K. & Wotjak, C.T. (2004) Nonassociative learning processes determine expression and extinction of conditioned fear in mice. Learn Mem 11, 770 786.
24. Karlsson, R.M., Holmes, A., Heilig, M. & Crawley, J.N. (2005) Anxiolytic-like actions of centrally-administered neuropeptide Y, but not galanin, in C57BL/6J mice. Pharmacol Biochem Behav 80, 427 436.
25. Kendler, K.S. (2001) Twin studies of psychiatric illness: an update. Arch Gen Psychiatry 58, 1005 1014.
26. Koike, H., Arguello, P.A., Kvajo, M., Karayiorgou, M. & Gogos, J.A. (2006) Disc1 is mutated in the 129S6/SvEv strain and modulates working memory in mice. Proc Natl Acad Sci U S A 103, 3693 3697.
27. McSweeney, F.K. & Swindell, S. (2002) Common processes may contribute to extinction and habituation. J Gen Psychol 129, 364 400.
28. Myers, K.M. & Davis, M. (2007) Mechanisms of fear extinction. Mol Psychiatry 12, 120 150.
29. Nguyen, P.V., Abel, T., Kandel, E.R. & Bourtchouladze, R. (2000) Strain-dependent differences in LTP and hippocampus-dependent memory in inbred mice. Learn Mem 7, 170 179.
30. Norcross, M., Mathur, P., Enoch, A.J., Karlsson, R.M., Brigman, J.L., Cameron, H.A., Harvey-White, J. & Holmes, A. (2008) Effects of adolescent fluoxetine treatment on fear-, anxiety- or stress-related behaviors in C57BL/6J or BALB/cJ mice. Psychopharmacology (Berl) 200, 413 424.
31. Owen, E.H., Logue, S.F., Rasmussen, D.L. & Wehner, J.M. (1997) Assessment of learning by the Morris water task and fear conditioning in inbred mouse strains and F1 hybrids: implications of genetic background for single gene mutations and quantitative trait loci analyses. Neuroscience 80, 1087 1099.
32. Pavlov, I.P. (1927) Conditioned Reflexes. Oxford University Press, London.
33. Pickens, C.L., Golden, S.A., Adams-Deutsch, T., Nair, S.G. & Shaham, Y. (2009) Long-lasting incubation of conditioned fear in rats. Biol Psychiatry 65, 881 886.
34. Ponder, C.A., Kliethermes, C.L., 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.
35. Ponnusamy, R., Nissim, H.A. & Barad, M. (2005) Systemic blockade of D2-like dopamine receptors facilitates extinction of conditioned fear in mice. Learn Mem 12, 399 406.
36. Quirk, G.J. & Mueller, D. (2008) Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 33, 56 72.
37. Schimanski, L.A. & Nguyen, P.V. (2005) Mouse models of impaired fear memory exhibit deficits in amygdalar LTP. Hippocampus 15, 502 517.
38. Siegmund, A., Langnaese, K. & Wotjak, C.T. (2005) Differences in extinction of conditioned fear in C57BL/6 substrains are unrelated to expression of alpha-synuclein. Behav Brain Res 157, 291 298.
39. Simpson, E.M., Linder, C.C., Sargent, E.E., Davisson, M.T., Mobraaten, L.E. & Sharp, J.J. (1997) Genetic variation among 129 substrains and its importance for targeted mutagenesis in mice. Nat Genet 16, 19 27.
40. Sotres-Bayon, F., Corcoran, K.A., Peters, J. & Sierra-Mercado, D. (2008) Neural correlates of individual variability in fear extinction. J Neurosci 28, 12147 12149.
41. Thomas, K.R. & Capecchi, M.R. (1987) Site-directed mutagenesis by gene targeting in mouse embryo-derived stem cells. Cell 51, 503 512.
42. Threadgill, D.W., Yee, D., Matin, A., Nadeau, J.H. & Magnuson, T. (1997) Genealogy of the 129 inbred strains: 129/SvJ is a contaminated inbred strain. Mamm Genome 8, 390 393.
43. Vidal-Gonzalez, I., Vidal-Gonzalez, B., Rauch, S.L. & Quirk, G.J. (2006) Microstimulation reveals opposing influences of prelimbic and infralimbic cortex on the expression of conditioned fear. Learn Mem 13, 728 733.
44. Wade, C.M. & Daly, M.J. (2005) Genetic variation in laboratory mice. Nat Genet 37, 1175 1180.
45. Wahlsten, D. (1982) Deficiency of corpus callosum varies with strain and supplier of the mice. Brain Res 239, 329 347.
46. Wolfer, D.P., Crusio, W.E. & Lipp, H.P. (2002) Knockout mice: simple solutions to the problems of genetic background and flanking genes. Trends Neurosci 25, 336 340.
47. Wolfer, D.P., Muller, U., Stagliar, M. & Lipp, H.P. (1997) Assessing the effects of the 129/Sv genetic background on swimming navigation learning in transgenic mutants: a study using mice with a modified beta-amyloid precursor protein gene. Brain Res 771, 1 13.