Selection for contextual fear conditioning affects anxiety-like behaviors and gene expression

Genes, Brain and Behavior

Volumn 6, Issue 8, 2007, Pages 736-749

  Ponder, C A ^a   Kliethermes, C L ^b   Drew, M R ^a   Muller, J ^a,c   Das, K ^d   Risbrough, V B ^e   Crabbe, J C ^f   Gilliam, T Conrad ^g   Palmer, A A ^g  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b UNIVERSITY OF CALIFORNIA SAN FRANCISCO   (United States)

^c NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

^d Taub Institute for Research on Alzheimer's Disease and the Aging Brain and the Gertrude H Sergievsky Center   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

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

^g UNIVERSITY OF CHICAGO   (United States)

Author keywords

Anxiety; Behavioral genetics; Contextual fear conditioning; Correlated traits; Emotionality; Gene expression; Selective breeding

Indexed keywords

CIS ACTING ELEMENT;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; BEHAVIOR; BEHAVIOR GENETICS; CHROMOSOME; CONDITIONING; CONTROLLED STUDY; CORRELATION ANALYSIS; EMOTIONALITY; FEAR; FEAR CONDITIONING; FEMALE; FOOTSHOCK; GENE CONSTRUCT; GENE EXPRESSION; GENE IDENTIFICATION; GENETIC DIFFERENCE; GENETIC IDENTIFICATION; GENETIC SELECTION; HIPPOCAMPUS; LEARNING; MALE; MAZE TEST; MOLECULAR PHYLOGENY; NONHUMAN; OPEN FIELD TEST; PRIORITY JOURNAL; QUANTITATIVE TRAIT LOCUS; SENSITIVITY ANALYSIS; STARTLE REFLEX; TASK PERFORMANCE; VALIDITY;

AMYGDALA; ANIMALS; ANXIETY; ASSOCIATION LEARNING; CONDITIONING, CLASSICAL; ENVIRONMENT; FEAR; FEMALE; FREEZING REACTION, CATALEPTIC; GENE EXPRESSION REGULATION; GENE FREQUENCY; HIPPOCAMPUS; MALE; MAZE LEARNING; MICE; MICE, INBRED STRAINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; QUANTITATIVE TRAIT LOCI; SELECTION (GENETICS); SPECIES SPECIFICITY; STARTLE REACTION;

EID: 34250188967     PISSN: 16011848     EISSN: 1601183X     Source Type: Journal    
DOI: 10.1111/j.1601-183X.2007.00306.x     Document Type: Article

References (61)

1. Baldi, E., Lorenzini, C.A. Bucherelli, C 2004) Footshock intensity and generalization in contextual and auditory-cued fear conditioning in the rat. Neurobiol Learn Mem 81, 162 166.
2. Belknap, J.K., Richards, S.P., O'Toole, L.A., Helms, M.L. Phillips, T.J 1997) Short-term selective breeding as a tool for QTL mapping: ethanol preference drinking in mice. Behav Genet 27, 55 66.
3. Bignami, G 1965) Selection for high rates and low rates of avoidance conditioning in the rat. Anim Behav 13, 221 227.
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. Broadhurst, P.L 1975) The Maudsley reactive and nonreactive strains of rats: a survey. Behav Genet 5, 299 319.
6. Caldarone, B., Saavedra, C., Tartaglia, K., Wehner, J.M., Dudek, B.C. Flaherty, L 1997) Quantitative trait loci analysis affecting contextual conditioning in mice [see comments]. Nat Genet 17, 335 337.
7. Cierpial, M.A., Murphy, C.A. McCarty, R 1990) Maternal behavior of spontaneously hypertensive and Wistar-Kyoto normotensive rats: effects of reciprocal cross-fostering of litters. Behav Neural Biol 54, 90 96.
8. Crabbe, J.C 1989) Genetic animal models in the study of alcoholism. Alcohol Clin Exp Res 13, 120 127.
9. Crabbe, J.C., Jr., Johnson, N.A., Gray, D.K., Kosobud, A. Young, E.R 1982) Biphasic effects of ethanol on open-field activity: sensitivity and tolerance in C57BL/6N and DBA/2N mice. J Comp Physiol Psychol 96, 440 451.
10. Crabbe, J.C., Young, E.R., Deutsch, C.M., Tam, B.R. Kosobud, A 1987) Mice genetically selected for differences in open-field activity after ethanol. Pharmacol Biochem Behav 27, 577 581.
11. Crawley, J. Goodwin, F.K 1980) Preliminary report of a simple animal behavior model for the anxiolytic effects of benzodiazepines. Pharmacol Biochem Behav 13, 167 170.
12. Davis, M 1979a) Diazepam and flurazepam: effects on conditioned fear as measured with the potentiated startle paradigm. Psychopharmacology (Berl) 62, 1 7.
13. Davis, M 1979b) Morphine and naloxone: effects on conditioned fear as measured with the potentiated startle paradigm. Eur J Pharmacol 54, 341 347.
14. Davis, M 1992) The role of the amygdala in fear-potentiated startle: implications for animal models of anxiety. Trends Pharmacol Sci 13, 35 41.
15. DeFries, J.C., Gervais, M.C. Thomas, E.A 1978) Response to 30 generations of selection for open-field activity in laboratory mice. Behav Genet 8, 3 13.
16. Dichter, G.S., Brunelli, S.A. Hofer, M.A 1996) Elevated plus-maze behavior in adult offspring of selectively bred rats. Physiol Behav 60, 299 304.
17. Ellenbroek, B.A., Sluyter, F. Cools, A.R 2000) The role of genetic and early environmental factors in determining apomorphine susceptibility. Psychopharmacology (Berl) 148, 124 131.
18. Falconer, D.S. Mackay, T.F.C 1996) Introduction to Quantitative Genetics, 4th Edn. Longman, Essex, UK.
19. Falls, W.A., Carlson, S., Turner, J.G. Willott, J.F 1997) Fear-potentiated startle in two strains of inbred mice. Behav Neurosci 111, 855 861.
20. Fernández-Teruel, A., Escorihuela, R.M., Gray, J.A., Aguilar, R., Gil, L., Gimâenez-Llort, L., Tobeäna, A., Bhomra, A., Nicod, A., Mott, R., Driscoll, P., Dawson, G.R. Flint, J 2002) A quantitative trait locus influencing anxiety in the laboratory rat. Genome Res 12, 618 626.
21. Flint, J., Corley, R., DeFries, J.C., Fulker, D.W., Gray, J.A., Miller, S. Collins, A.C 1995) A simple genetic basis for a complex psychological trait in laboratory mice. Science 269, 1432 1435.
22. Francis, D., Diorio, J., Liu, D. Meaney, M.J 1999) Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 286, 1155 1158.
23. Gallistel, C.R., Fairhurst, S. Balsam, P 2004) The learning curve: implications of a quantitative analysis. Proc Natl Acad Sci USA 101, 13124 13131.
24. Gentleman, R.C., Carey, V.J., Bates, D.M., et al 2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5, R80.
25. Grillon, C., Dierker, L. Merikangas, K.R 1998) Fear-potentiated startle in adolescent offspring of parents with anxiety disorders. Biol Psychiatry 44, 990 997.
26. Hall, C.S 1934) Emotional Behavior in the Rat I. Defecation and urination as measures of individual differences in emotionality. J Comp Psychol 18, 385 403.
27. Hettema, J.M., Annas, P., Neale, M.C., Kendler, K.S. Fredrikson, M 2003) A twin study of the genetics of fear conditioning. Arch Gen Psychiatry 60, 702 708.
28. Irizarry, R.A., Hobbs, B., Collin, F., Beazer-Barclay, Y.D., Antonellis, K.J., Scherf, U. Speed, T.P 2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4, 249 264.
29. Kamprath, K. Wotjak, C.T 2004) Nonassociative learning processes determine expression and extinction of conditioned fear in mice. Learn Mem 11, 770 786.
30. Kliethermes, C.L., Cronise, K. Crabbe, J.C 2004) Anxiety-like behavior in mice in two apparatuses during withdrawal from chronic ethanol vapor inhalation. Alcohol Clin Exp Res 28, 1012 1019.
31. Kosten, T.A., Miserendino, M.J., Bombace, J.C., Lee, H.J. Kim, J.J 2005) Sex-selective effects of neonatal isolation on fear conditioning and foot shock sensitivity. Behav Brain Res 157, 235 244.
32. Kromer, S.A., Kessler, M.S., Milfay, D., Birg, I.N., Bunck, M., Czibere, L., Panhuysen, M., Putz, B., Deussing, J.M., Holsboer, F., Landgraf, R. Turck, C.W 2005) Identification of glyoxalase-I as a protein marker in a mouse model of extremes in trait anxiety. J Neurosci 25, 4375 4384.
33. LaBar, K.S., LeDoux, J.E., Spencer, D.D. Phelps, E.A 1995) Impaired fear conditioning following unilateral temporal lobectomy in humans. J Neurosci 15, 6846 6855.
34. Laxmi, T.R., Stork, O. Pape, H.C 2003) Generalisation of conditioned fear and its behavioural expression in mice [erratum appears in Behav Brain Res. 2994 May 5;141(1-2):337]. Behav Brain Res 145, 89 98.
35. LeDoux, J.E 2000) Emotion circuits in the brain. Annu Rev Neurosci 23, 155 184.
36. Liebsch, G., Montkowski, A., Holsboer, F. Landgraf, R 1998) Behavioural profiles of two Wistar rat lines selectively bred for high or low anxiety-related behaviour. Behav Brain Res 94, 301 310.
37. Lissek, S., Powers, A.S., McClure, E.B., Phelps, E.A., Woldehawariat, G., Grillon, C. Pine, D.S 2005) Classical fear conditioning in the anxiety disorders: a meta-analysis. Behav Res Ther 43, 1391 1424.
38. McCaughran, J.A., Jr., Bell, J., 3rd. Hitzemann, R.J 2000) Fear-potentiated startle response in mice: genetic analysis of the C57BL/6J and DBA/2J intercross. Pharmacol Biochem Behav 65, 301 312.
39. McNish, K.A., Gewirtz, J.C. Davis, M 1997) Evidence of contextual fear after lesions of the hippocampus: a disruption of freezing but not fear-potentiated startle. J Neurosci 17, 9353 9360.
40. Meshi, D., Drew, M.R., Saxe, M., Ansorge, M.S., David, D., Santarelli, L., Malapani, C., Moore, H. Hen, R 2006) Hippocampal neurogenesis is not required for behavioral effects of environmental enrichment. Nat Neurosci 9, 729 731.
41. Moldin, S.O 2000) Neurobiology of anxiety and fear: challenges for genomic science of the new millennium. Biol Psychiatry 48, 1144 1146.
42. 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.
43. Palmer, A.A. Phillips, T.J 2002) Effect of forward and reverse selection for ethanol-induced locomotor response on other measures of ethanol sensitivity. Alcohol Clin Exp Res 26, 1322 1329.
44. Palmer, A.A., Verbitsky, M., Suresh, R., Kamens, H.M., Reed, C.L., Li, N., Burkhart-Kasch, S., McKinnon, C.S., Belknap, J.K., Gilliam, T.C. Phillips, T.J 2005) Gene expression differences in mice divergently selected for methamphetamine sensitivity. Mamm Genome 16, 291 305.
45. Paylor, R., Tracy, R., Wehner, J. Rudy, J.W 1994) DBA/2 and C57BL/6 mice differ in contextual fear but not auditory fear conditioning. Behav Neurosci 108, 810 817.
46. Petkov, P.M., Ding, Y., Cassell, M.A., Zhang, W., Wagner, G., Sargent, E.E., Asquith, S., Crew, V., Johnson, K.A., Robinson, P., Scott, V.E. Wiles, M.V 2004) An efficient SNP system for mouse genome scanning and elucidating strain relationships. Genome Res 14, 1806 1811.
47. Radcliffe, R.A., Lowe, M.V. Wehner, J.M 2000) Confirmation of contextual fear conditioning QTLs by short-term selection. Behav Genet 30, 183 191.
48. Ramos, A., Correia, E.C., Izidio, G.S. Bruske, G.R 2003) Genetic selection of two new rat lines displaying different levels of anxiety-related behaviors. Behav Genet 33, 657 668.
49. Richardson, M.P., Strange, B.A. Dolan, R.J 2004) Encoding of emotional memories depends on amygdala and hippocampus and their interactions. Nature Neuroscience 7, 278 285.
50. Risbrough, V.B., Brodkin, J.D. Geyer, M.A 2003) GABA-A and 5-HT1A receptor agonists block expression of fear-potentiated startle in mice. Neuropsychopharmacology 28, 654 663.
51. Santos, J.M., Gâargaro, A.C., Oliveira, A.R., Masson, S. Brandäao, M.L 2005) Pharmacological dissociation of moderate and high contextual fear as assessed by freezing behavior and fear-potentiated startle. Eur Neuropsychopharmacol 15, 239 246.
52. Shumyatsky, G.P., Tsvetkov, E., Malleret, G., Vronskaya, S., Hatton, M., Hampton, L., Battey, J.F., Dulac, C., Kandel, E.R. Bolshakov, V.Y 2002) Identification of a signaling network in lateral nucleus of amygdala important for inhibiting memory specifically related to learned fear. Cell 111, 905 918.
53. Steinberger, D., Reynolds, D.S., Ferris, P., Lincoln, R., Datta, S., Stanley, J., Paterson, A., Dawson, G.R. Flint, J 2003) Genetic mapping of variation in spatial learning in the mouse. J Neurosci 23, 2426 2433.
54. Storey, J.D. Tibshirani, R 2003) Statistical methods for identifying differentially expressed genes in DNA microarrays. Methods Mol Biol 224, 149 157.
55. Talbot, C.J., Radcliffe, R.A., Fullerton, J., Hitzemann, R., Wehner, J.M. Flint, J 2003) Fine scale mapping of a genetic locus for conditioned fear. Mamm Genome 14, 223 230.
56. Valentinuzzi, V.S., Kolker, D.E., Vitaterna, M.H., Shimomura, K., Whiteley, A., Low-Zeddies, S., Turek, F.W., Ferrari, E.A., Paylor, R. Takahashi, J.S 1998) Automated measurement of mouse freezing behavior and its use for quantitative trait locus analysis of contextual fear conditioning in (BALB/cJ x C57BL/6J)F2 mice. Learn Mem 5, 391 403.
57. Verbitsky, M., Yonan, A.L., Malleret, G., Kandel, E.R., Gilliam, T.C. Pavlidis, P 2004) Altered hippocampal transcript profile accompanies an age-related spatial memory deficit in mice. Learn Mem 11, 253 260.
58. Villafuerte, S. Burmeister, M 2003) Untangling genetic networks of panic, phobia, fear and anxiety. Genome Biol 4, 224.
59. Wahlsten, D., Bachmanov, A., Finn, D.A. Crabbe, J.C 2006) Stability of inbred mouse strain differences in behavior and brain size between laboratories and across decades. Proc Natl Acad Sci USA 103, 16364 16369.
60. Walker, D.L. Davis, M 1997) Double dissociation between the involvement of the bed nucleus of the stria terminalis and the central nucleus of the amygdala in startle increases produced by conditioned versus unconditioned fear. J Neurosci 17, 9375 9383.
61. Wehner, J.M., Radcliffe, R.A., Rosmann, S.T., Christensen, S.C., Rasmussen, D.L., Fulker, D.W. Wiles, M 1997) Quantitative trait locus analysis of contextual fear conditioning in mice [see comment]. Nat Genet 17, 331 334.