Effects of environmental and physiological covariates on sex differences in unconditioned and conditioned anxiety and fear in a large sample of genetically heterogeneous (N/Nih-HS) rats

Behavioral and Brain Functions

Volumn 7, Issue , 2011, Pages

  López Aumatell, Regina ^a   Martínez Membrives, Esther ^b   Vicens Costa, Elia ^b   Cañete, Toni ^b   Blázquez, Gloria ^b   Mont Cardona, Carme ^b   Johannesson, Martina ^a   Flint, Jonathan ^a   Tobeña, Adolf ^b   Fernández Teruel, Alberto ^b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

Author keywords

Anxiety; Environmental covariates; Fear; Genetically heterogeneous rats; Large samples; Physiological covariates

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; AVOIDANCE BEHAVIOR; BODY WEIGHT; CONDITIONING; ENVIRONMENTAL FACTOR; FEAR; FEMALE; GENOME; MALE; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE TRAIT LOCUS; RAT; SEX DIFFERENCE; ANALYSIS OF VARIANCE; ANIMAL; BEHAVIOR GENETICS; CHROMOSOME MAP; GENETICS; GENOTYPE ENVIRONMENT INTERACTION; PHYSIOLOGY;

ANALYSIS OF VARIANCE; ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; CHROMOSOME MAPPING; CONDITIONING (PSYCHOLOGY); FEAR; FEMALE; GENE-ENVIRONMENT INTERACTION; GENETICS, BEHAVIORAL; MALE; QUANTITATIVE TRAIT LOCI; RATS; SEX FACTORS;

EID: 84855610073     PISSN: None     EISSN: 17449081     Source Type: Journal    
DOI: 10.1186/1744-9081-7-48     Document Type: Article

References (32)

1. Crabbe JC, Wahlsten D, Dudek BC. Genetics of mouse behaviour: interactions with laboratory environment. Science 1999, 284(5420):1670-1672. 10.1126/science.284.5420.1670, 10356397.
2. Chesler EJ, Wilson SG, Lariviere WR, Rodriguez-Zas SL, Mogil JS. Influences of laboratory environment on behaviour. Nat Neurosci 2002, 5(11):1101-1102. 10.1038/nn1102-1101, 12403996.
3. Mandillo S, Tucci V, Hölter SM, Meziane H, Banchaabouchi MA, Kallnik M, Lad HV, Nolan PM, Ouagazzal AM, Coghill EL, Gale K, Golini E, Jacquot S, Krezel W, Parker A, Riet F, Schneider I, Marazziti D, Auwerx J, Brown SD, Chambon P, Rosenthal N, Tocchini-Valentini G, Wurst W. Reliability, robustness, and reproducibility in mouse behavioral phenotyping: a cross-laboratory study. Physiol Genomics 2008, 34(3):243-255. 10.1152/physiolgenomics.90207.2008, 2519962, 18505770.
4. Milad MR, Igoe SA, Lebron-Milad K, Novales JE. Estrous cycle phase and gonadal hormones influence conditioned fear extinction. Neuroscience 2009, 164(3):887-895. 10.1016/j.neuroscience.2009.09.011, 2783784, 19761818.
5. Tucci V, Lad HV, Parker A, Polley S, Brown SD, Nolan PM. Gene-environment interactions differentially affect mouse strain behavioral parameters. Mamm Genome 2006, 17(11):1113-1120. 10.1007/s00335-006-0075-x, 17091318.
6. Valdar W, Solberg LC, Gauguier D, Cookson WO, Rawlins JNP, Mott R, Flint J. Genetic and environmental effects on complex traits in mice. Genetics 2006, 174:959-984. 10.1534/genetics.106.060004, 1602068, 16888333.
7. Valdar W, Solberg LC, Gauguier D, Burnett S, Klenerman P, Cookson WO, Taylor MS, Rawlins JN, Mott R, Flint J. Genome-wide genetic association of complex traits in heterogeneous stock mice. Nat Genet 2006, 38(8):879-887. 10.1038/ng1840, 16832355.
8. Plomin R. The role of inheritance in behaviour. Science 1990, 248:183-188. 10.1126/science.2183351, 2183351.
9. Thomas D. Methods for investigating gene-environment interactions in candidate pathway and genome-wide association studies. Annu Rev Public Health 2010, 31:21-36. 10.1146/annurev.publhealth.012809.103619, 2847610, 20070199.
10. Solberg LC, Valdar W, Gauguier D, Nunez G, Taylor A, Burnett S, Arboledas-Hita C, Hernandez-Pliego P, Davidson S, Burns P, Bhattacharya S, Hough T, Higgs D, Klenerman P, Cookson WO, Zhang Y, Deacon RM, Rawlins JN, Mott R, Flint J. A protocol for high-throughput phenotyping, suitable for quantitative trait analysis in mice. Mamm Genome 2006, 17(2):129-146. 10.1007/s00335-005-0112-1, 16465593.
11. Mott R, Flint J. Simultaneous detection and fine mapping of quantitative trait loci in mice using heterogeneous stocks. Genetics 2002, 160(4):1609-1618. 1462050, 11973314.
12. Johannesson M, Lopez-Aumatell R, Stridh P, Diez M, Tuncel J, Blázquez G, Martinez-Membrives E, Cañete T, Vicens-Costa E, Graham D, Copley RR, Hernandez-Pliego P, Beyeen AD, Ockinger J, Fernández-Santamaría C, Gulko PS, Brenner M, Tobeña A, Guitart-Masip M, Giménez-Llort L, Dominiczak A, Holmdahl R, Gauguier D, Olsson T, Mott R, Valdar W, Redei EE, Fernández-Teruel A, Flint J. A resource for the simultaneous high-resolution mapping of multiple quantitative trait loci in rats: the NIH heterogeneous stock. Genome Res 2008, 19(1):150-158. 10.1101/gr.081497.108, 2612958, 18971309.
13. Aitman TJ, Critser JK, Cuppen E, Dominiczak A, Fernandez-Suarez XM, Flint J, Gauguier D, Geurts AM, Gould M, Harris PC, Holmdahl R, Hubner N, Izsvák Z, Jacob HJ, Kuramoto T, Kwitek AE, Marrone A, Mashimo T, Moreno C, Mullins J, Mullins L, Olsson T, Pravenec M, Riley L, Saar K, Serikawa T, Shull JD, Szpirer C, Twigger SN, Voigt B, Worley K. Progress and prospects in rat genetics: a community view. Nat Genet 2008, 40(5):516-522. 10.1038/ng.147, 18443588.
14. Hansen C, Spuhler K. Development of the National Institutes of Health genetically heterogeneous rat stock. Alcohol Clin Exp Res 1984, 8(5):477-479. 10.1111/j.1530-0277.1984.tb05706.x, 6391259.
15. Aguilar R, Gil L, Flint J, Gray JA, Dawson GR, Driscoll P, Giménez-Llort L, Escorihuela RM, Fernández-Teruel A, Tobeña A. Learned fear, emotional reactivity and fear of heights: a factor analytic map from a large F(2) intercross of Roman rat strains. Brain Res Bull 2002, 57(1):17-26. 10.1016/S0361-9230(01)00632-3, 11827733.
16. Fernández-Teruel A, Escorihuela RM, Núñez JF, Zapata A, Boix F, Salazar W, Tobeña A. The early acquisition of two-way (shuttle-box) avoidance as an anxiety-mediated behaviour: psychopharmacological validation. Brain Res Bull 1991, 26(1):173-176. 10.1016/0361-9230(91)90205-X, 1673080.
17. Fernández-Teruel A, Escorihuela RM, Gray JA, Aguilar R, Gil L, Giménez-Llort L, Tobeña A, Bhomra A, Nicod A, Mott R, Driscoll P, Dawson GR, Flint J. A quantitative trait locus influencing anxiety in the laboratory rat. Genome Res 2002, 12(4):618-626. 187519, 11932246.
18. Gray JA, McNaughton N. The neuropsychology of anxiety: an enquiry into the functions of the septo-hippocampal system 2000, Oxford: Oxford University Press.
19. Lopez-Aumatell R, Guitart-Masip M, Vicens-Costa E, Gimenez-Llort L, Valdar W, Johannesson M, Flint J, Tobeña A, Fernández-Teruel A. Fearfulness in a large N/Nih genetically heterogeneous rat stock: differential profiles of timidity and defensive flight in males and females. Behav Brain Res 2008, 188(1):41-55. 10.1016/j.bbr.2007.10.015, 18079010.
20. Shepherd JK, Grewal SS, Fletcher A, Bill DJ, Dourish CT. Behavioural and pharmacological characterisation of the elevated "zero-maze" as an animal model of anxiety. Psychopharmacology 1994, 116:56-64. 10.1007/BF02244871, 7862931.
21. Pähkla R, Kask A, Rägo L. Differential effects of beta-carbolines and antidepressants on rat exploratory activity in the elevated zero-maze. Pharmacol Biochem Behav 2000, 65(4):737-742. 10.1016/S0091-3057(99)00265-8, 10764931.
22. Aguilar R, Gil L, Gray JA, Driscoll P, Flint J, Dawson GR, Giménez-Llort L, Escorihuela RM, Fernández-Teruel A, Tobeña A. Fearfulness and sex in F2 Roman rats: males display more fear though both sexes share the same fearfulness traits. Physiol Behav 2003, 78(4-5):723-732. 10.1016/S0031-9384(03)00043-X, 12782229.
23. Lopez-Aumatell R, Vicens-Costa E, Guitart-Masip M, Martínez-Membrives E, Valdar W, Johannesson M, Cañete T, Blázquez G, Driscoll P, Flint J, Tobeña A, Fernández-Teruel A. Unlearned anxiety predicts learned fear: a comparison among heterogeneous rats and the Roman rat strains. Behav Brain Res 2009, 202(1):92-101. 10.1016/j.bbr.2009.03.024, 19447285.
24. Vicens-Costa E, Martínez-Membrives E, López-Aumatell R, Guitart-Masip M, Cañete T, Blázquez G, Tobeña A, Fernández-Teruel A. Two-way avoidance acquisition is negatively related to conditioned freezing and positively associated with startle reactions: A dissection of anxiety and fear in genetically heterogeneous rats. Physiol Behav 2011, 103(2):148-156. 10.1016/j.physbeh.2010.12.009, 21163279.
25. Davis M, Whalen PJ. The amygdala: vigilance and emotion. Mol Psychiatry 2001, 6(1):13-34. 10.1038/sj.mp.4000812, 11244481.
26. LeDoux Emotion circuits in the brain. Annu Rev Neurosci 2000, 23:155-184. 10.1146/annurev.neuro.23.1.155, 10845062, LeDoux.
27. Fernandes C, González MI, Wilson CA, File SE. Factor analysis shows that female rat behavior is characterised primarily by activity, male rats are driven by sex and anxiety. Pharmacol Biochem Behav 1999, 64:731-738. 10.1016/S0091-3057(99)00139-2, 10593196.
28. Van der Staay FJ. Shift in the performance of 24-month-old Wistar rats in the Morris water escape task: a comparison across 36 experiments. Behav Brain Res 1997, 87(2):213-222. 10.1016/S0166-4328(97)02284-5, 9331490.
29. Cabib S, Orsini C, Le Moal M, Piazza PV. Abolition and reversal of strain differences in behavioural responses to drugs of abuse after a brief experience. Science 2000, 289(5478):463-465. 10.1126/science.289.5478.463, 10903209.
30. Munafò MR, Flint J. Replication and heterogeneity in gene X environment interaction studies. Int J Neuropsychopharmacol 2009, 12(6):727-729. 10.1017/S1461145709000479, 19476681.
31. Flint J, Valdar W, Shifman S, Mott R. Strategies for mapping and cloning quantitative trait genes in rodents. Nat Rev Genet 2005, 6(4):271-286. 10.1038/nrg1576, 15803197.
32. Flint J, Mackay TFC. Genetic architecture of quantitative traits in mice, flies, and humans. Genome Res 2010, 19:723-733.