Unlearned anxiety predicts learned fear: A comparison among heterogeneous rats and the Roman rat strains

Behavioural Brain Research

Volumn 202, Issue 1, 2009, Pages 92-101

  López Aumatell, Regina ^a   Vicens Costa, Elia ^a   Guitart Masip, Marc ^a   Martínez Membrives, Esther ^a   Valdar, William ^b   Johannesson, Martina ^b   Cañete, Toni ^a   Blázquez, Gloria ^a   Driscoll, Peter ^c   Flint, Jonathan ^b   Tobeña, Adolf ^a   Fernández Teruel, Alberto ^a  

^a Institute of Neuroscience   (Spain)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c ETH ZURICH   (Switzerland)

Author keywords

Anxiety; Genetically heterogeneous rats; Inbred Roman rat strains; Learned fear; Two way active avoidance; Unlearned fear

Indexed keywords

ANIMAL EXPERIMENT; ANXIETY; ARTICLE; AVOIDANCE BEHAVIOR; COMPARATIVE STUDY; CONTROLLED STUDY; FEAR; INBRED STRAIN; LEARNING; MALE; MAZE TEST; MYOTATIC REFLEX; NONHUMAN; PRIORITY JOURNAL; RAT; RAT STRAIN; REGRESSION ANALYSIS; RISK ASSESSMENT; STARTLE REFLEX; TASK PERFORMANCE;

ANALYSIS OF VARIANCE; ANIMALS; ANXIETY; AVOIDANCE LEARNING; EXPLORATORY BEHAVIOR; FEAR; MALE; MAZE LEARNING; RATS; RATS, INBRED STRAINS; REACTION TIME; REGRESSION ANALYSIS; RISK ASSESSMENT; SPECIES SPECIFICITY; STARTLE REACTION;

EID: 67349092458     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2009.03.024     Document Type: Article

References (62)

1. Aguilar R., Gil L., Tobeña A., Escorihuela R.M., and Fernandez-Teruel A. Differential effects of cohort removal stress on the acoustic startle response of the Roman/Verh rat strains. Behav Genet 30 (2000) 71-75
2. Aguilar R., Gil L., Flint J., Gray J.A., Dawson G.R., Driscoll P., et al. Learned fear, emotional reactivity and fear of heights: a factor analytic map from a large F2 intercross of Roman rat strains. Brain Res Bull 57 (2002) 17-26
3. Aguilar R., Gil L., Fernandez-Teruel A., and Tobeña A. Genetically-based behavioral traits influence the effects of shuttle box avoidance overtraining and extinction upon intertrial responding: a study with the Roman rat strains. Behav Process 66 (2004) 63-72
4. Carrasco J., Márquez C., Nadal R., Tobeña A., Fernandez-Teruel A., and Armario A. Characterization of central and peripheral components of the hypothalamus-pituitary-adrenal axis in the inbred Roman rat strains. Psychoneuroendocrinology 33 (2008) 437-445
5. Corda M.G., Piras G., Valentini V., Scano P., and Giorgi O. Differential sensitivity to shock-induced suppression of drinking in the Roman/Verh lines and strains of rats. Soc Neurosci Abs 24 (1998) 1182
6. Davis M., Falls W.A., Campeau S., and Kim M. Fear-potentiated startle: a neural and pharmacological analysis. Behav Brain Res 58 (1993) 175-198
7. Draski L.J., Spuhler K.P., Erwin V.G., Baker R.C., and Deitrich R.A. Selective breeding of rats differing in sensitivity to the effects of acute ethanol administration. Alcohol Clin Exp Res 16 (1992) 48-54
8. Driscoll P., and Bättig K. Behavioral, emotional and neurochemical profiles of rats selected for extreme differences in active, two-way avoidance performance. In: Lieblich I. (Ed). Genetics of the brain (1982), Elsevier Biomedical Press, Amsterdam 95-123
9. Driscoll P., Escorihuela R.M., Fernández-Teruel A., Giorgi O., Schwegler H., Steimer T., et al. Genetic selection and differential stress responses. The Roman lines/strains of rats. Ann NY Acad Sci 851 (1998) 501-510
10. Driscoll P., Fernández-Teruel A., Corda M.G., Giorgi O., and Steimer T. Some guidelines for defining personality differences in rats. In: Kim Y.K. (Ed). Handbook of behavior genetics (2009), Springer, New York pp. 281-300
11. Escorihuela R.M., Fernandez-Teruel A., Zapata A., Nuñez J.F., and Tobeña A. Flumazenil prevents the anxiolytic effects diazepam, alprazolam and adinazolam on the early acquisition of two-way active avoidance. Pharmacol Res 28 (1993) 53-58
12. Escorihuela R.M., Tobeña A., Driscoll P., and Fernández-Teruel A. Effects of training, early handling, and perinatal flumazenil on shuttle box acquisition in Roman low-avoidance rats: toward overcoming a genetic deficit. Neurosci Biobehav Rev 19 (1995) 353-367
13. Escorihuela R.M., Fernandez-Teruel A., Tobeña A., Langhans W., Bättig K., and Driscoll P. Labyrinth exploration. Emotional reactivity, and conditioned fear in young Roman/Verh inbred rats. Behav Genet 27 (1997) 573-578
14. Escorihuela R.M., Fernandez-Teruel A., Gil L., Aguilar R., Tobeña A., and Driscoll P. Inbred Roman high- and low-avoidance rats: differences in anxiety, novelty seeking and shuttle box behaviors. Physiol Behav 67 (1999) 19-26
15. Fernandez-Teruel A., Escorihuela R.M., Driscoll P., Tobeña A., and Bättig K. Infantile (handling) stimulation and behavior in young Roman high- and low-avoidance rats. Physiol Behav 50 (1991) 563-565
16. Fernandez-Teruel A., Escorihuela R.M., Nuñez J.F., Zapata A., Boix F., Salazar W., et al. The early acquisition of two-way (shuttle-box) avoidance as an anxiety-mediated behavior: psychopharmacological validation. Brain Res Bull 26 (1991) 173-176
17. Fernandez-Teruel A., Escorihuela R.M., Boix F., and Tobeña A. Effects of different handling-stimulation procedures and benzodiazepines on two-way active avoidance acquisition in rats. Pharmacol Res 24 (1991) 273-282
18. Fernandez-Teruel A., Escorihuela R.M., Tobeña A., and Driscoll P. Stress and putative endogenous ligands for benzodiazepine receptors: The importance of characteristics of the aversive situation and of differential emotionality in experimental animals. Experientia 47 (1991) 1051-1056
19. Fernandez-Teruel A., Escorihuela R.M., Driscoll P., Tobeña A., and Bättig K. Differential effects of early stimulation and/or perinatal flumazenil treatment in young low- and high-avoidance rats. Psychopharmacology 108 (1992) 170-176
20. Fernandez-Teruel A., Escorihuela R.M., Nuñez J.F., Goma M., Driscoll P., and Tobeña A. Early stimulation effects on novelty-induced behavior in two psychogenetically-selected rat lines with divergent emotionality profiles. Neurosci Lett 137 (1992) 185-188
21. Fernandez-Teruel A., Escorihuela R.M., Castellano B., Gonzalez B., and Tobeña A. Neonatal handling and environmental enrichment effects on emotionality, novelty/reward seeking, and age-related cognitive and hippocampal impairments: focus on the Roman rat lines. Behav Genet 6 (1997) 513-526
22. Fernandez-Teruel A., Gimenez-Llort L., Escorihuela R.M., Gil L., Aguilar R., Steimer T., et al. Early-life handling stimulation and environmental enrichment: are some of their effects mediated by similar neural mechanisms?. Pharmacol Biochem Behav 73 (2002) 233-245
23. Fernandez-Teruel A., Escorihuela R.M., Gray J.A., Aguilar R., Gil L., Gimenez-Llort L., et al. A quantitative trait locus influencing anxiety in the laboratory rat. Genome Res 12 (2002) 618-626
24. Ferré P., Fernandez-Teruel A., Escorihuela R.M., Driscoll P., Corda M.G., Giorgi O., et al. Behavior of the Roman/Verh high -and low- avoidance rat lines in anxiety tests: relationship with defecation and self-grooming. Phisiol Behav 58 (1995) 1209-1213
25. Gray J.A., and McNaughton N. The neuropsychology of anxiety: an enquiry into the functions of the septo-hippocampal system. 2nd ed. (2000), Oxford University Press, Oxford
26. Hansen C., and Spuhler K. Development of the National Institutes of Health genetically heterogeneous stock. Alcohol Clin Exp Res 8 (1984) 477-479
27. Josselyn S.A., Falls W.A., Gewirtz J.C., Pistell P., and Davis M. The nucleus accumbens is not critically involved in mediating the effects of a safety signal on behavior. Neuropsychopharmacology 30 (2005) 17-26
28. Kalisch R., Salomé N., Platzer S., Wigger A., Czisch M., Sommer W., et al. High trait anxiety and hyperactivity to stress of the dorsomedial prefrontal cortex: a combined ph MRI AND FOS study in rats. NeuroImage 23 (2004) 382-391
29. Koch L.G., and Britton S.L. Artificial selection for intrinsic aerobic endurance running capacity in rats. Physiol Genom 5 (2001) 45-52
30. Landgraf R., and Wigger A. High vs. low anxiety-related behavior in rats: an animal model of extremes in trait anxiety. Behav Genet 32 (2002) 301-314
31. Landgraf R., and Wigger A. Born to be anxious: neuroendocrine and genetic correlates of trait anxiety in HAB rats. Stress 6 (2003) 111-119
32. Lopez-Aumatell R., Guitart-Masip M., Vicens-Costa E., Gimenez-Llort L., Valdar W., Johannesson M., et al. Fearfulness in a large N/Nih genetically heterogeneous rat stock: Differential profiles of timidity and defensive flight in males and females. Behav Brain Res 188 (2008) 41-55
33. Lopez-Aumatell R., Blazquez G., Gil L., Aguilar R., Cañete T., Gimenez-Llort L., et al. The Roman high- and low-avoidance rat strains differ in fear-potentiated startle and classical aversive conditioning. Psicothema 21 (2009) 27-32
34. McNaughton N., and Gray J.A. Anxiolytic action on the behavioral inhibition system implies multiple types of arousal contribute to anxiety. J Affect Dis 61 (2000) 161-176
35. McNish K.A., Gewirtz J.C., and Davis M. Evidence of contextual fear after lesions of the hippocampus: A disruption of freezing but not fear-potentiated startle. J Neurosci 17 (1997) 9353-9360
36. Mott R., and Flint J. Simultaneous detection and fine mapping of quantitative trait loci using heterogeneous stocks. Genetics 160 (2002) 1609-1618
37. Mott R., Talbot C.J., Turri M.G., Collins A.C., and Flint J. A method for fine mapping quantitative trait loci in outbred animal stocks. Proc Natl Acad Sci USA 97 (2000) 12649-12654
38. Oliveira A.R., Reimer A.E., and Brandao M.L. Dopamine D2 receptor mechanisms in the expression of conditioned fear. Pharmacol Biochem Behav 84 (2006) 102-111
39. Overstreet D.H., Rezvani A.H., Pucilowski O., Gause L., and Janowsky D.S. Rapid selection for serotonin-1A sensitivity in rats. Psychiatr Genet 4 (1994) 57-62
40. Pähkla R., Kask A., and Rägo L. Differential effects of beta-carbolines and antidepressants on rat exploratory activity in the elevated zero-maze. Pharmacol Biochem Behav 65 (2000) 737-742
41. Phillips R.G., and LeDoux J.E. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 106 (1992) 274-285
42. Phillips R.G., and LeDoux J.E. Lesions of the dorsal hippocampal formation interfere with background but no foreground contextual fear conditioning. Learn Mem 1 (1994) 34-44
43. Reis F.L.V., Masson S., Oliveira A.R., and Brandao M.L. Dopaminergic mechanisms in the conditioned and unconditioned fear as assesed by the two-way avoidance and switch-off tests. Pharmacol Biochem Behav 79 (2004) 359-365
44. Rosas J.M., Callejas-Aguilera J.E., Escarabajal M.D., Gómez M.J., de la Torre L., Agüero A., et al. Successive negative contrast effect in instrumental runway behavior: A study with Roman high- (RHA) and Roman low- (RLA) avoidance rats. Behav Brain Res 185 (2007) 1-8
45. Savonenko A., Werka T., Nikolaev E., Zielinski K., and Kaczmarek L. Complex effects of NMDA receptor antagonist AVP in the basolateral amygdala on acquisition of two-way avoidance reaction and long-term fear memory. Learn Mem 10 (2003) 293-303
46. Schultz W. Getting formal with dopamine and reward. Neuron 36 (2002) 241-263
47. Schwegler H., Pilz P.K.D., Koch M., Fendt M., Linke R., and Driscoll P. The acoustic startle response in inbred Roman high- and low-avoidance rats. Behav Genet 27 (1997) 579-582
48. Shepherd J.K., Grewal S.S., Fletcher A., Bill D.J., and Dourish C.T. Behavioral and pharmacological characterisation of the elevated "zero-maze" as an animal model of anxiety. Psychopharmacology 116 (1994) 56-64
49. Siegel J., Sisson D.F., and Driscoll P. Augmenting and reducing of visual evoked potentials in Roman high- and low-avoidance rats. Physiol Behav 4 (1993) 707-711
50. Spuhler K., and Deitrich R.A. Correlative analysis of ethanol-related phenotypes in rat inbred strains. Alcohol Clin Exp Res 8 (1984) 480-484
51. Stark H., Rothe T., Wagner T., and Scheich H. Learning a new behavioral strategy in the shuttle-box increases prefrontal dopamine. Neuroscience 126 (2004) 21-29
52. Steimer T., laFleur S., and Schulz P.E. Neuroendocrine correlates of emotional reactivity and coping in male rats from the Roman high (RHA/Verh)- and low (RLA/Verh)-avoidance lines. Behav Genet 27 (1997) 503-512
53. Steimer T., and Driscoll P. Divergent stress responses and coping styles in psychogenetically selected Roman high-(RHA) and low-(RLA) avoidance rats: behavioral, neuroendocrine and developmental aspects. Stress 6 (2003) 87-100
54. Steimer T., and Driscoll P. Inter-individual vs line/strain differences in psychogenetically selected Roman high- (RHA) and low- (RLA) avoidance rats: neuroendocrine and behavioral aspects. Neurosci Biobehav Rev 29 (2005) 99-112
55. Torres M.C., Cándido A., Escarabajal M.D., de la Torre L., Maldonado A., Tobeña A., et al. Successive negative contrast effect in one-way avoidance learning in female roman rats. Physiol Behav 85 (2005) 377-382
56. Valdar W., Solberg L.C., Gauguier D., Burnett S., Klenerman P., Cookson W.O., et al. Genome-wide genetic association of complex traits in heterogeneous stock mice. Nat Genet 38 (2006) 879-887
57. Valdar W., Solberg L.C., Gauguier D., Cookson W.O., Rawlins J.N.P., Mott R., et al. Genetic and environmental effects on complex traits in mice. Genetics 174 (2006) 959-984
58. Werka T. The effects of the medial and cortical amygdala lesions on post-stress analgesia in rats. Behav Brain Res 86 (1997) 59-65
59. Werka T., and Zielinski K. CS modality transfer of two-way avoidance in rats with central and basolateral amygdala lesions. Behav. Brain Res 93 (1998) 11-24
60. Yalcin B., Willis-Owen S.A., Fullerton J., Meesaq A., Deacon R.M., Rawlins J.N., et al. Genetic dissection of a behavioral quantitative trait locus shows that Rgs2 modulates anxiety. Nat Genet 36 (2004) 1197-1202
61. Yilmazer-Hanke D.M., Faber-Zuschratter H., Linke R., and Schwegler H. Contribution of amygdala neurons containing peptides and calcium-binding proteins to fear-potentiated startle and exploration-related anxiety in inbred Roman high- and low-avoidance rats. Eur J Neurosci 15 (2002) 1206-1218
62. Yilmazer-Hanke D.M., Wigger A., Linke R., Landgraf R., and Schwegler H. Two Wistar rat lines selectively bred for anxiety-related behavior show opposite reactions in elevated plus maze and fear-sensitized acoustic startle tests. Behav Genet 34 (2004) 309-318