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

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

doi:10.1016/j.bbr.2009.03.024

Cited by 73 publications

(87 citation statements)

References 60 publications

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“…Two phenotypes with different emotional and motivational profiles have been developed through bidirectional selection and breeding of the Roman high-(RHA) and low-avoidance (RLA) rat lines/ strains (outbred or inbred, respectively), selected for rapid (RHA) vs extremely poor (RLA) acquisition of two-way active avoidance in the shuttle-box (Broadhurst and Bignami, 1965;Driscoll and Bättig, 1982) (for reviews, see Driscoll et al, 1990Driscoll et al, , 1998Driscoll et al, , 2009Escorihuela et al, 1995Escorihuela et al, , 1999Fernández-Teruel et al, 1997;Giorgi et al, 2007;Steimer and Driscoll, 2005). These lines/strains show consistent differences in sensation/novelty seeking and in stress/anxiety endocrine and behavioral responses when confronted with novel environments (ie, intended to measure anxiety, emotionality, fearfulness, or novelty seeking), such as the open-field test (Aubry et al, 1995;Carrasco et al, 2008;Escorihuela et al, 1999;Gentsch et al, 1991), elevated plus maze (Escorihuela et al, 1999;Steimer and Driscoll, 2003), elevated zero-maze (López-Aumatell et al, 2009b), blackwhite box test, dark-light open-field test, dark-light hexagonal tunnel maze (Fernández-Teruel et al, 2002b;Steimer and Driscoll, 2005), and hole-board test (Escorihuela et al, 1999;Fernández-Teruel et al, 1992). In all of these situations and in fear-conditioning procedures (eg, fear-potentiated startle; López-Aumatell et al, 2009a), RLA rats show increased anxiety or fear, a passive coping style, and increased stress responses by hypothalamus-pituitaryadrenal (HPA) axis activation (Carrasco et al, 2008;Steimer and Driscoll, 2003).…”

Section: Introductionmentioning

confidence: 99%

Impulsivity Characterization in the Roman High- and Low-Avoidance Rat Strains: Behavioral and Neurochemical Differences

Moreno

Cardona

Gómez

et al. 2010

Neuropsychopharmacol

131

106

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The selective breeding of Roman high-(RHA) and low-avoidance (RLA) rats for rapid vs extremely poor acquisition of active avoidance behavior in a shuttle-box has generated two phenotypes with different emotional and motivational profiles. The phenotypic traits of the Roman rat lines/strains (outbred or inbred, respectively) include differences in sensation/novelty seeking, anxiety/fearfulness, stress responsivity, and susceptibility to addictive substances. We designed this study to characterize differences between the inbred RHA-I and RLA-I strains in the impulsivity trait by evaluating different aspects of the multifaceted nature of impulsive behaviors using two different models of impulsivity, the delay-discounting task and five-choice serial reaction time (5-CSRT) task. Previously, rats were evaluated on a schedule-induced polydipsia (SIP) task that has been suggested as a model of obsessive-compulsive disorder. RHA-I rats showed an increased acquisition of the SIP task, higher choice impulsivity in the delay-discounting task, and poor inhibitory control as shown by increased premature responses in the 5-CSRT task. Therefore, RHA-I rats manifested an increased impulsivity phenotype compared with RLA-I rats. Moreover, these differences in impulsivity were associated with basal neurochemical differences in striatum and nucleus accumbens monoamines found between the two strains. These findings characterize the Roman rat strains as a valid model for studying the different aspects of impulsive behavior and for analyzing the mechanisms involved in individual predisposition to impulsivity and its related psychopathologies.

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Section: Introductionmentioning

confidence: 99%

Impulsivity Characterization in the Roman High- and Low-Avoidance Rat Strains: Behavioral and Neurochemical Differences

Moreno

Cardona

Gómez

et al. 2010

Neuropsychopharmacol

131

106

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“…Animal models provide similarly strong models for comorbidity of traits, like evidence for a shared genetic substrate in anxiety and fear. For example, selective breeding paradigms in mice and rats have shown that selection of anxiety-like behavior also selects for differences in fear and vice versa (Ponder et al 2007a;López-Aumatell et al 2009). …”

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confidence: 99%

High-Resolution Genetic Mapping of Complex Traits from a Combined Analysis of F2 and Advanced Intercross Mice

et al. 2014

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Genetic influences on anxiety disorders are well documented; however, the specific genes underlying these disorders remain largely unknown. To identify quantitative trait loci (QTL) for conditioned fear and open field behavior, we used an F 2 intercross (n = 490) and a 34th-generation advanced intercross line (AIL) (n = 687) from the LG/J and SM/J inbred mouse strains. The F 2 provided strong support for several QTL, but within wide chromosomal regions. The AIL yielded much narrower QTL, but the results were less statistically significant, despite the larger number of mice. Simultaneous analysis of the F 2 and AIL provided strong support for QTL and within much narrower regions. We used a linear mixed-model approach, implemented in the program QTLRel, to correct for possible confounding due to familial relatedness. Because we recorded the full pedigree, we were able to empirically compare two ways of accounting for relatedness: using the pedigree to estimate kinship coefficients and using genetic marker estimates of "realized relatedness." QTL mapping using the marker-based estimates yielded more support for QTL, but only when we excluded the chromosome being scanned from the marker-based relatedness estimates. We used a forward model selection procedure to assess evidence for multiple QTL on the same chromosome. Overall, we identified 12 significant loci for behaviors in the open field and 12 significant loci for conditioned fear behaviors. Our approach implements multiple advances to integrated analysis of F 2 and AILs that provide both power and precision, while maintaining the advantages of using only two inbred strains to map QTL.

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“…the rat does not cross to the opposite compartment neither during CS nor US presentation; this is the first "helplessness"-like variable); 3) the average response latency for the first ten trials ("10Latency", because this is the phase of training where most "R failures" are present, about 90% of them; this is the second "helplessness"-like variable); and 4) the number of avoidances (Avoidances) during the whole 50-trial training session. Context-conditioned freezing, was measured by two trained observers (between-observer reliability, r > 0.95) as the time a rat spent completely motionless except for breathing movements (see details and references on the validity of this task in [26][27][28][29][30]34]). …”

Section: Two-way Active Shuttle Box Escape/avoidancementioning

confidence: 99%

“…enhanced) hormone response profile. Thus, the anxiety/fear and stress hormone response profiles of NIH-HS rats are much closer to the (high anxious, stress prone) passive coper RLA-I rats than to the (low anxious, stress resistant) proactive coper RHA-I rats [23,[25][26][27][28][29][30].…”

Section: Introductionmentioning

confidence: 99%

“…Thus, taking advantage of the fact that we know the NIH-HS rats are, as a population, passive coping rats with very poor ability for the acquisition of the twoway-shuttle box-active escape/avoidance task (see [23,25,27,28]), we made the hypothesis that at least a subsample of the heterogeneous rat stock could display a kind of "spontaneous" (i.e. as we are not using any prior stress) helplessness in the shuttle box task, i.e.…”

Section: Introductionmentioning

confidence: 99%

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Helplessness-like escape deficits of NIH-HS rats predict passive behavior in the forced swimming test: Relevance for the concurrent validity of rat models of depression

Palència¹,

Díaz-Morán²,

Mont-Cardona³

et al. 2013

WJNS

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The genetically heterogeneous NIH-HS rat stock has been characterized by its response to anxiety-and fear-inducing situations, thus leading to the conclusion that they are a rather anxious and passive coping type of rats. Taking advantage of these profiles, and knowing that they show very poor performance in the two-way active (shuttle box) escape/avoidance task, we have tested NIH-HS rats (n = 80) in the forced swimming test (FST) as well as we have studied escape response deficits (i.e. response failures) of the same animals in the two-way shuttle box task. They were also tested for anxiety in the elevated zero-maze. The goal of such a study was that of investigating whether there are associations or relationships among helplessness-like or passive coping responses between both models of depression, i.e. the FST and the helplessness-like escape deficits in the shuttle box task. The results for the first time show associations among responses from both depression models and that selecting rats for displaying extreme (active or passive) responses in one of the models predict in a coherent manner (according to the hypothesis) their behaviour in the other model. These findings are discussed in the context of the concurrent validity of both models of depression as well as concerning the possible relevance of NIH-HS rats as a tool for future studies on this field.

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

Cited by 73 publications

References 60 publications

Impulsivity Characterization in the Roman High- and Low-Avoidance Rat Strains: Behavioral and Neurochemical Differences

Impulsivity Characterization in the Roman High- and Low-Avoidance Rat Strains: Behavioral and Neurochemical Differences

High-Resolution Genetic Mapping of Complex Traits from a Combined Analysis of F2 and Advanced Intercross Mice

Helplessness-like escape deficits of NIH-HS rats predict passive behavior in the forced swimming test: Relevance for the concurrent validity of rat models of depression

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