Successive negative contrast in one-way avoidance learning in female roman rats

Physiology & Behavior 85 (2005) 377 – 382

Successive negative contrast in one-way avoidance learning in female roman rats C. Torresa,T, A. Ca´ndidob, M.D. Escarabajala, L. de la Torrea, A. Maldonadob, A. Toben˜ac, A. Ferna´ndez-Teruelc a Department of Psychology, University of Jae´n (Spain) Department of Experimental Psychology and Behavioral Physiology, University of Granada (Spain) c Medical Psychology Unit, Department of Psychiatry and Forensic Medicine, Institute of Neurosciences, School of Medicine, Autonomous University of Barcelona (Spain) b

Received 7 October 2004; received in revised form 8 February 2005; accepted 23 February 2005

Abstract The inbred RLA (Roman Low-Avoidance) and RHA (Roman High-avoidance) rat strains have been psychogenetically selected for rapid (RHA) vs. extremely poor acquisition (RLA) of two-way active avoidance. As a consequence of this selective breeding, RLA animals exhibit a higher level of emotionality that can be observed in many anxiety models. The present study was conducted in order to analyze the performance of female RLA, RHA and Wistar rats in a behavioral test of anxiety that involves the reduction of the magnitude of an expected reward: the negative contrast effect that is obtained in one-way avoidance learning by reducing the time spent in the safe compartment. To this aim, three groups of animals (30–1/RLA, 30–1/RHA and 30–1/W) were trained to avoid an electric foot-shock administered in a bdangerQ compartment, by running from this compartment to a bsafeQ compartment. We observed an impairment of the avoidance response when time spent in the safe compartment was reduced from 30 to 1 s, when 30–1/RLA and 30–1/W groups were compared with control groups that were trained with a constant safe time (1–1/RLA and 1–1/W, respectively). We also obtained significant differences between 30– 1/RLA and 30–1/RHA groups in the postshift phase. These results indicate that RLA rats respond more negatively to the frustration triggered by the reduction in time spent in the safe compartment, suggesting that animal models based on negative contrast effects can be useful tools for studying the genetic basis of anxiety. D 2005 Elsevier Inc. All rights reserved. Keywords: Successive negative contrast; Avoidance learning; Roman rats; Female

1. Introduction How rats respond to a given reward often depends on their prior experience with other rewards. They compare the quantity and quality of the present reward with that of other rewards within their realm of experience, and respond accordingly [1]. An illustration of adjustment to the incentive value of a reward is the successive negative contrast paradigm (SNC). This effect basically consists of a behavioral suppression that is observed in animals shifted from a high to a lower magnitude of reinforcement, when T Corresponding author. Tel.: +34 953 21 22 92; fax: +34 953 21 18 81. E-mail address: [email protected] (C. Torres). 0031-9384/$ - see front matter D 2005 Elsevier Inc. All rights reserved. doi:10.1016/j.physbeh.2005.02.023

compared with the behavior of animals that receive the lower magnitude of the reward throughout the experiment. SNC has been used in a variety of testing situations, including operant runway [2], maze [3], instrumental aversion [4], as well as consummatory [5], and Pavlovian [6] tasks, and has been suggested to be partially the result of a negative emotional response (anxiety, frustration or disappointment) triggered by a denial of reward expectancies [7–9]. The involvement of negative affective states in SNC is supported by further behavioral [10–12], pharmacological [13–15] endocrinological [16] and neuroanatomical studies [1,17–19], and SNC has been considered to be an animal model for studying the psychobiological basis of anxiety [7,9,20]. Although SNC has been shown across

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different species [21], few studies have been interested in systematically studying behavioral differences among genetically selected strains of rodents. In this context, Flaherty and Rowan [22] tested Syracuse Low-Avoidance and Syracuse High-Avoidance rats (selectively bred for differences in performance in active avoidance) in a consummatory SNC task, showing that Syracuse LowAvoidance rats exhibited a substantially greater contrast than Syracuse High-Avoidance rats. Similarly, Rowan and Flaherty [23] found differences in consummatory contrast in the Maudsley strains, with the Maudsley Reactive rats showing a smaller SNC effect than the Maudsley Nonreactive rats. According to these studies, strains of rats psychogenetically selected for differences in fearfulness could be potentially useful for analyzing those theoretical explanations of SNC based on emotional processes. The Swiss sublines of Roman High-Avoidance (RHA/ Verh) and Low-Avoidance (RLA/Verh) rats have been initially selected and bred for rapid (RHA/Verh) vs. extremely poor (RLA/Verh) acquisition of active, two-way avoidance behavior [24], using stock from the original RHA and RLA rats [25]. A large body of evidence shows that, as a consequence of this selection, RLA/Verh rats are characterized by more pronounced, anxious reactions to novel, conflict and threatening situations, less noveltyseeking behaviors, and a blunted response to addictive drugs when they are compared with their RHA/Verh rats counterparts (e.g. [26–28]). Briefly, when exposed to a novel environment (e.g. open-field, holeboard, or elevated plusmaze), RLA/Verh animals show greater behavioral and neuroendocrine indices of anxiety than RHA/Verh rats, such as increased defecation, freezing and self-grooming, decreased exploration, and a higher activation of the HPA axis [29,30]. Behavioral differences have also been observed when animals are exposed to fear-conditioning stimuli. RLA/Verh rats show a more pronounced acoustic startle reflex, and enhanced freezing in classical fear conditioning tests [26,31,32]. These results consistently indicate that the RLA/Verh line presents higher emotionality and reactivity to a variety of stressful situations [33]. However, these genetically based differences in emotionality have not been tested in animal models of anxiety related to frustrative non-reward, such as extinction procedures or the SNC described above. The main aim of the present experiment was to study the performance of RHA/Verh and RLA/Verh rats (referred to in this study as RHA and RLA), and outbred Wistar rats in a one-way avoidance learning SNC task [4]. This test consists of a danger compartment in which the rat receives a warning signal followed by an electric foot-shock, and a safe compartment in which the warning signal or the shock never appear. Subjects placed in the danger compartment can run to the safe compartment when the warning signal is turned on, thus avoiding the shock. From modern btwo factorsQ and bhomeostatic opponent processQ theories [34,35], this avoidance response could be considered as a

mixture of flight from fear and approach to safety, the weight of each component being a function of the relative time spent in the danger and safe compartments, respectively (see Ref. [36] for review). In this context, SNC can be obtained by reducing the time spent by the animals in the safe compartment. Once subjects acquire the avoidance response with the time spent in the safe compartment being 30 s (preshift phase), this time is reduced to 1 s (postshift phase). The performance of this group is compared to that of a control group in which the time spent in the safe compartment remains constant (1 s) during both preshift and postshift phases. A previous study [4] showed that the performance of the shifted group on the postshift phase was worse than in the nonshifted group. This behavioral impairment implies an aversive emotional reaction triggered by a reduction in magnitude of an expected reward (in this case, the time spent in the safe compartment), as it has been consistently shown that this SNC effect can be attenuated, or even abolished, by injecting GABAergic anxiolytic compounds such as diazepam [14,37,38] or thiopental sodium [20]. Given that SNC in one-way avoidance learning has been consistently obtained in female Wistar rats [4,14,20,37,38], female RHA, RLA and Wistar rats were used in the experiment we present below.

2. Method 2.1. Subjects Twenty female RHA, 20 female RLA (from the colony of inbred RHA and RLA rats maintained at the Autonomous University of Barcelona), and 20 female Wistar rats (from the University of Granada experimental animal stock), at about 90 days of age at the start of the experiment, weighing 190–230 g, were used. Animals were housed individually with food and tapwater ad lib. Room temperature was kept to about 20 8C with a 12-h light/dark cycle. Training took place during the light phase, and the period needed to complete the whole experiment was 4 weeks. In order to avoid the influence of the oestrus cycle on the performance of rats in the behavioral test, the day of testing was counterbalanced across groups, in such a way that every testing day rats belonging to each of the 6 experimental groups were submitted (counterbalancing also the time of the day across groups) to the avoidance task. 2.2. Apparatus A Letica one-way avoidance chamber was used. It consisted of two equal compartments 27 cm long  25 cm wide  28 cm high, made of black Plexiglas. The compartments were separated by a 0.5 cm-thick partition 25 cm wide  28 cm high, with a square 9  9 cm hole at floor level and a removable automatic gate to allow movement between compartments. Only the danger compartment was

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Table 1 Time spent in the safe compartment during pre- and postshift phases

2.4. Statistical analysis

Groups

The dependent variable used was the number of trials needed to reach the acquisition criteria in each phase. There were two criteria employed: (a) In the preshift phase, number of trials to achieve five consecutive avoidance responses and (b) In the postshift phase, number of trials to achieve five consecutive avoidance responses. When an animal did not reach one of these criteria after 80 trials had elapsed, it was removed from the avoidance box and a value of 80 was assigned for that criterion. The means in each criterion were submitted to a Kruskal–Wallis test for global significance. Comparisons between the different groups were performed using a Mann–Whitney U-test. For all statistical analysis, alpha was set at 0.05.

30–1/RHA 1–1/RHA 30–1/RLA 1–1/RLA 30–1/W 1–1/W

N

10 9 9 10 10 10

Time in the safe compartment (s) Preshift

Postshift

30 1 30 1 30 1

1 1 1 1 1 1

Strain

Roman Roman Roman Roman Wistar Wistar

high-avoidance high-avoidance low-avoidance low-avoidance

fitted with a grid floor, consisting of 19 stainless steel rods 4 mm in diameter and spaced 2 cm apart, connected in series to a Letica LI-2900 module capable of delivering a continuous, scrambled shock. The floor in both compartments was hinged to operate a microswitch when depressed, allowing the apparatus, procedure and responses to be automatically controlled by a PC-XT microcomputer. A speaker was placed in the lateral wall between the danger compartment and the safe compartment. The warning signal was a 2000 Hz tone of 88 dB. The roof of the danger compartment consisted of a black glass panel, which was removed only to put the rat into the chamber. A rigid, nontransparent white plastic carrying box 24 cm long  14 cm wide  19 cm high was placed in the safe compartment, and was used to move the rat when the safe time was completed. The carrying box had a handle on top and no wall on the side facing the communication hole and gate. An air extractor installed outside the avoidance chamber produced a background noise of 70 dB. 2.3. Procedure Rats were removed from their cages and put into the avoidance box, placed in an adjacent quiet room, where they were allowed 5 min to explore both compartments without interference. Thereafter, the communication gate was closed, shutting the rat in the danger compartment, and the trials began. These trials consisted of a warning signal followed after 5 s by an electric shock of 1 mA. Both the warning signal and the shock were continued until the animal moved into the safe compartment, or until 30 s had elapsed. The gate between the two compartments was opened when the warning signal commenced and closed when the rat entered the safe compartment. Time in the danger compartment before the onset of the warning signal was the same for all experimental conditions (15 s). Once the safe time had been completed, the transportation box was lifted over the apparatus and the rat was returned to the danger compartment (the roof of this compartment was opened briefly for this, for about 2 s, and then closed). The box was then replaced in the safe compartment of the avoidance chamber. The rats were assigned to one of six groups (see Table 1).

3. Results During the performance of two rats the computer failed and did not adequately display the stimuli. The performance of these animals was not included into the statistical analysis, so the number of subjects was 9 for groups 1–1/ RHA and 30–1/RLA, respectively. Overall analysis of the results showed statistically significant differences among groups in preshift, H(5) = 23.089 p b 0.0005, and postshift phases, H(5) = 20.496, p b 0.001. The results are summarized in Table 2. In preshift phase, significant differences were found between the contrast group and the control group in Wistar rats (30–1/W vs. 1–1/W; U = 9.50, p b 0.001) and in RHA rats (30–1/RHA vs. 1–1/RHA; U = 22.00, p b 0.035). These differences were not obtained when groups 30–1/RLA and 1–1/RLA were compared in this phase (U = 23.00, p b 0.136). In other hand, statistical analysis did not reveal significant differences on this phase between groups 30–1/ RHA and 30–1/RLA (U = 31.00, p b 0.278) or between groups 1–1/RHA and 1–1/RLA (U = 38.00, p b 0.604). Finally, group 1–1/W significantly needed a greater number of trials to reach the preshift criterion as compared to groups 1–1/RHA (U = 20.50, p b 0.023) and 1–1/RLA (U = 18.00, p b 0.028). Table 2 Mean number of trials to reach the criteria of acquisition in the preshift and postshift phases Groups

Preshift phase (FS.E.M.)

Postshift phase (FS.E.M.)

30–1/RHA 1–1/RHA 30–1/RLA 1–1/RLA 30–1/W 1–1/W

11(F 1.88) 15.6(F 1.48) 8(F 1.14) 14.4(F 2.85) 11.1(F 1.71) 22.60(F2.14)

8.1(F2.03) 2.8(F0.83) 16.3(F3.24)a,b 5.1(F1.56) 11.50(F1.47)c 4.7(F2.66)

a b c

p b 0.05 as compared to group 1–1/RLA. p b 0.05 as compared to group 30–1/RHA. p b 0.05 as compared to group 1–1/W.

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In postshift phase, statistical analysis revealed significant differences between contrast and control groups in Wistar rats (30–1/W vs. 1–1/W; U = 17.50, p b 0.011) and in RLA rats (30–1/RLA vs. 1–1/RLA; U = 12.00, p b 0.011). By contrast, although the reduction of time spent in safe compartment seemed to impair the performance of the avoidance response in group 30–1/RHA as compared to group 1–1/RHA, this difference did not quite reach statistical significance (U = 25.50, p b 0.063). Finally, statistically significant differences were obtained between the groups 30–1/RLA and 30–1/RHA (U = 20.50, p b 0.043). These results replicate the SNC effect in one-way avoidance learning obtained in female Wistar rats [4,14,20,37,38] and suggest that the reduction in time spent in the safe compartment produces a greater interfering effect on the avoidance response in RLA rats as compared to RHA rats.

4. Discussion The results obtained in the present experiment replicate those obtained previously in Wistar female rats [4]; that is, when time spent in the safe compartment was shifted from a large reward (30 s) to a small reward (1 s), avoidance response in contrast groups was poorer than in small reward, nonshifted control groups. Our results also suggest, however, that genetically based differences in reactivity to anxiogenic situations can modulate the magnitude of the SNC described above, given that the behavioral suppression that defines the contrast effect was greater for the highly emotional RLA rats as compared to the less anxious RHA rats. Several lines of evidence suggest that SNC phenomena obtained in appetitive, consummatory and aversive tasks can be described in terms of aversive emotional processes which are triggered as a consequence of the reduction in the magnitude of an expected reward [5,8,11,39,40]. From this perspective, the SNC obtained in one-way avoidance learning can be explained by considering that the time spent in the safe compartment may act as an appetitive reinforcer [41–43]. A sudden reduction of the time spent in safety would produce an emotional response of anxiety [9], frustration [39] or disappointment [7], giving rise to the observed impairment in the performance of the avoidance response. This theoretical explanation of SNC, together with its sensitivity to the action of anxiolytic drugs [14,20,37,38] has enabled the SNC in avoidance learning to be considered as an animal model of anxiety [20]. The results obtained in the present study seem to be in accordance with the predictions that can be derived from this theory, given that the impairment of the avoidance response observed in the postshift phase in the contrast groups was significantly greater for those animals with a more pronounced emotional reactivity to aversive/stressful situations (RLA) than for less fearful subjects (RHA). On the other hand, there were no differences in one-way avoidance acquisition (preshift phase) between RHA and

RLA groups. Such a result cannot be considered as unexpected, provided that one-way avoidance is a lowcomplexity task which does not involve conflict between behavioral tendencies (i.e. the safe compartment is clearly different from the danger compartment, and the required response of crossing to the safe side is always in the same direction) nor between the cues to be used by the animals to achieve the required response [e.g. ([44]). This is clearly in contrast to the high complexity of cues and the bidirectional avoidance conflict involved in the acquisition of the twoway avoidance task (i.e. the animal receives shock in both sides of the shuttlebox, and both compartments are identical), which lead to competing behavioral tendencies (i.e. freezing vs. running to the opposite side) and high levels of anxiety especially during the early stages of acquisition (e.g. [27,45,46]). In fact, going back to the present data on one-way avoidance acquisition (preshift phase) in RHA and RLA groups, our results are essentially congruent with those reported by Satinder [44], indicating that RLA/Lu rats (from his colony of RHA/Lu and RLA/Lu sublines, maintained in Canada since the early 1970s) showed progressive and significant improvements of active avoidance behavior when the task complexity became lower, reaching the same levels of avoidance acquisition as RHA/Lu rats when tested in a simple unidirectional (oneway) avoidance task (in which rats had to cross from the danger side—where shock was administered—to the opposite-safe-side of a box and climb onto a platform in order to avoid the shock [44]. Finally, this lack of differences during the preshift phase clarifies and gives more value to the postshift results. The greater impairment of the avoidance response after reducing the time spent in the safe compartment observed in RLA rats, as compared to their RHA counterparts, suggests that these genetically selected animals differed in their emotional reactivity to the reduction in the magnitude of an expected reward. These results are in agreement with those reported by Flaherty and Rowan in consummatory contrast with Syracuse High-Avoidance (SHA) and Syracuse Low-Avoidance (SLA) rats, and also with the results obtained by Rowan and Flaherty with Maudsley Reactive and Nonreactive rats [22,23]. Overall, the data obtained from experiments conducted with animals selectively bred for other purposes suggests that there may be a heritable component in the degree of susceptibility to SNC [47]. In addition, our results are in accordance with the frequently observed differences between RHA and RLA rats when they are exposed to other anxiogenic environments. Thus, RLA rats show a more pronounced tachycardia when exposed to various unconditioned stressful conditions, a more intense bradycardia in response to a conditioned emotional stressor, increased novelty-induced self-grooming, defecation and freezing responses, a greater acoustic startle response, and a stronger conflict-induced suppression of drinking (see Refs. [48,49] for review). In keeping with this view, our results indicate that RLA rats show a

C. Torres et al. / Physiology & Behavior 85 (2005) 377–382

more pronounced SNC effect as compared to RHA animals, extending the stressful conditions where behavioral divergences between RLA vs. RHA rats are observed to those related to frustrative non-reward. Although the biological substrates underlying the divergences observed in fearfulness between RHA and RLA animals remain to be elucidated, several studies suggest that genetically based neurochemical differences could be the reason. It has been observed that a variety of stressors and anxiogenic drugs activate the mesocortical dopaminergic pathway of RHA, but not of RLA rats (see Ref. [28] for review). Genetic differences in the pharmacological properties of the GABAA receptor complex have also been studied, although controversial results have been reported (see Ref. [50] for review). Altogether, these findings suggest that the selective breeding of the Roman lines has produced two phenotypes that consistently differ in the functional properties of a variety of neurotransmitter systems [28], leading to the line-dependent differences observed in anxiety, noveltyseeking behavior and vulnerability to abuse drugs. In summary, the present results suggest that RHA and RLA rats differently react to the SNC effect obtained in oneway avoidance learning by reducing the time spent in the safe compartment. A greater contrast effect was obtained in the RLA contrast group as compared to the RHA contrast group. Given that these strains of Roman rats markedly differ in their emotional reactivity under a high variety of stressful situations, it may be concluded that SNC in oneway avoidance learning can be a useful animal model for exploring the genetic basis of anxiety.

Acknowledgments This study was partially supported by SAF2003-03480, BS02003-0723, and SEJ2004-03231/PSIC. The authors would like to thank Dr. J. Rosas for his help with the translation of the manuscript.

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