Explorations of Coping Strategies,Learned Persistence, and Resiliencein Long-Evans Rats

Innate versus Acquired Characteristics

KELLY G. LAMBERT,a KELLY TU,a ASHLEY EVERETTE,a

GENNIFER LOVE,a ILAN MCNAMARA,b MASSIMO BARDI,b

AND CRAIG H. KINSLEYb

aDepartment of Psychology, Randolph-Macon College, Ashland, Virginia, USAbDepartment of Psychology, University of Richmond, Richmond, Virginia, USA

ABSTRACT: In the current investigation, predispositions for coping styles(i.e., passive, flexible, and active) were determined in juvenile male rats.In subsequent behavioral tests, flexible copers exhibited more active re-sponses. In another study, animals were exposed to chronic stress andflexible coping rats had lower levels of corticosteroids. Focusing on theacquired nature of coping strategies, rats receiving extensive trainingin a task requiring them to dig for food rewards (i.e., effort-based re-wards) persisted longer in a challenging task than control animals. Thus,the results suggest that both predisposed coping strategies and acquiredbehavioral experience contribute to resilience in challenging situations.

KEYWORDS: resilience; coping; effort-based rewards; learned persis-tence

INTRODUCTION

Although the stress response is adaptive for overcoming acute stressors,it can lead to the emergence of stress-related disease when stress becomeschronic.1,2 Recent research suggests that an individual’s day-to-day copingstrategies may also be an important factor in the genesis of stress-mediateddiseases such as depression.3–5 Consequently, the development of animal mod-els for the investigation of coping responses may be a valuable approach forthe identification of neurobiological factors serving as potential buffers against

Address for correspondence: Kelly G. Lambert, Ph.D., Department of Psychology, Randolph-MaconCollege, Ashland, VA 23005. Voice: 804-752-4717; fax: 804-752-4724.

e-mail: klambert@rmc.edu

Ann. N.Y. Acad. Sci. 1094: 319–324 (2006). C© 2006 New York Academy of Sciences.doi: 10.1196/annals.1376.042

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the onset of stress-related mental illness. In the current investigation, predispo-sitions for coping styles were determined in juvenile male Long-Evans rats sothat the consistency of these coping profiles could be determined in subsequentbehavioral and hormonal assessments.3

Recent research also suggests that animals’ response strategies upon ex-posure to less intense novelty stress may yield important information aboutphysical and neurobiological health (i.e., stress-resilience6,7). For example, onestudy demonstrated that rats exhibiting higher levels of exploratory behaviorupon the introduction of a novel object had lower levels of novelty-induced cor-ticosteroid secretion and lived approximately 30% longer lives than their inhib-ited counterparts.6 Considering these findings, an animal’s response in a chal-lenging novel task may provide important information about the persistenceof an animal’s responses in novel situations—providing additional informationabout the animal’s stress-resilience and predisposition toward anxiety-relateddisorders. Although past research has suggested that diminished associationsbetween directed effort and outcomes (i.e., stimulus–response associations)may lead to nonresponsiveness, similar to the behavior observed in depression(i.e., learned helplessness8), there is little research investigating the comple-mentary hypothesis that repeated experience strengthening stimulus–responseassociations may provide a buffer against mental illnesses such as depression.Considering that the brain’s motor circuit, the basal ganglia, shares extensiveconnections with the nucleus accumbens, a structure known for its involve-ment in pleasure and reward, the final experiment in this series of studiesexplored the utility of an animal model of effort-based rewards to determineif such training would lead to enhanced persistence, or learned persistence, insubsequent challenging tasks.

EXPERIMENTS AND RESULTS

Experiment 1: The Persistence of Innate Coping Characteristics

Coping strategies were examined in 30 male Long-Evans rats (23 days old)by gently restraining them on their backs for 1 min and recording the numberof times each animal tried to escape. Subsequently, animals were assigned toeither a passive or active category based on their responses. A second back-test was conducted 1 week later and the animals were assigned to their finalcoping group: passive (received a passive score on both tests); active (receivedan active score on both tests); or flexible (received a passive score on one testand an active score on the other test). Each coping category was comprisedof 10 animals. A one-way ANOVA was conducted to determine the effect ofcoping strategy on several ecologically relevant stress tests including exposureto a small clip on their tail (to simulate a bug bite), a predator odor, a novel toystimulus, and, finally, exposure to an open field. Flexible animals attempted to

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remove the clip from their tails more than either the passive or active groups(P < 0.01 and 0.03, respectively; see FIG. 1A); in addition, the flexible groupcontacted the novel toy stimulus more than the passive copers (P = 0.013; see

FIGURE 1. Performance of passive, flexible, and active rats exposed to a tail-clip (A),a novel toy stimulus (B), and an open field environment (C). ∗denotes statistical significantdifference from passive animals; + denotes difference from active animals; bars represents.e.m. values (see the EXPERIMENTS and RESULTS section for details).

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FIG. 1B). In the open-field test, the flexible animals were more active than boththe passive and active copers (P = 0.03 and 0.002, respectively; see FIG. 1C).No differences were observed in the predator odor test.

Experiment 2: Influence of Coping Strategy on Levels of FecalCorticosterone in Chronically Stressed Rats

A total of 24 male Long-Evans rats were assessed in the backtest (as de-scribed in Experiment 1) and categorized into passive, active, or flexible groups(n = 8 each group). After being housed in activity wheels, fecal samples werecollected to assess corticosterone levels. Animals were then exposed to theactivity-stress paradigm2 during which the rats were housed in the activitywheels and fed 2 h per day. After 4 days of activity-stress, fecal samples wereonce again collected for determination of corticosterone levels. In the prestressperiod, the flexible copers had significantly lower levels than the passive ani-mals (P = 0.04); in addition, during the chronic stress phase, the active copers’corticosterone levels was 170% higher than the flexible copers’ levels (P =0.05). See FIGURE 2.

Experiment 3: Acquired Coping Characteristics and Learned Persistence

A total of 16 male Long-Evans rats were matched for “emotionality” in anopen-field test and randomly assigned to either a control or a worker group ofrats. During the next 5 weeks, the animals were trained daily in an open field

FIGURE 2. Fecal corticosterone levels in animals exhibiting the various coping strate-gies assessed prior to a chronic stressor and during the chronic exposure to activity-stress.In the prestress condition, flexible copers had lower levels of corticosterone than passivecopers; in the stress condition, flexible copers had lower levels than their active copingcounterparts (see the EXPERIMENTS and RESULTS section for details).

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FIGURE 3. Rats trained to work for Froot Loop rewards in the digging task interactedwith the novel challenge task longer than the animals that received the rewards independentof directed effort (see the EXPERIMENTS and RESULTS section for details).

apparatus with corncob bedding placed on the floor. Control animals were giventhe reward of four small pieces of Froot Loops regardless of physical effortexpended in the training session whereas the worker rats were trained to dig forFroot Loops and received the reward only as a consequence of their physicaleffort. Following the 5 weeks of training, a persistence test was administeredto the animals by exposing them to a novel manipulandum task for 3 min. Thistask consisted of a ventilated plastic cat toy with a bell and Froot Loop placedinside requiring the animals to overcome their anxiety related to the novel balland bell and persist with their efforts to try to solve the problem of removingthe Froot Loop from the stimulus. The duration of attempts to remove the FrootLoop was recorded. A one-way ANOVA indicated that the worker group ofrats spent significantly more time with the challenging object than the controlgroup (P = 0.04; one-tailed test). See FIGURE 3.

DISCUSSION

The present series of studies provides preliminary evidence that copingstrategies are persistent across various stress assessments. Specifically, thebacktest, adapted from a model used with piglets,9 provided a means to char-acterize the rat pups as active, passive, or flexible copers. Interestingly, uponexposure to subsequent acute stressors, the flexible copers were the most re-sponsive. In Experiment 2, the various coping strategies were assessed in achronic stress paradigm (i.e., the activity-stress paradigm). Prior to the com-mencement of the stress paradigm, the flexible copers had lower corticosteronelevels than the passive animals; further, during the chronic stress, the flexiblecopers exhibited lower levels of stress hormones than the active copers. Con-sidering the toxic effects of prolonged durations of elevated stress hormones,

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these data suggest that the flexible copers exhibited the most adaptive responseto stressful situations.

In the third experiment, animals were trained in a task requiring them to digfor Froot Loop rewards. When compared to animals that were not required toexpend effort for the reward, the worker animals persisted longer in a novelchallenge task. Corroborating earlier findings documenting learned helpless-ness when associations between effort and consequences were diminished,the rats in this study exhibited a form of learned persistence following ex-tensive exposure to effort-contingent positive consequences (i.e., effort-basedrewards).

In sum, flexible, rather than fixed, coping strategies may facilitate stress-resilience and provide a buffer against the development of psychiatric disorderssuch as anxiety disorders or depression.10 In addition, coping responses maybe modified through experience with effort-based rewards—leading to an in-creased sense of control over one’s environment—and enhanced resilience instressful situations.11

REFERENCES

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2. LAMBERT, K.G., S.K. BUCKELEW, G. STAFFISO-SANDOZ, et al. 1998. Activity-stressinduces atrophy of apical dendrites of hippocampal pyramidal neurons in malerats. Physiol. Behav. 65: 43–49.

3. KOOLHAAS, J.M., S.M. KORTE, S.F. DEBOER, et al. 1999. Coping styles in animals:current status in behavior and stress-physiology. Neuro. Bio. Rev. 23: 925–935.

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8. SELIGMAN, M.E.P. & J.M. WEISS. 1980. Coping behavior: learned helplessness,physiological change and learned inactivity. Behav. Res. Ther. 18: 459–512.

9. SCHOUTEN, W.G.P. & V.M. WIEGANT. 1997. Individual responses to acute andchronic stress in pigs. Acta Physiol. Scand. 640: 188–191.

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11. LAMBERT, K.G. 2006. Rising rates of depression in today’s society: considera-tion of the roles of effort-based rewards and enhanced resilience in day-to-dayfunctioning. Neurosci. Biobehav. Rev. 30: 497–510.