Learned helplessness: Effects of response requirement and interval between treatment and testing

doi:10.1016/j.beproc.2007.02.012

Behavioural Processes

Volume 76, Issue 3, November 2007, Pages 183-191

https://doi.org/10.1016/j.beproc.2007.02.012 Get rights and content

Abstract

Three experiments investigated learned helplessness in rats manipulating response requirements, shock duration, and intervals between treatment and testing. In Experiment 1, rats previously exposed to uncontrollable or no shocks were tested under one of four different contingencies of negative reinforcement: FR 1 or FR 2 escape contingency for running, and FR1 escape contingency for jumping (differing for the maximum shock duration of 10 s or 30 s). The results showed that the uncontrollable shocks produced a clear operant learning deficit (learned helplessness effect) only when the animals were tested under the jumping FR 1 escape contingency with 10-s max shock duration. Experiment 2 isolated of the effects of uncontrollability from shock exposure per se and showed that the escape deficit observed using the FR 1 escape jumping response (10-s shock duration) was produced by the uncontrollability of shock. Experiment 3 showed that using the FR 1 jumping escape contingency in the test, the learned helplessness effect was observed one, 14 or 28 days after treatment. These results suggest that running may not be an appropriate test for learned helplessness, and that many diverging results found in the literature might be accounted for by the confounding effects of respondent and operant contingencies present when running is required of rats.

Section snippets

Experiment 1

As mentioned above, rats fail to show learned helplessness when a single escape response (FR 1) is required during test. The present experiment compared the effects of uncontrollable shocks on the subsequent learning of two different responses (running and jumping) with different ratio requirements (FR 1 and FR 2) and maximum shock duration.

Experiment 2

Results from the previous experiment showed that jumping under FR1 provides a way to assess learned helplessness. However, the effects of uncontrollability were not isolated from the stress that comes from shock exposure per se. The isolation of these effects have been traditionally done with the use of a triadic design, where uncontrollable animals are yoked to controllable ones, which are exposed to electric shocks as well, but have the opportunity to terminate them. Thus, Experiment 2

Experiment 3

The previous experiments showed that learned helplessness can be obtained with rats under FR 1 on a task that isolated the operant nature of the response. This experiment was designed to assess the effects of the passage of time on learned helplessness, using a clearly operant task. Rats were exposed to a treatment of either uncontrollable electric shocks or no shocks at all. Then they were tested under the escape contingency for jumping either 1, 14, or 28 days after treatment.

General discussion

Learned helplessness has been defined over the years as the difficulty to learn an operant response due to the previous exposure to uncontrollable shocks. However, in order to demonstrate that past experiences with uncontrollable aversive events interfere with subsequent operant learning, it is necessary to demonstrate that, without such history, learning actually takes place. When measuring response latency (the most common measure of performance under an escape contingency), learning is

Acknowledgements

The present research was supported by FAPESP (process number 01/13097-5) and CNPq (process number 550987/2002-9). Correspondence and requests for reprints may be sent to the first author at the Departamento de Psicologia Experimental, Instituto de Psicologia, Universidade de São Paulo. Av. Prof. Mello Moraes, 1721 CEP 05508-030 - Cidade Universitária - São Paulo (e-mail [email protected]).

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In this study, we investigated whether (a) animals demonstrating the learned helplessness effect during an escape contingency also show learning deficits under positive reinforcement contingencies involving stimulus control and (b) the exposure to positive reinforcement contingencies eliminates the learned helplessness effect under an escape contingency. Rats were initially exposed to controllable (C), uncontrollable (U) or no (N) shocks. After 24 h, they were exposed to 60 escapable shocks delivered in a shuttlebox. In the following phase, we selected from each group the four subjects that presented the most typical group pattern: no escape learning (learned helplessness effect) in Group U and escape learning in Groups C and N. All subjects were then exposed to two phases, the (1) positive reinforcement for lever pressing under a multiple FR/Extinction schedule and (2) a re-test under negative reinforcement (escape). A fourth group (n = 4) was exposed only to the positive reinforcement sessions. All subjects showed discrimination learning under multiple schedule. In the escape re-test, the learned helplessness effect was maintained for three of the animals in Group U. These results suggest that the learned helplessness effect did not extend to discriminative behavior that is positively reinforced and that the learned helplessness effect did not revert for most subjects after exposure to positive reinforcement. We discuss some theoretical implications as related to learned helplessness as an effect restricted to aversive contingencies and to the absence of reversion after positive reinforcement.
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In the FR2 schedule, animals had to cross twice; in other words, rats had to run back to the compartment where the shock was initiated in order to escape the shock. This escape contingency was done for 25 trials and required more time to complete; therefore, if the subject failed to perform the appropriate response, the shock automatically terminated after 30 s. FR1 jump and FR1/FR2 run were performed to determine the optimum contingency for measuring learned helplessness (Hunziker and Dos Santos, 2007). Latency to escape was automatically scored using MED-PC software.
This is the first metabolic mapping study of the effects of fluoxetine after learned helplessness training. Antidepressants are the most commonly prescribed medications, but the regions underlying treatment effects in affectively disordered brains are poorly understood. We hypothesized the antidepressant action of fluoxetine would produce adaptations in mesolimbic regions after 2 weeks of treatment. We used Holtzman rats, a genetic strain showing susceptibility to novelty-evoked hyperactivity and stress-evoked helplessness, to map regional brain metabolic effects caused by fluoxetine treatment. Animals underwent learned helplessness, and subsequently immobility time was scored in the forced swim test (FST). On the next day, animals began receiving 2 weeks of fluoxetine (5 mg/kg/day) or vehicle and were retested in the FST at the end of drug treatment. Antidepressant behavioral effects of fluoxetine were analyzed using a ratio of immobility during pre- and post-treatment FST sessions. Brains were analyzed for regional metabolic activity using quantitative cytochrome oxidase histochemistry as in our previous study using congenitally helpless rats. Fluoxetine exerted a protective effect against FST-induced immobility behavior in Holtzman rats. Fluoxetine also caused a significant reduction in the mean regional metabolism of the nucleus accumbens shell and the ventral hippocampus as compared to vehicle-treated subjects. Additional networks affected by fluoxetine treatment included the prefrontal–cingulate cortex and brainstem nuclei linked to depression (e.g., habenula, dorsal raphe and interpeduncular nucleus). We concluded that corticolimbic regions such as the prefrontal–cingulate cortex, nucleus accumbens, ventral hippocampus and key brainstem nuclei represent important contributors to the neural network mediating fluoxetine antidepressant action.
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It is important to note that our data do not refute the learned helplessness hypothesis, given that control groups not exposed to inescapable shocks were not run in the present study. Control subjects, however, do learn to jump barriers to escape shocks, as reported elsewhere (Hunziker and Santos, 2007; Sanavio and Savardi, 1980). The reduction in response latencies when nose-poking was required that we observed here also is evidence of learning, and this response pattern is in clear contrast to the pattern observed with jumping.
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Learned helplessness: Effects of response requirement and interval between treatment and testing

Abstract

Section snippets

Experiment 1

Experiment 2

Experiment 3

General discussion

Acknowledgements

Learn. Motiv.

Biol. Psychiat.

Neurosci. Biobehav. Rev.

Neuropharmacology

Behav. Neural Biol.

Brain Res. Rev.

Life Sci.

Partial control and learned helplessness in rats: control over shock intensity prevents interference with subsequent escape

Anim. Learn. Behav.

Acquisition of instrumental responding following non-contingent reinforcement: failure to observe “learned laziness” in rats

Bull. Psychonomic Soc.

Experimental depression in animals

Learning and Complex Behavior

A functional analysis of depression

Am. Psychol.

Uncontrollability and unpredictability in post-traumatic stress disorder: an animal model

Psychol. Bull.

Generality of failure-to-escape (helplessness) phenomenon in rats

Anim. Learn. Behav.

A study of the antidepressant activity of Hypericum perforatum on animal models

Pharmacopsychiatry

Effect of imipramine in the “learned helplessness” model of depression in rats is not mimicked by combinations of specific reuptake inhibitors and scopolamine

Psychopharmacology

Efeitos da administração aguda de imipramina sobre o desamparo aprendido em ratos machos e fêmeas

Acta Comportamentalia

Effects of ipsapirone and Bay R 1531 on learned helplessness

Braz. J. Med. Biol. Res.

Opioid nature of learned helplessness and stress-induced analgesia observed without re-exposure to shock

Behav. Pharmacol.