Sensitivity to negative and positive feedback as a stable and enduring behavioural trait in rats

Abstract

Rationale According to psychological theories, cognitive distortions play a pivotal role in the aetiology and recurrence of mood disorders. Although clinical evidence for the coexistence of depression and altered sensitivity to performance feedback is relatively coherent, we still do not know whether increased or decreased sensitivity to positive or negative feedback is associated with ‘pro-depressive’ profile in healthy subjects. Objective Our research has been designed to answer this question, and here, we present the first steps in that direction. Methods Using a rat version of the probabilistic reversal-learning (PRL) paradigm, we evaluated how sensitivity to negative and positive feedback influences other cognitive processes associated with mood disorders, such as motivation in the progressive ratio schedule of reinforcement (PRSR) paradigm, hedonic status in the sucrose preference (SP) test, locomotor and exploratory activity in the open field (OF) test, and anxiety in the light/dark box (LDB) test. Results The results of our study demonstrated for the first time that in rodents, sensitivity to negative and positive feedback could be considered a stable and enduring behavioural trait. Importantly, we also showed that these traits are independent of each other and that trait sensitivity to positive feedback is associated with cognitive flexibility in the PRL test. The computational modelling results also revealed that in animals classified as sensitive to positive feedback, the α learning rates for both positive and negative reward prediction errors were higher than those in animals classified as insensitive. We observed no statistically significant interactions between sensitivity to negative or positive feedback and the parameters measured in the PRSR, SP, OF or LDB tests. Conclusions Further studies using animal models of depression based on chronic stress should reveal whether sensitivity to feedback is a latent trait that when interacts with stressful life events, could produce correlates of depressive symptoms in rats.

Trait Sensitivity to Negative and Positive Feedback Does Not Interact With the Effects of Acute Antidepressant Treatment on Hedonic Status in Rats

“…They also showed that biased judgement, as a trait, is associated with alterations in the effectivity of antidepressant drug treatment (Drozd et al, 2019 ). Other studies suggested that trait sensitivity to NF and/or PF could be candidates for a cognitive biomarker of depression (Noworyta-Sokolowska et al, 2019 ). Although we did not observe statistically significant interactions between trait sensitivity to feedback and the hedonic capacity of tested animals in the present study, this result was not surprising and has already been explained elsewhere (Noworyta-Sokolowska et al, 2019 ) using Beck’s cognitive model of depression (Beck, 1987 , 2008 ).…”

“…The data were analyzed using a custom-written R programme. The experimental procedure for the PRL task used in this study was a modified version of the procedures used and described previously by Bari et al ( 2010 ) and has been described in detail elsewhere (Noworyta-Sokolowska et al, 2019 ).…”

“…After the initial instrumental training described elsewhere (Noworyta-Sokolowska et al, 2019 ), the rats were trained in the PRL paradigm. Each PRL training session consisted of 200 trials, and each trial lasted for a maximum of 22 s. The start of a trial was signalled by the house light, which remained on until the end of the trial.…”

“…The advantages of this test, which explain its popularity in laboratories throughout the world, are its simplicity and reliability. The method itself has been used in our laboratory for several years and has been thoroughly validated using various behavioral and pharmacological manipulations (Rygula et al, 2005 , 2006 , 2008 , 2013 ; Noworyta-Sokolowska et al, 2019 ). During the SP test, the rats were separated into single cages and were offered a voluntary choice between two bottles for 1 h, where one bottle contained a 2% (w/v) sucrose solution and the other bottle contained tap water.…”

“…The recent implementation of the preclinical version of the probabilistic reversal learning (PRL) paradigm (Bari et al, 2010 ) allowed for the investigation of this question in animal models. The results of our previous studies demonstrated that in rodents, sensitivity to NF and PF are stable and enduring behavioral traits (Noworyta-Sokolowska et al, 2019 ) and that even single doses of agomelatine or mirtazapine could change this sensitivity in the PRL test (Drozd et al, 2019 ). In that latter study, acute agomelatine treatment reduced the sensitivity of rats to NF, as indexed by the decreased proportion of lose-shift behaviors, while mirtazapine increased the sensitivity of rats to PF, as indexed by the increased proportion of win-stay behaviors.…”