Circadian modulation of passive avoidance is not eliminated in arrhythmic hamsters with suprachiasmatic nucleus lesions

doi:10.1016/j.bbr.2012.02.022

Behavioural Brain Research

Volume 230, Issue 1, 21 April 2012, Pages 288-290

https://doi.org/10.1016/j.bbr.2012.02.022 Get rights and content

Abstract

The expression of passive avoidance (PA) learning in rats displays a daily or circadian rhythm in that optimal performance is displayed when the time of testing matches the time of training. Lesions of the suprachiasmatic nucleus (SCN) were later shown to abolish this rhythm. Using golden hamsters, we have since demonstrated similar rhythms of performance in a conditioned place avoidance (CPA) task but unlike the PA results in rats, the rhythmic expression of CPA was maintained in arrhythmic hamsters with lesions of the SCN. We determined whether PA performance in hamsters is dependent on the SCN (as in the rat) or independent (as in the hamster CPA). Performance on the PA task was rhythmic in intact control animals with optimal performance occurring when training and testing time matched and significantly diminished at both 6 h before and 6 h after training time. SCN-lesions, verified by the loss of behavioral circadian rhythms, had no effect on the rhythmic expression. Therefore, time of day modulation of PA performance in the hamster does not depend on the SCN circadian clock.

Highlights

► Hamsters display 24-h rhythms in memory retrieval for tasks involving several days of training. ► We demonstrate that hamsters display optimal performance at a 24-h interval for a task that was learned on only one training trial. ► Arrhythmic hamsters with lesions of the suprachiasmatic nucleus (SCN) continue to demonstrate this rhythm in memory retrieval. ► A non-SCN oscillator may control this memory retrieval rhythm.

Introduction

The expression of a conditioned place preference (CPP) and conditioned place avoidance (CPA) in the hamster, and CPP in the rat and marmoset, is regulated such that the place preference/avoidance is exhibited strongly at the circadian time of prior training, but not at other circadian times [1], [2], [3], [4], [5], [6]. This finding that the temporal match between training and testing is an important determinant of performance is not novel. Holloway and Wansley [7], [8] demonstrated that optimal performance in a passive avoidance task occurred at 24 h intervals in rats. Though they referred to this effect as a “retention” deficit, it is more accurately a periodic deficit in retrieval or motivation to perform, as animals clearly displayed retention of the task for the entire study.

Stephan and Kovacevic [9] hypothesized that the passive avoidance (PA) rhythm was mediated by the suprachiasmatic nucleus (SCN), the site of the master circadian oscillator in mammals [10], [11], [12]. They confirmed that intact and sham-operated rats displayed a rhythm in PA, with peak performance (avoidance of the chamber associated with shock) at the time of day that matched the training time. However, rats with SCN-lesions did not display this rhythm, consistent with their hypothesis. Other types of learning (e.g. fear conditioning, spatial learning) also appear to rely on the SCN [13], [14], [15].

Unlike the findings of Stephan and Kovacevic, we have found that rhythmicity in the recall of CPA is retained in arrhythmic animals with complete SCN lesions [3]. Although there are procedural differences, the CPA and PA tasks are similar, as each is a place learning task involving the avoidance of a chamber in which footshock has been experienced and both elicit strong rhythms in performance with peaks at the time of prior experience. Nonetheless, a major difference between the two procedures is that CPA involves multiple experiences with a shock-paired chamber and also with an unpaired chamber, whereas PA involves a one-trial learning experience. It is possible that the multiple trials could reinforce associations and that other mechanisms for predicting the likelihood of the foot shock according to time of day might be recruited.

The published data, therefore, suggest two alternative hypotheses: (1) that performance rhythms in PA and CPA are driven by the same mechanism that is independent of the SCN; and (2) that non-SCN timing mechanisms are recruited in CPA but not in PA. The first test of these hypotheses, which we report here, was to determine whether the PA performance rhythm in the hamster requires a functional SCN clock.

Section snippets

Animals

Seventy-two male Golden hamsters (Mesocricetus auratus) were obtained from Harlan Bioproducts, Inc., (Indianapolis, Indiana), and were between 90 and 120 days old at the beginning of the experiment. Animals were housed individually in polypropylene cages (22 cm × 44 cm × 20 cm) with free access to food, water, and a stainless steel running-wheel (17 cm in diameter). Cages were kept inside light-tight ventilated boxes (up to six cages per box).

Lighting conditions

Illumination was provided by two GE Cool White fluorescent

Results

For initial step-through latency (STL), escape latency, number of re-entries to shock chamber and total shock received during training, t-tests revealed no significant differences between SCN-lesioned and intact groups (p > 0.05 for all measures).

For untrained control animals the time of testing (Early, Matching, Late) had no effect on STL (one-way ANOVA [F (2,21) = 0.29, p > 0.05]). A 2 × 3 (surgical group × testing time) ANOVA performed on STL revealed a main effect of testing time [F (2,36) = 3.32, p <

Discussion

Two main results of this study are simple and clear: (1) rhythms in performance are displayed following PA conditioning in hamsters, with a performance peak near the time of prior training. This is similar to the “multiple retention deficit” described previously in rats [7], [8]. (2) The rhythm is not eliminated in arrhythmic hamsters with lesions of the SCN, in contrast to the findings of Stephan and Kovacevic [9] in rats. Thus, the data support the first of our two alternative hypotheses –

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Citation Excerpt :
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Research reportCircadian modulation of passive avoidance is not eliminated in arrhythmic hamsters with suprachiasmatic nucleus lesions

Abstract

Highlights

Introduction

Section snippets

Animals

Lighting conditions

Results

Discussion

Behav Brain Res

Behav Brain Res

Neurobiol Learn Mem

Neurobiol Learn Mem

Neurobiol Learn Mem

Neurobiol Learn Mem

Behav Biol

Behav Biol

Research report
Circadian modulation of passive avoidance is not eliminated in arrhythmic hamsters with suprachiasmatic nucleus lesions