Contextual and Serial Discriminations: A New Learning Paradigm to Assess Simultaneously the Effects of Acute Stress on Retrieval of Flexible or Stable Information in Mice

Abstract

The present study was aimed at simultaneously determining on the same subject, the effects of stress on retrieval of flexible (contextual or temporal) or stable (spatial) information. Three behavioral paradigms carried out in a four-hole board were designed as follows: (1) Simple Discrimination (SD), in which mice learned a single discrimination; (2) Contextual and Serial Discriminations (CSD), in which mice learned two successive discriminations on two different internal contexts; (3) Spatial Serial Discriminations (SSD), in which mice learned two successive discriminations on an identical internal context. The stressor (three inescapable electric footshocks) was delivered 5 min before retention, occurring 5 min or 24 h after acquisition. Results showed that this stressor increased plasmatic corticosterone levels and fear reactivity in an elevated-plus-maze, as compared with nonstressed mice. The stressor reversed the normal pattern of retrieval observed in nonstressed controls in the CSD task, this effect being context dependent, as it was not observed in the SSD task. Overall, our study shows that stress affected the retrieval of flexible and old information, but spared the retrieval of stable or recent ones. Therefore, these behavioral paradigms allow us to study simultaneously, on the same animal, the effects of stress on distinct forms of memory retrieval.Extensive evidence indicates that stress or pharmacologically induced modifications of the emotional state can influence cognitive function (Kirschbaum et al. 1996;Lupien and McEwen 1997;Belanoff et al. 2001;Wolf et al. 2001). It has been demonstrated that the stress-induced release of glucocorticoids is one of the main factors responsible for these effects. However, glucocorticoids have differential effects depending on the memory phase or the memory system concerned in animal and human subjects (Roozendaal 2002). Glucocorticoids enhance the consolidation of new memories for emotionally arousing experiences (Kovacs et al. 1977;Buchanan and Lovallo 2001), whereas glucocorticoids impair retrieval of long-term spatial memory in rats (De Quervain et al. 1998) and free recall of verbal material in humans (De Quervain et al. 2000;Wolf et al. 2001). Interestingly, even though the modification of the affective state can act on different memory and neurobiological systems (Packard and Cahill 2001), it has been shown that working and declarative memory retrieval are particularly sensitive to glucocorticoids' administration (Lupien et al. 1999;De Quervain et al. 2003).Animal studies have focused mainly on the effects of stress on acquisition, consolidation, and long-term storage of newly acquired information (Lupien and McEwen 1997). Only a few studies have been carried out in animals to determine the effects of stress on retrieval processes (De Quervain et al. 1998;Bats et al. 2001). More specifically, De Quervain et al. (1998) have shown that stress and glucocorticoids impaired retention performance in a water-maze spatial task, as a function of the time interval...

Glucocorticoid Effects on Memory Retrieval Require Concurrent Noradrenergic Activity in the Hippocampus and Basolateral Amygdala

“…These findings are consistent with extensive previous evidence indicating that stress exposure or glucocorticoids administered systemically or into the hippocampus shortly before testing on a variety of learning tasks that differ in their behavioral demands, including water maze, inhibitory avoidance, and hole board, induce comparable temporary retention performance impairments (de Quervain et 2004; Célérier et al, 2004). Because those previous studies also reported that the same treatments administered before training do not affect either water maze acquisition or performance on a probe trial given immediately after acquisition, the findings strongly suggest that the GR agonist-induced retention impairment reflects a direct effect on retrieval of long-term memory.…”

Rapid stress‐induced corticosterone rise in the hippocampus reverses serial memory retrieval pattern

“…In other words, mice spontaneously expressed a specific delayed serial order memory retrieval pattern. Interestingly, using the 24-h RI, we showed that an acute stress (electric footshocks) delivered before the test session improved the retrieval of D2 but impaired the retrieval of D1 (Celerier et al, 2004;Chauveau et al, 2008). Thus, stress reversed the serial memory retrieval pattern and induced in parallel a rapid plasma corticosterone rise (Celerier et al, 2004;Chauveau et al, 2008).…”

“…In the CSD task, normal, nonstressed animals retrieved accurately both discriminations when the test session occurred shortly after acquisition (retention interval (RI) of 5 min); in contrast, they exhibited higher discrimination rates for discrimination 1 (D1) than for discrimination 2 (D2) when a 24-h RI was interpolated between the acquisition and test sessions (Celerier et al, 2004;Chauveau et al, 2008). In other words, mice spontaneously expressed a specific delayed serial order memory retrieval pattern.…”

Detective mice assess relatedness in baboons using olfactory cues

“…First, data collection is entirely automatic, which generates strict and unbiased measurements of behaviour. Second, it allows the tests to be conducted in a soft light and silent atmosphere without human presence; thus, minimising stress for the mice (Célérier et al, 2004). Third, this method is particularly well suited for mice because it is based on the exploration of a novel environment, on locomotor activity and on head dipping in a hole-board, all of which are behavioural aptitudes spontaneously expressed by mice (Kliethermes and Crabbe, 2006).…”

“…Before each mouse was tested, and between each phase of a test, the apparatus was cleaned with 50% ethanol and then with water. Photocells placed in each hole were used to automatically evaluate the number of sniff bouts (head dips) in each hole (Célérier et al, 2004). When only one hole was active (i.e.…”