Research report
Age-related modifications of contextual information processing in rats: role of emotional reactivity, arousal and testing procedure

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Abstract

Two experiments were conducted to examine contextual information processing in adult (7 months) and aged (22 months) Wistar rats. In Experiment 1, rats were tested for contextual fear conditioning when exposed to six series, one per day, of ten pairings of a tone (CS) with a foot-shock (US) delivered in one of a two-compartment apparatus. Conditioned fear was estimated by recording: (1) the amount of freezing in the shock compartment; and (2) the time spent avoiding the shock compartment. Results show that, after only one series of ten CS–US pairings, all rats showed freezing in the shock compartment, with aged rats exhibiting the stronger response. Adult rats also avoided the shock compartment during place preference tests in contrast to aged rats, that spent an equivalent time — with an intense freezing reaction — in both the shock and the safe compartments. After 60 CS–US pairings, contextual freezing in the shock compartment decreased in both groups, but, contrary to adults, aged rats were still not avoiding that compartment. In Experiment 2, radial maze performance was studied under distinct quantitative extra-maze cueing conditions (poor versus rich) and successive context shifts. Compared to adults, aged rats were impaired when trained initially under poor cueing conditions. No group difference was evident when rats were transferred to a context involving more cues (rich cueing conditions), but age-related impairments re-emerged when rats were returned to the original poor cueing conditions. Thus, the fact that performance deficits in a given task were restricted to certain testing procedures suggests that aging affects more the utilization than the processing of contextual information.

Introduction

Decline in learning and remembering newly acquired information has been frequently reported in aged animals. In spite of the large variability of paradigms and of species examined, the studies conducted in this field show a general agreement on the following points. (1) Senescent animals do not all show the same rate of performance impairment, thus indicating that a large inter-individual variability in cognitive abilities can be expected among aged subjects [12], [17], [29], [34]. (2) In many cases, performance decrements of aged subjects are more likely to be a slowness rather than an incapability to learn [2], [10], [26], [34], [40], [45]. Thus, the possibility is raised that associative and cognitive operations involved in learning or retrieving information might be relatively well-preserved in aged animals in comparison with the decreased efficiency of mechanisms that ensure rapid adaptive responses like motor coordination [17] or that permit adequate information gathering, like exploration [38], [46] and attention to the context [20], [43].

In particular, the question of whether contextual information processing decreases as a function of age has been extensively analyzed in humans by comparing memory for the content of a message and memory for the context associated with it. Interestingly, the results of the meta-analysis of 46 studies revealed that memory for context is more vulnerable to aging than memory for content [39]. Indeed, poor encoding of contextual information might prevent integration of to-be remembered items with contextual cues, a mechanism known to facilitate recall in young subjects as in adults [15].

In rodents, the context is also known to play a key role in both encoding and retrieval operations. For example, in Pavlovian conditioning, involving the pairing of a conditioned stimulus (CS: tone, light) with an unconditioned stimulus (US: electrical foot-shock, food), contextual stimuli have been shown to acquire excitatory strength by becoming associated with the US and therefore, facilitate recall of the conditioned response or, alternatively, block the development of conditioning to a new CS [9], [11], [14], [35]. Also, in the particular case of conditioned taste aversion (CTA), where a novel conditional stimulus (CS: saccharin drinking solution) is paired with an illness-inducing unconditioned stimulus (US: lithium chloride injection), contextual stimuli appear to overshadow the CS and permit CTA to be elicited over consistent CS–US intervals [21], [22]. Finally, in maze learning tasks, the recall of explicit information is facilitated by pretest exposure to contextual stimuli related to the original training experience [13], [18]. In general, contextual stimuli are helpful in clarifying the meaning of ambiguous stimuli [9], [11] and in facilitating the selection of context-depending behaviors [48]. Thus, it could be that age-related impairments in contextual representations might prevent the binding of target stimuli to contextual cues and decrease performance in a variety of tasks.

Indeed, the literature dealing with learning, aging and context clearly shows that young and old rats react differently to manipulations of contextual cues [43], [48]. However, the data collected to date make it difficult to state whether aged rats abnormally rely on, or neglect, contextual information. For instance, as an example of age-related increased sensitivity to contextual factors, retention of a passive avoidance response over a 3-week training-testing interval was diminished in aged but not in young rats, when additional approach training-exposure to a passive avoidance apparatus without any shock-between training and testing was given in a similar but not in a different apparatus [47]. In the same fashion, aged rats trained to run a radial maze according to a forced choice procedure, showed difficulties in running the maze subsequently according to a free choice procedure when the new task was presented in the same but not in a different context [30].

Conversely, decreased processing or encoding of contextual information is supported by the fact that aged rats exhibited some, though mild, long-term retention deficits in contextual fear conditioning [23], [31], [41] and showed long-term CTA irrespective of the context in which they were detained during the CS–US interval [21]. Clearly, the abundant literature showing spatial learning deficits in senescent rats [4], [17], [24], [37], may also indicate a poor utilization of background stimuli, in particular in view of data showing age-related differences in the modifications of hippocampal place cell activity following manipulations of contextual cues [5], [30], [42], [43].

Therefore, the present series of experiments examines the extent to which aged rats show defective processing of contextual information by using a variety of tasks and testing procedures. In Experiment 1, adult and aged rats were tested for contextual fear conditioning. Conditioned fear was estimated according to an experimental procedure that allows measurement of both the amount of freezing in the shock compartment and the avoidance of this compartment [19]. In Experiment 2, spatial performance of the same adult and aged rats was examined under distinct quantitative extra-maze cueing conditions (poor versus rich cueing) and successive context shifts.

Section snippets

Experiment 1

Rats were tested for contextual fear conditioning when exposed to six series, one per day, of ten pairings of a tone (CS) with a foot-shock (US) delivered in one of a two-compartment apparatus.

Subjects

Nineteen male Wistar rats (Harlan Nossan, Italy) served as subjects. At the beginning of testing, adult rats (N=10) were 7 months old and weighed ≈400–460 g, whereas aged rats (N=9) were 22 months old and weighed between 500 and 590 g. They were housed in pairs with water and food ad libitum in a temperature-controlled room (23°C) and on a 12-h light/dark cycle (lights on at 08:00 h). Rats were handled and weighed daily for 1 week before the start of the experiment.

Apparatus

The place-preference

Results

Two aged rats that died before the end of conditioning and one adult rat that did not move during the first place preference test (P0) were discarded from statistical treatments. Analyses were performed on data recorded in seven aged and nine adults rats.

Discussion

The results show that, in adult rats, contextual freezing developed after a single ten CS–US conditioning session, then progressively decreased over successive sessions. At the same time, the amount of freezing observed during CS presentation and after the last US of all sessions remained high, thus indicating that conditioning to the CS as well as the aversion for the US did not vary throughout testing. This finding confirms previous observations [19]) and suggests in agreement with several

Experiment 2

The effect of aging on the processing of contextual information was investigated next by comparing performance of adult and aged rats in spatial learning under distinct quantitative extra-maze cueing conditions (poor versus rich cueing) and successive context shifts.

Subjects

The subjects were the same as in Experiment 1, less three rats that either died during the experiment or did not move in the radial arm maze. Experiment 2 was therefore carried out with five 24-month aged rats and eight 9-month adult rats. One week before pre-training, rats were placed on a food-deprivation schedule. The daily food ration was adjusted to bring their weight to 85% of the initial level.

Apparatus

Two eight-arm radial mazes elevated to 70 cm above the floor were used. The first maze was made

Original training under poor cueing conditions

As rats were trained until a criterion of two errors or less over 2 consecutive days, or until 21 trials, the number of trials per subject was variable, thus precluding a day per day comparison of rats performance. We decided, therefore, to compare in each group the percentage of errors [(number of errors/total number of visited arms)×100] recorded during the first two trials and the last two trials preceding context change (Fig. 3A). Statistical comparisons were performed by a one-way (block

Discussion

All adult rats reached criterion when trained under poor cueing conditions. Subsequently, they showed an initial performance disruption followed by rapid improvement when tested under rich cueing as well as when returned to the initial poor cueing conditions. On the one hand, it can be assumed that the rapid improvement of performance following the first context shift likely depends on the fact that the learning paradigm was kept constant from one context to the other and also, that rats might

General discussion

Taken together, the present results show a number of age-related differences in contextual information processing. First, aged rats were found to display stronger freezing than adults when placed in the shock compartment on the day following the first series of CS–US pairings. On the one hand, this observation demonstrates that aged rats have stored some representation of the experimental context and are able to use it at a short retention interval. On the other hand, their intense freezing

Acknowledgements

The authors sincerely thank Paulette Richer for excellent technical assistance. They are also grateful to Hugh T. Blair, Center for Neural Science, New York University, New York and Bruce L. Brown, Queens College, New York, for reading and correcting the manuscript.

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