Elsevier

Behavioural Brain Research

Volume 136, Issue 1, 17 October 2002, Pages 113-126
Behavioural Brain Research

Research report
Attenuation of context-specific inhibition on reversal learning of a stimulus–response task in rats with neurotoxic hippocampal damage

https://doi.org/10.1016/S0166-4328(02)00104-3Get rights and content

Abstract

Rats with hippocampal or sham lesions were trained on a stimulus–response task developed for the 8-arm radial maze. After reaching a stringent learning criterion, different context manipulations were performed. In Experiment I, the different groups were transferred to an identical radial maze in a different room to determine the context specificity of the discrimination learning. Experiment I revealed that although rats with hippocampal lesions did not show a normal context detection effect, the expression of the discrimination was not context dependent for either the lesion or sham groups. In Experiment II, animals were trained to criterion on the discrimination task and then both groups were divided into sub-groups based on whether they would experience reversal training in the same or different context from original training. Experiment II indicated that animals with hippocampal lesions and shams reversed in a different context were significantly enhanced in reaching the learning criterion compared to either counterparts that were reversed in the same context. Reversal learning in rats with hippocampal lesions was faster than sham animals in the same context suggesting that the context-specific inhibition effect was hippocampal-based. After learning the reversal task, the groups of animals trained and reversed in different contexts were brought back into the original training context to test for competitive effects. Animals with hippocampal lesions that were reversed in the different context, did not show a competition between the most recently acquired discrimination and a context-specific association acquired during original training whereas sham animals in the same condition did. Taken together these results suggest that rats with hippocampal lesions do not acquire normal context-specific inhibition during discrimination learning.

Introduction

There is evidence suggesting that the rat hippocampus is involved in place [45], [47], [41]; context [20], [57]; and relational learning and memory [53], [7]. Although debate persists on the precise conditions under which the rat hippocampus is critical for these paradigms, one theory suggests that rats with hippocampal damage have difficulty in acquiring these tasks when simple associative solutions are not available to them during training [44], [58], [35]. This view suggests that rats with hippocampal damage are impaired on these different categories of learning and memory paradigms (place, context, relational learning) because the computational requirements are similar. This critical computation may be the formation of a representation that encompasses various elements that define a specific event and the context in which it occurred [58]. In the intact animal, the hippocampus always appears to be encoding relationships among all elements of an experience into a representation of the event [33], [16], [43].

Early theorists have posited a general role for the hippocampus in a neural process similar to that of inhibition [10], [29], [17] in which associative processes lead to inhibition of behaviour because a conditioned stimulus (CS) becomes associated with non-reinforcement. This rather limited view of hippocampal function was initially abandoned and replaced by spatial, contextual, and relational theories of the hippocampus [21], [21], [44], [58], [11]. However, recent work suggests that the idea of the hippocampus being involved to some extent in inhibition of certain behaviours is worth reconsidering, and may not be entirely incompatible with more recent functions ascribed to the hippocampus.

Of particular interest to the present study is the function of the hippocampus and the relationship between discrimination learning and reversal, as well as latent inhibition and context conditioning. Modern views of reversal learning suggest that it should be considered an interference paradigm because the original contextual cues of the testing situation are the same but the stimulus–response (S–R) requirements are different. That is, the context acts as a retrieval cue for the S–R memory and when the discrimination is reversed the context re-activates the old S–R representation thereby interfering with new learning in that situation [20], [6].

One discrimination task that was developed for the eight-arm radial maze is an example of a task that lends itself to contextual manipulations because the task solution does not involve the use of spatial cues. Briefly, for this task lights were affixed along the inner side of each arm on the radial maze. On each day four of the eight arms were pseudo-randomly chosen to be lit and contained food. A rat was then placed on the central platform and allowed to forage throughout the maze. If a rat obtained a pellet from a lit arm the light for that arm would be turned off. Entries into the unlit arms were scored as errors. Following each training day, a new selection of baited arms was made. This task requires extensive amounts of training, the acquisition curve is slow, and is not dependent on stimulus-outcome associations [48], [39], [40], [54] which taken together is consistent with the idea that this task is acquired in an incremental S–R manner [25].

Using the S–R task described above, McDonald et al. [36] have shown that reversal learning in this paradigm was enhanced when animals were reversed in a context that was different from the one used during original training. One possible explanation for the interference effect shown in the group of rats reversed in the same context is that an inhibitory association was accrued to the non-reinforced dark arm. A similar explanation is used for the well-known latent inhibition paradigm that is characterized by a behavioural profile of reduced conditioned responding to a CS that has a history of non-reinforcement.

Since evidence suggests that inhibitory associations acquired during latent inhibition training show strong context specificity [59], [9], [31], [18] and the hippocampus has been implicated in context memory processes, the effects of hippocampal lesions on the context-specific inhibitory association found in the S–R task paradigm should be of considerable importance in understanding these processes and brain areas mediating such effects. Therefore, the purpose of the present experiment was to further evaluate the role of hippocampus in context detection, reversal learning and context-specific inhibition.

Section snippets

Animals and handling

Fifty-eight Long Evans male rats from Charles River colonies were used for the study. Upon arrival, animals were housed individually on a 12:12 light/dark cycle, and had food and water available to them ad libitum. A week following surgery animals were placed on a food deprivation schedule to reduce them to 90% of their free-feeding body weights. All rats weighed approximately 300–340 g at the beginning of the experiment. Animals were handled for 5 min each by the experimenter for 4–5 days

Experiment I: context detection in S–R learning

McDonald et al. [36] have previously shown that the expression of a S–R task on the radial maze was not dependent on the context in which it was learned. Results suggested that transient disruptions in performance were likely due to a novelty effect associated with the new context, and this was confirmed by an additional experiment that showed no decline in choice accuracy scores or alterations in latencies when novelty was controlled for. In the present study, Experiment I was performed to

Experiment II: effects of context on reversal learning of the S–R task

Previous work has shown that rats given reversal training in the same context, as original training, were impaired compared to rats reversed in a different context [36]. One interpretation of this pattern of data is that during initial acquisition in the original training context, an inhibitory association was acquired to the dark arm which interfered with reversal learning in rats remaining in that context [59], [36]. We were interested in using this task on rats with hippocampal lesions to

Discussion

The results reported in the present study support the idea that the hippocampus is involved in context-specific learning and memory processes. Experiment I showed that during a context shift, although choice accuracy scores remained high in animals with hippocampal damage their trial latencies was altered. Sham animals were more affected by the context shift as their choice accuracy and latency scores were transiently disrupted. These data are interpreted as evidence that shows that both groups

Acknowledgements

We wish to thank Tim Hong for excellent technical assistance, and the Vaccarino lab for generous use of their cryostat. This research was supported by a grant awarded to Dr Robert McDonald by the Natural Sciences and Engineering Research Council of Canada.

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