Elsevier

Neuroscience

Volume 117, Issue 4, 10 April 2003, Pages 1025-1035
Neuroscience

Original contribution
Contribution of hippocampal place cell activity to learning and formation of goal-directed navigation in rats

https://doi.org/10.1016/S0306-4522(02)00700-5Get rights and content

Abstract

Although extensive behavioral studies have demonstrated that hippocampal lesions impair navigation toward specific places, the role of hippocampal neuronal activity in the development of efficient navigation during place learning remains unknown. The aim of the present study was to investigate how hippocampal neuronal activity changes as rats learn to navigate efficiently to acquire rewards in an open field. Rats were pre-trained in a random reward task where intracranial self-stimulation rewards were provided at random locations. Then, the rats were trained in a novel place task where they were rewarded at two specific locations as they repeatedly shuttled between them. Hippocampal neuronal activity was recorded during the course of learning of the place task. The rats learned reward sites within several sessions, and gradually developed efficient navigation strategies throughout the learning sessions. Some hippocampal neurons gradually changed spatial firing as the learning proceeded, and discharged robustly near the reward sites when efficient navigation was established. Over the learning sessions, the neuronal activity was highly correlated to formation of efficient shuttling trajectories between the reward sites. At the end of the experiment, spatial firing patterns of the hippocampal neurons were re-examined in the random reward task. The specific spatial firing patterns of the neurons were preserved if the rats navigated, as if they expected to find rewards at the previously valid locations. However, those specific spatial firing patterns were not observed in rats pursuing random trajectories.

These results suggest that hippocampal neurons have a crucial role in formation of an efficient navigation.

Section snippets

Subjects

Thirteen male albino Wistar rats (Sankyo Lab Service, Hamamatsu, Japan) were used. The rats weighed 270–320 g at the time of surgery, and were individually housed in a room with constant temperature and had food and water freely available. Efforts were made to minimize the number of animals used and their suffering. All rats were treated in strict compliance with the United States Public Health Service Policy on Human Care and Use of Laboratory Animals and the National Institutes of Health

Behavioral performance

Figure 2 summarizes the results of behavioral performance of 13 rats during learning of the PLT. The rats acquired 19.54±4.68 (mean±S.E.M.) rewards in the first session, and 46.54±3.14 rewards in the last session of the PLT (Fig. 2A). There was a significant improvement in the number of rewards between the first and last sessions of the PLT (Student’s t-test, P<0.01). The efficiency of acquiring rewards was quantified by dividing the traveled distance by the total number of rewards that the

Discussion

The present study investigated changes in the spatial firing of HF principal neurons during learning of a novel place task as measured by the efficiency of navigation strategies. We found that spatial firing of the HF neurons changed as learning proceeded. That is, changes of the HF neuron activity were well correlated to changes in rats’ shuttling behaviors between reward sites. Furthermore, spatial correlates established during learning of the PLT were preserved in the RRPST after the PLT to

Conclusions

The present study showed that plasticity of the HF neuron activity contributed to the formation of efficient navigation strategies to goals, and suggests that the activity of HF neurons might not merely serve to represent the current position of animals, but be associated with variables which have a major behavioral significance to solve a task. The HF neuron activity might represent the manner how animals have a significant relation to an environment as well as physical structures which

Acknowledgements

This work was supported by Japanese Ministry of Education, Culture, Sports, Science and Technology Grant-in-Aid for Scientific Research (11308033, 12210009, and 12680792). We thank Dr. Sidney I. Wiener, CNRS-College de France, for suggestions on a draft of the manuscript.

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