Complementary Roles of the Hippocampus and the Dorsomedial Striatum during Spatial and Sequence-Based Navigation Behavior

Céline Fouquet,Aurélie Watilliaux,Bénédicte M Babayan,Christine Tobin,Bruno Bontempi,Laure Rondi-Reig,Warren Meck

doi:10.1371/journal.pone.0067232

Céline Fouquet, Aurélie Watilliaux + Show 5 more

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https://doi.org/10.1371/journal.pone.0067232

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Abstract

We investigated the neural bases of navigation based on spatial or sequential egocentric representation during the completion of the starmaze, a complex goal-directed navigation task. In this maze, mice had to swim along a path composed of three choice points to find a hidden platform. As reported previously, this task can be solved by using two hippocampal-dependent strategies encoded in parallel i) the allocentric strategy requiring encoding of the contextual information, and ii) the sequential egocentric strategy requiring temporal encoding of a sequence of successive body movements associated to specific choice points. Mice were trained during one day and tested the following day in a single probe trial to reveal which of the two strategies was spontaneously preferred by each animal. Imaging of the activity-dependent gene c-fos revealed that both strategies are supported by an overlapping network involving the dorsal hippocampus, the dorsomedial striatum (DMS) and the medial prefrontal cortex. A significant higher activation of the ventral CA1 subregion was observed when mice used the sequential egocentric strategy. To investigate the potential different roles of the dorsal hippocampus and the DMS in both types of navigation, we performed region-specific excitotoxic lesions of each of these two structures. Dorsal hippocampus lesioned mice were unable to optimally learn the sequence but improved their performances by developing a serial strategy instead. DMS lesioned mice were severely impaired, failing to learn the task. Our data support the view that the hippocampus organizes information into a spatio-temporal representation, which can then be used by the DMS to perform goal-directed navigation.

Highlights

IntroductionExtensive research in rodents using navigation tasks has made a distinction between simple egocentric (response learning based on stimulus response-like associations) and allocentric (or placelearning) navigation [1]
Extensive research in rodents using navigation tasks has made a distinction between simple egocentric and allocentric navigation [1]
On the other hand, using a more complex paradigm, the starmaze task, we previously demonstrated that an additional strategy we called sequential egocentric is encoded concomitantly with the allocentric strategy [9], [10]

Summary

Introduction

Extensive research in rodents using navigation tasks has made a distinction between simple egocentric (response learning based on stimulus response-like associations) and allocentric (or placelearning) navigation [1] In such tasks, the dorso-striatal system mediates habit or response learning [2], [3], [4] and the hippocampal system predominantly supports place learning [5], [6]. The dorso-striatal system mediates habit or response learning [2], [3], [4] and the hippocampal system predominantly supports place learning [5], [6] This parallel functioning of the dorsal striatum and the hippocampus is not always clear-cut as revealed by recent findings. We hypothesized that the hippocampus and the dorsomedial striatum (DMS) could support together a spatial task which can be solved by mice using either an allocentric or a sequential egocentric strategy

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