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

PLoS One. 2013 Jun 27;8(6):e67232. doi: 10.1371/journal.pone.0067232. Print 2013.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Corpus Striatum / cytology
  • Corpus Striatum / physiology*
  • Corpus Striatum / physiopathology
  • Hippocampus / cytology
  • Hippocampus / physiology*
  • Hippocampus / physiopathology
  • Ibotenic Acid
  • Male
  • Maze Learning / physiology
  • Mice, Inbred C57BL
  • Orientation / physiology
  • Proto-Oncogene Proteins c-fos
  • Random Allocation
  • Spatial Navigation / physiology*

Substances

  • Proto-Oncogene Proteins c-fos
  • Ibotenic Acid

Grants and funding

This work was supported by the Fondation pour la Recherche Médicale DEQ20120323730, France, and National Agency for Research ANR-REG-071220-01-01, France. CF was supported by a Region Ile de France PhD grant and France Alzheimer grants n°RAK09011DDA. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.