Dataset Information

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

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.

SUBMITTER: Fouquet C

PROVIDER: S-EPMC3695082 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

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

Fouquet Céline C Babayan Bénédicte M BM Watilliaux Aurélie A Bontempi Bruno B Tobin Christine C Rondi-Reig Laure L

PloS one 20130627 6

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 sequentia ...[more]

PMID: 23826243

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Project description:Humans and non-human animals show great flexibility in spatial navigation, including the ability to return to specific locations based on as few as one single experience. To study spatial navigation in the laboratory, watermaze tasks, in which rats have to find a hidden platform in a pool of cloudy water surrounded by spatial cues, have long been used. Analogous tasks have been developed for human participants using virtual environments. Spatial learning in the watermaze is facilitated by the hippocampus. In particular, rapid, one-trial, allocentric place learning, as measured in the delayed-matching-to-place variant of the watermaze task, which requires rodents to learn repeatedly new locations in a familiar environment, is hippocampal dependent. In this article, we review some computational principles, embedded within a reinforcement learning framework, that utilise hippocampal spatial representations for navigation in watermaze tasks. We consider which key elements underlie their efficacy, and discuss their limitations in accounting for hippocampus-dependent navigation, both in terms of behavioural performance (i.e. how well do they reproduce behavioural measures of rapid place learning) and neurobiological realism (i.e. how well do they map to neurobiological substrates involved in rapid place learning). We discuss how an actor-critic architecture, enabling simultaneous assessment of the value of the current location and of the optimal direction to follow, can reproduce one-trial place learning performance as shown on watermaze and virtual delayed-matching-to-place tasks by rats and humans, respectively, if complemented with map-like place representations. The contribution of actor-critic mechanisms to delayed-matching-to-place performance is consistent with neurobiological findings implicating the striatum and hippocampo-striatal interaction in delayed-matching-to-place performance, given that the striatum has been associated with actor-critic mechanisms. Moreover, we illustrate that hierarchical computations embedded within an actor-critic architecture may help to account for aspects of flexible spatial navigation. The hierarchical reinforcement learning approach separates trajectory control via a temporal-difference error from goal selection via a goal prediction error and may account for flexible, trial-specific, navigation to familiar goal locations, as required in some arm-maze place memory tasks, although it does not capture one-trial learning of new goal locations, as observed in open field, including watermaze and virtual, delayed-matching-to-place tasks. Future models of one-shot learning of new goal locations, as observed on delayed-matching-to-place tasks, should incorporate hippocampal plasticity mechanisms that integrate new goal information with allocentric place representation, as such mechanisms are supported by substantial empirical evidence.

Dataset Information

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

Publications

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

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