Spontaneous object-location memory based on environmental geometry is impaired by both hippocampal and dorsolateral striatal lesions.

Steven L Poulter,David J Sanderson,Anthony Mcgregor,Yutaka Kosaki

doi:10.1177/2398212820972599

Steven L Poulter, David J Sanderson + Show 2 more

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https://doi.org/10.1177/2398212820972599

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Abstract

We examined the role of the hippocampus and the dorsolateral striatum in the representation of environmental geometry using a spontaneous object recognition procedure. Rats were placed in a kite-shaped arena and allowed to explore two distinctive objects in each of the right-angled corners. In a different room, rats were then placed into a rectangular arena with two identical copies of one of the two objects from the exploration phase, one in each of the two adjacent right-angled corners that were separated by a long wall. Time spent exploring these two objects was recorded as a measure of recognition memory. Since both objects were in different locations with respect to the room (different between exploration and test phases) and the global geometry (also different between exploration and test phases), differential exploration of the objects must be a result of initial habituation to the object relative to its local geometric context. The results indicated an impairment in processing the local geometric features of the environment for both hippocampus and dorsolateral striatum lesioned rats compared with sham-operated controls, though a control experiment showed these rats were unimpaired in a standard object recognition task. The dorsolateral striatum has previously been implicated in egocentric route-learning, but the results indicate an unexpected role for the dorsolateral striatum in processing the spatial layout of the environment. The results provide the first evidence that lesions to the hippocampus and dorsolateral striatum impair spontaneous encoding of local environmental geometric features.

Highlights

The hippocampus (HPC) is often said to support a cognitive map of the environment (O’Keefe and Nadel, 1978; Poulter et al, 2018) but what exactly is meant by a cognitive map is more equivocal (Bennett, 1996; Mackintosh, 2002)
To test whether animals form a representation of macroscopic geometric relations, animals trained in one environment are tested in another, which shares some of its geometric features with that of the training environment
Numerous studies have demonstrated that rodents with hippocampal lesions are not impaired in standard object recognition (Ainge et al, 2006; Mumby et al, 2002)

Summary

Introduction

The hippocampus (HPC) is often said to support a cognitive map of the environment (O’Keefe and Nadel, 1978; Poulter et al, 2018) but what exactly is meant by a cognitive map is more equivocal (Bennett, 1996; Mackintosh, 2002). If a cognitive map is a representation of the inter-relations among stimuli in the environment (Leonard and McNaughton, 1990), an animal that possessed one could represent the global layout of the environment. This notion is captured in the interpretation that when animals navigate relative to environmental geometry, they do so based on a configural representation of the shape of the environment, abstracted from the elements creating it (Cheng and Spetch, 1998; Gallistel, 1990). The test environment differs in its global shape to the training environment, so non-random search at test indicates that animals did not rely solely on a global representation of space in the initial exposure to the training environment, but instead were guided by local spatial features that the two environments shared (McGregor et al, 2006; Pearce et al, 2004; Tommasi and Polli, 2004). Pearce et al (2004) and subsequently Jones et al (2007) demonstrated that lesions to the HPC impaired navigation based on these local geometric properties of space

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