Hippocampal and Retrosplenial Goal Distance Coding After Long-term Consolidation of a Real-World Environment.

E Zita Patai,Cheryl Grady,Jason D Ozubko,Gordon Winocur,Andrew O’Callaghan,Amir-Homayoun Javadi,Jessica Robin,Hugo J Spiers,R Shayna Rosenbaum,Shuman Ji,Morris Moscovitch

doi:10.1093/cercor/bhz044

Abstract

Recent research indicates the hippocampus may code the distance to the goal during navigation of newly learned environments. It is unclear however, whether this also pertains to highly familiar environments where extensive systems-level consolidation is thought to have transformed mnemonic representations. Here we recorded fMRI while University College London and Imperial College London students navigated virtual simulations of their own familiar campus (>2 years of exposure) and the other campus learned days before scanning. Posterior hippocampal activity tracked the distance to the goal in the newly learned campus, as well as in familiar environments when the future route contained many turns. By contrast retrosplenial cortex only tracked the distance to the goal in the familiar campus. All of these responses were abolished when participants were guided to their goal by external cues. These results open new avenues of research on navigation and consolidation of spatial information and underscore the notion that the hippocampus continues to play a role in navigation when detailed processing of the environment is needed for navigation.

Highlights

Understanding how the brain consolidates memories is a central question in neuroscience (Mcgaugh 2000)
Because multiple trace theory (MTT)/transformation theory (TTT) argues that the posterior hippocampus is involved in processing detailed information even after extensive consolidation (Moscovitch et al 2005) we examined whether the hippocampal activity might code the distance to the goal when the route ahead required the consideration of many possible turns
In agreement with the proposal of MTT/TTT that the hippocampus would play a greater role in the processing of detailed memories after extensive consolidation, we found that hippocampal activity tracked the distance to the goal in the familiar environments when detailed information about the future route was required

Summary

Introduction

Understanding how the brain consolidates memories is a central question in neuroscience (Mcgaugh 2000). Despite substantial interest in the neural circuits that support navigation, there has been little systematic investigation directly comparing consolidated spatial memories and representations of environments learned long ago (“familiar” environments) with those learned recently (Rosenbaum et al 2001; Spiers and Maguire 2007a; Winocur et al 2010). This dearth of research is surprising considering that current theories disagree about the contribution of the hippocampus to processing spatial representations over time: the standard consolidation theory (SCT) argues that initially the hippocampus is involved in processing the spatial memories, and that over time the representations in neocortical regions are strengthened, reducing the demand on the hippocampus (Squire 1992; Squire and Zola-Morgan 1998). For we cannot rule out whether the differences in hippocampal findings relate to the demands of navigating different cities, with London placing greater demands on mental simulation of future familiar routes than Toronto, or whether the structure of the environment is key to these differences (Spiers and Maguire 2007b)

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