Allocentric representation in the human amygdala and ventral visual stream

Hallvard Røe Evensmoen,Lars M Rimol,Anderson M Winkler,Richard Betzel,Tor Ivar Hansen,Hamed Nili,Asta Håberg

doi:10.1016/j.celrep.2020.108658

Abstract

The hippocampus and the entorhinal cortex are considered the main brain structures for allocentric representation of the external environment. Here, we show that the amygdala and the ventral visual stream are involved in allocentric representation. Thirty-one young men explored 35 virtual environments during high-resolution functional magnetic resonance imaging (fMRI) of the medial temporal lobe (MTL) and were subsequently tested on recall of the allocentric pattern of the objects in each environment-in other words, the positions of the objects relative to each other and to the outer perimeter. We find increasingly unique brain activation patterns associated with increasing allocentric accuracy in distinct neural populations in the perirhinal cortex, parahippocampal cortex, fusiform cortex, amygdala, hippocampus, and entorhinal cortex. In contrast to the traditional view of a hierarchical MTL network with the hippocampus at the top, we demonstrate, using recently developed graph analyses, a hierarchical allocentric MTL network without a main connector hub.

Highlights

Mental representation of the external environment without reference to self-position, or allocentric representation, is critical for our way-finding ability (O’Keefe and Conway, 1978; Tolman, 1948)
A virtual navigation study in monkeys revealed that neuronal activity in a part of the ventral visual stream called the parahippocampal cortex (PHC) (Rosenke et al, 2018) conveyed more information about spatial location than activity in other medial temporal lobe (MTL) structures (Furuya et al, 2014), suggesting that the ventral visual stream is critically involved in spatial processing in primates
Assessment of environmental encoding To investigate allocentric representation in the human MTL, we acquired high-resolution functional magnetic resonance imaging (fMRI) (1.9 mm isotropic) data while healthy, right-handed young men freely explored 35 unique virtual environments, each of which contained 5 objects that were placed inside the room in a unique positional pattern

Summary

Introduction

Mental representation of the external environment without reference to self-position, or allocentric representation, is critical for our way-finding ability (O’Keefe and Conway, 1978; Tolman, 1948) It has long been a goal of neuroscientific research to identify the brain structures involved in allocentric representation and understand how these structures interact (Ekstrom et al, 2014, 2017; Epstein et al, 2017). The hippocampus and entorhinal cortex are considered the primary brain regions for allocentric representation in rats and humans (Ekstrom et al, 2014; Epstein et al, 2017; Evensmoen et al, 2015). The amygdala, well known for its role in emotional processing (LaBar and Cabeza, 2006), has a high percentage of place-responsive cells in

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Conclusion