Behavior-dependent directional tuning in the human visual-navigation network

Matthias Nau,Markus Frey,Christian F Doeller,Tobias Navarro Schröder

doi:10.1038/s41467-020-17000-2

Matthias Nau, Markus Frey + Show 2 more

Open Access

https://doi.org/10.1038/s41467-020-17000-2

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Abstract

The brain derives cognitive maps from sensory experience that guide memory formation and behavior. Despite extensive efforts, it still remains unclear how the underlying population activity unfolds during spatial navigation and how it relates to memory performance. To examine these processes, we combined 7T-fMRI with a kernel-based encoding model of virtual navigation to map world-centered directional tuning across the human cortex. First, we present an in-depth analysis of directional tuning in visual, retrosplenial, parahippocampal and medial temporal cortices. Second, we show that tuning strength, width and topology of this directional code during memory-guided navigation depend on successful encoding of the environment. Finally, we show that participants’ locomotory state influences this tuning in sensory and mnemonic regions such as the hippocampus. We demonstrate a direct link between neural population tuning and human cognition, where high-level memory processing interacts with network-wide visuospatial coding in the service of behavior.

Highlights

The brain derives cognitive maps from sensory experience that guide memory formation and behavior
We modeled world-centered virtual head direction using basis sets of circular–Gaussian vHD kernels (Fig. 2a)
We developed an iterative kernel-based encoding model of the navigation behavior to map directional tuning across the human cortex

Summary

Introduction

The brain derives cognitive maps from sensory experience that guide memory formation and behavior. Previous studies revealed directional representations and activity related to heading perception in several areas, including the medial parietal lobe and retrosplenial cortex[15,16,17,18], the parahippocampal gyrus[17,19,20,21,22,23], the entorhinal/subicular cortex region[16,22,23,24,25], the thalamus[18], and the superior parietal cortex[26,27] Most of these studies used dedicated and constrained directional judgment- and mental imagery tasks, and often examined direction in a self-centered frame of reference. We examined how this tuning relates to the participants’ behavior and memory

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