Mesoscopic Neural Representations in Spatial Navigation

Kunz, Lukas; Maidenbaum, Shachar; Chen, Dong; Wang, Liang; Jacobs, Joshua; Axmacher, Nikolai

doi:10.1016/j.tics.2019.04.011

Cited by 64 publications

(68 citation statements)

References 154 publications

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“…9A-C), could reconstruct the modeled behavioral features more dynamically 28,29,87,88 . This could especially be helpful when combined with high temporal resolution measures, such as magnetoencephalography (MEG) or intracranial recordings, in combination with VR tasks 89 to monitor trial-by-trial changes in tuning as a function of behavioral performance. In addition, the influence of different sensory and behavioral variables on the present results could be further examined by removing the landmarks and testing which areas maintain their tuning, or by comparing the results to the ones of other visual encoding models.…”

Section: Discussionmentioning

confidence: 99%

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

Nau

Schröder²,

Frey

et al. 2020

Nat Commun

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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.

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Section: Discussionmentioning

confidence: 99%

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

Nau

Schröder²,

Frey

et al. 2020

Nat Commun

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show abstract

“…7) could address these questions directly by reconstructing the modeled behavioral features more dynamically (Gardner and Liu, 2019;Kriegeskorte and Douglas, 2019;Liu et al, 2018;Naselaris et al, 2011;Sprague et al, 2018Sprague et al, , 2019. In addition, high temporal resolution measures such as magnetoencephalography (MEG) or intracranial recordings in combination with VR-tasks (Kunz et al, 2019) could monitor trial by trial changes in tuning as a function of behavioral performance.…”

Section: Memory Retrieval and Learningmentioning

confidence: 99%

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

Nau

Schröder²,

Frey

et al. 2019

Preprint

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The brain derives cognitive maps from sensory experience to guide memory formation and behavior. Despite extensive efforts, it still remains unclear how the underlying population activity relates to active behavior and memory performance. Here, we combined 7T-fMRI with a kernelbased 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 and parahippocampal cortices and the hippocampus. 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 and show that high-level memory processing interacts with network-wide environmental coding in the service of behavior.

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“…After having established a relationship between theta oscillations and spatial memory, we sought to examine whether theta power exhibited hexagonal modulation with respect to the participants' head direction during walking. This effect is thought to resemble the grid cell system for navigation in rodents and has been observed in stationary human participants performing stationary 2-D virtual navigation 13,14,24,25 (Fig. 4a, b; Methods), however, has not yet been explored in freely moving humans navigating a real environment.…”

Section: Mainmentioning

confidence: 79%

Modulation of human intracranial theta oscillations during freely moving spatial navigation and memory

Aghajan

Villaroman

Hiller

et al. 2019

Preprint

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How the human brain supports accurate navigation of a learned environment has been an active topic of research for nearly a century 1-5 . In rodents, the theta rhythm within the medial temporal lobe (MTL) has been proposed as a neural basis for fragmenting incoming information and temporally organizing experiences and is thus widely implicated in spatial and episodic memory 6 . In addition, high-frequency theta (~8Hz) is associated with navigation, and loss of theta results in spatial memory deficits in rats 7 . Recently, high-frequency theta oscillations during ambulatory movement have been identified in humans 8,9 , though their relationship to spatial memory remains unexplored. Here, we were able to record MTL activity during spatial memory and navigation in freely moving humans immersed in a room-scale virtual reality (VR) environment. Naturalistic movements were captured using motion tracking combined with wireless VR in participants implanted with an intracranial electroencephalographic (iEEG) recording system for the treatment of epilepsy. We found that prevalence of theta oscillations across brain sites during both learning and recall of spatial locations during ambulatory navigation is critically linked to memory performance. This finding supports the reinstatement hypothesis of episodic memory-thought to underlie our ability to recreate a prior experience 10-12 -and suggests that theta prevalence within the MTL may act as a potential representational state for memory reinstatement during spatial navigation. Additionally, we found that theta power is hexadirectionally modulated 13-15 as a function of the direction of physical movement, most prominently after learning has occurred. This effect bears a resemblance to the rodent grid cell system 16 and suggests an analog in human navigation. Taken together, our results provide the first characterization of neural oscillations in the human MTL during ambulatory spatial memory tasks and provide a platform for future investigations of neural mechanisms underlying freely moving navigation in humans.

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Mesoscopic Neural Representations in Spatial Navigation

Cited by 64 publications

References 154 publications

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

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

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

Modulation of human intracranial theta oscillations during freely moving spatial navigation and memory

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