Grid-like hexadirectional modulation of human entorhinal theta oscillations

Maidenbaum, Shachar; Miller, Jonathan; Stein, Joel M.; Jacobs, Joshua

doi:10.1073/pnas.1805007115

Cited by 53 publications

(67 citation statements)

References 35 publications

(46 reference statements)

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“…The idea of a 2-D semantic-temporal space suggests that other signatures of 2-D spatial navigation, such as hexadirectional modulation of neural activity, may also be detectable during episodic recall. Two groups recently showed that theta power in the human entorhinal cortex is hexadirectionally modulated during virtual navigation [58,59]. In the fMRI literature, it has been shown that hippocampal activity encodes for spatial [60] and abstract representational distances [61], and that hexadirectional modulation of the BOLD signal is observed during mental travel through abstract or imagined spaces [62,63].…”

Section: Discussionmentioning

confidence: 99%

Hippocampal theta codes for distances in semantic and temporal spaces

Solomon

Lega

Sperling

et al. 2019

Preprint

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The medial temporal lobe (MTL) is known to support episodic memory and spatial navigation, raising the possibility that its true function is to form "cognitive maps" of any kind of information. Studies in humans and animals support the idea that the hippocampal theta rhythm (4-8 Hz) is key to this mapping function, as it has been repeatedly observed during spatial navigation tasks. If episodic memory and spatial navigation are two sides of the same coin, we hypothesized that theta oscillations would also reflect relations between explicitly nonspatial items, such as words. We asked 189 neurosurgical patients to perform a verbal free-recall task, of which 96 had indwelling electrodes placed in the MTL. Subjects were instructed to remember short lists of sequentially-presented nouns. We found that hippocampal theta power and connectivity during item retrieval coded for semantic distances between words, as measured using word2vec-derived subspaces. Additionally, hippocampal theta indexed temporal distances between words after filtering lists on recall performance, to ensure adequate dynamic range in time. Theta effects were only noted for semantic subspaces of 1-dimension, indicating a substantial compression of the possible semantic feature space. These results lend further support to our growing confidence that the MTL forms cognitive maps of arbitrary representational spaces, reconciling longstanding differences between the spatial and episodic memory literatures.

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Section: Discussionmentioning

confidence: 99%

Hippocampal theta codes for distances in semantic and temporal spaces

Solomon

Lega

Sperling

et al. 2019

Preprint

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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: 78%

“…We employed methods that were previously applied to fMRI data from immobile participants 15 and were recently adapted to human iEEG data also in immobile participants who completed a view-based 2-D VR spatial navigation task 13,14 . First, we computed the allocentric head-direction of the participant (defined as the orientation of the rigid body tracked with the motion capture system) with respect to the physical room.…”

Section: Hexadirectional Modulation Of Theta Powermentioning

confidence: 99%

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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“…We developed AR and VR paradigms that adapted the "Treasure Hunt" spatial memory task, previously used in [17,18,20,31]. Treasure Hunt is an object-location associative memory task in which subjects are asked to remember the locations of various hidden objects in a virtual environment.…”

Section: Methodsmentioning

confidence: 99%

Studying Spatial Memory in Augmented and Virtual reality

Maidenbaum

Patel

Garlin

et al. 2019

Preprint

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Highlights• We built matching spatial memory tasks in VR and AR• Subjectively, subjects find the AR easier, more immersive and more fun• Objectively, subjects are significantly more accurate in AR compared to VR• Pointing based tasks did not fully show the same advantages • Only AR walking significantly correlated with SBSoD, suggesting mobile AR better captures more natural spatial performance Abstract Spatial memory is a crucial part of our lives. Spatial memory research and rehabilitation in humans is typically performed either in real environments, which is challenging practically, or in Virtual Reality (VR), which has limited realism. Here we explored the use of Augmented Reality (AR) for studying spatial cognition. AR combines the best features of real and VR paradigms by allowing subjects to learn spatial information in a flexible fashion while walking through a real-world environment. To compare these methods, we had subjects perform the same spatial memory task in VR and AR settings. Although subjects showed good performance in both, subjects reported that the AR task version was significantly easier, more immersive, and more fun than VR. Importantly, memory performance was significantly better in AR compared to VR. Our findings validate that integrating AR can lead to improved techniques for spatial memory research and suggest their potential for rehabilitation.

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Grid-like hexadirectional modulation of human entorhinal theta oscillations

Cited by 53 publications

References 35 publications

Hippocampal theta codes for distances in semantic and temporal spaces

Hippocampal theta codes for distances in semantic and temporal spaces

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

Studying Spatial Memory in Augmented and Virtual reality

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