Hexadirectional Modulation of Theta Power in Human Entorhinal Cortex during Spatial Navigation

Chen, Dong; Kunz, Lukas; Wang, Wenjing; Zhang, Hui; Wang, Wen-Xu; Schulze‐Bonhage, Andreas; Reinacher, Peter C.; Zhou, Wenjing; Liang, Shuli; Axmacher, Nikolai; Wang, Liang

doi:10.1016/j.cub.2018.08.029

Cited by 49 publications

(54 citation statements)

References 49 publications

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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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“…Although a single grid cell intuitively exhibits hexadirectional activity, a hexadirectional bias on the population level might result if orientations (78,79) and spatial offsets to boundaries (160) of the firing patterns are clustered across cells. Further, this could potentially be reflected in directional biases in the local field potential in the EC; see also recent findings in MEG and intracranial electroencephalography (161)(162)(163). Additionally, conjunctive grid cells (25) also modulated by heading direction might contribute to the hexadirectional signal if the preferred directions of these cells align with the axes of the cells' grid pattern (22).…”

Section: Of 11mentioning

confidence: 99%

Navigating cognition: Spatial codes for human thinking

Bellmund

Gärdenfors

Moser

et al. 2018

Science

500

375

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The hippocampal formation has long been suggested to underlie both memory formation and spatial navigation. We discuss how neural mechanisms identified in spatial navigation research operate across information domains to support a wide spectrum of cognitive functions. In our framework, place and grid cell population codes provide a representational format to map variable dimensions of cognitive spaces. This highly dynamic mapping system enables rapid reorganization of codes through remapping between orthogonal representations across behavioral contexts, yielding a multitude of stable cognitive spaces at different resolutions and hierarchical levels. Action sequences result in trajectories through cognitive space, which can be simulated via sequential coding in the hippocampus. In this way, the spatial representational format of the hippocampal formation has the capacity to support flexible cognition and behavior.

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“…During experimental sessions, patients sat in bed and performed an object-location memory 480 task on a laptop computer ( Fig. 1), which was adapted from previous studies (16,(38)(39)(40)(41).…”

Section: Taskmentioning

confidence: 99%

A neural code for egocentric spatial maps in the human medial temporal lobe

Kunz

Brandt

Reinacher

et al. 2020

Preprint

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Spatial navigation relies on neural systems that encode spatial information relative to the external world or in relation to the navigating organism. Ever since the proposal of cognitive maps, the neuroscience of spatial navigation has focused on allocentric (world-referenced) neural representations such as place cells. Here, using single-neuron recordings during virtual 30 navigation, we reveal a neural code of egocentric (self-centered) spatial information in the human brain: We describe "anchor cells", which represent egocentric directions towards local "anchor points" distributed across the environmental center and periphery. Anchor-cell activity was abundant in parahippocampal cortex, signaled anchor-point distances, and showed memory modulation. Anchor cells may thus facilitate egocentric navigation 35 strategies, may assist in transforming percepts into allocentric spatial representations, and may underlie the first-person perspective in episodic memories. One Sentence Summary:Anchor cells in the human brain provide the neural basis for a self-centered coordinate 40 system during spatial navigation.3 Main text:Detailed neural representations of space form the neurobiological basis of successful navigation and accurate spatial memory. Traditionally, the neuroscience of spatial navigation has focused on allocentric representations, which encode spatial information in relation to the 45 external world: the place field of a place cell may be located in the "northeast" corner of an environment (1, 2), a head-direction cell may activate whenever navigating "south" (3), and a boundary vector/border cell may respond to a spatial boundary located "west" (4, 5). However, spatial environments are primarily experienced from a first-person, egocentric perspective -requiring neural codes that provide spatial information in relation to the self. 50 Via transformation circuits (6, 7), egocentric representations (8-10) may then be converted into their allocentric counterparts (4, 5, 11) for abstract knowledge and long-term storage (12).Despite abundant behavioral evidence that humans employ egocentric spatial information to accomplish wayfinding (12-15), little is known about the neural basis of egocentric spatial 55 representations in humans. Here, we hypothesized that neurons in human medial temporal lobe (MTL) keep track of the instantaneous relationship between the navigating subject and proximal areas of the environment. Specifically, we targeted the identification of "anchor cells" whose activity encodes the subject's egocentric direction towards local reference points (termed "anchor points"). Such a coding scheme would be instrumental for egocentric 60 navigation, because it provides orientation in relation to the proximal spatial layout.To detect and characterize human anchor cells, we recorded single-neuron activity from the MTL of ten neurosurgical epilepsy patients (table S1), while patients performed an objectlocation memory task in a virtual environment (Fig. 1, A and B). In this task (16), patients learne...

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Hexadirectional Modulation of Theta Power in Human Entorhinal Cortex during Spatial Navigation

Cited by 49 publications

References 49 publications

Hippocampal theta codes for distances in semantic and temporal spaces

Hippocampal theta codes for distances in semantic and temporal spaces

Navigating cognition: Spatial codes for human thinking

A neural code for egocentric spatial maps in the human medial temporal lobe

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