An independent, landmark-dominated head-direction signal in dysgranular retrosplenial cortex

Philippe, J; Casali, Giulio; Spieser, Laure; Page, Hector; Overington, Dorothy W. U.; Jeffery, Kate J.

doi:10.1038/nn.4465

Cited by 223 publications

(337 citation statements)

References 18 publications

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“…The latter have been shown to switch between active and inactive states, providing a directional representation that is controlled by visual landmarks instead of attractordynamics (Kornienko et al, 2018). Our present results are in line with the function and the location of these sensory HD-cells found in the entorhinal and parahippocampal cortex (Kornienko et al, 2018) as well as potentially in the RSC (Jacob et al, 2017). Some of these cells also alternate between several preferred directions depending on context, potentially explaining the variation in RSC tuning width we observed (Fig.…”

Section: Visual Information and Head Directionsupporting

confidence: 91%

“…We observed that multiple brain areas encoded direction, many of which overlap with regions known to contain HDcells in rodents and monkey. These regions include the RSC (Chen et al, 1994;Cho and Sharp, 2001;Jacob et al, 2017), the postsubiculum (part of the hippocampal formation) (Taube et al, 1990) and the entorhinal cortex (EC) (Giocomo et al, 2014;Kornienko et al, 2018;Sargolini et al, 2006). The latter consists of at least two subdivisions in rodents, the medial (MEC) and the lateral entorhinal cortex (LEC), likely corresponding to the pmEC and alEC in humans (Maass et al, 2015;Navarro Schröder et al, 2015).…”

Section: Visual Information and Head Directionmentioning

confidence: 99%

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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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Section: Visual Information and Head Directionsupporting

confidence: 91%

Section: Visual Information and Head Directionmentioning

confidence: 99%

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

Nau

Schröder²,

Frey

et al. 2019

Preprint

View full text Add to dashboard Cite

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“…One explanation could be that visual cues might be more salient for the vertical axis compared to the horizontal axis. Within the HD system, RSC is directly connected to early visual cortex (Kobayashi & Amaral, ) and HD cells in RSC are dominated by local visual landmarks (Jacob et al, ). Of note, presubiculum is also known to have direct connections with V2 in rodents (Vogt & Miller, ), but we are not aware of direct connections between the presubiculum and early visual cortex in primates.…”

Section: Discussionmentioning

confidence: 99%

Encoding of 3D head direction information in the human brain

Kim

Maguire

2018

Hippocampus

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Head direction cells are critical for navigation because they convey information about which direction an animal is facing within an environment. To date, most studies on head direction encoding have been conducted on a horizontal two‐dimensional (2D) plane, and little is known about how three‐dimensional (3D) direction information is encoded in the brain despite humans and other animals living in a 3D world. Here, we investigated head direction encoding in the human brain while participants moved within a virtual 3D “spaceship” environment. Movement was not constrained to planes and instead participants could move along all three axes in volumetric space as if in zero gravity. Using functional magnetic resonance imaging (fMRI) multivoxel pattern similarity analysis, we found evidence that the thalamus, particularly the anterior portion, and the subiculum encoded the horizontal component of 3D head direction (azimuth). In contrast, the retrosplenial cortex was significantly more sensitive to the vertical direction (pitch) than to the azimuth. Our results also indicated that vertical direction information in the retrosplenial cortex was significantly correlated with behavioral performance during a direction judgment task. Our findings represent the first evidence showing that the “classic” head direction system that has been identified on a horizontal 2D plane also seems to encode vertical and horizontal heading in 3D space in the human brain.

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“…RSC neurons have further been shown to 68 encode context as well as task-related cues such as goal location ( RSC and visual cortex. Finally, a subset of cells in RSC encode head direction in a way 73 that is particularly sensitive to local environmental cues (Jacob et al, 2017). A common 74 theme across these studies is the importance of visual inputs for RSC function.…”

Section: Introduction 23mentioning

confidence: 99%

Representation of Visual Landmarks in Retrosplenial Cortex

Fischer

Soto-Albors

Buck

et al. 2019

Preprint

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8The process by which visual information is incorporated into the brain's spatial framework 9to represent landmarks is poorly understood. Studies in humans and rodents suggest that 10 retrosplenial cortex (RSC) plays a key role in these computations. We developed an RSC-11 dependent behavioral task in which head-fixed mice learned the spatial relationship 12 between visual landmark cues and hidden reward locations. Two-photon imaging 13revealed that these cues served as dominant reference points for most task-active 14neurons and anchored the spatial code in RSC. Presenting the same environment but 15 decoupled from mouse behavior degraded encoding fidelity. Analyzing visual and motor 16responses showed that landmark codes were the result of supralinear integration. 17Surprisingly, V1 axons recorded in RSC showed similar receptive fields. However, they 18 were less modulated by task engagement, indicating that landmark representations in 19RSC are the result of local computations. Our data provide cellular-and network-level 20insight into how RSC represents landmarks. 21 22

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An independent, landmark-dominated head-direction signal in dysgranular retrosplenial cortex

Cited by 223 publications

References 18 publications

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

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

Encoding of 3D head direction information in the human brain

Representation of Visual Landmarks in Retrosplenial Cortex

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