Computing distance information from landmarks and self-motion cues - Differential contributions of anterior-lateral vs. posterior-medial entorhinal cortex in humans

The hippocampus receives its major cortical input from the medial entorhinal cortex (MEC) and the lateral entorhinal cortex (LEC). It is commonly believed that the MEC provides spatial input to the hippocampus, whereas the LEC provides non-spatial input. We review new data which suggest that this simple dichotomy between ‘where’ versus ‘what’ needs revision. We propose a refinement of this model, which is more complex than the simple spatial–non-spatial dichotomy. MEC is proposed to be involved in path integration computations based on a global frame of reference, primarily using internally generated, self-motion cues and external input about environmental boundaries and scenes; it provides the hippocampus with a coordinate system that underlies the spatial context of an experience. LEC is proposed to process information about individual items and locations based on a local frame of reference, primarily using external sensory input; it provides the hippocampus with information about the content of an experience.

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Medial entorhinal cortex lesions induce degradation of CA1 place cell firing stability when self-motion information is used

Brain and Neuroscience Advances ◽

10.1177/2398212820953004 ◽

2020 ◽

Vol 4 ◽

pp. 239821282095300

Author(s):

Pierre-Yves Jacob ◽

Tiffany Van Cauter ◽

Bruno Poucet ◽

Francesca Sargolini ◽

Etienne Save

Keyword(s):

Entorhinal Cortex ◽

Place Cell ◽

Motion Information ◽

Baseline Session ◽

Place Field ◽

Medial Entorhinal Cortex ◽

Motion Cues ◽

Place Fields ◽

Cell Firing ◽

Self Motion

The entorhinal–hippocampus network plays a central role in navigation and episodic memory formation. To investigate these interactions, we examined the effect of medial entorhinal cortex lesions on hippocampal place cell activity. Since the medial entorhinal cortex is suggested to play a role in the processing of self-motion information, we hypothesised that such processing would be necessary for maintaining stable place fields in the absence of environmental cues. Place cells were recorded as medial entorhinal cortex–lesioned rats explored a circular arena during five 16-min sessions comprising a baseline session with all sensory inputs available followed by four sessions during which environmental (i.e. visual, olfactory, tactile) cues were progressively reduced to the point that animals could rely exclusively on self-motion cues to maintain stable place fields. We found that place field stability and a number of place cell firing properties were affected by medial entorhinal cortex lesions in the baseline session. When rats were forced to rely exclusively on self-motion cues, within-session place field stability was dramatically decreased in medial entorhinal cortex rats relative to SHAM rats. These results support a major role of the medial entorhinal cortex in processing self-motion cues, with this information being conveyed to the hippocampus to help anchor and maintain a stable spatial representation during movement.

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Mouse entorhinal cortex encodes a diverse repertoire of self-motion signals

Nature Communications ◽

10.1038/s41467-021-20936-8 ◽

2021 ◽

Vol 12 (1) ◽

Author(s):

Caitlin S. Mallory ◽

Kiah Hardcastle ◽

Malcolm G. Campbell ◽

Alexander Attinger ◽

Isabel I. C. Low ◽

...

Keyword(s):

Entorhinal Cortex ◽

Medial Temporal Lobe ◽

Visual Cues ◽

Neural Circuits ◽

Sensory Cues ◽

Medial Entorhinal Cortex ◽

Representation Of Space ◽

Self Motion ◽

Information Streams ◽

Representations Of Space

AbstractNeural circuits generate representations of the external world from multiple information streams. The navigation system provides an exceptional lens through which we may gain insights about how such computations are implemented. Neural circuits in the medial temporal lobe construct a map-like representation of space that supports navigation. This computation integrates multiple sensory cues, and, in addition, is thought to require cues related to the individual’s movement through the environment. Here, we identify multiple self-motion signals, related to the position and velocity of the head and eyes, encoded by neurons in a key node of the navigation circuitry of mice, the medial entorhinal cortex (MEC). The representation of these signals is highly integrated with other cues in individual neurons. Such information could be used to compute the allocentric location of landmarks from visual cues and to generate internal representations of space.

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Independence of landmark and self-motion-guided navigation: a different role for grid cells

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2013.0370 ◽

2014 ◽

Vol 369 (1635) ◽

pp. 20130370 ◽

Cited By ~ 23

Author(s):

Bruno Poucet ◽

Francesca Sargolini ◽

Eun Y. Song ◽

Balázs Hangya ◽

Steven Fox ◽

...

Keyword(s):

Cell Activity ◽

Place Cell ◽

Grid Cells ◽

Distance Information ◽

Motion Cues ◽

Neuronal Populations ◽

System Changes ◽

Navigational System ◽

Self Motion ◽

Contrary Evidence

Recent interest in the neural bases of spatial navigation stems from the discovery of neuronal populations with strong, specific spatial signals. The regular firing field arrays of medial entorhinal grid cells suggest that they may provide place cells with distance information extracted from the animal's self-motion, a notion we critically review by citing new contrary evidence. Next, we question the idea that grid cells provide a rigid distance metric. We also discuss evidence that normal navigation is possible using only landmarks, without self-motion signals. We then propose a model that supposes that information flow in the navigational system changes between light and dark conditions. We assume that the true map-like representation is hippocampal and argue that grid cells have a crucial navigational role only in the dark. In this view, their activity in the light is predominantly shaped by landmarks rather than self-motion information, and so follows place cell activity; in the dark, their activity is determined by self-motion cues and controls place cell activity. A corollary is that place cell activity in the light depends on non-grid cells in ventral medial entorhinal cortex. We conclude that analysing navigational system changes between landmark and no-landmark conditions will reveal key functional properties.

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Visual cue-related activity of cells in the medial entorhinal cortex during navigation in virtual reality

eLife ◽

10.7554/elife.43140 ◽

2020 ◽

Vol 9 ◽

Cited By ~ 2

Author(s):

Amina A Kinkhabwala ◽

Yi Gu ◽

Dmitriy Aronov ◽

David W Tank

Keyword(s):

Entorhinal Cortex ◽

Path Integration ◽

Visual Cues ◽

Spatial Navigation ◽

Related Activity ◽

Estimation Errors ◽

Medial Entorhinal Cortex ◽

Cell Class ◽

Left And Right ◽

Self Motion

During spatial navigation, animals use self-motion to estimate positions through path integration. However, estimation errors accumulate over time and it is unclear how they are corrected. Here we report a new cell class (‘cue cell’) encoding visual cues that could be used to correct errors in path integration in mouse medial entorhinal cortex (MEC). During virtual navigation, individual cue cells exhibited firing fields only near visual cues and their population response formed sequences repeated at each cue. These cells consistently responded to cues across multiple environments. On a track with cues on left and right sides, most cue cells only responded to cues on one side. During navigation in a real arena, they showed spatially stable activity and accounted for 32% of unidentified, spatially stable MEC cells. These cue cell properties demonstrate that the MEC contains a code representing spatial landmarks, which could be important for error correction during path integration.

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Sense of self impacts spatial navigation and hexadirectional coding in human entorhinal cortex

10.1101/2020.09.13.295246 ◽

2020 ◽

Author(s):

Hyuk-June Moon ◽

Baptiste Gauthier ◽

Hyeong-Dong Park ◽

Nathan Faivre ◽

Olaf Blanke

Keyword(s):

Entorhinal Cortex ◽

Sense Of Self ◽

Spatial Navigation ◽

Cell Activity ◽

Grid Cell ◽

Retrosplenial Cortex ◽

Data Link ◽

Motion Cues ◽

Posterior Parietal ◽

Self Motion

AbstractGrid cells in entorhinal cortex (EC) encode an individual’s location in space and rely on environmental cues and self-motion cues derived from the individual’s body. Body-derived signals are also primary signals for the sense of self as located in space (i.e. bodily self-consciousness, BSC). However, it is currently unknown whether BSC impacts grid cell activity and how such changes relate to experimental modulations of BSC. Integrating BSC with a spatial navigation task and an fMRI measure to detect grid cell-like representation (GCLR) in humans, we report a robust GCLR modulation in EC when participants navigated during an enhanced BSC state. These changes were further associated with improved spatial navigation performance and increased activity in posterior parietal and retrosplenial cortex. These data link entorhinal grid cell activity with BSC and show that BSC modulates ego-versus allocentric spatial processes about an individual’s location in space in a distributed spatial navigation system.

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Medial entorhinal cortex and medial septum contribute to self-motion-based linear distance estimation

Brain Structure and Function ◽

10.1007/s00429-017-1368-4 ◽

2017 ◽

Vol 222 (6) ◽

pp. 2727-2742 ◽

Cited By ~ 21

Author(s):

Pierre-Yves Jacob ◽

Marta Gordillo-Salas ◽

Justine Facchini ◽

Bruno Poucet ◽

Etienne Save ◽

...

Keyword(s):

Entorhinal Cortex ◽

Distance Estimation ◽

Medial Septum ◽

Medial Entorhinal Cortex ◽

Linear Distance ◽

Self Motion

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Visual cue-related activity of cells in the medial entorhinal cortex during navigation in virtual reality

10.1101/453787 ◽

2018 ◽

Cited By ~ 1

Author(s):

Amina A. Kinkhabwala ◽

Yi Gu ◽

Dmitriy Aronov ◽

David W. Tank

Keyword(s):

Entorhinal Cortex ◽

Path Integration ◽

Visual Cues ◽

Large Fraction ◽

Estimation Errors ◽

Medial Entorhinal Cortex ◽

Visual Cue ◽

Visual Inputs ◽

Cell Class ◽

Self Motion

AbstractDuring spatial navigation, animals use self-motion to estimate positions through path integration. However, estimation errors accumulate over time and it is unclear how they are corrected. Here we report a new cell class (“cue cell”) in mouse medial entorhinal cortex (MEC) that encoded visual cue information that could be used to correct errors in path integration. Cue cells accounted for a large fraction of unidentified MEC cells. They exhibited firing fields only near visual cues during virtual navigation and spatially stable activity during navigation in a real arena. Cue cells’ responses occurred in sequences repeated at each cue and were likely driven by visual inputs. In layers 2/3 of the MEC, cue cells formed clusters. Anatomically adjacent cue cells responded similarly to cues. These cue cell properties demonstrate that the MEC circuits contain a code representing spatial landmarks that could play a significant role in error correction during path integration.

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