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

2014 ◽  
Vol 369 (1635) ◽  
pp. 20130370 ◽  
Author(s):  
Bruno Poucet ◽  
Francesca Sargolini ◽  
Eun Y. Song ◽  
Balázs Hangya ◽  
Steven Fox ◽  
...  

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.

2011 ◽  
Vol 105 (6) ◽  
pp. 2989-3001 ◽  
Author(s):  
Ryan M. Yoder ◽  
Benjamin J. Clark ◽  
Joel E. Brown ◽  
Mignon V. Lamia ◽  
Stephane Valerio ◽  
...  

Successful navigation requires a constantly updated neural representation of directional heading, which is conveyed by head direction (HD) cells. The HD signal is predominantly controlled by visual landmarks, but when familiar landmarks are unavailable, self-motion cues are able to control the HD signal via path integration. Previous studies of the relationship between HD cell activity and path integration have been limited to two or more arenas located in the same room, a drawback for interpretation because the same visual cues may have been perceptible across arenas. To address this issue, we tested the relationship between HD cell activity and path integration by recording HD cells while rats navigated within a 14-unit T-maze and in a multiroom maze that consisted of unique arenas that were located in different rooms but connected by a passageway. In the 14-unit T-maze, the HD signal remained relatively stable between the start and goal boxes, with the preferred firing directions usually shifting <45° during maze traversal. In the multiroom maze in light, the preferred firing directions also remained relatively constant between rooms, but with greater variability than in the 14-unit maze. In darkness, HD cell preferred firing directions showed marginally more variability between rooms than in the lighted condition. Overall, the results indicate that self-motion cues are capable of maintaining the HD cell signal in the absence of familiar visual cues, although there are limits to its accuracy. In addition, visual information, even when unfamiliar, can increase the precision of directional perception.


2018 ◽  
Author(s):  
Samuel Ocko ◽  
Kiah Hardcastle ◽  
Lisa Giocomob ◽  
Surya Ganguli

Upon encountering a novel environment, an animal must construct a consistent environmental map, as well as an internal estimate of its position within that map, by combining information from two distinct sources: self-motion cues and sensory landmark cues. How do known aspects of neural circuit dynamics and synaptic plasticity conspire to accomplish this feat? Here we show analytically how a neural attractor model that combines path integration of self-motion cues with Hebbian plasticity in synaptic weights from landmark cells can self-organize a consistent map of space as the animal explores an environment. Intriguingly, the emergence of this map can be understood as an elastic relaxation process between landmark cells mediated by the attractor network. Moreover, our model makes several experimentally testable predictions, including: (1) systematic path-dependent shifts in the firing field of grid cells towards the most recently encountered landmark, even in a fully learned environment, (2) systematic deformations in the firing fields of grid cells in irregular environments, akin to elastic deformations of solids forced into irregular containers, and (3) the creation of topological defects in grid cell firing patterns through specific environmental manipulations. Taken together, our results conceptually link known aspects of neurons and synapses to an emergent solution of a fundamental computational problem in navigation, while providing a unified account of disparate experimental observations.


2018 ◽  
Vol 115 (50) ◽  
pp. E11798-E11806 ◽  
Author(s):  
Samuel A. Ocko ◽  
Kiah Hardcastle ◽  
Lisa M. Giocomo ◽  
Surya Ganguli

Upon encountering a novel environment, an animal must construct a consistent environmental map, as well as an internal estimate of its position within that map, by combining information from two distinct sources: self-motion cues and sensory landmark cues. How do known aspects of neural circuit dynamics and synaptic plasticity conspire to accomplish this feat? Here we show analytically how a neural attractor model that combines path integration of self-motion cues with Hebbian plasticity in synaptic weights from landmark cells can self-organize a consistent map of space as the animal explores an environment. Intriguingly, the emergence of this map can be understood as an elastic relaxation process between landmark cells mediated by the attractor network. Moreover, our model makes several experimentally testable predictions, including (i) systematic path-dependent shifts in the firing fields of grid cells toward the most recently encountered landmark, even in a fully learned environment; (ii) systematic deformations in the firing fields of grid cells in irregular environments, akin to elastic deformations of solids forced into irregular containers; and (iii) the creation of topological defects in grid cell firing patterns through specific environmental manipulations. Taken together, our results conceptually link known aspects of neurons and synapses to an emergent solution of a fundamental computational problem in navigation, while providing a unified account of disparate experimental observations.


2019 ◽  
Author(s):  
Dmitri Laptev ◽  
Neil Burgess

AbstractPlace cells and grid cells in the hippocampal formation are thought to integrate sensory and self-motion information into a representation of estimated spatial location, but the precise mechanism is unknown. We simulated a parallel attractor system in which place cells form an attractor network driven by environmental inputs and grid cells form an attractor network performing path integration driven by self-motion, with inter-connections between them allowing both types of input to influence firing in both ensembles. We show that such a system is needed to explain the spatial patterns and temporal dynamics of place cell firing when rats run on a linear track in which the familiar correspondence between environmental and self-motion inputs is changed (Gothard et al., 1996b; Redish et al., 2000). In contrast, the alternative architecture of a single recurrent network of place cells (performing path integration and receiving environmental inputs) cannot reproduce the place cell firing dynamics. These results support the hypothesis that grid and place cells provide two different but complementary attractor representations (based on self-motion and environmental sensory inputs respectively). Our results also indicate the specific neural mechanism and main predictors of hippocampal map realignment and make predictions for future studies.


2020 ◽  
Vol 4 ◽  
pp. 239821282095300
Author(s):  
Pierre-Yves Jacob ◽  
Tiffany Van Cauter ◽  
Bruno Poucet ◽  
Francesca Sargolini ◽  
Etienne Save

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.


2020 ◽  
Author(s):  
Hyuk-June Moon ◽  
Baptiste Gauthier ◽  
Hyeong-Dong Park ◽  
Nathan Faivre ◽  
Olaf Blanke

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.


Author(s):  
Alex F. Lim ◽  
Jonathan W. Kelly ◽  
Nathan C. Sepich ◽  
Lucia A. Cherep ◽  
Grace C. Freed ◽  
...  

2005 ◽  
Vol 565 (2) ◽  
pp. 579-591 ◽  
Author(s):  
Franco A. Taverna ◽  
John Georgiou ◽  
Robert J. McDonald ◽  
Nancy S. Hong ◽  
Alexander Kraev ◽  
...  

2022 ◽  
pp. 1-29
Author(s):  
Andrew R. Wagner ◽  
Megan J. Kobel ◽  
Daniel M. Merfeld

Abstract In an effort to characterize the factors influencing the perception of self-motion rotational cues, vestibular self-motion perceptual thresholds were measured in 14 subjects for rotations in the roll and pitch planes, as well as in the planes aligned with the anatomic orientation of the vertical semicircular canals (i.e., left anterior, right posterior; LARP, and right anterior, left posterior; RALP). To determine the multisensory influence of concurrent otolith cues, within each plane of motion, thresholds were measured at four discrete frequencies for rotations about earth-horizontal (i.e., tilts; EH) and earth-vertical axes (i.e., head positioned in the plane of the rotation; EV). We found that the perception of rotations, stimulating primarily the vertical canals, was consistent with the behavior of a high-pass filter for all planes of motion, with velocity thresholds increasing at lower frequencies of rotation. In contrast, tilt (i.e, EH rotation) velocity thresholds, stimulating both the canals and otoliths (i.e., multisensory integration), decreased at lower frequencies and were significantly lower than earth-vertical rotation thresholds at each frequency below 2 Hz. These data suggest that multisensory integration of otolithic gravity cues with semicircular canal rotation cues enhances perceptual precision for tilt motions at frequencies below 2 Hz. We also showed that rotation thresholds, at least partially, were dependent on the orientation of the rotation plane relative to the anatomical alignment of the vertical canals. Collectively these data provide the first comprehensive report of how frequency and axis of rotation influence perception of rotational self-motion cues stimulating the vertical canals.


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