scholarly journals Both visual and idiothetic cues contribute to head direction cell stability during navigation along complex routes

2011 ◽  
Vol 105 (6) ◽  
pp. 2989-3001 ◽  
Author(s):  
Ryan M. Yoder ◽  
Benjamin J. Clark ◽  
Joel E. Brown ◽  
Mignon V. Lamia ◽  
Stephane Valerio ◽  
...  
Keyword(s):  
Visual Information ◽  
Path Integration ◽  
Visual Cues ◽  
Cell Activity ◽  
Neural Representation ◽  
Head Direction ◽  
Motion Cues ◽  
Cell Stability ◽  
Self Motion ◽  
The Relationship

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.

scholarly journals Active Locomotion Increases Peak Firing Rates of Anterodorsal Thalamic Head Direction Cells

2001 ◽  
Vol 86 (2) ◽  
pp. 692-702 ◽  
Author(s):  
Michaël B. Zugaro ◽  
Eiichi Tabuchi ◽  
Céline Fouquier ◽  
Alain Berthoz ◽  
Sidney I. Wiener
Keyword(s):  
Visual Cues ◽  
Head Direction ◽  
Small Reservoir ◽  
Motion Cues ◽  
Preferred Direction ◽  
State Dependent ◽  
Command Signals ◽  
Rats And Mice ◽  
Foraging Task ◽  
Self Motion

Head direction (HD) cells discharge selectively in macaques, rats, and mice when they orient their head in a specific (“preferred”) direction. Preferred directions are influenced by visual cues as well as idiothetic self-motion cues derived from vestibular, proprioceptive, motor efferent copy, and command signals. To distinguish the relative importance of active locomotor signals, we compared HD cell response properties in 49 anterodorsal thalamic HD cells of six male Long-Evans rats during active displacements in a foraging task as well as during passive rotations. Since thalamic HD cells typically stop firing if the animals are tightly restrained, the rats were trained to remain immobile while drinking water distributed at intervals from a small reservoir at the center of a rotatable platform. The platform was rotated in a clockwise/counterclockwise oscillation to record directional responses in the stationary animals while the surrounding environmental cues remained stable. The peak rate of directional firing decreased by 27% on average during passive rotations ( r 2 = 0.73, P< 0.001). Individual cells recorded in sequential sessions ( n = 8) reliably showed comparable reductions in peak firing, but simultaneously recorded cells did not necessarily produce identical responses. All of the HD cells maintained the same preferred directions during passive rotations. These results are consistent with the hypothesis that the level of locomotor activity provides a state-dependent modulation of the response magnitude of AD HD cells. This could result from diffusely projecting neuromodulatory systems associated with motor state.

scholarly journals Deciphering the hippocampal polyglot: the hippocampus as a path integration system.

1996 ◽  
Vol 199 (1) ◽  
pp. 173-185 ◽  
Author(s):  
B L McNaughton ◽  
C A Barnes ◽  
J L Gerrard ◽  
K Gothard ◽  
M W Jung ◽  
...  
Keyword(s):  
Visual Information ◽  
Path Integration ◽  
Dimensional Space ◽  
Internal Representation ◽  
Place Cells ◽  
Head Direction ◽  
Integration System ◽  
Spatial Reference ◽  
Self Motion ◽  
Path Integrator

Hippocampal 'place' cells and the head-direction cells of the dorsal presubiculum and related neocortical and thalamic areas appear to be part of a preconfigured network that generates an abstract internal representation of two-dimensional space whose metric is self-motion. It appears that viewpoint-specific visual information (e.g. landmarks) becomes secondarily bound to this structure by associative learning. These associations between landmarks and the preconfigured path integrator serve to set the origin for path integration and to correct for cumulative error. In the absence of familiar landmarks, or in darkness without a prior spatial reference, the system appears to adopt an initial reference for path integration independently of external cues. A hypothesis of how the path integration system may operate at the neuronal level is proposed.

scholarly journals Functional correlates of the lateral and medial entorhinal cortex: objects, path integration and local–global reference frames

2014 ◽  
Vol 369 (1635) ◽  
pp. 20130369 ◽  
Author(s):  
James J. Knierim ◽  
Joshua P. Neunuebel ◽  
Sachin S. Deshmukh
Keyword(s):  
Entorhinal Cortex ◽  
Path Integration ◽  
Sensory Input ◽  
Reference Frames ◽  
External Input ◽  
Frame Of Reference ◽  
Medial Entorhinal Cortex ◽  
Motion Cues ◽  
Cortical Input ◽  
Self Motion

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.

scholarly journals The brain compass: a perspective on how self-motion updates the head direction cell attractor

2017 ◽  
Author(s):  
Jean Laurens ◽  
Dora E. Angelaki
Keyword(s):  
Degrees Of Freedom ◽  
Three Dimensional ◽  
Head Tilt ◽  
Head Direction ◽  
Motion Velocity ◽  
Head Direction Cells ◽  
Motion Cues ◽  
Head Direction Cell ◽  
On Line ◽  
Self Motion

ABSTRACTHead Direction cells form an internal compass that signals head azimuth orientation even in the absence of visual landmarks. It is well accepted that head direction properties are generated through a ring attractor that is updated using rotation self-motion cues. The properties and origin of this self-motion velocity drive remain, however, unknown. We propose a unified, quantitative framework whereby the attractor velocity input represents a multisensory self-motion estimate computed through an internal model that uses sensory prediction error based on vestibular, visual, and somatosensory cues to improve on-line motor drive. We show how context-dependent strength of recurrent connections within the attractor itself, rather than the self-motion input, explain differences in head direction cell firing between free foraging and restrained movements. We also summarize recent findings on how head tilt relative to gravity influences the azimuth coding of head direction cells, and explain why and how these effects reflect an updating self-motion velocity drive that is not purely egocentric. Finally, we highlight recent findings that the internal compass may be three-dimensional and hypothesize that the additional vertical degrees of freedom are defined based on global allocentric gravity cues.

scholarly journals Sources of path integration error in young and aging humans

2018 ◽  
Author(s):  
Matthias Stangl ◽  
Ingmar Kanitscheider ◽  
Martin Riemer ◽  
Ila Fiete ◽  
Thomas Wolbers
Keyword(s):  
Path Integration ◽  
Age Groups ◽  
Motion Cues ◽  
Elapsed Time ◽  
Integration Error ◽  
Age Related ◽  
Langevin Diffusion ◽  
Self Motion ◽  
Velocity Input ◽  
Shed Light

AbstractPath integration is a vital function in navigation: it enables the continuous tracking of one’s position in space by integrating self-motion cues. Path integration abilities vary across individuals but tend to deteriorate in old age. The specific causes of path integration errors, however, remain poorly characterized. Here, we combined tests of path integration performance with a novel analysis based on the Langevin diffusion equation, which allowed us to decompose errors into distinct causes that can corrupt path integration computations. Across age groups, the dominant errors were due to noise and a bias in speed estimation. Noise-driven errors accumulated with travel distance not elapsed time, suggesting that the dominant noise originates in the velocity input rather than within the integrator. Age-related declines were traced primarily to a growth in this unbiased noise. Together, these findings shed light on the contributors to path integration error and the mechanisms underlying age-related navigational deficits.

scholarly journals Head direction cell activity in the anterodorsal thalamus requires intact supragenual nuclei

2012 ◽  
Vol 108 (10) ◽  
pp. 2767-2784 ◽  
Author(s):  
Benjamin J. Clark ◽  
Joel E. Brown ◽  
Jeffrey S. Taube
Keyword(s):  
Horizontal Plane ◽  
Essential Role ◽  
Critical Role ◽  
Cell Activity ◽  
Head Direction ◽  
Vestibular Information ◽  
Familiar Environment ◽  
Cell Circuit ◽  
Bilateral Lesions ◽  
Self Motion

Neural activity in several limbic areas varies as a function of the animal's head direction (HD) in the horizontal plane. Lesions of the vestibular periphery abolish this HD cell signal, suggesting an essential role for vestibular afference in HD signal generation. The organization of brain stem pathways conveying vestibular information to the HD circuit is poorly understood; however, recent anatomical work has identified the supragenual nucleus (SGN) as a putative relay. To test this hypothesis, we made lesions of the SGN in rats and screened for HD cells in the anterodorsal thalamus. In animals with complete bilateral lesions, the overall number of HD cells was significantly reduced relative to control animals. In animals with unilateral lesions of the SGN, directional activity was present, but the preferred firing directions of these cells were unstable and less influenced by the rotation of an environmental landmark. In addition, we found that preferred directions displayed large directional shifts when animals foraged for food in a darkened environment and when they were navigating from a familiar environment to a novel one, suggesting that the SGN plays a critical role in projecting essential self-motion (idiothetic) information to the HD cell circuit.

Inference of perceptual priors from path dynamics of passive self-motion

2015 ◽  
Vol 113 (5) ◽  
pp. 1400-1413 ◽  
Author(s):  
Mario Prsa ◽  
Danilo Jimenez-Rezende ◽  
Olaf Blanke
Keyword(s):  
Path Integration ◽  
Bayesian Estimator ◽  
Whole Body ◽  
Movement Trajectory ◽  
Motion Cues ◽  
Movement Dynamics ◽  
History Of ◽  
Average Size ◽  
Self Motion ◽  
Over Time

The monitoring of one's own spatial orientation depends on the ability to estimate successive self-motion cues accurately. This process has become to be known as path integration. A feature of sequential cue estimation, in general, is that the history of previously experienced stimuli, or priors, biases perception. Here, we investigate how during angular path integration, the prior imparted by the displacement path dynamics affects the translation of vestibular sensations into perceptual estimates. Subjects received successive whole-body yaw rotations and were instructed to report their position within a virtual scene after each rotation. The overall movement trajectory either followed a parabolic path or was devoid of explicit dynamics. In the latter case, estimates were biased toward the average stimulus prior and were well captured by an optimal Bayesian estimator model fit to the data. However, the use of parabolic paths reduced perceptual uncertainty, and a decrease of the average size of bias and thus the weight of the average stimulus prior were observed over time. The produced estimates were, in fact, better accounted for by a model where a prediction of rotation magnitude is inferred from the underlying path dynamics on each trial. Therefore, when passively displaced, we seem to be able to build, over time, from sequential vestibular measurements an internal model of the vehicle's movement dynamics. Our findings suggest that in ecological conditions, vestibular afference can be internally predicted, even when self-motion is not actively generated by the observer, thereby augmenting both the accuracy and precision of displacement perception.

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 ◽  
...  
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.

scholarly journals Distance Estimation in Reproduction Tasks in a Harbor Seal (Phoca vitulina)

Water ◽  
2021 ◽  
Vol 13 (7) ◽  
pp. 938
Author(s):  
Eric Maaß ◽  
Frederike D. Hanke
Keyword(s):  
Visual Information ◽  
Path Integration ◽  
Visual Cues ◽  
Distance Estimation ◽  
Harbor Seal ◽  
Phoca Vitulina ◽  
Harbor Seals ◽  
Experimental Paradigm ◽  
Feeding Grounds ◽  
Specific Distance

Harbor seals commute between haul-out places and feeding grounds close to the shore or in the open ocean, which is considered a low structured environment, at first sight not providing many cues for orientation/navigation. Nevertheless, seals are well-oriented. For returning to a specific location, seals may use both external and internal cues to, for example, perform path integration requiring the integration of distances traveled and angles steered. We herein assessed the seal’s ability to estimate distances, previously swum or unknown, in reproduction tasks. Reproduction tasks refer to an experimental paradigm in which the experimental animal is required to swim a specific distance first and subsequently reproduce this distance, with visual cues present or absent. The seal was able to estimate and then reproduce distances (0.5–18.5 m) with the smallest error below 10% of the actual distance, and its precision was higher with distances repeatedly swum compared to its performance with unfamiliar distances. In the absence of visual cues, the seal’s performance slightly dropped; however, it was still able to perform the task with an error of 21%. In conclusion, distance estimation may help seals to navigate precisely towards their goals, even if, for example, visual information is not available.

scholarly journals Visual self-motion cues are impaired in Parkinson’s disease yet over-weighted during visual-vestibular integration

2019 ◽  
Author(s):  
Sol Yakubovich ◽  
Simon Israeli-Korn ◽  
Orly Halperin ◽  
Gilad Yahalom ◽  
Sharon Hassin-Baer ◽  
...  
Keyword(s):  
Parkinson’S Disease ◽  
Parkinson's Disease ◽  
Motion Perception ◽  
Visual Cues ◽  
Early Stage ◽  
Vestibular Function ◽  
Motion Platform ◽  
Motion Cues ◽  
Vestibular Cues ◽  
Self Motion

AbstractBackgroundParkinson’s disease (PD) is prototypically a movement disorder. Although perceptual and motor functions are interdependent, much less is known about perceptual dysfunction in PD. Perceptual deficits can impact activities of daily living, and contribute to motor symptoms, but might go unnoticed if not tested directly. Posture, gait and balance, affected in PD, rely on veridical perception of one’s own motion in space. Yet it is unknown whether self-motion perception is impaired in PD.ObjectivesTo test self-motion perception in PD, separately for visual and vestibular cues (unisensory), and multisensory integration thereof.MethodsParticipants (19 early stage PD, 23 age-matched and 20 young adult controls) experienced vestibular (motion platform), visual (optic flow), and combined visual-vestibular self-motion stimuli, and discriminated whether the stimulus headings were rightward or leftward of straight ahead. PD participants and age-matched controls were tested on two visits (PD on and off medication).ResultsPD participants had significantly impaired visual self-motion perception, both on and off medication. This deficit correlated significantly with clinical disease severity. By contrast, their vestibular performance was unimpaired. Remarkably, despite impaired visual self-motion perception, PD participants significantly over-weighted visual cues during multisensory (visual-vestibular) integration.ConclusionsSelf-motion perception is affected already in early stage PD, specifically by impaired visual (vs. vestibular) function, and by suboptimal visual-vestibular integration. This may contribute to impaired balance and gait control. Future investigation into this connection might open up new avenues for alternative therapies to better treat these symptoms. Furthermore, these results may also impact early PD diagnosis and subtyping.

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