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 A gravity-based three-dimensional compass in the mouse brain

2019 ◽  
Author(s):  
Dora E Angelaki ◽  
J Ng ◽  
AM Abrego ◽  
HX Cham ◽  
JD Dickman ◽  
...  
Keyword(s):  
Horizontal Plane ◽  
Degrees Of Freedom ◽  
Mammalian Species ◽  
Three Dimensional ◽  
Retrosplenial Cortex ◽  
Orientation Tuning ◽  
Head Direction ◽  
Head Direction Cells ◽  
Dimensional Gravity ◽  
Three Degrees Of Freedom

SummaryHead direction cells in the mammalian limbic system are thought to function as an allocentric neuronal compass. Although traditional views hold that the compass of ground-dwelling species is planar, we show that head-direction cells in the rodent thalamus, retrosplenial cortex and cingulum fiber bundle are tuned to conjunctive combinations of azimuth, pitch or roll, similarly to presubicular cells in flying bats. Pitch and roll orientation tuning is ubiquitous, anchored to gravity, and independent of visual landmarks. When head tilts, azimuth tuning is affixed to the head-horizontal plane, but also uses gravity to remain anchored to the terrestrial allocentric world. These findings suggest that gravity defines all three degrees of freedom of the allocentric orientation compass, and only the azimuth component can flexibly remap to local cues in different environments. Collectively, these results demonstrate that a three-dimensional, gravity-based, neural compass is likely a ubiquitous property of mammalian species, including ground-dwelling animals.

Hippocampal Place-Cell Firing During Movement in Three-Dimensional Space

2001 ◽  
Vol 85 (1) ◽  
pp. 105-116 ◽  
Author(s):  
James J. Knierim ◽  
Bruce L. McNaughton
Keyword(s):  
Hippocampal Neurons ◽  
Horizontal Plane ◽  
Three Dimensional ◽  
Place Cell ◽  
Place Cells ◽  
Limbic Cortex ◽  
Head Direction ◽  
Head Direction Cells ◽  
Recording Apparatus ◽  
Place Fields

“Place” cells of the rat hippocampus are coupled to “head direction” cells of the thalamus and limbic cortex. Head direction cells are sensitive to head direction in the horizontal plane only, which leads to the question of whether place cells similarly encode locations in the horizontal plane only, ignoring the z axis, or whether they encode locations in three dimensions. This question was addressed by recording from ensembles of CA1 pyramidal cells while rats traversed a rectangular track that could be tilted and rotated to different three-dimensional orientations. Cells were analyzed to determine whether their firing was bound to the external, three-dimensional cues of the environment, to the two-dimensional rectangular surface, or to some combination of these cues. Tilting the track 45° generally provoked a partial remapping of the rectangular surface in that some cells maintained their place fields, whereas other cells either gained new place fields, lost existing fields, or changed their firing locations arbitrarily. When the tilted track was rotated relative to the distal landmarks, most place fields remapped, but a number of cells maintained the same place field relative to the x-y coordinate frame of the laboratory, ignoring the z axis. No more cells were bound to the local reference frame of the recording apparatus than would be predicted by chance. The partial remapping demonstrated that the place cell system was sensitive to the three-dimensional manipulations of the recording apparatus. Nonetheless the results were not consistent with an explicit three-dimensional tuning of individual hippocampal neurons nor were they consistent with a model in which different sets of cells are tightly coupled to different sets of environmental cues. The results are most consistent with the statement that hippocampal neurons can change their “tuning functions” in arbitrary ways when features of the sensory input or behavioral context are altered. Understanding the rules that govern the remapping phenomenon holds promise for deciphering the neural circuitry underlying hippocampal function.

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 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 A model-based reassessment of the three-dimensional tuning of head direction cells in rats

2019 ◽  
Vol 122 (3) ◽  
pp. 1274-1287 ◽  
Author(s):  
Jean Laurens ◽  
Dora E. Angelaki
Keyword(s):  
Experimental Data ◽  
Model Comparison ◽  
Three Dimensional ◽  
Orientation Tuning ◽  
Head Orientation ◽  
Published Data ◽  
Head Direction ◽  
Head Direction Cells ◽  
Vertical Orientation ◽  
Model Based

In a recent study, Shinder and Taube (Shinder ME, Taube JS. J Neurophysiol 121: 4–37, 2019) concluded that head direction cells in the anterior thalamus of rats are tuned to one-dimensional (1D, yaw-only) motion, in contrast to recent findings in bats, mice, and rats. Here we reinterpret the author’s experimental results using model comparison and demonstrate that, contrary to their conclusions, experimental data actually supports the dual-axis rule (lson JJ, Jeffery KJ. J Neurophysiol 119: 192–208, 2018) and tilted azimuth model (Laurens J, Angelaki DE. Neuron 97: 275–289, 2018), where head direction cells use gravity to integrate 3D rotation signals about all cardinal axes of the head. We further show that the Shinder and Taube study is inconclusive regarding the presence of vertical orientation tuning; i.e., whether head direction cells encode 3D orientation in the horizontal and vertical planes conjunctively. Using model simulations, we demonstrate that, even if 3D tuning existed, the experimental protocol and data analyses used by Shinder and Taube would not have revealed it. We conclude that the actual experimental data of Shinder and Taube are compatible with the 3D properties of head direction cells discovered by other groups, yet incorrect conclusions were reached because of incomplete and qualitative analyses. NEW & NOTEWORTHY We conducted a model-based analysis previously published data where rat head direction cells were recorded during three-dimensional motion (Shinder ME, Taube JS. J Neurophysiol 121: 4–37, 2019). We found that these data corroborate previous models (“dual-axis rule,” Page HJI, Wilson JJ, Jeffery KJ. J Neurophysiol 119: 192–208, 2018; and “tilted azimuth model,” Laurens J, Angelaki DE. Neuron 97: 275–289, 2018) where head direction cells integrate rotations along all three head axes to encode head orientation in a gravity-anchored reference frame.

scholarly journals A re-interpretation of the experimental data of Shinder and Taube “Three-dimensional Tuning of Head Direction Cells in Rats”, Journal of Neurophysiology 121(1), 2019

2019 ◽  
Author(s):  
Jean Laurens ◽  
Dora E. Angelaki
Keyword(s):  
Experimental Data ◽  
Model Comparison ◽  
Three Dimensional ◽  
Orientation Tuning ◽  
Head Direction ◽  
Experimental Protocol ◽  
Head Direction Cells ◽  
Vertical Orientation ◽  
One Dimensional ◽  
Anterior Thalamus

AbstractIn a recent study, Shinder and Taube (2019) concluded that head direction cells in the anterior thalamus of rats are tuned to one-dimensional (1D, yaw-only) motion exclusively, in contrast to recent findings in bats (Finkelstein et al. 2015), mice (Angelaki et al. 2016; Cham et al. 2017; Laurens et al. 2017), and rats (Page et al. 2017). Here we re-interpret the author’s experimental results using model comparison and demonstrate that, contrary to their conclusions, their data actually supports the dual-axis rule (Page et al. 2017) and tilted azimuth model (Laurens and Angelaki 2018), where head direction cells use gravity to integrate 3D rotation signals about all cardinal axes of the head. We further show that this study is inconclusive regarding the presence of vertical orientation tuning; i.e. whether head direction cells encode 3D orientation in the horizontal and vertical planes conjunctively. Using model simulations, we demonstrate that, even if 3D tuning existed, the experimental protocol and data analyses used by Shinder and Taube (2019) would not have revealed it. We conclude that the actual experimental data of Shinder and Taube (2019) are compatible with the 3D properties of head direction cells discovered by other groups, yet incorrect conclusions were reached because of incomplete and qualitative analyses.

Design and calibration of an IVEM for general 3-dimensional imaging of non-diffracting materials

1992 ◽  
Vol 50 (2) ◽  
pp. 1040-1041
Author(s):  
Neil Rowlands ◽  
Jeff Price ◽  
Michael Kersker ◽  
Seichi Suzuki ◽  
Steve Young ◽  
...  
Keyword(s):  
3D Imaging ◽  
Tomographic Reconstruction ◽  
Three Dimensional ◽  
3 Dimensional ◽  
3D Microstructure ◽  
Image Translation ◽  
Digital Correlation ◽  
On Line ◽  
Mechanical Stage ◽  
Projection Angle

Three-dimensional (3D) microstructure visualization on the electron microscope requires that the sample be tilted to different positions to collect a series of projections. This tilting should be performed rapidly for on-line stereo viewing and precisely for off-line tomographic reconstruction. Usually a projection series is collected using mechanical stage tilt alone. The stereo pairs must be viewed off-line and the 60 to 120 tomographic projections must be aligned with fiduciary markers or digital correlation methods. The delay in viewing stereo pairs and the alignment problems in tomographic reconstruction could be eliminated or improved by tilting the beam if such tilt could be accomplished without image translation.A microscope capable of beam tilt with simultaneous image shift to eliminate tilt-induced translation has been investigated for 3D imaging of thick (1 μm) biologic specimens. By tilting the beam above and through the specimen and bringing it back below the specimen, a brightfield image with a projection angle corresponding to the beam tilt angle can be recorded (Fig. 1a).

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