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

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.

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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

10.1101/559336 ◽

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.

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

10.1101/570382 ◽

2019 ◽

Cited By ~ 2

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.

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Reply to Laurens and Angelaki: A model-based reassessment of the three-dimensional tuning of head direction cells in rats

Journal of Neurophysiology ◽

10.1152/jn.00525.2019 ◽

2019 ◽

Vol 122 (3) ◽

pp. 1288-1289 ◽

Cited By ~ 1

Author(s):

Jeffrey S. Taube

Keyword(s):

Three Dimensional ◽

Head Direction ◽

Head Direction Cells ◽

Model Based

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

Journal of Neurophysiology ◽

10.1152/jn.2001.85.1.105 ◽

2001 ◽

Vol 85 (1) ◽

pp. 105-116 ◽

Cited By ~ 44

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.

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

10.1101/189464 ◽

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.

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A Mathematical Model for the Morphology of the Pulmonary Acinus

Journal of Biomechanical Engineering ◽

10.1115/1.2795961 ◽

1996 ◽

Vol 118 (2) ◽

pp. 210-215 ◽

Cited By ~ 12

Author(s):

E. Denny ◽

R. C. Schroter

Keyword(s):

Experimental Data ◽

Mathematical Model ◽

Dimensional Space ◽

Three Dimensional ◽

Computational Method ◽

Published Data ◽

Space Filling ◽

Pulmonary Acinus ◽

Path Lengths ◽

Three Dimensional Space

A computational method is proposed for the construction of a three-dimensional space-filling model of an acinar ventilatory unit. Its geometry consists of truncated octahedra arranged in a cuboidal block. The ducts and alveoli are formed by opening specific common faces between polyhedra. The branching structure is automatically computed using algorithms solely to maximise the number of alveoli and minimise the average path lengths; it is not formed with reference to published experimental data. Properties of the model such as the total alveolar and ductal volumes, the distribution of individual path lengths to the alveolar sacs, and the average number of ducts per generation are calculated. The predicted morphology of the model compares well with published data for rat lungs.

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