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 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.

scholarly journals Functional connectivity of the entorhinal–hippocampal space circuit

2014 ◽  
Vol 369 (1635) ◽  
pp. 20120516 ◽  
Author(s):  
Sheng-Jia Zhang ◽  
Jing Ye ◽  
Jonathan J. Couey ◽  
Menno Witter ◽  
Edvard I. Moser ◽  
...  
Keyword(s):  
Entorhinal Cortex ◽  
Cell Types ◽  
Place Cells ◽  
Projection Neurons ◽  
Border Cells ◽  
Head Direction ◽  
Grid Cells ◽  
Head Direction Cells ◽  
Dynamic Interactions ◽  
Cell Groups

The mammalian space circuit is known to contain several functionally specialized cell types, such as place cells in the hippocampus and grid cells, head-direction cells and border cells in the medial entorhinal cortex (MEC). The interaction between the entorhinal and hippocampal spatial representations is poorly understood, however. We have developed an optogenetic strategy to identify functionally defined cell types in the MEC that project directly to the hippocampus. By expressing channelrhodopsin-2 (ChR2) selectively in the hippocampus-projecting subset of entorhinal projection neurons, we were able to use light-evoked discharge as an instrument to determine whether specific entorhinal cell groups—such as grid cells, border cells and head-direction cells—have direct hippocampal projections. Photoinduced firing was observed at fixed minimal latencies in all functional cell categories, with grid cells as the most abundant hippocampus-projecting spatial cell type. We discuss how photoexcitation experiments can be used to distinguish the subset of hippocampus-projecting entorhinal neurons from neurons that are activated indirectly through the network. The functional breadth of entorhinal input implied by this analysis opens up the potential for rich dynamic interactions between place cells in the hippocampus and different functional cell types in the entorhinal cortex (EC).

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 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.

Bio-Inspired Robotics: A Spatial Cognition Model integrating Place Cells, Grid Cells and Head Direction Cells

2018 ◽  
Vol 91 (1) ◽  
pp. 85-99 ◽  
Author(s):  
Gonzalo Tejera ◽  
Martin Llofriu ◽  
Alejandra Barrera ◽  
Alfredo Weitzenfeld
Keyword(s):  
Spatial Cognition ◽  
Place Cells ◽  
Head Direction ◽  
Grid Cells ◽  
Head Direction Cells ◽  
Cognition Model

scholarly journals Three-dimensional tuning of head direction cells in rats

2019 ◽  
Vol 121 (1) ◽  
pp. 4-37 ◽  
Author(s):  
Michael E. Shinder ◽  
Jeffrey S. Taube
Keyword(s):  
Horizontal Plane ◽  
Reference Frames ◽  
Three Dimensional ◽  
Vertical Axis ◽  
Ventral Surface ◽  
Three Dimensions ◽  
Head Direction ◽  
Horizontal Canal ◽  
Cell Responses ◽  
The Earth

Head direction (HD) cells fire when the animal faces that cell’s preferred firing direction (PFD) in the horizontal plane. The PFD response when the animal is oriented outside the earth-horizontal plane could result from cells representing direction in the plane of locomotion or as a three-dimensional (3D), global-referenced direction anchored to gravity. To investigate these possibilities, anterodorsal thalamic HD cells were recorded from restrained rats while they were passively positioned in various 3D orientations. Cell responses were unaffected by pitch or roll up to ~90° from the horizontal plane. Firing was disrupted once the animal was oriented >90° away from the horizontal plane and during inversion. When rolling the animal around the earth-vertical axis, cells were active when the animal’s ventral surface faced the cell’s PFD. However, with the rat rolled 90° in an ear-down orientation, pitching the rat and rotating it around the vertical axis did not produce directionally tuned responses. Complex movements involving combinations of yaw-roll, but usually not yaw-pitch, resulted in reduced directional tuning even at the final upright orientation when the rat had full visual view of its environment and was pointing in the cell’s PFD. Directional firing was restored when the rat’s head was moved back-and-forth. There was limited evidence indicating that cells contained conjunctive firing with pitch or roll positions. These findings suggest that the brain’s representation of directional heading is derived primarily from horizontal canal information and that the HD signal is a 3D gravity-referenced signal anchored to a direction in the horizontal plane. NEW & NOTEWORTHY This study monitored head direction cell responses from rats in three dimensions using a series of manipulations that involved yaw, pitch, roll, or a combination of these rotations. Results showed that head direction responses are consistent with the use of two reference frames simultaneously: one defined by the surrounding environment using primarily visual landmarks and a second defined by the earth’s gravity vector.

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