Interactions Between Idiothetic Cues and External Landmarks in the Control of Place Cells and Head Direction Cells

1998 ◽  
Vol 80 (1) ◽  
pp. 425-446 ◽  
Author(s):  
James J. Knierim ◽  
Hemant S. Kudrimoti ◽  
Bruce L. McNaughton
Keyword(s):  
Visual Cues ◽  
Place Cells ◽  
Exact Nature ◽  
Head Direction ◽  
Sources Of Information ◽  
Visual Landmarks ◽  
Head Direction Cells ◽  
Directional Information ◽  
Idiothetic Cues ◽  
Firing Properties

Knierim, James J., Hemant S. Kudrimoti, and Bruce L. McNaughton. Interactions between idiothetic cues and external landmarks in the control of place cells and head direction cells. J. Neurophysiol. 80: 425–446, 1998. Two types of neurons in the rat brain have been proposed to participate in spatial learning and navigation: place cells, which fire selectively in specific locations of an environment and which may constitute key elements of cognitive maps, and head direction cells, which fire selectively when the rat's head is pointed in a specific direction and which may serve as an internal compass to orient the cognitive map. The spatially and directionally selective properties of these cells arise from a complex interaction between input from external landmarks and from idiothetic cues; however, the exact nature of this interaction is poorly understood. To address this issue, directional information from visual landmarks was placed in direct conflict with directional information from idiothetic cues. When the mismatch between the two sources of information was small (45°), the visual landmarks had robust control over the firing properties of place cells; when the mismatch was larger, however, the firing fields of the place cells were altered radically, and the hippocampus formed a new representation of the environment. Similarly, the visual cues had control over the firing properties of head direction cells when the mismatch was small (45°), but the idiothetic input usually predominated over the visual landmarks when the mismatch was larger. Under some conditions, when the visual landmarks predominated after a large mismatch, there was always a delay before the visual cues exerted their control over head direction cells. These results support recent models proposing that prewired intrinsic connections enable idiothetic cues to serve as the primary drive on place cells and head direction cells, whereas modifiable extrinsic connections mediate a learned, secondary influence of visual landmarks.

scholarly journals The irregular firing properties of thalamic head direction cells mediate turn-specific modulation of the directional tuning curve

2014 ◽  
Vol 112 (9) ◽  
pp. 2316-2331 ◽  
Author(s):  
Marian Tsanov ◽  
Ehsan Chah ◽  
Muhammad S. Noor ◽  
Catriona Egan ◽  
Richard B. Reilly ◽  
...  
Keyword(s):  
High Voltage ◽  
Tuning Curve ◽  
Current Injection ◽  
Head Direction ◽  
Separation Angle ◽  
Head Direction Cells ◽  
Thalamic Neurons ◽  
Directional Information ◽  
Sinusoidal Current ◽  
Firing Properties

Head direction cells encode an animal's heading in the horizontal plane. However, it is not clear why the directionality of a cell's mean firing rate differs for clockwise, compared with counterclockwise, head turns (this difference is known as the “separation angle”) in anterior thalamus. Here we investigated in freely behaving rats whether intrinsic neuronal firing properties are linked to this phenomenon. We found a positive correlation between the separation angle and the spiking variability of thalamic head direction cells. To test whether this link is driven by hyperpolarization-inducing currents, we investigated the effect of thalamic reticular inhibition during high-voltage spindles on directional spiking. While the selective directional firing of thalamic neurons was preserved, we found no evidence for entrainment of thalamic head direction cells by high-voltage spindle oscillations. We then examined the role of depolarization-inducing currents in the formation of separation angle. Using a single-compartment Hodgkin-Huxley model, we show that modeled neurons fire with higher frequencies during the ascending phase of sinusoidal current injection (mimicking the head direction tuning curve) when simulated with higher high-threshold calcium channel conductance. These findings demonstrate that the turn-specific encoding of directional signal strongly depends on the ability of thalamic neurons to fire irregularly in response to sinusoidal excitatory activation. Another crucial factor for inducing phase lead to sinusoidal current injection was the presence of spike-frequency adaptation current in the modeled neurons. Our data support a model in which intrinsic biophysical properties of thalamic neurons mediate the physiological encoding of directional information.

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 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 Non-rhythmic head-direction cells in the parahippocampal region are not constrained by attractor network dynamics

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Olga Kornienko ◽  
Patrick Latuske ◽  
Mathis Bassler ◽  
Laura Kohler ◽  
Kevin Allen
Keyword(s):  
Entorhinal Cortex ◽  
Computational Models ◽  
Tuning Curve ◽  
Rhythmic Activity ◽  
External World ◽  
Head Direction ◽  
Visual Landmarks ◽  
Head Direction Cells ◽  
Medial Entorhinal Cortex ◽  
Attractor Network

Computational models postulate that head-direction (HD) cells are part of an attractor network integrating head turns. This network requires inputs from visual landmarks to anchor the HD signal to the external world. We investigated whether information about HD and visual landmarks is integrated in the medial entorhinal cortex and parasubiculum, resulting in neurons expressing a conjunctive code for HD and visual landmarks. We found that parahippocampal HD cells could be divided into two classes based on their theta-rhythmic activity: non-rhythmic and theta-rhythmic HD cells. Manipulations of the visual landmarks caused tuning curve alterations in most HD cells, with the largest visually driven changes observed in non-rhythmic HD cells. Importantly, the tuning modifications of non-rhythmic HD cells were often non-coherent across cells, refuting the notion that attractor-like dynamics control non-rhythmic HD cells. These findings reveal a new population of non-rhythmic HD cells whose malleable organization is controlled by visual landmarks.

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
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