scholarly journals Uncoupling of dysgranular retrosplenial “head direction” cells from the global head direction network

2016 ◽  
Author(s):  
Pierre-Yves Jacob ◽  
Giulio Casali ◽  
Laure Spieser ◽  
Hector Page ◽  
Dorothy Overington ◽  
...  
Keyword(s):  
Brain Regions ◽  
Retrosplenial Cortex ◽  
Head Direction ◽  
Visual Landmarks ◽  
Head Direction Cells ◽  
Cognitive Representations ◽  
Sense Of Direction ◽  
Rotationally Symmetric ◽  
Subcortical Regions ◽  
Animal Faces

AbstractSpatial cognition is an important model system with which to investigate how sensory signals are transformed into cognitive representations. Head direction cells, found in several cortical and subcortical regions, fire when an animal faces a given direction and express a global directional signal which is anchored by visual landmarks and underlies the “sense of direction”. We investigated the interface between visual and spatial cortical brain regions and report the discovery that a population of neurons in the dysgranular retrosplenial cortex, which we co-recorded with classic head direction cells in a rotationally symmetrical two-compartment environment, were dominated by a local visually defined reference frame and could be decoupled from the main head direction signal. A second population showed rotationally symmetric activity within a single sub-compartment suggestive of an acquired interaction with the head direction cells. These observations reveal an unexpected incoherence within the head direction system, and suggest that dysgranular retrosplenial cortex may mediate between visual landmarks and the multimodal sense of direction. Importantly, it appears that this interface supports a bi-directional exchange of information, which could explain how it is that landmarks can inform the direction sense while at the same time, the direction sense can be used to interpret landmarks.

scholarly journals Oscillatory synchrony between head direction cells recorded bilaterally in the anterodorsal thalamic nuclei

2017 ◽  
Vol 117 (5) ◽  
pp. 1847-1852 ◽  
Author(s):  
William N. Butler ◽  
Jeffrey S. Taube
Keyword(s):  
High Frequency ◽  
Brain Regions ◽  
High Frequency Oscillation ◽  
Head Direction ◽  
Thalamic Nuclei ◽  
Head Direction Cells ◽  
Oscillatory Pattern ◽  
Cross Correlations ◽  
Left And Right ◽  
The Cross

The head direction (HD) circuit is a complex interconnected network of brain regions ranging from the brain stem to the cortex. Recent work found that HD cells corecorded ipsilaterally in the anterodorsal nucleus (ADN) of the thalamus displayed coordinated firing patterns. A high-frequency oscillation pattern (130–160 Hz) was visible in the cross-correlograms of these HD cell pairs. Spectral analysis further found that the power of this oscillation was greatest at 0 ms and decreased at greater lags, and demonstrated that there was greater synchrony between HD cells with similar preferred firing directions. Here, we demonstrate that the same high-frequency synchrony exists in HD cell pairs recorded contralaterally from one another in the bilateral ADN. When we examined the cross-correlograms of HD cells that were corecorded bilaterally, we observed the same high-frequency (~150- to 200-Hz) oscillatory relationship. The strength of this synchrony was similar to the synchrony seen in ipsilateral HD cell pairs, and the degree of synchrony in each cross-correlogram was dependent on the difference in tuning between the two cells. Additionally, the frequency rate of this oscillation appeared to be independent of the firing rates of the two cross-correlated cells. Taken together, these results imply that the left and right thalamic HD network are functionally related despite an absence of direct anatomical projections. However, anatomical tracing has found that each of the lateral mammillary nuclei (LMN) project bilaterally to both of the ADN, suggesting the LMN may be responsible for the functional connectivity observed between the two ADN. NEW & NOTEWORTHY This study used bilateral recording electrodes to examine whether head direction cells recorded simultaneously in both the left and right thalamus show coordinated firing. Cross-correlations of the cells’ spike trains revealed a high-frequency oscillatory pattern similar to that seen in cross-correlations between pairs of ipsilateral head direction cells, demonstrating that the bilateral thalamic head direction signals may be part of a single unified network.

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.

scholarly journals Retrosplenial and postsubicular head direction cells compared during visual landmark discrimination

2017 ◽  
Vol 1 ◽  
pp. 239821281772185 ◽  
Author(s):  
Yave Roberto Lozano ◽  
Hector Page ◽  
Pierre-Yves Jacob ◽  
Eleonora Lomi ◽  
James Street ◽  
...  
Keyword(s):  
Cell Activity ◽  
Place Cell ◽  
Retrosplenial Cortex ◽  
Head Direction ◽  
Visual Landmarks ◽  
Tuning Curves ◽  
Visual Inputs ◽  
Visual Areas ◽  
Cortical Regions ◽  
Rapid Processing

Background: Visual landmarks are used by head direction (HD) cells to establish and help update the animal’s representation of head direction, for use in orientation and navigation. Two cortical regions that are connected to primary visual areas, postsubiculum (PoS) and retrosplenial cortex (RSC), possess HD cells: we investigated whether they differ in how they process visual landmarks. Methods: We compared PoS and RSC HD cell activity from tetrode-implanted rats exploring an arena in which correct HD orientation required discrimination of two opposing landmarks having high, moderate or low discriminability. Results: RSC HD cells had higher firing rates than PoS HD cells and slightly lower modulation by angular head velocity, and anticipated actual head direction by ~48 ms, indicating that RSC spiking leads PoS spiking. Otherwise, we saw no differences in landmark processing, in that HD cells in both regions showed equal responsiveness to and discrimination of the cues, with cells in both regions having unipolar directional tuning curves and showing better discrimination of the highly discriminable cues. There was a small spatial component to the signal in some cells, consistent with their role in interacting with the place cell navigation system, and there was also slight modulation by running speed. Neither region showed theta modulation of HD cell spiking. Conclusions: That the cells can immediately respond to subtle differences in spatial landmarks is consistent with rapid processing of visual snapshots or scenes; similarities in PoS and RSC responding may be due either to similar computations being performed on the visual inputs, or to rapid sharing of information between these regions. More generally, this two-cue HD cell paradigm may be a useful method for testing rapid spontaneous visual discrimination capabilities in other experimental settings.

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 Global and Local Head Direction Coding in the Human Brain

2021 ◽  
Author(s):  
J. P. Shine ◽  
T. Wolbers
Keyword(s):  
Reference Frames ◽  
Brain Regions ◽  
Retrosplenial Cortex ◽  
Specific Reference ◽  
Head Direction ◽  
Imaging Data ◽  
Neural Basis ◽  
Local Environments ◽  
Human Participants ◽  
Global And Local

AbstractOrientation-specific head direction (HD) cells increase their firing rate to indicate one’s facing direction in the environment. Rodent studies suggest HD cells in distinct areas of thalamus and retrosplenial cortex (RSC) code either for global (relative to the wider environment) or local (e.g., room-specific) reference frames. To investigate whether similar neuroanatomical dissociations exist in humans, we reanalysed functional magnetic resonance imaging data in which participants learned the orientation of unique images in separate local environments relative to distinct global landmarks (Shine, Valdés-Herrera, Hegarty, & Wolbers, 2016). The environment layout meant that we could establish two separate multivariate analysis models in which the HD on individual trials was coded relative either to global (North, South, East, West) or local (Front, Back, Right, Left) reference frames. Examining the data first in key regions of interest (ROI) for HD coding, we replicated our previous results and found that global HD was decodable in the thalamus and precuneus; the RSC, however, was sensitive only to local HD. Extending recent findings in both humans and rodents, V1 was sensitive to both HD reference frames. Additional small volume-corrected searchlight analyses supported the ROI results and indicated that the anatomical locus of the thalamic global HD coding was located in the medial thalamus, bordering the anterior thalamus, a region critical for global HD coding in rodents. Our findings elucidate further the putative neural basis of HD coding in humans, and suggest that distinct brain regions code for different frames of reference in HD.Significance statementHead direction (HD) cells provide a neural signal as to one’s orientation in the environment. HD can be coded relative to global or local (e.g., room-specific) reference frames, with studies suggesting that distinct areas of thalamus and retrosplenial cortex (RSC) code for this information. We reanalysed fMRI data where human participants associated images with global HDs before undergoing scanning. The design enabled us to examine both global and local HD coding. Supporting previous findings, global HD was decodable in thalamus, however the RSC coded only for local HD. We found evidence also for both reference frames in V1. These findings elucidate the putative neural basis of HD coding in humans, with distinct brain regions coding for different HD reference frames.

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 Middle-scale navigation: the vertebrate case

1996 ◽  
Vol 199 (1) ◽  
pp. 163-164
Author(s):  
DF Sherry
Keyword(s):  
Path Integration ◽  
Brain Regions ◽  
Place Cells ◽  
Cognitive Map ◽  
Head Direction ◽  
Neural Basis ◽  
Head Direction Cells ◽  
Complete Rejection ◽  
Neural Bases

Few ideas have had a greater impact on the study of navigation at the middle scale than the theory of the cognitive map. As papers in this section show, current views of the cognitive map range from complete rejection of the idea (Bennett, 1996) to new proposals for the behavioural and neural bases of the cognitive map (Gallistel and Cramer, 1996; McNaughton et al. 1996). The papers in this section also make it clear that path integration has taken centre stage in theorizing about navigation at the middle scale. Path integration is the use of information generated by locomotion to determine the current distance and direction to the origin of the path. Etienne (1980) provided one of the first experimental demonstrations of path integration by a vertebrate, and in this section Etienne et al. (1996) describe recent research with animals and humans on the interaction between path integration and landmark information. Path integration is also the fundamental means of navigation in the model described by Gallistel and Cramer (1996). McNaughton et al. (1996) suggest that the neural basis of path integration is found in the place cells and head direction cells of the hippocampus and associated brain regions.

scholarly journals A neural-level model of spatial memory and imagery

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Andrej Bicanski ◽  
Neil Burgess
Keyword(s):  
Spatial Memory ◽  
Novelty Detection ◽  
Cell Activity ◽  
Cell Types ◽  
Brain Regions ◽  
Retrosplenial Cortex ◽  
Head Direction ◽  
Grid Cells ◽  
Level Model ◽  
Key Aspects

We present a model of how neural representations of egocentric spatial experiences in parietal cortex interface with viewpoint-independent representations in medial temporal areas, via retrosplenial cortex, to enable many key aspects of spatial cognition. This account shows how previously reported neural responses (place, head-direction and grid cells, allocentric boundary- and object-vector cells, gain-field neurons) can map onto higher cognitive function in a modular way, and predicts new cell types (egocentric and head-direction-modulated boundary- and object-vector cells). The model predicts how these neural populations should interact across multiple brain regions to support spatial memory, scene construction, novelty-detection, ‘trace cells’, and mental navigation. Simulated behavior and firing rate maps are compared to experimental data, for example showing how object-vector cells allow items to be remembered within a contextual representation based on environmental boundaries, and how grid cells could update the viewpoint in imagery during planning and short-cutting by driving sequential place cell activity.

scholarly journals Head-direction cells escaping attractor dynamics in the parahippocampal region

2018 ◽  
Author(s):  
Olga Kornienko ◽  
Patrick Latuske ◽  
Laura Kohler ◽  
Kevin Allen
Keyword(s):  
Entorhinal Cortex ◽  
Computational Models ◽  
Head Direction ◽  
Grid Cells ◽  
Visual Landmarks ◽  
Head Direction Cells ◽  
Medial Entorhinal Cortex ◽  
Attractor Dynamics ◽  
Freely Moving ◽  
Uniform Population

AbstractNavigation depends on the activity of head-direction (HD) cells. Computational models postulate that HD cells form a uniform population that reacts coherently to changes in landmarks. We tested whether this applied to HD cells of the medial entorhinal cortex and parasubiculum, areas where the HD signal contributes to the periodic firing of grid cells. Manipulations of the visual landmarks surrounding freely-moving mice altered the tuning of HD cells. Importantly, these tuning modifications were often non-coherent across cells, refuting the notion that HD cells form a uniform population constrained by attractor-like dynamics. Instead, examination of theta rhythmicity 1revealed two types of HD cells, theta rhythmic and non-rhythmic cells. Larger tuning alterations were observed predominantly in non-rhythmic HD cells. Moreover, only non-rhythmic HD cells reorganized their firing associations in response to visual land-mark changes. These findings reveal a theta non-rhythmic HD signal whose malleable organization is controlled by visual landmarks.

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