scholarly journals Dynamic control of cortical head-direction signal by angular velocity

2019 ◽  
Author(s):  
Arseny Finkelstein ◽  
Hervé Rouault ◽  
Sandro Romani ◽  
Nachum Ulanovsky

AbstractThe sense of direction requires accurate tracking of head direction at different turning-velocities, yet it remains unclear how this is achieved in the mammalian brain. Here we recorded head-direction cells in bat dorsal presubiculum and found that, surprisingly, the head-direction signal in this cortical region was dynamically controlled by angular velocity. In most neurons, a sharp head-direction tuning emerged at some angular velocity, but was absent at other velocities – resulting in a 4-fold increase in head-direction cell abundance. The head-direction tuning changed as a function of angular velocity primarily via a redistribution of spikes between the neuron’s preferred and null directions – while keeping the average firing-rate constant. These results could not be explained by existing ‘ring-attractor’ models of the head-direction system. We propose a novel recurrent network model that accounts for the observed dynamics of head-direction cells. This model predicts that the new classes of cells we found can improve the sensitivity of the head-direction system to directional sensory cues, and support angular-velocity integration.

1991 ◽  
Vol 3 (2) ◽  
pp. 190-202 ◽  
Author(s):  
B. L. McNaughton ◽  
L. L. Chen ◽  
E. J. Markus

Behavioral and neurophysiological evidence strongly suggests that, within certain limits, rodents and humans can keep track of their directional heading relative to an inertial, and hence allocentric coordinate system. This “sense of direction” appears to involve the integration of angular velocity signals that arise primarily in the vestibular system. A hypothesis is proposed in which the integration process, an operation that may be difficult for neurons to implement, is replaced by a linear associative mapping, an operation that is at least theoretically easy to implement with neurons. The proposed system makes use of a set of linearly independent vectors representing the combination of the current head direction, and head angular velocity representations to “recall” the resulting head direction. It is then proposed that visual landmarks become incorporated into the directional system, enabling both the correction of cumulative error and, ultimately, the computation of novel, optimal trajectories between locations. According to the hypothesis, this occurs through the association of hippo-campal “local-view” cells (i.e., direction selective “place cells”) with “head-direction” cells located downstream in the dorsal presubiculum. The possible neurophysiological and neuroan-atomical bases for the proposed system are discussed.


2016 ◽  
Author(s):  
Pierre-Yves Jacob ◽  
Giulio Casali ◽  
Laure Spieser ◽  
Hector Page ◽  
Dorothy Overington ◽  
...  

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.


2017 ◽  
Author(s):  
Gilad Tocker ◽  
Eli Borodach ◽  
Tale L. Bjerknes ◽  
May-Britt Moser ◽  
Edvard I. Moser ◽  
...  

SummaryThe sense of direction is a vital computation, whose neural basis is considered to be carried out by head-direction cells. One way to estimate head-direction is by integrating head angular-velocity over time. However, this process results in error accumulation resembling a random walk, proportional to , which constitutes a mark for a path integration process. In the present study we analyzed previously recorded data to quantify the drift in head-direction cells of rat pups before and after eye-opening. We found that in rat pups before eye-opening the drift propagated as a random walk, while in rats after eye-opening the drift was lower. This suggests that a path-integration process underlies the estimation of head-direction, such that before eye-opening the head-direction system runs in an open-loop manner and accumulates error. After eye-opening, visual-input, such as arena shape, helps to correct errors and thus compute the sense of direction accurately.


IEEE Access ◽  
2021 ◽  
pp. 1-1
Author(s):  
Baozhong Li ◽  
Yanming Liu ◽  
Lei Lai

2001 ◽  
Vol 85 (1) ◽  
pp. 105-116 ◽  
Author(s):  
James J. Knierim ◽  
Bruce L. McNaughton

“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.


2008 ◽  
Vol 122 (4) ◽  
pp. 827-840 ◽  
Author(s):  
Jeffrey L. Calton ◽  
Carol S. Turner ◽  
De-Laine M. Cyrenne ◽  
Brian R. Lee ◽  
Jeffrey S. Taube

2021 ◽  
Vol 7 (25) ◽  
pp. eabg4693
Author(s):  
Yangfan Peng ◽  
Federico J. Barreda Tomas ◽  
Paul Pfeiffer ◽  
Moritz Drangmeister ◽  
Susanne Schreiber ◽  
...  

In cortical microcircuits, it is generally assumed that fast-spiking parvalbumin interneurons mediate dense and nonselective inhibition. Some reports indicate sparse and structured inhibitory connectivity, but the computational relevance and the underlying spatial organization remain unresolved. In the rat superficial presubiculum, we find that inhibition by fast-spiking interneurons is organized in the form of a dominant super-reciprocal microcircuit motif where multiple pyramidal cells recurrently inhibit each other via a single interneuron. Multineuron recordings and subsequent 3D reconstructions and analysis further show that this nonrandom connectivity arises from an asymmetric, polarized morphology of fast-spiking interneuron axons, which individually cover different directions in the same volume. Network simulations assuming topographically organized input demonstrate that such polarized inhibition can improve head direction tuning of pyramidal cells in comparison to a “blanket of inhibition.” We propose that structured inhibition based on asymmetrical axons is an overarching spatial connectivity principle for tailored computation across brain regions.


eLife ◽  
2014 ◽  
Vol 3 ◽  
Author(s):  
Maciej M Jankowski ◽  
Md Nurul Islam ◽  
Nicholas F Wright ◽  
Seralynne D Vann ◽  
Jonathan T Erichsen ◽  
...  

Discrete populations of brain cells signal heading direction, rather like a compass. These ‘head direction’ cells are largely confined to a closely-connected network of sites. We describe, for the first time, a population of head direction cells in nucleus reuniens of the thalamus in the freely-moving rat. This novel subcortical head direction signal potentially modulates the hippocampal CA fields directly and, thus, informs spatial processing and memory.


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