scholarly journals Population dynamics of the thalamic head direction system during drift and reorientation

2021 ◽  
Author(s):  
Zaki Ajabi ◽  
Alexandra T. Keinath ◽  
Xue-Xin Wei ◽  
Mark P. Brandon
Keyword(s):  
Memory Trace ◽  
Large Population ◽  
Angular Distance ◽  
Head Direction ◽  
Visual Landmark ◽  
Continuous Rotation ◽  
Stable Representation ◽  
Familiar Environment ◽  
Reliable Representation ◽  
Dependent Mechanism

AbstractThe head direction (HD) system is classically modeled as a ring attractor network1,2 which ensures a stable representation of the animal’s head direction. This unidimensional description popularized the view of the HD system as the brain’s internal compass3,4. However, unlike a globally consistent magnetic compass, the orientation of the HD system is dynamic, depends on local cues and exhibits remapping across familiar environments5. Such a system requires mechanisms to remember and align to familiar landmarks, which may not be well described within the classic 1-dimensional framework. To search for these mechanisms, we performed large population recordings of mouse thalamic HD cells using calcium imaging, during controlled manipulations of a visual landmark in a familiar environment. First, we find that realignment of the system was associated with a continuous rotation of the HD network representation. The speed and angular distance of this rotation was predicted by a 2nd dimension to the ring attractor which we refer to as network gain, i.e. the instantaneous population firing rate. Moreover, the 360-degree azimuthal profile of network gain, during darkness, maintained a ‘memory trace’ of a previously displayed visual landmark. In a 2nd experiment, brief presentations of a rotated landmark revealed an attraction of the network back to its initial orientation, suggesting a time-dependent mechanism underlying the formation of these network gain memory traces. Finally, in a 3rd experiment, continuous rotation of a visual landmark induced a similar rotation of the HD representation which persisted following removal of the landmark, demonstrating that HD network orientation is subject to experience-dependent recalibration. Together, these results provide new mechanistic insights into how the neural compass flexibly adapts to environmental cues to maintain a reliable representation of the head direction.

The effects of disorientation on visual landmark control of head direction cell orientation

1997 ◽  
Vol 115 (2) ◽  
pp. 375-380 ◽  
Author(s):  
P. A. Dudchenko ◽  
Jeremy P. Goodridge ◽  
J. S. Taube
Keyword(s):  
Head Direction ◽  
Cell Orientation ◽  
Visual Landmark ◽  
Head Direction Cell

scholarly journals Population adaptation in efficient balanced networks

2017 ◽  
Author(s):  
Gabrielle J. Gutierrez ◽  
Sophie Denève
Keyword(s):  
Metabolic Cost ◽  
Population Level ◽  
Efficient Coding ◽  
Global Cost ◽  
Stable Representation ◽  
Reliable Representation ◽  
Sensory Responses ◽  
The Cost ◽  
External Stimuli ◽  
Accuracy Tradeoff

AbstractAdaptation is a key component of efficient coding in sensory neurons. However, it remains unclear how neurons can provide a stable representation of external stimuli given their history-dependent responses. Here we show that a stable representation is maintained if efficiency is optimized by a population of neurons rather than by neurons individually. We show that spike-frequency adaptation and E/I balanced recurrent connectivity emerge as solutions to a global cost-accuracy tradeoff. The network will re-distribute sensory responses from highly excitable neurons to less excitable neurons as the cost of neural activity increases. This does not change the representation at the population level, despite causing dynamic changes in individual neurons. By applying this framework to an orientation coding network, we reconcile neural and behavioral findings. Our approach underscores the common mechanisms behind the diversity of neural adaptation and its role in producing a reliable representation of the stimulus while minimizing metabolic cost.

scholarly journals Lateral entorhinal cortex suppresses drift in cortical memory representations.

2021 ◽  
Author(s):  
Maryna Pilkiw ◽  
Justin Jarovi ◽  
Kaori Takehara-Nishiuchi
Keyword(s):  
Entorhinal Cortex ◽  
Memory Retrieval ◽  
Firing Pattern ◽  
Memory Trace ◽  
Male Rats ◽  
Memory Representations ◽  
Familiar Environment ◽  
Functional Relevance ◽  
The Stability ◽  
Cortical Representations

Memory retrieval is thought to depend on the reinstatement of cortical memory representations guided by pattern completion processes in the hippocampus. The lateral entorhinal cortex (LEC) is one of the intermediary regions supporting hippocampal-cortical interactions and houses neurons that prospectively signal past events in a familiar environment. To investigate the functional relevance of the LEC's activity for cortical reinstatement, we pharmacologically inhibited the LEC and examined its impact on the stability of ensemble firing patterns in one of the LEC's efferent targets, the medial prefrontal cortex (mPFC). When male rats underwent multiple epochs of identical stimulus sequences in the same environment, the mPFC maintained a stable ensemble firing pattern across repetitions, particularly when the sequence included pairings of neutral and aversive stimuli. With LEC inhibition, the mPFC still formed an ensemble pattern that accurately captured stimuli and their associations within each epoch. However, LEC inhibition markedly disrupted its consistency across the epochs by decreasing the proportion of mPFC neurons that stably maintained firing selectivity for stimulus associations. Thus, the LEC stabilizes cortical representations of learned stimulus associations, thereby facilitating the recovery of the original memory trace without generating a new, redundant trace for familiar experiences. Failure of this process might underlie retrieval deficits in conditions associated with degeneration of the LEC, such as normal aging and Alzheimer's disease.

Head direction cell activity monitored in a novel environment and during a cue conflict situation

1995 ◽  
Vol 74 (5) ◽  
pp. 1953-1971 ◽  
Author(s):  
J. S. Taube ◽  
H. L. Burton
Keyword(s):  
Cell Activity ◽  
Sensory Information ◽  
The Novel ◽  
Head Direction ◽  
Sensory Cues ◽  
Thalamic Nuclei ◽  
Novel Environment ◽  
Preferred Direction ◽  
Anterior Thalamic Nuclei ◽  
Familiar Environment

1. Recent conceptualizations of the neural systems used during navigation have classified two types of sensory information used by animals: landmark cues and internally based (idiothetic; e.g., vestibular, kinesthetic) sensory cues. Previous studies have identified neurons in the postsubiculum and the anterior thalamic nuclei that discharge as a function of the animal's head direction in the horizontal plane. The present study was designed to determine how animals use head direction (HD) cells for spatial orientation and the types of sensory cues involved. 2. HD cell activity was monitored in the postsubiculum and anterior thalamic nucleus of rats in a dual-chamber apparatus in an experiment that consisted of two phases. In the first phase, HD cell activity was monitored as an animal moved from a familiar environment to a novel environment. It was hypothesized that if HD cells were capable of using idiothetic sensory information, then the direction of maximal discharge should remain relatively unchanged as the animal moved into an environment where it was unfamiliar with the landmark cues. In the second phase, HD cells were monitored under conditions in which a conflict situation was introduced between the established landmark cues and the animal's internally generated sensory cues. 3. HD cells were initially recorded in a cylinder containing a single orientation cue (familiar environment). A door was then opened, and the rat entered a U-shaped passageway leading to a rectangular chamber containing a different prominent cue (novel environment). For most HD cells, the preferred direction remained relatively constant between the cylinder and passageway/rectangle, although many cells showed a small (6-30 degrees) shift in their preferred direction in the novel environment. This directional shift was maintained across different episodes in the passageway/rectangle. 4. Before the next session, the orientation cue in the cylinder was rotated 90 degrees, and the animal returned to the cylinder. The cell's preferred direction usually shifted between 45 and 90 degrees in the same direction. 5. The rat was then permitted to walk back through the passageway into the now-familiar rectangle. Immediately upon entering the passageway, the preferred direction returned to its original (prerotation) orientation and remained at this value while the rat was in the rectangle. When the rat was allowed to walk back into the cylinder, one of three outcomes occurred: 1) the cell's preferred direction shifted, such that it remained linked to the cylinder's rotated cue card; 2) the cell's preferred direction remained unchanged from its orientation in the rectangle; or 3) the cell's preferred direction shifted to a new value that lay between the preferred directions for the rotated cylinder condition and rectangle. 6. There was little change in the HD cell's background firing rate, peak firing rate, or directional firing range for both the novel and cue-conflict situations. 7. Simultaneous recordings from multiple cells in different sessions showed that the preferred directions remained "in register" with one another. Thus, when one HD cell shifted its preferred direction a specific amount, the other HD cell also shifted its preferred direction the same amount. 8. Results across different series within the same animal showed that the amount the preferred direction shifted in the first Novel series was about the same amount as the shifts observed in subsequent Novel series. In contrast, as the animal experienced more Conflict series, HD cells tended to use the cylinder's cue card less as an orientation cue when the animal returned to the rotated cylinder condition from the rectangle. 9. These results suggest that HD cells in the postsubiculum and anterior thalamic nuclei receive information from both landmark and idiothetic sensory cues, and when both types of cues are available, HD cells preferentially use the landmark cues as long as they are perceived

scholarly journals Head direction cell activity in the anterodorsal thalamus requires intact supragenual nuclei

2012 ◽  
Vol 108 (10) ◽  
pp. 2767-2784 ◽  
Author(s):  
Benjamin J. Clark ◽  
Joel E. Brown ◽  
Jeffrey S. Taube
Keyword(s):  
Horizontal Plane ◽  
Essential Role ◽  
Critical Role ◽  
Cell Activity ◽  
Head Direction ◽  
Vestibular Information ◽  
Familiar Environment ◽  
Cell Circuit ◽  
Bilateral Lesions ◽  
Self Motion

Neural activity in several limbic areas varies as a function of the animal's head direction (HD) in the horizontal plane. Lesions of the vestibular periphery abolish this HD cell signal, suggesting an essential role for vestibular afference in HD signal generation. The organization of brain stem pathways conveying vestibular information to the HD circuit is poorly understood; however, recent anatomical work has identified the supragenual nucleus (SGN) as a putative relay. To test this hypothesis, we made lesions of the SGN in rats and screened for HD cells in the anterodorsal thalamus. In animals with complete bilateral lesions, the overall number of HD cells was significantly reduced relative to control animals. In animals with unilateral lesions of the SGN, directional activity was present, but the preferred firing directions of these cells were unstable and less influenced by the rotation of an environmental landmark. In addition, we found that preferred directions displayed large directional shifts when animals foraged for food in a darkened environment and when they were navigating from a familiar environment to a novel one, suggesting that the SGN plays a critical role in projecting essential self-motion (idiothetic) information to the HD cell circuit.

scholarly journals Decoding of neural data using cohomological learning

2018 ◽  
Author(s):  
Erik Rybakken ◽  
Nils Baas ◽  
Benjamin Dunn
Keyword(s):  
Spatial Organization ◽  
Large Population ◽  
Dimensional Structure ◽  
Neural Population ◽  
Head Direction ◽  
Population Activity ◽  
Neural Data ◽  
Neural Recordings ◽  
Data Driven Approach ◽  
Low Dimensional

AbstractWe introduce a novel data-driven approach to discover and decode features in the neural code coming from large population neural recordings with minimal assumptions, using cohomological learning. We apply our approach to neural recordings of mice moving freely in a box, where we find a circular feature. We then observe that the decoded value corresponds well to the head direction of the mouse. Thus we capture head direction cells and decode the head direction from the neural population activity without having to process the behaviour of the mouse. Interestingly, the decoded values convey more information about the neural activity than the tracked head direction does, with differences that have some spatial organization. Finally, we note that the residual population activity, after the head direction has been accounted for, retains some low-dimensional structure which is correlated with the speed of the mouse.

scholarly journals Population adaptation in efficient balanced networks

eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Gabrielle J Gutierrez ◽  
Sophie Denève
Keyword(s):  
Metabolic Cost ◽  
Population Level ◽  
Efficient Coding ◽  
Global Cost ◽  
Stable Representation ◽  
Reliable Representation ◽  
Sensory Responses ◽  
The Cost ◽  
External Stimuli ◽  
Accuracy Tradeoff

Adaptation is a key component of efficient coding in sensory neurons. However, it remains unclear how neurons can provide a stable representation of external stimuli given their history-dependent responses. Here we show that a stable representation is maintained if efficiency is optimized by a population of neurons rather than by neurons individually. We show that spike-frequency adaptation and E/I balanced recurrent connectivity emerge as solutions to a global cost-accuracy tradeoff. The network will redistribute sensory responses from highly excitable neurons to less excitable neurons as the cost of neural activity increases. This does not change the representation at the population level despite causing dynamic changes in individual neurons. By applying this framework to an orientation coding network, we reconcile neural and behavioral findings. Our approach underscores the common mechanisms behind the diversity of neural adaptation and its role in producing a reliable representation of the stimulus while minimizing metabolic cost.

scholarly journals Decoding of Neural Data Using Cohomological Feature Extraction

2019 ◽  
Vol 31 (1) ◽  
pp. 68-93 ◽  
Author(s):  
Erik Rybakken ◽  
Nils Baas ◽  
Benjamin Dunn
Keyword(s):  
Feature Extraction ◽  
Spatial Organization ◽  
Large Population ◽  
Dimensional Structure ◽  
Neural Population ◽  
Head Direction ◽  
Population Activity ◽  
Neural Recordings ◽  
Data Driven Approach ◽  
Low Dimensional

We introduce a novel data-driven approach to discover and decode features in the neural code coming from large population neural recordings with minimal assumptions, using cohomological feature extraction. We apply our approach to neural recordings of mice moving freely in a box, where we find a circular feature. We then observe that the decoded value corresponds well to the head direction of the mouse. Thus, we capture head direction cells and decode the head direction from the neural population activity without having to process the mouse's behavior. Interestingly, the decoded values convey more information about the neural activity than the tracked head direction does, with differences that have some spatial organization. Finally, we note that the residual population activity, after the head direction has been accounted for, retains some low-dimensional structure that is correlated with the speed of the mouse.

scholarly journals Passive Transport Disrupts Directional Path Integration by Rat Head Direction Cells

2003 ◽  
Vol 90 (5) ◽  
pp. 2862-2874 ◽  
Author(s):  
Robert W. Stackman ◽  
Edward J. Golob ◽  
Joshua P. Bassett ◽  
Jeffrey S. Taube
Keyword(s):  
Optic Flow ◽  
Path Integration ◽  
Efference Copy ◽  
The Novel ◽  
Head Direction ◽  
Passive Transport ◽  
Novel Environment ◽  
Preferred Direction ◽  
Idiothetic Cues ◽  
Familiar Environment

A subset of neurons in the rat limbic system encodes head direction (HD) by selectively discharging when the rat points its head in a preferred direction in the horizontal plane. The preferred firing direction is sensitive to the location of landmark cues, as well as idiothetic or self-motion cues (i.e., vestibular, motor efference copy, proprioception, and optic flow). Previous studies have shown that the preferred firing direction remains relatively stable (average shift ± 18°) after the rat walks from a familiar environment into a novel one, suggesting that without familiar landmarks, the preferred firing direction can be maintained using idiothetic cues, a process called directional path integration. This study repeated this experiment and manipulated the idiothetic cues available to the rat as it moved between the familiar and novel environment. Motor efference copy/proprioceptive cues were disrupted by passively transporting the animal between the familiar and novel environment. Darkening the room as the animal moved to the novel environment eliminated optic flow cues. HD cell preferred firing directions shifted in the novel environment by an average of 30° after locomotion from the familiar environment with the room lights off; by an average of 70° after passive transport from the familiar environment with the room lights on; and by an average of 67° after passive transport with the room lights off. These findings are consistent with the view that motor efference copy/proprioception cues are important for maintaining the preferred firing direction of HD cells under conditions requiring path integration.

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