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Jeffrey S Taube - One of the best experts on this subject based on the ideXlab platform.
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functional and anatomical relationships between the medial precentral cortex dorsal striatum and Head Direction Cell circuitry ii neuroanatomical studies
Journal of Neurophysiology, 2019Co-Authors: Max L Mehlman, Shawn S Winter, Jeffrey S TaubeAbstract:Head Direction (HD) Cells are located primarily within the limbic system, but small populations of extralimbic HD Cells are found in the medial precentral cortex (PrCM) and dorsal striatum (DS). Th...
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Head Direction Cell Activity Is Absent in Mice without the Horizontal Semicircular Canals.
The Journal of neuroscience : the official journal of the Society for Neuroscience, 2016Co-Authors: Stephane Valerio, Jeffrey S TaubeAbstract:Head Direction (HD) Cells fire when an animal faces a particular Direction in its environment, and they are thought to represent the neural correlate of the animal's perceived spatial orientation. Previous studies have shown that vestibular information is critical for generating the HD signal but have not delineated whether information from all three semicircular canals or just the horizontal canals, which are primarily sensitive to angular Head rotation in the horizontal (yaw) plane, are critical for the signal. Here, we monitored Cell activity in the anterodorsal thalamus (ADN), an area known to contain HD Cells, in epstatic circler (Ecl) mice, which have a bilateral malformation of the horizontal (lateral) semicircular canals. Ecl mice and their littermates that did not express the mutation (controls) were implanted with recording electrodes in the ADN. Results confirm the important role the horizontal canals play in forming the HD signal. Although normal HD Cell activity (Raleigh's r > 0.4) was recorded in control mice, no such activity was found in Ecl mice, although some Cells had activity that was mildly modulated by HD (0.4 > r > 0.2). Importantly, we also observed activity in Ecl mice that was best characterized as bursty--a pattern of activity similar to an HD signal but without any preferred firing Direction. These results suggest that the neural structure for the HD network remains intact in Ecl mice, but the absence of normal horizontal canals results in an inability to control the network properly and brings about an unstable HD signal. Significance statement: Cells in the anterior dorsal thalamic nucleus normally fire in relation to the animal's Directional Heading with respect to the environment--so-called Head Direction Cells. To understand how these Head Direction Cells generate their activity, we recorded single-unit activity from the anterior dorsal thalamus in transgenic mice that lack functional horizontal semicircular canals. We show that the neural network for the Head Direction signal remains intact in these mice, but that the absence of normal horizontal canals results in an inability to control the network properly and brings about an unstable Head Direction signal.
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disruption of the Head Direction Cell network impairs the parahippocampal grid Cell signal
Science, 2015Co-Authors: Shawn S Winter, Benjamin J Clark, Jeffrey S TaubeAbstract:Navigation depends on multiple neural systems that encode the moment-to-moment changes in an animal’s Direction and location in space. These include Head Direction (HD) Cells representing the orientation of the Head and grid Cells that fire at multiple locations, forming a repeating hexagonal grid pattern. Computational models hypothesize that generation of the grid Cell signal relies upon HD information that ascends to the hippocampal network via the anterior thalamic nuclei (ATN). We inactivated or lesioned the ATN and subsequently recorded single units in the entorhinal cortex and parasubiculum. ATN manipulation significantly disrupted grid and HD Cell characteristics while sparing theta rhythmicity in these regions. These results indicate that the HD signal via the ATN is necessary for the generation and function of grid Cell activity.
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the nucleus prepositus hypoglossi contributes to Head Direction Cell stability in rats
The Journal of Neuroscience, 2015Co-Authors: William N Butler, Jeffrey S TaubeAbstract:Head Direction (HD) Cells in the rat limbic system fire according to the animal's orientation independently of the animal's environmental location or behavior. These HD Cells receive strong inputs from the vestibular system, among other areas, as evidenced by disruption of their Directional firing after lesions or inactivation of vestibular inputs. Two brainstem nuclei, the supragenual nucleus (SGN) and nucleus prepositus hypoglossi (NPH), are known to project to the HD network and are thought to be possible relays of vestibular information. Previous work has shown that lesioning the SGN leads to a loss of spatial tuning in downstream HD Cells, but the NPH has historically been defined as an oculomotor nuclei and therefore its role in contributing to the HD signal is less clear. Here, we investigated this role by recording HD Cells in the anterior thalamus after either neurotoxic or electrolytic lesions of the NPH. There was a total loss of Direction-specific firing in anterodorsal thalamus Cells in animals with complete NPH lesions. However, many Cells were identified that fired in bursts unrelated to the animals' Directional Heading and were similar to Cells seen in previous studies that damaged vestibular-associated areas. Some animals with significant but incomplete lesions of the NPH had HD Cells that were stable under normal conditions, but were unstable under conditions designed to minimize the use of external cues. These results support the hypothesis that the NPH, beyond its traditional oculomotor function, plays a critical role in conveying vestibular-related information to the HD circuit.
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self motion improves Head Direction Cell tuning
Journal of Neurophysiology, 2014Co-Authors: Michael E Shinder, Jeffrey S TaubeAbstract:Head Direction (HD) Cells respond when an animal faces a particular Direction in the environment and form the basis for the animal's perceived Directional Heading. When an animal moves through its ...
Paul A Dudchenko - One of the best experts on this subject based on the ideXlab platform.
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lesions of the Head Direction Cell system impair Direction discrimination
Behavioral Neuroscience, 2019Co-Authors: Anna E Smith, Paul A Dudchenko, Olivia A Cheek, Emily L C Sweet, Emma R WoodAbstract:Previous results suggest that Directional information from the Head Direction Cell circuit may inform hippocampal place Cell firing when an animal is confronted with visually identical environments. To investigate whether such information might also be essential for spatial behavior, we tested adult, male Lister Hooded rats that had received either bilateral lateral mammillary nuclei (LMN) lesions or sham lesions on a four-way, conditional odor-location discrimination in compartments arranged at 60° to one another. We found that significantly fewer rats in the LMN lesion group were able to learn the task compared to the Sham group. We also found that the extent of the behavioral impairment was highly correlated with the degree of tissue loss in the LMN resulting from the lesion. Animals with LMN lesions were also impaired in a nonmatching-to-sample task in a T maze, and the extent of impairment likewise depended on the extent of the lesion. Performance in the odor-location and T-maze tasks was not affected by tissue loss in the medial mammillary nuclei. Together, these results indicate that the LMN, a key node in the Head Direction circuit, is critical for solving a spatial task that requires a Directional discrimination. (PsycINFO Database Record (c) 2019 APA, all rights reserved).
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a new perspective on the Head Direction Cell system and spatial behavior
Neuroscience & Biobehavioral Reviews, 2019Co-Authors: Paul A Dudchenko, Emma R Wood, Anna E SmithAbstract:The Head Direction Cell system is an interconnected set of brain structures containing neurons whose firing is Directionally tuned. The robust representation of allocentric Direction by Head Direction Cells suggests that they provide a neural compass for the animal. However, evidence linking Head Direction Cells and spatial behavior has been mixed. Whereas damage to the hippocampus yields profound deficits in a range of spatial tasks, lesions to the Head Direction Cell system often yield milder impairments in spatial behavior. In addition, correlational approaches have shown a correspondence between Head Direction Cells and spatial behavior in some tasks, but not others. These mixed effects may be explained in part by a new view of the Head Direction Cell system arising from recent demonstrations of at least two types of Head Direction Cells: 'traditional' Cells, and a second class of 'sensory' Cells driven by polarising features of an environment. The recognition of different kinds of Head Direction Cells now allows a nuanced assessment of this system's role in guiding navigation.
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lesions of the Head Direction Cell system increase hippocampal place field repetition
Current Biology, 2017Co-Authors: Bruce Harland, Roddy M Grieves, David Bett, Rachael Stentiford, Emma R Wood, Paul A DudchenkoAbstract:Summary A central tenet of systems neuroscience is that the mammalian hippocampus provides a cognitive map of the environment. This view is supported by the finding of place Cells, neurons whose firing is tuned to specific locations in an animal's environment, within this brain region. Recent work, however, has shown that these Cells repeat their firing fields across visually identical maze compartments [1, 2]. This repetition is not observed if these compartments face different Directions, suggesting that place Cells use a Directional input to differentiate otherwise similar local environments [3, 4]. A clear candidate for this input is the Head Direction Cell system. To test this, we disrupted the Head Direction Cell system by lesioning the lateral mammillary nuclei and then recorded place Cells as rats explored multiple, connected compartments, oriented in the same or in different Directions. As shown previously, we found that place Cells in control animals exhibited repeated fields in compartments arranged in parallel, but not in compartments facing different Directions. In contrast, the place Cells of animals with lesions of the Head Direction Cell system exhibited repeating fields in both conditions. Thus, Directional information provided by the Head Direction Cell system appears essential for the angular disambiguation by place Cells of visually identical compartments.
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The formation of cognitive maps of adjacent environments: evidence from the Head Direction Cell system.
Behavioral neuroscience, 2005Co-Authors: Paul A Dudchenko, Larissa E. ZinyukAbstract:In 2 experiments the authors tested whether the Head Direction (HD) Cell system underlies a sense of Direction maintained across environments. In Experiment 1, HD neurons failed to maintain their firing Directions across T mazes in adjacent environments but rather reoriented to the T maze within each environment. Such reorientation suggests that familiar landmarks override an internal Directional sense, so in Experiment 2 the authors recorded HD neurons as rats walked between novel and familiar "rooms" of a 4-chamber apparatus. In novel rooms, HD neurons maintained the firing Direction of the preceding environment. However, in familiar rooms, HD neuron firing Directions shifted to agree with the landmarks therein. With repeated experience, a homogeneous representation of all rooms developed in a subset of the rats.
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hippocampal place Cell instability after lesions of the Head Direction Cell network
The Journal of Neuroscience, 2003Co-Authors: Jeffrey L Calton, Paul A Dudchenko, Robert W Stackman, Jeremy P Goodridge, William B Archey, Jeffrey S TaubeAbstract:The occurrence of Cells that encode spatial location (place Cells) or Head Direction (HD Cells) in the rat limbic system suggests that these Cell types are important for spatial navigation. We sought to determine whether place fields of hippocampal CA1 place Cells would be altered in animals receiving lesions of brain areas containing HD Cells. Rats received bilateral lesions of anterodorsal thalamic nuclei (ADN), postsubiculum (PoS), or sham lesions, before place Cell recording. Although place Cells from lesioned animals did not differ from controls on many place-field characteristics, such as place-field size and infield firing rate, the signal was significantly degraded with respect to measures of outfield firing rate, spatial coherence, and information content. Surprisingly, place Cells from lesioned animals were more likely modulated by the Directional Heading of the animal. Rotation of the landmark cue showed that place fields from PoS-lesioned animals were not controlled by the cue and shifted unpredictably between sessions. Although fields from ADN-lesioned animals tended to have less landmark control than fields from control animals, this impairment was mild compared with Cells recorded from PoS-lesioned animals. Removal of the prominent visual cue also led to instability of place-field representations in PoS-lesioned, but not ADN-lesioned, animals. Together, these findings suggest that an intact HD system is not necessary for the maintenance of place fields, but lesions of brain areas that convey the HD signal can degrade this signal, and lesions of the PoS might lead to perceptual or mnemonic deficits, leading to place-field instability between sessions.
Benjamin J Clark - One of the best experts on this subject based on the ideXlab platform.
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disruption of the Head Direction Cell network impairs the parahippocampal grid Cell signal
Science, 2015Co-Authors: Shawn S Winter, Benjamin J Clark, Jeffrey S TaubeAbstract:Navigation depends on multiple neural systems that encode the moment-to-moment changes in an animal’s Direction and location in space. These include Head Direction (HD) Cells representing the orientation of the Head and grid Cells that fire at multiple locations, forming a repeating hexagonal grid pattern. Computational models hypothesize that generation of the grid Cell signal relies upon HD information that ascends to the hippocampal network via the anterior thalamic nuclei (ATN). We inactivated or lesioned the ATN and subsequently recorded single units in the entorhinal cortex and parasubiculum. ATN manipulation significantly disrupted grid and HD Cell characteristics while sparing theta rhythmicity in these regions. These results indicate that the HD signal via the ATN is necessary for the generation and function of grid Cell activity.
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Head Direction Cell activity in the anterodorsal thalamus requires intact supragenual nuclei
Journal of Neurophysiology, 2012Co-Authors: Benjamin J Clark, Joel E Brown, Jeffrey S TaubeAbstract: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...
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vestibular and attractor network basis of the Head Direction Cell signal in subcortical circuits
Frontiers in Neural Circuits, 2012Co-Authors: Benjamin J Clark, Jeffrey S TaubeAbstract:Accurate navigation depends on a network of neural systems that encode the moment-to-moment changes in an animal’s Directional orientation and location in space. Within this navigation system are Head Direction (HD) Cells, which fire persistently when an animal’s Head is pointed in a particular Direction (Sharp et al., 2001a; Taube, 2007). HD Cells are widely thought to underlie an animal’s sense of spatial orientation, and research over the last 25+ years has revealed that this robust spatial signal is widely distributed across subcortical and cortical limbic areas. Much of this work has been directed at understanding the functional organization of the HD Cell circuitry, and precisely how this signal is generated from sensory and motor systems. The purpose of the present review is to summarize some of the recent studies arguing that the HD Cell circuit is largely processed in a hierarchical fashion, following a pathway involving the dorsal tegmental nuclei → lateral mammillary nuclei → anterior thalamus → parahippocampal and retrosplenial cortical regions. We also review recent work identifying “bursting” Cellular activity in the HD Cell circuit after lesions of the vestibular system, and relate these observations to the long held view that attractor network mechanisms underlie HD signal generation. Finally, we summarize the work to date suggesting that this network architecture may reside within the tegmento-mammillary circuit.
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both visual and idiothetic cues contribute to Head Direction Cell stability during navigation along complex routes
Journal of Neurophysiology, 2011Co-Authors: Ryan M Yoder, Benjamin J Clark, Michael E Shinder, Joel E Brown, Stephane Valerio, Mignon V Lamia, Jeffrey S TaubeAbstract:Successful navigation requires a constantly updated neural representation of Directional Heading, which is conveyed by Head Direction (HD) Cells. The HD signal is predominantly controlled by visual landmarks, but when familiar landmarks are unavailable, self-motion cues are able to control the HD signal via path integration. Previous studies of the relationship between HD Cell activity and path integration have been limited to two or more arenas located in the same room, a drawback for interpretation because the same visual cues may have been perceptible across arenas. To address this issue, we tested the relationship between HD Cell activity and path integration by recording HD Cells while rats navigated within a 14-unit T-maze and in a multiroom maze that consisted of unique arenas that were located in different rooms but connected by a passageway. In the 14-unit T-maze, the HD signal remained relatively stable between the start and goal boxes, with the preferred firing Directions usually shifting <45° during maze traversal. In the multiroom maze in light, the preferred firing Directions also remained relatively constant between rooms, but with greater variability than in the 14-unit maze. In darkness, HD Cell preferred firing Directions showed marginally more variability between rooms than in the lighted condition. Overall, the results indicate that self-motion cues are capable of maintaining the HD Cell signal in the absence of familiar visual cues, although there are limits to its accuracy. In addition, visual information, even when unfamiliar, can increase the precision of Directional perception.
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impaired Head Direction Cell representation in the anterodorsal thalamus after lesions of the retrosplenial cortex
The Journal of Neuroscience, 2010Co-Authors: Benjamin J Clark, Joshua P Bassett, Sarah S Wang, Jeffrey S TaubeAbstract:The retrosplenial cortex (RSP), a brain region frequently linked to processes of spatial navigation, contains neurons that discharge as a function of a rat's Head Direction (HD). HD Cells have been identified throughout the limbic system including the anterodorsal thalamus (ADN) and postsubiculum (PoS), both of which are reciprocally connected to the RSP. The functional relationship between HD Cells in the RSP and those found in other limbic regions is presently unknown, but given the intimate connectivity between the RSP and regions such as the ADN and PoS, and the reported loss of spatial orientation in rodents and humans with RSP damage, it is likely that the RSP plays an important role in processing the limbic HD signal. To test this hypothesis, we produced neurotoxic or electrolytic lesions of the RSP and recorded HD Cells in the ADN of female Long-Evans rats. HD Cells remained present in the ADN after RSP lesions, but the stability of their preferred firing Directions was significantly reduced even in the presence of a salient visual landmark. Subsequent tests revealed that lesions of the RSP moderately impaired landmark control over the Cells' preferred firing Directions, but spared the Cells Directional stability when animals were required to update their orientation using self-movement cues. Together, these results suggest that the RSP plays a prominent role in processing landmark information for accurate HD Cell orientation and may explain the poor Directional sense in humans that follows damage to the RSP.
Hector J I Page - One of the best experts on this subject based on the ideXlab platform.
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a speed accurate self sustaining Head Direction Cell path integration model without recurrent excitation
IEEE Network, 2018Co-Authors: Hector J I Page, Daniel Walters, Simon M StringerAbstract:The Head Direction (HD) system signals HD in an allocentric frame of reference. The system is able to update firing based on internally derived information about self-motion, a process known as pat...
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a dual axis rotation rule for updating the Head Direction Cell reference frame during movement in three dimensions
Journal of Neurophysiology, 2018Co-Authors: Hector J I Page, Jonathan J Wilson, Kate JefferyAbstract:Maintaining a sense of Direction is complicated when moving in three-dimensional (3D) space. Head Direction Cells, which update the Direction sense based on Head rotations, may accommodate 3D movem...
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a proposed rule for updating of the Head Direction Cell reference frame following rotations in three dimensions
bioRxiv, 2016Co-Authors: J Wilson, Hector J I Page, Kathryn J JefferyAbstract:In the mammalian brain, allocentric (Earth-referenced) Heading Direction, called azimuth, is encoded by Head Direction (HD) Cells, which fire according to the facing Direction of the rat's Head. If the animal is on a horizontal surface then egocentric (self-referenced) rotations of the Head around the dorso-ventral axis, called yaw, correspond to changes in azimuth, and elicit appropriate updating of the HD signal. However, if the surface is sloping steeply then yaw rotations no longer map linearly to changes in azimuth. The brain could solve this problem simply by always firing according to Direction on the local (sloping) surface instead; however, if the animal moves between surfaces having different compass orientations then errors would accumulate in the subsequent azimuth signal. These errors could be avoided if the HD system instead combines two updating rules: yaw rotations around the D-V axis and rotations of the D-V axis around the gravity-defined vertical axis. We show here that when rats move between vertical walls of different orientations then HD Cells indeed rotate their activity by an amount corresponding to the amount of vertical-axis rotation. With modelling, we then show how this reference-frame rotation, which may be driven by inputs from the vestibular nuclei or vestibulocerebellum, allows animals to maintain a simple yaw-based updating rule while on a given plane, but also to avoid accumulation of Heading errors when moving between planes.
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architectural constraints are a major factor reducing path integration accuracy in the rat Head Direction Cell system
Frontiers in Computational Neuroscience, 2015Co-Authors: Hector J I Page, Daniel Walters, Simon M StringerAbstract:Head Direction Cells fire to signal the Direction in which an animal's Head is pointing. They are able to track Head Direction using only internally-derived information (path integration). In this simulation study we investigate the factors that affect path integration accuracy. Specifically, two major limiting factors are identified: rise time, the time after stimulation it takes for a neuron to start firing, and the presence of symmetric non-offset within-layer recurrent collateral connectivity. On the basis of the latter, the important prediction is made that Head Direction Cell regions directly involved in path integration will not contain this type of connectivity; giving a theoretical explanation for architectural observations. Increased neuronal rise time is found to slow path integration, and the slowing effect for a given rise time is found to be more severe in the context of short conduction delays. Further work is suggested on the basis of our findings, which represent a valuable contribution to understanding of the Head Direction Cell system.
Anna E Smith - One of the best experts on this subject based on the ideXlab platform.
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lesions of the Head Direction Cell system impair Direction discrimination
Behavioral Neuroscience, 2019Co-Authors: Anna E Smith, Paul A Dudchenko, Olivia A Cheek, Emily L C Sweet, Emma R WoodAbstract:Previous results suggest that Directional information from the Head Direction Cell circuit may inform hippocampal place Cell firing when an animal is confronted with visually identical environments. To investigate whether such information might also be essential for spatial behavior, we tested adult, male Lister Hooded rats that had received either bilateral lateral mammillary nuclei (LMN) lesions or sham lesions on a four-way, conditional odor-location discrimination in compartments arranged at 60° to one another. We found that significantly fewer rats in the LMN lesion group were able to learn the task compared to the Sham group. We also found that the extent of the behavioral impairment was highly correlated with the degree of tissue loss in the LMN resulting from the lesion. Animals with LMN lesions were also impaired in a nonmatching-to-sample task in a T maze, and the extent of impairment likewise depended on the extent of the lesion. Performance in the odor-location and T-maze tasks was not affected by tissue loss in the medial mammillary nuclei. Together, these results indicate that the LMN, a key node in the Head Direction circuit, is critical for solving a spatial task that requires a Directional discrimination. (PsycINFO Database Record (c) 2019 APA, all rights reserved).
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a new perspective on the Head Direction Cell system and spatial behavior
Neuroscience & Biobehavioral Reviews, 2019Co-Authors: Paul A Dudchenko, Emma R Wood, Anna E SmithAbstract:The Head Direction Cell system is an interconnected set of brain structures containing neurons whose firing is Directionally tuned. The robust representation of allocentric Direction by Head Direction Cells suggests that they provide a neural compass for the animal. However, evidence linking Head Direction Cells and spatial behavior has been mixed. Whereas damage to the hippocampus yields profound deficits in a range of spatial tasks, lesions to the Head Direction Cell system often yield milder impairments in spatial behavior. In addition, correlational approaches have shown a correspondence between Head Direction Cells and spatial behavior in some tasks, but not others. These mixed effects may be explained in part by a new view of the Head Direction Cell system arising from recent demonstrations of at least two types of Head Direction Cells: 'traditional' Cells, and a second class of 'sensory' Cells driven by polarising features of an environment. The recognition of different kinds of Head Direction Cells now allows a nuanced assessment of this system's role in guiding navigation.
