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Jeffrey S Taube

Publications and source records attributed to Jeffrey S Taube.

10 recordsLinked to original sources

Path integration and lesions within the head direction cell circuit: comparison between the roles of the anterodorsal thalamus and dorsal tegmental nucleus.

Experiments were designed to determine whether 2 regions of the head direction cell circuit, the anterodorsal thalamic nucleus (ADN) and the dorsal tegmental nucleus (DTN), contribute to navigation. Rats were trained to perform a food-carrying task with and without blindfolds prior to receiving sham lesions or bilateral lesions of the ADN or DTN. ADN-lesioned rats were mildly impaired in both versions of the task. DTN-lesioned rats, however, were severely impaired and showed reduced heading accuracy in both task versions. These findings suggest that although both the DTN and ADN contribute to navigation based on path integration and landmarks, disruption of the head direction cell circuit at the level of the DTN has a significantly greater effect on spatial behavior than lesions of the ADN.

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Degradation of head direction cell activity during inverted locomotion.

Head direction (HD) cells in the rat limbic system carry information about the direction the head is pointing in the horizontal plane. Most previous studies of HD functioning have used animals locomoting in an upright position or ascending/descending a vertical wall. In the present study, we recorded HD cell activity from the anterodorsal thalamic nucleus while the animal was locomoting in an upside-down orientation. Rats performed a shuttle-box task requiring them to climb a vertical wall and locomote across the ceiling of the apparatus while inverted to reach an adjoining wall before ascending into the reward compartment. The apparatus was oriented toward the preferred direction of the recorded cell, or the 180 degrees opposite direction. When the animal was traversing the vertical walls of the apparatus, the HD cells remained directionally tuned as if the walls were an extension of the floor. When the animal was locomoting inverted on the ceiling, however, cells showed a dramatic change in activity. Nearly one-half (47%) of the recorded cells exhibited no directional specificity during inverted locomotion, despite showing robust directional tuning on the walls before and after inversion. The remaining cells showed significantly degraded measures of directional tuning and random shifts of the preferred direction relative to the floor condition while the animal was inverted. It has previously been suggested that the HD system uses head angular velocity signals from the vestibular system to maintain a consistent representation of allocentric direction. These findings suggest that being in an inverted position causes a distortion of the vestibular signal controlling the HD system.

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Passive movements of the head do not abolish anticipatory firing properties of head direction cells.

Neurons in the anterior dorsal thalamic nucleus (ADN) of the rat selectively discharge in relation to the animal's head direction (HD) in the horizontal plane. Temporal analyses of cell firing properties reveal that their discharge is optimally correlated with the animal's future directional heading by approximately 24 ms. Among the hypotheses proposed to explain this property is that ADN HD cells are informed of future head movement via motor efference copy signals. One prediction of this hypothesis is that when the rat's head is moved passively, the anticipatory time interval (ATI) will be attenuated because the motor efference signal reflects only the active contribution to the movement. The present study tested this hypothesis by loosely restraining the animal and passively rotating it through the cell's preferred direction. Contrary to our prediction, we found that ATI values did not decrease during passive movement but in fact increased significantly. HD cells in the postsubiculum did not show the same effect, suggesting independence between the two sites with respect to anticipatory firing. We conclude that it is unlikely that a motor efference copy signal alone is responsible for generating anticipatory firing in ADN HD cells.

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Head direction cell activity and behavior in a navigation task requiring a cognitive mapping strategy.

Head direction (HD) cells fire in relation to an animal's directional heading. To examine how these cells may be involved in spatial behavior, HD cells were recorded while animals performed a navigation task requiring the use of a cognitive mapping strategy. Results showed no relationship between performance on the task and the directional stability of the HD cell activity. The HD cell signal, therefore, appears to not always be used by the animal to guide its behavior during all navigation tasks.

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Rat head direction cell responses in zero-gravity parabolic flight.

Astronauts working in zero-gravity (0-G) often experience visual reorientation illusions (VRIs). For example, when floating upside down, they commonly misperceive the spacecraft floor as a ceiling and have a reversed sense of direction. Previous studies have identified a population of neurons in the rat's brain that discharge as a function of the rat's head direction (HD) in a gravitationally horizontal plane and is dependent on an intact vestibular system. Our goal was to characterize HD cell discharge under conditions of acute weightlessness. Seven HD cells in the anterior dorsal thalamus were monitored from rats aboard an aircraft in 0-G parabolic flight. Unrestrained rats locomoted in a clear plexiglas rectangular chamber that had wire mesh covering the floor, ceiling, and one wall. The chamber and surrounding visual environment were relatively up-down symmetrical. Each HD cell was recorded across forty 20-s episodes of 0-G. All HD cells maintained a significant direction-specific discharge when the rat was on the chamber floor during the 0-G and also during the hypergravity pull-out periods. Three of five cells also showed direction-specific responses on the wall in 1-G. In contrast, direction-specific discharge was usually not maintained when the rat locomoted on the vertical wall or ceiling in 0-G. The loss of direction-specific firing was accompanied by an overall increase in background firing. However, while the rat was on the ceiling, some cells showed occasional bursts of firing when the rat's head was oriented in directions that were flipped relative to the long axis of symmetry of the chamber compared with the cell's preferred firing direction on the floor. This finding is consistent with what might be expected if the rat had experienced a VRI. These responses indicate that rats maintain a normal allocentric frame of reference in 0-G and 1-G when on the floor, but may lose their sense of directional heading when placed on a wall or ceiling during acute exposures to 0-G.

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Hippocampal place cell instability after lesions of the head direction cell network.

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.

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Passive transport disrupts directional path integration by rat head direction cells.

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 degrees ) 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 degrees after locomotion from the familiar environment with the room lights off; by an average of 70 degrees after passive transport from the familiar environment with the room lights on; and by an average of 67 degrees 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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Persistent neural activity in head direction cells.

Many neurons throughout the rat limbic system discharge in relation to the animal's directional heading with respect to its environment. These so-called head direction (HD) cells exhibit characteristics of persistent neural activity. This article summarizes where HD cells are found, their major properties, and some of the important experiments that have been conducted to elucidate how this signal is generated. The number of HD and angular head velocity cells was estimated for several brain areas involved in the generation of the HD signal, including the postsubiculum, anterior dorsal thalamus, lateral mammillary nuclei and dorsal tegmental nucleus. The HD cell signal has many features in common with what is known about how neural integration is accomplished in the oculomotor system. The nature of the HD cell signal makes it an attractive candidate for using neural network models to elucidate the signal's underlying mechanisms. The conditions that any network model must satisfy in order to accurately represent how the nervous system generates this signal are highlighted and areas where key information is missing are discussed.

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Differences between appetitive and aversive reinforcement on reorientation in a spatial working memory task.

Tasks using appetitive reinforcers show that following disorientation rats use the shape of an arena to reorient, and cannot distinguish two geometrically similar corners to obtain a reward, despite the presence of a prominent visual cue that provides information to differentiate the two corners. Other studies show that disorientation impairs performance on certain appetitive, but not aversive, tasks. This study evaluated whether rats would make similar geometric errors in a working memory task that used aversive reinforcement. We hypothesized that in a task that used aversive reinforcement rats that were initially disoriented would not reorient by arena shape and thus make similar geometric errors. Tests were performed in a rectangular arena having one polarizing cue. In the appetitive condition water consumption was the reward. The aversive condition was a water maze task with reinforcement provided by escape to a hidden platform. In the aversive condition rats returned to the reinforced corner significantly more often than in the dry condition, and did not favor the diagonally opposite corner. Results show that rats can use cues besides arena shape to reorient in an aversive reinforcement condition. These findings may also reflect different strategies, with an escape/homing strategy in the wet condition and a foraging strategy in the dry condition.

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Hippocampal spatial representations require vestibular input.

The hippocampal formation is essential for forming declarative representations of the relationships among multiple stimuli. The rodent hippocampal formation, including the entorhinal cortex and subicular complex, is critical for spatial memory. Two classes of hippocampal neurons fire in relation to spatial features. Place cells collectively map spatial locations, with each cell firing only when the animal occupies that cell's "place field," a particular subregion of the larger environment. Head direction (HD) cells encode directional heading, with each HD cell firing when the rat's head is oriented in that cell's particular "preferred firing direction." Both landmarks and internal cues (e.g., vestibular, motor efference copy) influence place and HD cell activity. However, as is the case for navigation, landmarks are believed to exert greater influence over place and HD cell activity. Here we show that temporary inactivation of the vestibular system led to the disruption of location-specific firing in hippocampal place cells and direction-specific discharge of postsubicular HD cells, without altering motor function. Place and HD cell activity recovered over a time course similar to that of the restoration of vestibular function. These results indicate that vestibular signals provide an important influence over the expression of hippocampal spatial representations, and may explain the navigational deficits of humans with vestibular dysfunction.

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