Biomedical subjects

J S Taube

Publications and source records attributed to J S Taube.

At least 19 recordsLinked to original sources

PubMed2002

Does the vestibular system contribute to head direction cell activity in the rat?

Head direction cells (HDC) located in several regions of the brain, including the anterior dorsal nucleus of the thalamus (ADN), postsubiculum (PoS), and lateral mammillary nuclei (LMN), provide the neural substrate for the determination of head direction. Although activity of HDC is influenced by various sensory signals and internally generated cues, lesion studies and some anatomical and physiological evidence suggest that vestibular inputs are critical for the maintenance of directional sensitivity of these cells. However, vestibular inputs must be transformed considerably in order to signal head direction, and the neuronal circuitry that accomplishes this signal processing has not been fully established. Furthermore, it is unclear why the removal of vestibular inputs abolishes the directional sensitivity of HDC, as visual and other sensory inputs and motor feedback signals strongly affect the firing of these neurons and would be expected to maintain their directional-related activity. Further physiological studies will be required to establish the role of vestibular system in producing HDC responses, and anatomical studies are needed to determine the neural circuitry that mediates vestibular influences on determination of head direction.

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PubMed2001

Neural correlates for angular head velocity in the rat dorsal tegmental nucleus.

Many neurons in the rat lateral mammillary nuclei (LMN) fire selectively in relation to the animal's head direction (HD) in the horizontal plane independent of the rat's location or behavior. One hypothesis of how this representation is generated and updated is via subcortical projections from the dorsal tegmental nucleus (DTN). Here we report the type of activity in DTN neurons. The majority of cells (75%) fired as a function of the rat's angular head velocity (AHV). Cells exhibited one of two types of firing patterns: (1) symmetric, in which the firing rate was positively correlated with AHV during head turns in both directions, and (2) asymmetric, in which the firing rate was positively correlated with head turns in one direction and correlated either negatively or not at all in the opposite direction. In addition to modulation by AHV, some of the AHV cells (40.1%) were weakly modulated by the rat's linear velocity, and a smaller number were modulated by HD (11%) or head pitch (15.9%). Autocorrelation analyses indicated that with the head stationary, AHV cells displayed irregular discharge patterns. Because afferents from the DTN are the major source of information projecting to the LMN, these results suggest that AHV information from the DTN plays a significant role in generating the HD signal in LMN. A model is proposed showing how DTN AHV cells can generate and update the LMN HD cell signal.

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PubMed2001

Statistical and information properties of head direction cells.

The human channel capacity for identifying sensory stimuli is compared with channel capacities based on neurophysiological findings. Studies have shown that cells in the postsubiculum (PoS) and the anterior dorsal thalamus (ADN) of the rat discharge as a function of the animal's head direction in the horizontal plane. We compute the statistical properties of the firing rates of head direction (HD) cells and the potential amount of information transmitted by these cells according to two theoretical models. The ceU response model for single cells indicates that information transmitted is much less than 0.5 bits. The population response model developed for cell ensembles generates values in the range of 1-3.2 bits, suggesting that a cell population can distinguish between two and nine head directions, depending on the value used for the standard deviation of directions over which a cell fires. These values are similar to those found in human psychophysical studies of the channel capacity for unidimensional sensory attributes.

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PubMed2001

On the behavioral significance of head direction cells: neural and behavioral dynamics during spatial memory tasks.

Current theories assume that rats use the directional information reflected by head direction (HD) cells when performing spatial tasks. This assumption was assessed by monitoring anterior thalamic HD cell activity and relating it to the subject's behavioral response on 2 spatial memory tasks that tested either reference memory or working memory. In both tasks, there was a significant number of trials where there was not a tight coupling between the preferred firing direction of HD cells and the direction of the behavioral response. In addition, it was possible to intentionally change the preferred direction of HD cells without affecting performance accuracy. An additional experiment showed that manipulations that affected internal, but not external, cues impaired performance on the reference memory task. These findings suggest that HD cell activity was not consistently guiding the subjects' behavior on these 2 spatial tasks.

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PubMed2000

Maintenance of rat head direction cell firing during locomotion in the vertical plane.

Previous studies have identified a subset of neurons in the rat anterodorsal thalamus (ADN) that encode head direction (HD) in absolute space and may be involved in navigation. These HD cells discharge selectively when the rat points its head in a specific direction (the preferred firing direction) in the horizontal plane. HD cells are typically recorded during free movement about a single horizontal surface. The current experiment examined how HD cell firing was influenced by 1) locomotion in the vertical plane and 2) locomotion on two different horizontal surfaces separated in height. Rats were trained in a cylindrical enclosure containing a single polarizing cue card attached to the cylinder wall, covering approximately 100 degrees of arc. The enclosure contained two horizontal surfaces: the cylinder floor and an annulus around the cylinder top 76 cm above the floor. A 90 degrees vertical mesh ladder that could be affixed at any angular position on the cylinder wall allowed the rats to locomote back and forth between the two horizontal surfaces. Rats were trained to retrieve food pellets on the cylinder floor as well as climb the mesh ladder to retrieve food pellets on the annulus. HD cell activity was monitored as the rat traversed the horizontal and vertical surfaces of the apparatus. When the angular position of the mesh corresponded to the cell's preferred firing direction, the HD cells maintained their peak discharge rate as the rat climbed up the mesh, but did not fire when the rat climbed down the mesh. In contrast, when the mesh was positioned 180 degrees opposite the preferred firing direction, HD cells did not fire when the rat climbed up the mesh, but exhibited maximal firing when the rat climbed down the mesh. When the mesh was placed 90 or 270 degrees from the preferred firing direction, HD cells exhibited background firing rates during climbing up or down the mesh. While preferred firing directions were maintained between the two horizontal surfaces, peak firing rate increased significantly (approximately 30%) on the annulus as compared with the cylinder floor. These data demonstrate that HD cells continue to discharge in the vertical plane if the vertical locomotion began with the rat's orientation corresponding to the preferred firing direction. One model consistent with these data are that HD cells define the horizontal reference frame as the animal's plane of locomotion. Further, we propose that HD cell firing, as viewed within a three-dimensional coordinate system, can be characterized as the surface of a hemitorus.

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PubMed1999

Head direction cells in rats with hippocampal or overlying neocortical lesions: evidence for impaired angular path integration.

Rodents use two distinct navigation strategies that are based on environmental cues (landmark navigation) or internal cues (path integration). Head direction (HD) cells are neurons that discharge when the animal points its head in a particular direction and are responsive to the same cues that support path integration and landmark navigation. Experiment 1 examined whether HD cells in rats with lesions to the hippocampus plus the overlying neocortex or to just the overlying neocortex could maintain a stable preferred firing direction when the rats locomoted from a familiar to a novel environment, a process thought to require path integration. HD cells from both lesion groups were unable to maintain a similar preferred direction between environments, with cells from hippocampal rats showing larger shifts than cells from rats sustaining only cortical damage. When the rats first explored the novel environment, the preferred directions of the cells drifted for up to 4 min before establishing a consistent firing orientation. The preferred direction was usually maintained during subsequent visits to the novel environment but not across longer time periods (days to weeks). Experiment 2 demonstrated that a novel landmark cue was able to establish control over HD cell preferred directions in rats from both lesion groups, showing that the impairment observed in experiment 1 cannot be attributed to an impairment in establishing cue control. Experiment 3 showed that the preferred direction drifted when HD cells in lesioned animals were recorded in the dark. It was also shown that the anticipatory property of anterodorsal thalamic nucleus HD cells was still present in lesioned animals; thus, this property cannot be attributed to an intact hippocampus. These findings suggest that the hippocampus and the overlying neocortex are involved in path integration mechanisms, which enable an animal to maintain an accurate representation of its directional heading when exploring a novel environment.

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PubMed1999

Some thoughts on place cells and the hippocampus.

This commentary addresses five issues related to the functional role of place cells and the hippocampus. 1. Is the cognitive map located in the hippocampus? Not exclusively. 2. Is the hippocampus required for path integration? Not exclusively. 3. Is the hippocampus involved in selecting the appropriate reference frame? Not exclusively. 4. Are all episodic memories encoded by the hippocampus? No. 5. Does the hippocampus use attractor networks? Not exclusively.

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PubMed1998

Firing properties of rat lateral mammillary single units: head direction, head pitch, and angular head velocity.

Many neurons in the rat anterodorsal thalamus (ADN) and postsubiculum (PoS) fire selectively when the rat points its head in a specific direction in the horizontal plane, independent of the animal's location and ongoing behavior. The lateral mammillary nuclei (LMN) are interconnected with both the ADN and PoS and, therefore, are in a pivotal position to influence ADN/PoS neurophysiology. To further understand how the head direction (HD) cell signal is generated, we recorded single neurons from the LMN of freely moving rats. The majority of cells discharged as a function of one of three types of spatial correlates: (1) directional heading, (2) head pitch, or (3) angular head velocity (AHV). LMN HD cells exhibited higher peak firing rates and greater range of directional firing than that of ADN and PoS HD cells. LMN HD cells were modulated by angular head velocity, turning direction, and anticipated the rat's future HD by a greater amount of time (approximately 95 msec) than that previously reported for ADN HD cells (approximately 25 msec). Most head pitch cells discharged when the rostrocaudal axis of the rat's head was orthogonal to the horizontal plane. Head pitch cell firing was independent of the rat's location, directional heading, and its body orientation (i.e., the cell discharged whenever the rat pointed its head up, whether standing on all four limbs or rearing). AHV cells were categorized as fast or slow AHV cells depending on whether their firing rate increased or decreased in proportion to angular head velocity. These data demonstrate that LMN neurons code direction and angular motion of the head in both horizontal and vertical planes and support the hypothesis that the LMN play an important role in processing both egocentric and allocentric spatial information.

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PubMed1998

Recordings of postsubiculum head direction cells following lesions of the laterodorsal thalamic nucleus.

Areas of the rodent limbic system are important for solving spatial tasks and accurate navigation. Previous studies have identified cells in the postsubiculum (PoS) and the lateral dorsal thalamus (LDN) which discharge as a function of the animal's head direction in the horizontal plane. These two brain areas are reciprocally connected with one another. To determine the contribution of the LDN to the functioning of PoS head direction cells, we lesioned the LDN and recorded single units in the PoS. We report here that lesions of the LDN had little effect upon the firing properties of PoS HD cells. In addition, HD cells from lesioned animals showed normal responses to two environmental manipulations: (1) when the salient visual cue was rotated the preferred firing directions of PoS HD cells shifted a similar amount and (2) cells frequently ceased firing, or had reductions in their peak firing rate, when the animal was restrained and passively rotated through the preferred firing direction. These results indicate that the LDN does not play a substantive role in either the generation or the stability of the HD cell signal in the PoS.

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PubMed1998

Comparisons of head direction cell activity in the postsubiculum and anterior thalamus of freely moving rats.

Single cells in the rat anterior thalamic nucleus (ATN) and postsubiculum (PoS) discharge as a function of the rat's directional heading in the horizontal plane, independent of its location. A previous study that compared cell firing during clockwise and counterclockwise head turns concluded that ATN 'head direction' (HD) cell discharge anticipates the rat's future directional heading, while PoS HD cell discharge is in register with the rat's current directional heading (Blair and Sharp [1995] J Neurosci 15:6260-6270). In the current study we extend these findings by using a different method of analysis. HD cells in the ATN and PoS were first characterized by three different measures: peak firing rate, range width, and information content. We then examined how these measures varied when cell firing was aligned with past (negative time shift) or future (positive time shift) head direction of the rat. We report that all three measures were optimized when ATN cell firing was aligned with the animal's future directional heading by about +23 msec. In contrast, PoS HD cell firing was optimized when cell firing was aligned with the rat's past head direction by about -7 msec. When the optimal value was plotted as a function of the amount of time spikes were shifted relative to head orientation, the mean ATN function was shifted to the right of the PoS function only at negative time shifts; at positive time shifts the two functions overlapped. Analysis of two recording sessions from the same cell indicated that each cell in a particular brain area is 'tuned' to a specific time shift so that all cells within a brain area are not uniformly tuned to the same time shift. Other analyses showed that the clockwise and counterclockwise tuning functions were not skewed in the direction of the head turn as postulated by Redish et al. ([1996] Network: Computation in Neural Systems 7:671-685) and Blair et al. ([1997] J Neurophysiol 17:145-159). Additional analysis on episodes when the rat happened to continually point its head in the preferred direction indicated that HD cell firing undergoes little adaptation. In the Discussion, we argue that these results are best accounted for by a motor efference copy signal operating on both types of HD cells such that the copy associated with the PoS HD cells is delayed in time by about 30 msec relative to the copy associated with ATN HD cells.

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PubMed1998

Head direction cells and the neurophysiological basis for a sense of direction.

Animals require two types of fundamental information for accurate navigation: location and directional heading. Current theories hypothesize that animals maintain a neural representation, or cognitive map, of external space in the brain. Whereas cells in the rat hippocampus and parahippocampal regions encode information about location, a second type of allocentric spatial cell encodes information about the animal's directional heading, independent of the animal's on-going behaviors. These head direction (HD) cells are found in several areas of the classic Papez circuit. This review focuses on experimental studies conducted on HD cells and describes their discharge properties, functional significance, role in path integration, and responses to different environmental manipulations. The anterior dorsal thalamic nucleus appears critical for the generation of the directional signal. Both motor and vestibular cues also play important roles in the signal's processing. The neural network models proposed to account for HD cell firing are compared with known empirical findings. Examples from clinical cases of patients with topographical disorientation are also discussed. It is concluded that studying the neural mechanisms underlying the HD signal provides an excellent opportunity for understanding how the mammalian nervous system processes a high level cognitive signal.

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PubMed1998

Cue control and head direction cells.

Previous research has shown that head direction (HD) cells in both the anterior dorsal thalamus (ADN) and the postsubiculum (PoS) in rats discharge in relation to familiar, visual landmarks in the environment. This study assessed whether PoS and ADN HD cells would be similarly responsive to nonvisual or unfamiliar environmental cues. After visual input was eliminated by blindfolding the rats, HD cells maintained direction-specific discharge, but their preferred firing directions became less stable. In addition, rotations of the behavioral apparatus indicated that some nonvisual cues (presumably tactile, olfactory, or both) exerted above chance stimulus control over a cell's preferred firing direction. However, a prominent auditory cue was not effective in exerting stimulus control over a cell's preferred direction. HD cell activity also was assessed after rotation of a novel visual cue exposed to the rat for 1, 3, or 8 min. An 8-min exposure was enough time for a novel visual cue to gain control over a cell's preferred direction, whereas an exposure of 1 or 3 min led to control in only about half the sessions. These latter results indicate that HD cells rely on a rapid learning mechanism to develop associations with landmark cues.

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PubMed1997

Interaction between the postsubiculum and anterior thalamus in the generation of head direction cell activity.

Previous research has identified neurons in the postsubiculum (PoS) and anterior dorsal thalamic nucleus (AD) of the rat that discharge as a function of the animal's head direction. In addition, anatomical studies have shown that the AD and PoS are reciprocally connected with one another. The current study examined whether head direction (HD) cells in each of the two areas is dependent on input from the other structure. After both electrolytic or neurotoxic lesions of the AD, no cells were identified with direction-specific discharge in the PoS. In contrast, AD HD cell activity was still present after neurotoxic lesions to the PoS. However, AD HD cells in PoS-lesioned rats exhibited three important differences compared with AD HD cells in intact animals: (1) their directional firing range was significantly larger, (2) their firing predicted the animal's future head direction by a larger amount, and (3) their preferred firing direction was substantially less influenced by a prominent visual landmark within the recording environment. These results indicate that information critical for HD cell activity is conveyed in both directions between the AD and the PoS; whereas the AD is necessary for the presence of HD cell activity in the PoS, the PoS appears important in allowing visual landmarks to exert control over the preferred firing direction of AD HD cells. These findings have implications for several computational models that propose to account for the generation of the HD cell signal.

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PubMed1997

Head direction cells and episodic spatial information in rats without a hippocampus.

To successfully navigate through the environment animals rely on information concerning their directional heading and location. Many cells within the postsubiculum and anterior thalamus discharge as a function of the animal's head direction (HD), while many cells in the hippocampus discharge in relation to the animal's location. We placed lesions in the hippocampus and recorded from HD cells in the postsubiculum and anterior thalamus. Lesions of the hippocampus did not disrupt the HD cell signal in either brain area, indicating that the HD cell signal must be generated by structures external to the hippocampus. In addition, each cell's preferred firing direction remained stable across days when the lesioned animal was placed into a novel environment. This stability appeared to weaken after several weeks of nonexposure to the new enclosure for two out of five animals, and subsequently recorded cells from these two animals established a new angular relationship between the familiar and novel environments. Our results suggest that extra-hippocampal structures are capable of creating and maintaining a novel representation of the animal's environmental context. This representation shares features in common with mnemonic processes involving episodic memory that until now were assumed to require an intact hippocampus.

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PubMed1997

Firing properties of head direction cells in the rat anterior thalamic nucleus: dependence on vestibular input.

Vestibular information influences spatial orientation and navigation in laboratory animals and humans. Neurons within the rat anterior thalamus encode the directional heading of the animal in absolute space. These neurons, referred to as head direction (HD) cells, fire selectively when the rat points its head in a specific direction in the horizontal plane with respect to the external laboratory reference frame. HD cells are thought to represent an essential component of a neural network that processes allocentric spatial information. The functional properties of HD cells may be dependent on vestibular input. Here, anterior thalamic HD cells were recorded before and after sodium arsanilate-induced vestibular system lesion. Vestibular lesions abolished the directional firing properties of HD cells. The time course of disruption in the directional firing properties paralleled the loss of vestibular function. Arsanilate-treated rats exhibited only minor changes in locomotor behavior, which were unlikely to account for the loss of direction-specific firing. Vestibular lesions also disrupted the influence of angular head velocity on anterior thalamic single-unit firing rates. Finally, a subset of anterior thalamic neurons recorded from vestibular-lesioned rats exhibited a pattern of intermittent firing bursts that were distinctly unrelated to HD. This novel anterior thalamic firing pattern has not been encountered in any vestibular-intact rat. These data suggest that: (1) the neural code for directional bearing is critically dependent on vestibular information; and (2) this loss of HD cell information may represent a neurobiological mechanism to account for the orientation and navigational deficits observed after vestibular dysfunction.

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PubMed1997

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

Head direction (HD) and place cells were recorded in rats that had previously exhibited significant acquisition deficits on a radial arm maze task following disorientation treatment. In this study we determined whether this behavioral impairment was associated with a lack of landmark stimulus control over the preferred orientations of HD and place cells. Neurons were recorded as animals retrieved food pellets in a cylindrical apparatus containing a single cue card. Some of these HD cells were also recorded while animals explored an eight-arm radial maze in a similar cue-controlled environment. The stimulus control of the landmarks in each environment was assessed by rotating the landmark and examining the subsequent preferred orientations of HD and place cells. Animals underwent disorientation treatment before and after each recording session. Despite this disorientation, rotation of the cue card in the cylindrical apparatus resulted in a corresponding shift in the preferred orientations of HD and place cells in 13 of 15 and 7 of 7 recording sessions, respectively. On the radial arm maze, rotation of the landmark cue was associated with a corresponding shift in the HD cell's preferred orientation in 7 of 9 sessions. These results suggest that a visual landmark's stimulus control may not require a learned association between that landmark and an animal's stable experience in an environment. Furthermore, instability in the HD cell system is unlikely to account for the impaired performance of the disoriented animals in the radial arm maze. Rather, these impairments may be due to the animal's inability to utilize stable representations of the environment provided by HD and place cells.

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PubMed1997

Effects of repeated disorientation on the acquisition of spatial tasks in rats: dissociation between the appetitive radial arm maze and aversive water maze.

This study examined the effects of disorientation on the acquisition of different spatial reference memory tasks. In an appetitively motivated radial arm maze task in which 1 arm was consistently baited, rats that were disoriented before each trial were impaired in their ability to acquire the task relative to rats placed in a clear container and not disoriented. However, disoriented rats were able to learn a Morris water maze and a water version of the radial arm maze under similar training conditions, suggesting that the effects of disorientation may interact with the quality or quantity of motivation involved in a given task. These results suggest that appetitive and aversive spatial tasks are dissociable, and that any impairment that is due to disorientation is specific to the appetitive radial arm maze task.

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PubMed1997

Correlation between head direction cell activity and spatial behavior on a radial arm maze.

This study assessed the activity of head direction (HD) cells during performance of a spatial reference memory task on a radial arm maze. Rats were trained to select a maze arm located in a constant position in relation to a salient extramaze visual landmark. HD cell discharge properties remained relatively stable across task acquisition in most rats. Following acquisition, rotation of the landmark by 90 degrees or 180 degrees usually led to a corresponding shift in the maze arm selected and the HD cell's preferred firing direction. When the cell's preferred direction did not shift, rats usually selected the wrong arm. HD cell activity was not influenced by the rat's approach to the goal, reward consumption, or exit from the reward area. This demonstration of landmark control over behavior and the cell's preferred direction supports the hypothesis that HD cells contribute to an absolute representation of the environment that can be used to guide spatial behavior.

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