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Objective: Head direction cell and place cell spatially tuned firing is often anchored to salient visual landmarks on the periphery of a recording environment. What is less well understood is whether structural features of an environment, such as orientation of a maze sub‐compartment or a polarizing barrier, can likewise control spatial firing. Method: We recorded from 54 head direction cells in the medial entorhinal cortex and subicular region of male Lister Hooded rats while they explored an apparatus with four parallel or four radially arranged compartments (Experiment 1). In Experiment 2, we recorded from 130 place cells (in Lister‐ and Long‐Evans Hooded rats) and 30 head direction cells with 90° rotations of a cue card and a barrier in a single environment (Experiment 2). Results: We found that head direction cells maintained a similar preferred firing direction across four separate maze compartments even when these faced different directions (Experiment 1). However, in an environment with a single compartment, we observed that both a barrier and a cue card exerted comparable amounts of stimulus control over head direction cells and place cells (Experiment 2). Conclusion: The maintenance of a stable directional orientation across maze compartments suggests that the head direction cell system has the capacity to provide a global directional reference that allows the animal to distinguish otherwise similar maze compartments based on the compartment's orientation. A barrier is, however, capable of controlling spatially tuned firing in an environment in which it is the sole polarizing feature. [ABSTRACT FROM AUTHOR]

• Damage to the head direction circuit produces only modest impairments in spatial behavior. • Head direction cells predict spatial behavior in some tasks, but not others. • New evidence suggests that there are different kinds of head direction cells. • Different head direction cells may underlie different spatial abilities. 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. [ABSTRACT FROM AUTHOR]

The head direction system is composed of neurons found in a number of connected brain areas that fire in a sharply tuned, directional way. The function of this system, however, has not been fully established. To assess this, we devised a novel spatial landmark task, comparable to the paradigms in which stimulus control has been assessed for spatially tuned neurons. The task took place in a large cylinder and required rats to dig in a specific sand cup, from among 16 alternatives, to obtain a food reward. The reinforced cup was in a fixed location relative to a salient landmark, and probe sessions confirmed that the landmark exerted stimulus control over the rats' cup choices. To assess the contribution of the head direction cell system to this memory task, half of the animals received ibotenic acid infusions into the lateral mammillary nuclei (LMN), an essential node in the head direction network, while the other received sham lesions. No differences were observed in performance of this task between the 2 groups. Animals with LMN lesions were impaired, however, in reversal learning on a water maze task. These results suggest that the LMN, and potentially the head direction cell system, are not essential for the use of visual landmarks to guide spatial behavior. [ABSTRACT FROM AUTHOR]

Path integration, the ability to maintain a representation of location and direction on the basis of internal cues, is thought to be important for navigation and the learning of spatial relationships. Representations of location and direction in the brain, such as head direction cells, grid cells, and place cells in the limbic system, are thought to underlie navigation by path integration. While this idea is generally consistent with lesion studies, the relationship between such neural activity and behavior has not been studied on a task where animals demonstrably use a path integration strategy. Here we report the development of such a task in rats: by slowly rotating rats before their return to a trial-unique home base, we could show subjects relied on internal cues only to navigate. To illustrate how this task can be combined with recording, we show examples of simultaneously recorded head direction cells in which neural activity is closely related to rats' homing direction. These results support the notion that rats can navigate by path integration, that this ability depends on head direction cells, and suggest a convenient behavioral paradigm for investigating the neural basis of navigation. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]