The anatomical and computational basis of the rat head-direction cell signal

doi:10.1016/S0166-2236(00)01797-5

Trends in Neurosciences

Volume 24, Issue 5, 1 May 2001, Pages 289-294

https://doi.org/10.1016/S0166-2236(00)01797-5 Get rights and content

Abstract

As a rat navigates through space, neurons called head-direction (HD) cells provide a signal of the rat's momentary directional heading. Although partly guided by landmarks, the cells also show a remarkable ability to track directional heading based on angular head movement. Theoretical models suggest that the HD cells are linked together to form an attractor network, and that cells which signal angular velocity update the directional setting of the attractor. Recently, cell types similar to those required theoretically have been discovered in the lateral mammillary and dorsal tegmental nuclei. Lesion and anatomical data suggest these nuclei might constitute the postulated attractor-path integration mechanism, and that they provide the HD cell signal to cortical areas where it has been observed.

Section snippets

HD cells are not sensitive to the geomagnetic field

One possibility for how these direction-specific firing patterns are generated could be that the cells are somehow sensitive to the local geomagnetic field, so that they can detect heading, in earth-centered coordinates, directly. Numerous observations, however, have suggested that this is not the case 3, 4, 5, 6. For example, Taube et al.³ recorded from HD cells in the postsubiculum as rats foraged in a cylindrical enclosure equipped with a single, white card located on one portion of the wall

HD cells are linked together to form an attractor network

Interestingly, almost all the models developed to explain the HD cells are similar in their basic features 11, 12, 13, 14, 15, 16. Most begin with the idea that the HD cells are somehow linked together, via a set of excitatory and inhibitory connections, to form an attractor network. One example of such a network is provided in Fig. 3a. In this network, cells that are meant to represent adjacent directions are located next to one another. The excitatory HD cells provide excitatory input to

HD cells are located in a set of interconnected brain regions

HD cells were initially discovered in the postsubicular cortex of the hippocampal formation 1, 2. Subsequently, they have been discovered in several additional, closely-related brain regions, including the retrosplenial cortex 17, 18, the anterior thalamic nucleus (ATN) (Refs 19,20), the lateral dorsal thalamic nucleus (LDN) (Ref. 21), the lateral mammillary nucleus (LMN) (Refs 22,23), the dorsal tegmental nucleus (DTN) of Gudden ²⁴ and the striatum 25, 26.

Fig. 4 depicts these areas and their

LMN and DTN might constitute the attractor-path integration network

The fact that HD cells exist in so many different brain regions raises the question of whether the postulated attractor-path integration functions are distributed across all (or many) of these areas, or whether, by contrast, the crucial network is located in just a subset of these regions. As noted elsewhere ⁴², recent data have suggested that the LMN and DTN might constitute crucial components of the HD cell system.

Concluding remarks

The HD cell system provides a remarkably salient, robust, and tractable neural signal. Because of this, it has been possible to make quite rapid progress in the characterization of the basic behavioral features of these cells, in addition to obtaining clues about where and how the signal might be generated. Although recent evidence suggests that the signal might be generated in the LMN–DTN complex, further work is necessary to substantiate this claim.

If these two nuclei do, in fact, constitute

Acknowledgements

Research support was from NIH (MH11102 and NS35191), Whitehall Foundation (A94-06), and NSF (9120131). We thank three anonymous reviewers who provided helpful comments on this manuscript.

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The head orientation was upward in upslope walking and downward in downslope walking. Previous studies have shown that there are head direction cells in several brain areas that differentially respond to particular head directions (Sharp et al., 2001). Thus, the difference in head orientation could directly influence cortical activity.
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Trends in Neurosciences

ReviewThe anatomical and computational basis of the rat head-direction cell signal

Abstract

Section snippets

HD cells are not sensitive to the geomagnetic field

HD cells are linked together to form an attractor network

HD cells are located in a set of interconnected brain regions

LMN and DTN might constitute the attractor-path integration network

Concluding remarks

Acknowledgements

Neuron

Brain Res.

Brain Res.

Brain Res.

Brain Res.

Neuron

Head-direction cells in the deep cell layers of the dorsal presubiculum in freely-moving rats

Soc. Neurosci. Abstr.

Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis

J. Neurosci.

Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations

J. Neurosci.

Preferential use of the landmark navigational system by Head Direction cells in rats

Behav. Neurosci.

Cue control and Head Direction cells

Behav. Neurosci.

Interactions between idiothetic cues and external landmarks in the control of place cells and head direction cells

J. Neurophysiol.

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

J. Neurophysiol.

Place cells, Head Direction cells, and the learning of landmark stability

J. Neurosci.

Visual and vestibular influences on head direction cells in the anterior thalamus of the rat

Behav Neurosci.

Firing properties of Head Direction cells in the rat anterior thalamic nucleus: Dependence on vestibular input

J. Neurosci.

Dead reckoning’, landmark learning, and the sense of direction: a neurophysiological and computational hypothesis

J. Cogn. Neurosci.

A model of the neural basis of the rat's sense of direction

A coupled attractor model of the rodent head direction system

Network

Neural network modeling of the hippocampal formation signals and their possible role in navigation: A modular approach

Hippocampus

Representation of spatial orientation by the intrinsic dynamics of the head direction cell ensemble: A theory

J. Neurosci.

Modeling attractor deformation in the rodent Head-Direction cell system

J. Neurophysiol.

Head direction cells in the rat posterior cortex. I. Anatomical distribution and behavioral modulation

Exp. Brain Res.

Head direction cells recorded in the anterior thalamic nuclei of freely moving rats

J. Neurosci.

Review
The anatomical and computational basis of the rat head-direction cell signal