Vestibular and Attractor Network Basis of the Head Direction Cell Signal in Subcortical Circuits

Accurate navigation depends on a network of neural systems that encode the moment-to-moment changes in an animal\u27s directional orientation and location in space. Within this navigation system are head direction (HD) cells, which fire persistently when an animal\u27s head is pointed in a particular direction (Sharp et al., 2001a; Taube, 2007). HD cells are widely thought to underlie an animal\u27s 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. The purpose of the present review is to summarize some of the recent studies arguing that the origin of the HD signal resides subcortically, specifically within the reciprocal connections of the dorsal tegmental and lateral mammillary nuclei. Furthermore, we 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 anatomical and physiological work suggesting that this attractor network architecture may reside within the tegmento-mammillary circuit

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

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

Acetylcholine Contributes to Head Direction Cell Stability During Path Integration and Landmark Navigation

Perceived directional heading is represented in the brain by head direction (HD) cells, which fire rapidly when the head is pointed in one direction and become virtually silent when the head is pointed in all other directions. The HD signal is dominantly controlled by the position of visual landmarks, but can be maintained by path integration when familiar landmarks are not available. The neural mechanism(s) that allow path integration to maintain the HD signal have not been investigated, but a possible component of this mechanism is acetylcholine, given that selective cholinergic lesions impair path integration-based navigation. To test this, we recorded HD cell activity from the anterodorsal thalamus while rats foraged for food within a cylinder, or navigated within a dual chamber apparatus, after systemic injection of saline or atropine sulfate. In the cylinder, a prominent cue card served as the sole landmark for a standard session, after which the cue was removed for a no-cue session. Saline or atropine sulfate was then injected, and a second no-cue session was conducted, followed by standard, 90° cue rotation, standard, and no-cue sessions. During the first no-cue session after injection, some cells in atropine-treated rats showed slightly more drift in preferred firing direction (PFD) than control cells, but otherwise appeared to be unaffected by atropine. With the cue rotated 90º, 10 of the 19 (53%) cells in atropine-treated rats and 12 of the 17 (71%) control cells shifted within ± 30° of 90º. In the dual chamber apparatus, rats walked from a familiar cylinder to a novel rectangle via an alleyway, and then returned to the familiar cylinder. Control HD cells (n = 7) showed a slight PFD shift as the rat entered the novel rectangle (mean absolute shift = 17.14 ± 3.80°, range = -30 to 12°), suggesting the HD signal was maintained relatively well between arenas by path integration; upon return, the PFD returned to that of the first session (mean absolute shift = 5.14 ± 1.56°, range = -12 to 6°). In contrast, 7 of the 9 HD cells in atropine-treated rats (78%) showed greater PFD shifts between the familiar cylinder and novel rectangle (mean absolute shift = 86.00 ± 12.17°, angular shift range = -102 to 114°) and between the first and last sessions in the familiar cylinder (mean absolute shift = 24.00 ± 10.16°, angular shift range = 0 to -72°); 2 of the 9 cells (22%) showed considerable PFD drift during the novel rectangle or return cylinder sessions. Thus, acetylcholine is not critical for normal HD cell activity within a familiar environment, but facilitates the stability of the HD signal during both path integration and landmark navigation

A Comparison of Neural Decoding Methods and Population Coding Across Thalamo-Cortical Head Direction Cells

Head direction (HD) cells, which fire action potentials whenever an animal points its head in a particular direction, are thought to subserve the animal’s sense of spatial orientation. HD cells are found prominently in several thalamo-cortical regions including anterior thalamic nuclei, postsubiculum, medial entorhinal cortex, parasubiculum, and the parietal cortex. While a number of methods in neural decoding have been developed to assess the dynamics of spatial signals within thalamo-cortical regions, studies conducting a quantitative comparison of machine learning and statistical model-based decoding methods on HD cell activity are currently lacking. Here, we compare statistical model-based and machine learning approaches by assessing decoding accuracy and evaluate variables that contribute to population coding across thalamo-cortical HD cells