Comparison of head direction cell firing characteristics across thalamo‐parahippocampal circuitry

Clark, Benjamin J.; LaChance, Patrick A.; Winter, Shawn S.; Mehlman, Max L.; Butler, Will; LaCour, Ariyana; Taube, Jeffrey S.

doi:10.1002/hipo.23596

Cited by 4 publications

References 119 publications

(289 reference statements)

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Angular head velocity cells within brainstem nuclei projecting to the head direction circuit

Graham

Dumont

Winter

et al. 2023

Preprint

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An animal's perceived sense of orientation depends upon the head direction (HD) system found in several limbic structures and depends upon an intact peripheral vestibular labyrinth. However, how the vestibular system influences the generation, maintenance, and updating of the HD signal remains poorly understood. Anatomical and lesion studies point towards three key brainstem nuclei as being potential critical components in generating the HD signal: nucleus prepositus hypoglossi (NPH), supragenual nucleus (SGN), and dorsal paragigantocellularis reticular nuclei (PGRNd). Collectively, these nuclei are situated between the vestibular nuclei and the dorsal tegmental and lateral mammillary nuclei, which are thought to serve as the origin of the HD signal. To test this hypothesis, extracellular recordings were made in these areas while rats either freely foraged in a cylindrical environment or were restrained and rotated passively. During foraging, a large subset of cells in all three nuclei exhibited activity that correlated with changes in the rat's angular head velocity (AHV). Two fundamental types of AHV cells were observed: 1) symmetrical AHV cells increased or decreased their neural firing with increases in AHV regardless of the direction of rotation; 2) asymmetrical AHV cells responded differentially to clockwise (CW) and counter-clockwise (CCW) head rotations. When rats were passively rotated, some AHV cells remained sensitive to AHV whereas others had attenuated firing. In addition, a large number of AHV cells were modulated by linear head velocity. These results indicate the types of information conveyed in the ascending vestibular pathways that are responsible for generating the HD signal.

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Angular head velocity cells within brainstem nuclei projecting to the head direction circuit

Graham

Dumont

Winter

et al. 2023

Preprint

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Medial Entorhinal VIP-expressing interneurons receive direct input from Anterior Dorsal Thalamus and are critical for spatial memory

Oulé,

Badrinarayanan,

Sundar-Maccagno

et al. 2024

Preprint

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Head-direction (HD) cells are found across several regions in the brain, including the anterodorsal thalamic nucleus (ADN), the subicular complex, and the medial entorhinal cortex (MEC). A fundamental role of head direction cells is to provide input to MEC grid cells, which are thought to translate information about head direction into a metric code for spatial location. However, classic anatomical studies indicate that most thalamic HD projections pass indirectly to the MEC via the post- and para-subiculum, with only a small subset of ADN fibers terminating in the MEC. To further investigate the smaller and direct projection to the MEC, we use rabies-mediated retrograde tracing in mice to determine if this projection explicitly targets a subset of MEC neurons. Our findings reveal that ADN neurons specifically project onto MEC interneurons, with a preference for MEC VIP-expressing cells. Additionally, MEC VIP cells receive input from the hippocampus, the subicular complex, and the retrosplenial cortex - key centers for spatial memory - suggesting a specialized role for MEC VIP cells in spatial memory. Indeed, we find that MEC VIP cells exhibit increased c-Fos expression in a spatial memory task and show that chemogenetic inhibition of these neurons impairs task performance. Together, these data uncover a specific projection of head direction information onto MEC interneurons and confirm that MEC VIP-expressing cells are critical for spatial memory.

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Pathological tau alters head direction signaling and induces spatial disorientation

Jiang,

Hijazi,

Sarkany

et al. 2024

Preprint

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Disorientation is an early symptom of dementia, suggesting impairments in neural circuits responsible for head direction signaling. The anterodorsal thalamic nucleus (ADn) exhibits early and selective vulnerability to pathological misfolded forms of tau (ptau), a major hallmark of Alzheimer's disease and ageing. The ADn contains a high density of head direction (HD) cells; their disruption may contribute to spatial disorientation. To test this, we virally expressed human tau in the ADn of adult mice. HD-ptau mice were defined by ptau+ cells in the ADn and ptau+ axon terminals in postsynaptic target regions. Despite being able to learn spatial memory tasks, HD-ptau mice exhibited increased looping behavior during spatial learning and made a greater number of head turns during memory recall, consistent with disorientation. Using in vivo extracellular recordings, we identified ptau-expressing ADn cells and found that ADn cells from HD-ptau mice had reduced directionality and altered burst firing. These data suggest that ptau alters HD signaling, leading to impairments in spatial orientation.

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Comparison of head direction cell firing characteristics across thalamo‐parahippocampal circuitry

Cited by 4 publications

References 119 publications

Angular head velocity cells within brainstem nuclei projecting to the head direction circuit

Angular head velocity cells within brainstem nuclei projecting to the head direction circuit

Medial Entorhinal VIP-expressing interneurons receive direct input from Anterior Dorsal Thalamus and are critical for spatial memory

Pathological tau alters head direction signaling and induces spatial disorientation

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