Angular Head Velocity Cells within Brainstem Nuclei Projecting to the Head Direction Circuit.

The sense of orientation of an animal is derived from the head direction (HD) system found in several limbic structures and depends on an intact vestibular labyrinth. However, how the vestibular system influences the generation and updating of the HD signal remains poorly understood. Anatomical and lesion studies point toward three key brainstem nuclei as key components for generating the HD signal-nucleus prepositus hypoglossi, supragenual nucleus, and dorsal paragigantocellularis reticular nuclei. 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 determine the types of information these brain areas convey to the HD network, we recorded neurons from these regions while female rats actively foraged in a cylindrical enclosure or were restrained and rotated passively. During foraging, a large subset of cells in all three nuclei exhibited activity that correlated with the angular head velocity (AHV) of the rat. Two fundamental types of AHV cells were observed; (1) symmetrical AHV cells increased or decreased their firing with increases in AHV regardless of the direction of rotation, and (2) asymmetrical AHV cells responded differentially to clockwise and counterclockwise head rotations. When rats were passively rotated, some AHV cells remained sensitive to AHV, whereas firing was attenuated in other cells. In addition, a large number of AHV cells were modulated by linear head velocity. These results indicate the types of information conveyed from the vestibular nuclei that are responsible for generating the HD signal.SIGNIFICANCE STATEMENT Extracellular recording of brainstem nuclei (nucleus prepositus hypoglossi, supragenual nucleus, and dorsal paragigantocellularis reticular nucleus) that project to the head direction circuit identified different types of AHV cells while rats freely foraged in a cylindrical environment. The firing of many cells was also modulated by linear velocity. When rats were restrained and passively rotated, some cells remained sensitive to AHV, whereas others had attenuated firing. These brainstem nuclei provide critical information about the rotational movement of the head of the rat in the azimuthal plane.

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

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. Significance Statement: Extracellular recording of brainstem nuclei (nucleus prepositus hypoglossi, supragenual nucleus, and dorsal paragigantocellularis reticular nucleus) that project to the head direction circuit identified different types of angular head velocity (AHV) cells while rats freely foraged in a cylindrical environment. The firing of many cells was also modulated by linear velocity. When rats were restrained and passively rotated some cells remained sensitive to AHV, whereas others had attenuated firing. These brainstem nuclei provide critical information about the rotational movement of the rat's head in the azimuthal plane.