Abstract
Gravity sensing provides a robust verticality signal for three-dimensional navigation. Head direction cells in the mammalian limbic system implement an allocentric neuronal compass. Here we show that head-direction cells in the rodent thalamus, retrosplenial cortex and cingulum fiber bundle are tuned to conjunctive combinations of azimuth and tilt, i.e. pitch or roll. Pitch and roll orientation tuning is anchored to gravity and independent of visual landmarks. When the head tilts, azimuth tuning is affixed to the head-horizontal plane, but also uses gravity to remain anchored to the allocentric bearings in the earth-horizontal plane. Collectively, these results demonstrate that a three-dimensional, gravity-based, neural compass is likely a ubiquitous property of mammalian species, including ground-dwelling animals.
Highlights
Gravity sensing provides a robust verticality signal for three-dimensional navigation
The spatial properties of azimuth tuning are independent of tilt tuning (Fig. 3g), and the two are separable; i.e. a cell’s entire 3D head orientation tuning curve can be computed given its tilt and azimuth tuning (Fig. 4)
Azimuth tuning is anchored to visual landmarks[25] but, during 3D motion, it is defined by rotating the gravitationally defined earth-horizontal compass in alignment with the head-horizontal compass[13,14] (Fig. 3; Fig. 6g)
Summary
Gravity sensing provides a robust verticality signal for three-dimensional navigation. Azimuth tuning is affixed to the head-horizontal plane, and uses gravity to remain anchored to the allocentric bearings in the earth-horizontal plane. These results demonstrate that a three-dimensional, gravity-based, neural compass is likely a ubiquitous property of mammalian species, including ground-dwelling animals. We tested whether mouse HD cells, which encode allocentric head orientation analogous to a neural compass, use gravity-anchored tilt signals (orientation relative to vertical) and azimuth signals
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