Three-dimensional head-direction coding in the bat brain

Arseny Finkelstein, Dori Derdikman, Alon Rubin, Jakob N. Foerster, Liora Las, Nachum Ulanovsky

Research output: Contribution to journalArticlepeer-review

Abstract

Navigation requires a sense of direction (‘compass’), which in mammals is thought to be provided by head-direction cells, neurons that discharge when the animal’s head points to a specific azimuth. However, it remains unclear whether a three-dimensional (3D) compass exists in the brain. Here we conducted neural recordings in bats, mammals well-adapted to 3D spatial behaviours, and found head-direction cells tuned to azimuth, pitch or roll, or to conjunctive combinations of 3D angles, in both crawling and flying bats. Head-direction cells were organized along a functional–anatomical gradient in the presubiculum, transitioning from 2D to 3D representations. In inverted bats, the azimuth-tuning of neurons shifted by 180°, suggesting that 3D head direction is represented in azimuth × pitch toroidal coordinates. Consistent with our toroidal model, pitch-cell tuning was unimodal, circular, and continuous within the available 360° of pitch. Taken together, these results demonstrate a 3D head-direction mechanism in mammals, which could support navigation in 3D space.

Original languageEnglish
Pages (from-to)159-164
Number of pages6
JournalNature
Volume517
Issue number7533
DOIs
StatePublished - 3 Dec 2014
Externally publishedYes

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