Three-dimensional head-direction coding in the bat brain

Nature. 2015 Jan 8;517(7533):159-64. doi: 10.1038/nature14031. Epub 2014 Dec 3.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Brain / anatomy & histology
  • Brain / cytology*
  • Brain / physiology*
  • Chiroptera / anatomy & histology
  • Chiroptera / physiology*
  • Flight, Animal / physiology
  • Head / physiology*
  • Male
  • Models, Neurological*
  • Orientation / physiology
  • Posture / physiology
  • Rotation*
  • Space Perception / physiology*
  • Spatial Memory / physiology