Israeli researchers have identified three-dimensional ‘compass’ cells in the bat brain, explaining how the winged mammals can navigate their environments so deftly and perform complex flight manoeuvres without getting disoriented.

All mammals – including, probably, humans - have a global positioning system in their brains, which consists of at least three different cellular components. John O’Keefe, a neuroscientist at University College London, discovered the first component of the brain’s GPS in 1971. While recording nerve cell activity in the hippocampus of freely moving rats, he found neurons that fire only when the animals are in a specific area of their enclosure, and speculated that these ‘place’ cells play an important role in creating mental maps of the environment.

The second component was identified in the mid-1980s, as a system of ‘head direction’ cells, also in the rat hippocampus. These act as the brain’s internal compass, each of them firing when the animal is facing a specific direction in the horizontal plane, or azimuth. May-Britt and Edvard Moser of the Norwegian University of Science and Technology in Trondheim discovered the third component in 2005 – the ‘grid’ cells, which fire periodically as the animal traverses a space, generating a co-ordinate system of its surroundings.

Three years later, the Mosers identified a fourth component - border cells, which encode the rat’s distance from the boundaries of its environment - and, meanwhile, explored how these separate parts work together.

This work revealed a great deal about how cells in the hippocampus enable organisms to map, memorise and navigate their surroundings, and O’Keefe and the Mosers shared this year’s Nobel Prize in Physiology for their discoveries. But since most spatial navigation research is done on rats running around on flat surfaces, we still know very little about how the brain encodes 3D representations of space.

To investigate, Arseny Finkelstein and his colleagues at the Weismann Institute of Science in Israel recorded neuronal activity in the brains of crawling and free-flying Egyptian fruit bats. Using wireless microelectrodes implanted into a region of the hippocampus called the presubiculum, they recorded from a total of about 550 cells in six bats, while also recording the animals’ head movements with high-speed video cameras and a custom-built LED-based tracking device.

About half the cells they examined exhibited the properties of head direction cells. When the bats crawled across the floor, each fired only when they were moving in a specific direction along the azimuth. When they climbed a wall, the same cells re-calibrated themselves using the vertical surface for reference, and again fired only when they moved in specific directions within that plane.

The recordings taken during flight confirmed that the bat’s neural compass encodes space in three dimensions. About one fifth of the cells were tuned to specific ranges of pitch, firing only when the bats flew at a certain angle in the vertical plane, and about one tenth to roll angles. A significant proportion of the cells were sensitive to a combination of angles in the horizontal and vertical planes, and some to angles in all three planes.

At rest, bats suspend themselves head downward but, unlike some bird species, are incapable of flying upside down. Both take-off and landing therefore involve aerial rotations that invert the entire body, so that the bat ends up facing the direction opposite to that in which it started. The movements required for these acrobatic flight manoeuvres occur mostly in the horizontal and vertical planes, with very little rolling taking place.



Facebook Twitter Pinterest High-speed video footage shows Egyptian fruit bats executing 180° pitch manoeuvres during take-off and landing. From Finkelstein, et al. (2014).

To understand how the compass might behave during such manoeuvres, the researchers carried out another set of experiments, in which they recorded neuronal activity while the bats crawled through a vertical ring, and while they were held upside down and moved. This showed that azimuth cells invert their tuning by 180° with the bats, encoding first one direction when the animals were upright, and then the opposite one when they were upside-down. The experiments also showed that the pitch neurons cover the entire 360° range of the vertical plane.



Thus, the same azimuth cells remain active throughout the entire take-off and landing manoeuvres, so that the compass maintains a steady representation of the bat’s direction, while different sets of pitch cells fire in sequence during the aerial rotation to encode body orientation. The information from both cell types thus gives the bat its precise orientation in three dimensions, as well as whether it is upright, upside-down, or somewhere in between.

The recordings also showed that the cells seem to be arranged according to their function, with ‘pure’ azimuth cells, tuned to a specific range along just the horizontal axis, being most abundant at the outer region at the front of the presubiculum and decreasing with distance further back and inwards. Pure pitch and roll neurons, and cells responding to combinations of positions in two or three axes, had the opposite arrangement.

This suggests that two-dimensional, grid-like spatial representations are encoded at the one end of the presubiculum, and three-dimensional representations at the other. On the basis of their recordings, Finkelstein and his colleagues believe that the bat brain represents 3D space with a torroidal (or doughnut-shaped) system of co-ordinates, rather than a spherical one.

(Imagine a spherical representation of space, with the bat at its centre. The bat’s movements could be described as a line from the centre to any point on the surface, with three co-ordinates, but one of these would need a landmark as a reference, so the spatial representations would change as the bat moves. In a torroidal system, direction can be described as a point around the doughnut, and pitch by a smaller intersecting ring around any of one of those points. A torroidal system therefore provides 360° x 360° coverage in both the horizontal and vertical planes, and also allows for stable representations because it is independent of landmarks.)

“These are exciting results,” says Hugo Spiers, a spatial navigation researcher at UCL. “They’ve not only uncovered the existence of the 3D compass in mammals, but they’ve also characterised how it operates.” Finkelstein and his colleagues suspect that the neural compasses of other mammals, including cats, dogs, dolphins, and primates, likely operate in a similar way. The human brain, too, probably encodes 3D representations of space, but, says Spiers, “I’d imagine our 3D compass would never quite match that of a bat.”

In 2011, Finkelstein’s colleagues identified 3D place cells in the bat hippocampus, and showed that they have nearly spherical receptive fields. But they also noticed that the cells work differently from their rodent counterparts. In rats, populations of place and grid cells fire in synchrony to produce a brainwave pattern called the theta rhythm, which is thought to be crucial for the encoding and retrieval of spatial memories. Bats’ place cells do not exhibit this pattern, however. “The sensory organs of rats are strongly entrained to theta rhythms, but those of bats are not,” says Finkelstein. “It’s possible that we don’t see theta rhythms in bats because of differences in the way they use their senses to navigate.”

The researchers are now investigating how information from the compass is integrated into the brain’s mental maps. “These systems sometimes fail, such as when we leave a subway station and temporarily loose our sense of direction,” says Finkelstein. “We feel disoriented until our mental map suddenly realigns. We think this is caused by the head direction system updating the map, and think it is important to understand exactly how it happens.”

Finkelstein says that learning more about the neural compass could help pilots deal with aviator’s vertigo, a form of spatial disorientation that occurs as a result of excessive head movements. This can leave the pilot unable to tell up from down, or left from right, and can therefore have fatal consequences - according to Federal Aviation Administration statistics, it is at least partly responsible for about 15% of all general aircraft accidents. “Understanding the basic properties of the compass, and what happens when it malfunctions, could potentially lead to new methods for preventing these accidents.”

Reference: Finkelstein, A., et al. (2014). Three-dimensional head-direction coding in the bat brain. Nature, DOI: 10.1038/nature14031.