Looking inside a pigeon’s ear using quantum technology

Quantum microscopy is able to image tiny biological magnetic structures inside a pigeon’s ear and may help to explain how animals use magnetic fields to navigate

By Robert Walter De Gille and Dr David Simpson, University of Melbourne

Migratory birds have an uncanny ability to navigate vast distances using the geomagnetic field lines from the Earth. Pigeons are a fantastic example of this with the homing pigeon able to navigate over hundreds of kilometres using its magnetic sense.

These animals were used for communication over 2000 years ago – Julius Caesar sent news of his conquest of Gaul back to Rome by carrier pigeon. Pigeons were also critical for messaging in the two World Wars and were studied as possible guidance systems for missiles in World War II under a code name Project Pigeon.

Migratory birds have an uncanny ability to navigate vast distances using the geomagnetic field lines from the Earth. Picture: Getty Images

The magnetic sense was revealed by Wolfgang Wiltschko and Friedrich Merkel in the 1960s who tracked pigeons within circular flight simulators at a time close to the beginning of their normal migration.

The direction of the magnetic field was then artificially adjusted, and the flight was again tracked. The results showed a statistically significant association between the direction of the pigeon’s flight and the direction of the magnetic field within the chamber

Although we know that pigeons and other animals have indeed developed this incredible magnetic sense, we are yet to uncover the actual biophysical mechanisms that give rise to magnetoreception.

One model is that some organisms contain magnetic particles.

Magnetotactic bacteria, for instance, navigate by synthesising chains of magnetite or maghemite nanocrystals, allowing them to align themselves along the Earth’s magnetic field lines.

Magnetic materials have also been observed in a range of animals beyond magnetotactic bacteria. Notable examples include the human brain, the head, abdomen, and wing of certain species of a bumblebee, and the head, thorax, and abdomen of certain species of termites.

Entrance of a dovecote for carrier pigeons in Paris, France used during the Siege of Paris in 1870-1871 during the Franco-Prussian War. Picture: vintage etching circa mid 19th century/ Getty Images

Professor David Keays and his team at the Institute of Molecular Pathology in Vienna have been looking carefully within the inner ears of a range of animals where sensory systems are known to be well developed.

Professor Keays’ team has discovered single isolated iron-based structures in a variety of avian species, including the common homing pigeon.

These intriguing structures called cuticulosomes are of particular interest due to their location within the inner ear, however, determining whether cuticulosomes possess sufficient magnetisation to respond to the Earth’s magnetic field presents a significant technological challenge.

For a start, the cuticulosomes are small – at 300-600 nanometres, they are less than 1 per cent of the thickness of a polymer banknote. Also, the magnetic fields they produce are weak and cuticulosomes they only sparsely populated within the layer of inner ear hair cells.

This got our research team thinking, could an emerging technology known as quantum magnetic microscopy help shed light on this century-old problem?

Quantum magnetic microscopy is a relatively new imaging technique that uses a thin sheet of synthetic diamond crystal about four millimetres square to image weak magnetic fields with extremely high resolution.

For their experiments, the researchers mounted a sample containing pigeon inner ear hair cells to a diamond magnetic imaging device. The diamond contains a quantum sensor, known as the nitrogen vacancy center, which fluoresces red when illuminated with a green laser with a fluorescence intensity that depends on the magnetic environment. Picture: Supplied

To create the magnetic sensors in diamond, two carbon atoms are removed from the crystal structure and replaced with a single nitrogen atom and an atomic void, or vacancy, where the other carbon atom should be.

The combination of the nitrogen atom, the vacancy and an additional electron creates the so-called Nitrogen Vacancy (NV) defect, which acts as the magnetic sensor.

When green light from an optical microscope is shone onto the diamond surface, the NV defects fluoresce, the strength of which is dependent on the local magnetic field. The NV defects are incredibly sensitive and can detect magnetic fields one million times weaker than your standard fridge magnet.

Using this technology our group teamed up with Professor Keays’s group in Vienna to explore whether quantum magnetic microscopy can be applied to study the magnetic properties of iron cuticulosomes found within the inner ear of pigeons and results have recently been published in Proceedings of the National Academy of Sciences.

Detailed studies were carried out in two distinct regions of the pigeon inner ear. The sensitivity of our quantum magnetic microscope allowed us to detect the magnetic field from single iron cuticulosomes, and correlate their position within the anatomy of the pigeon’s ear.

Optical image of a thin section of the pigeon inner ear with the hair cells stained with Prussian blue dye. The blue regions identify iron rich regions, with a single magnetic iron cuticulosome highlighted. Picture: Supplied

By taking stray magnetic images from single iron cuticulosomes produced under a range of applied magnetic field strengths we were able to estimate the magnetic susceptibility from each iron cuticulosome by comparing the images obtained to a detailed analytical model.

The results suggest that the magnetic susceptibility of cuticulosomes is five orders of magnitude too small to act as particle-based magnetoreceptors, leaving iron storage and stabilisation of stereocilia (structures required for hearing and balance) as possible functions for cuticulosomes.

Although the true mechanism to describe magnetoreception in pigeons remains unresolved for now, the findings of this study are of great value to biologists wishing to explain the physiological functions of cuticulosomes. They are also valuable to neurobiologists trying to explain the perplexing problem of magnetoreception, and to physicists developing new applications for quantum magnetic microscopy.

These findings narrow the plausible physiological functions that could be performed by cuticulosomes and provide a clear demonstration of the utility of quantum magnetic imaging and its role in unravelling the decades-old problem in magnetoreception.

A logical next step for our research is to image samples taken from a range of different species with a known magnetic sense.

The techniques demonstrated in this study may elucidate the magnetic properties of many other iron-based particles found within other animals like bumblebees. Picture: Getty Images

Some rodents for example are known to use the Earth’s magnetic field to navigate given they spend the majority of their time underground in the dark.

The techniques demonstrated here may elucidate the magnetic properties of many other iron-based particles found within the anatomy of animals, provide clues to their physiological roles and critically determine whether their properties are consistent with the requirements of particle-based magnetoreceptors.

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