Quantum magnetic imaging of iron organelles within the pigeon cochlea

Abstract

The ability of pigeons to sense geomagnetic fields has been conclusively established despite a notable lack of determination of the underlying biophysical mechanisms. Quasi-spherical iron organelles previously termed “cuticulosomes” in the cochlea of pigeons have potential relevance to magnetoreception due to their location and iron composition; however, data regarding the magnetic susceptibility of these structures are currently limited. Here quantum magnetic imaging techniques are applied to characterize the magnetic properties of individual iron cuticulosomes in situ. The stray magnetic fields emanating from cuticulosomes are mapped and compared to a detailed analytical model to provide an estimate of the magnetic susceptibility of the individual particles. The images reveal the presence of superparamagnetic and ferrimagnetic domains within individual cuticulosomes and magnetic susceptibilities within the range 0.029 to 0.22. These results provide insights into the elusive physiological roles of cuticulosomes. The susceptibilities measured are not consistent with a torque-based model of magnetoreception, placing iron storage and stereocilia stabilization as the two leading putative cuticulosome functions. This work establishes quantum magnetic imaging as an important tool to complement the existing array of techniques used to screen for potential magnetic particle–based magnetoreceptor candidates.

Prussian blue technique is prone to yield false negative results in magnetoreception research

“…Here it was most likely the advancing lysosomal degradation of the magnetosome membranes which was conducive to the PB staining method. A lipase/protease pretreatment mimicking lysosomal processes may be necessary for detecting membrane-enclosed magnetite crystals with the PB technique, but given the likely side effects on the tissue (disintegration, denaturation), we instead suggest to use an altogether different combination of screening techniques that do not require acid dissolution and instead are sensitive to distinct properties of magnetite crystals, such as confocal reflectance combined with Raman-spectroscopy 80 and nitrogen-vacancy based magnetometry, which has recently been applied to measuring in situ magnetic properties of cuticulosomes 39 . Once candidate structures are detected, contamination has to be ruled out beyond doubt to establish a bona fide anatomical structure for the study of magnetic-particle based magnetoreception.…”

“…Although the PB method detects ultrafine iron oxide nanoparticles (< 10 nm) in tissue when present as dense accumulations measuring several hundreds of nm in diameter 31 , 36 , such nanoparticulate structures are far from representing an optimized solution for realizing a sensor that should be capable of detecting the small magnetic field differences which were implied from the magnetic map experiments mentioned above. For instance, cuticulosomes, which are iron-rich vesicles found in the cuticular plate of hair cells in the Avian inner ear 36 – 38 , are so weakly magnetic that they would not even qualify for a compass sense to begin with 39 . In contrast, magnetite crystals with particle-sizes between 40 and 100 nm have superior magnetic properties, forming single-domain magnets, which makes them much more suitable as magnetic field sensitive structures 40 , as can be best seen in the example of magnetotactic bacteria (Fig.…”

Prussian Blue Technique is Prone To Yield False Negative Results In Magnetoreception Research

“…Although the PB method detects ultra ne iron oxide nanoparticles (< 10 nm) in tissue when present as dense accumulations measuring several hundreds of microns in diameter (Hanzlik et al, 2000;Nimpf et al, 2017), such nanoparticulate structures are far from representing an optimized solution for realizing a sensor that should be capable of detecting the small magnetic eld differences which were implied from the magnetic map experiments mentioned above. For instance, cuticulosomes, which are iron-rich vesicles found in the cuticular plate of hair cells in the Avian inner ear (Lauwers et al, 2013;Nimpf et al, 2017;Malkemper et al 2019), are so weakly magnetic that they would not even qualify for a compass sense to begin with (de Gille et al, 2021). In contrast, magnetite crystals with particle-sizes between 40 and 100 nm have superior magnetic properties, forming single-domain magnets, which makes them much more suitable as magnetic eld sensitive structures (Kirschink et al, 2010), as can be best seen in the example of magnetotactic bacteria (Fig.…”

“…Here it was most likely the advancing lysosomal degradation of the magnetosome membranes which was conducive to the PB staining method. A lipase/protease pretreatment mimicking lysosomal processes may be necessary for detecting membrane-enclosed magnetite crystals with the PB technique, but given the likely side effects on the tissue (disintegration, denaturation), we instead suggest to use an altogether different combination of techniques that do not require acid dissolution and instead are sensitive to distinct properties of magnetite crystals, such as confocal re ectance combined with Ramanspectroscopy(Eder et al, 2014) and nitrogen-vacancy based magnetometry, which has recently been applied to measuring in situ magnetic properties of cuticulosomes (deGille et al, 2021). Ironically, the Prussian Blue technique may be most useful in magnetoreception research for assessing the level of background contamination with iron-rich ne dust.…”

DC Quantum Magnetometry Below the Ramsey Limit

“…Magnetometers based on the nitrogen-vacancy (NV) center in diamond [1,2] provide µT -nT sensitivity for single centers at ambient temperature and mm-to-subµm length scales, making them attractive resources for studying biomagnetism [3], solid state systems [4,5] and nanoscale NMR [6] in challenging real-world sensing environments [7]. Since many magnetic phenomena of importance in navigation and biomagnetism manifest as slowly varying or static magnetic fields, intense effort has been devoted in particular to improving dc sensitivity [8], focusing on the diamond material [9,10], photon collection efficiency [11], quantum control sequences to eliminate decoherence [12][13][14] and more recently, the addition of ferrite flux-concentrators [15,16].…”