Magnetic characterization of isolated candidate vertebrate magnetoreceptor cells

Abstract

Over the past 50 y, behavioral experiments have produced a large body of evidence for the existence of a magnetic sense in a wide range of animals. However, the underlying sensory physiology remains poorly understood due to the elusiveness of the magnetosensory structures. Here we present an effective method for isolating and characterizing potential magnetite-based magnetoreceptor cells. In essence, a rotating magnetic field is employed to visually identify, within a dissociated tissue preparation, cells that contain magnetic material by their rotational behavior. As a tissue of choice, we selected trout olfactory epithelium that has been previously suggested to host candidate magnetoreceptor cells. We were able to reproducibly detect magnetic cells and to determine their magnetic dipole moment. The obtained values (4 to 100 fAm 2 ) greatly exceed previous estimates (0.5 fAm 2 ). The magnetism of the cells is due to a μm-sized intracellular structure of iron-rich crystals, most likely single-domain magnetite. In confocal reflectance imaging, these produce bright reflective spots close to the cell membrane. The magnetic inclusions are found to be firmly coupled to the cell membrane, enabling a direct transduction of mechanical stress produced by magnetic torque acting on the cellular dipole in situ. Our results show that the magnetically identified cells clearly meet the physical requirements for a magnetoreceptor capable of rapidly detecting small changes in the external magnetic field. This would also explain interference of ac powerline magnetic fields with magnetoreception, as reported in cattle.animal migration | biomineralization | salmoniformes | microrheology

No evidence for intracellular magnetite in putative vertebrate magnetoreceptors identified by magnetic screening

“…5 A-C). The morphology of these cells mirrored those previously reported, each with a notable opaque structure associated with the membrane (25). Assessment of their magnetic moment revealed that they vary between 2 and 152 fAm 2 , and have a profile consistent with the presence of remanence-bearing particles ( Fig.…”

“…S3 and Table S1). These results are analogous to those obtained by Eder et al, who observed cells with moments spanning 4-100 fAm 2 , with the majority (11 of 13) between 10 and 50 fAm 2 (25). To establish whether the cells possess remanent magnetism or alternatively superparamagnetism, we determined the moment at a variety of different magnetic intensities (0.5, 1, 1.25, 1.5, 1.75, and 2 mT).…”

“…To investigate this, we lightly dissociated and fixed cells from the olfactory rosette of juvenile trout (Austrian cohort) (25). We then screened these cells using a 2-mT field rotating at 0.33 Hz [the same parameters used by Eder et al (25)]. We screened 3.6 million cells (n = 10 trout), leading to the identification of 7 spinning cells (1 in 520,000), each of which was positive for the nuclear marker Hoechst (Movies S3 and S4, and Fig.…”

“…Next, we asked whether magnetic cells in the trout have a subcellular architecture consistent with a role in magnetosensation, or alternatively if their spinning behavior might also be explained by contamination. To investigate this, we lightly dissociated and fixed cells from the olfactory rosette of juvenile trout (Austrian cohort) (25). We then screened these cells using a 2-mT field rotating at 0.33 Hz [the same parameters used by Eder et al (25)].…”

“…This method has proved problematic as it has led investigators to conflate iron-rich macrophages with magnetoreceptors. An alternative approach developed by Eder et al [Eder SH, et al (2012) Proc Natl Acad Sci USA 109(30):12022-12027] is to identify candidate magnetoreceptive cells based on their magnetic moment. Here, we explore the utility of this method by undertaking a screen for magnetic cells in the pigeon.…”