A novel concept of Fe-mineral-based magnetoreception: histological and physicochemical data from the upper beak of homing pigeons

Abstract

Animals make use of the Earth's magnetic field for navigation and regulation of vegetative functions; however, the anatomical and physiological basis for the magnetic sense has not been elucidated yet. Our recent results from histology and X-ray analyses support the hypothesis that delicate iron-containing structures in the skin of the upper beak of homing pigeons might serve as a biological magnetometer. Histology has revealed various iron sites within dendrites of the trigeminal nerve, their arrangement along strands of axons, the existence of three dendritic fields in each side of the beak with specific 3D-orientations, and the bilateral symmetry of the whole system. Element mapping by micro-synchrotron X-ray fluorescence analysis has shown the distribution of iron and its quantities. Micro-synchrotron X-ray absorption near-edge-structure spectroscopy has allowed us to unambiguously identify maghemite as the predominating iron mineral (90 vs 10% magnetite). In this paper, we show that iron-based magnetoreception needs the presence of both of these iron minerals, their specific dimensions, shapes, and arrangements in three different subcellular compartments. We suggest that an inherent magnetic enhancement process via an iron-crusted vesicle and the attached chains of iron platelets might be sufficient to account for the sensitivity and specificity required by such a magnetoreceptor. The appropriate alignment between the Earth's magnetic field and the maghemite bands would induce a multiple attraction of the magnetite bullets perpendicular to the membrane, thus, triggering strain-sensitive membrane channels and a primary receptor potential. Due to its 3D architecture and physicochemical nature, the dendritic system should be able to separately sense the three vector components of the Earth's local field, simultaneously-allowing birds to detect their geographic position by the magnetic vector, i.e., amplitude and direction of the local magnetic field, irrespective of the animal's posture or movement and photoreception.

Magnetic field changes activate the trigeminal brainstem complex in a migratory bird

“…Therefore, our findings suggest that the ophthalmic branch of the trigeminal nerve (V1) is the only trigeminal branch to mediate the effects of the magnetic stimuli that were observed in PrV and SpV and that the "extra" labeling outside the primary V1 terminal zone probably represents magnetic activation via a multisynaptic mechanism. These results are entirely consistent with previous anatomical studies, which have shown that the ophthalmic branch of the trigeminal nerve (V1) is the only branch to innervate candidate ferromagnetic structures in the upper beak (8,13). It is almost certain that magnetic information is transmitted to higher brain centers.…”

“…More direct methods, such as electrophysiological recordings from trigeminal neurons in response to magnetic stimulation, would be required to prove this; however, as pointed out earlier here, such methods are very prone to the production of artifactual results (22-24); hence, the necessity for the present, strongly indicative study using more indirect methods. The data also suggest that the ophthalmic branch of the trigeminal nerve (V1) in European robins innervates a primary magnetic sensor in the upper beak and support the idea that iron-mineral-based structures found in the upper beak of birds (8,12,13) including European robins (15), can sense information from the ambient geomagnetic field.…”

“…In recent years, mounting behavioral and anatomical evidence has been accumulating that birds, at least, might have two independent magnetic senses: (i) iron-mineral-based sensors located in the upper beak, which are innervated by the ophthalmic branch of the trigeminal nerve (V1) (8,9,(11)(12)(13)(14)(15)(16), and (ii) a light-dependent chemical sense which is embedded in parts of the visual system (7,9,(16)(17)(18)(19)(20)(21). However, considerable scientific skepticism remains regarding both of these proposed magnetic senses because, so far, in birds, the studies that have reported changes in neurophysiological activity in response to magnetic field changes differ in their conclusions, could not be independently confirmed, and are likely to have been subject to artifactual difficulties (22)(23)(24).…”

Extremely low-frequency electromagnetic fields disrupt magnetic alignment of ruminants

“…We can only speculate about the physiological mechanisms of the magnetic alignment of ruminants. Of the numerous mechanisms proposed for the direct interaction of electromagnetic fields with the human or animal body, 3 stand out as operating potentially (also) at lower field levels: magnetically sensitive radical pair reactions (19), electric field ion cyclotron resonance interactions (20), and mechanisms based on biogenic magnetite (21)(22)(23)(24). Theoretically, each of these mechanisms (separately or in combination) could be responsible for magnetic alignment.…”

Chemical magnetoreception in birds: The radical pair mechanism

“…Throughout, the focus is firmly on the primary reception mechanism: We make no significant attempt to review the behavioral studies that led to and have since supported the radical pair model, or to comment on (neuro)-physiological aspects of magnetoreception, all of which have been covered authoritatively and extensively in recent reviews (3-5, 8, 24, 25). Nor do we presume here to debate the relative merits of the radical pair hypothesis versus proposals based on biogenic magnetite (Fe 3 O 4 ) (26)(27)(28)(29)(30)(31)(32). We close with a discussion of cryptochrome, the photoreceptor protein that is presently the only molecule under consideration as the magnetoreceptor (2), and make suggestions for further research.…”