Trigeminally innervated iron-containing structures in the beak of homing pigeons, and other birds

Williams, M.N.; Wild, J. Martin

doi:10.1016/s0006-8993(00)03114-0

Cited by 69 publications

(69 citation statements)

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“…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.…”

Section: Discussionsupporting

confidence: 70%

“…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).…”

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confidence: 99%

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

Heyers

Zapka

Hoffmeister

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

117

124

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The upper beak of birds, which contains putative magnetosensory ferro-magnetic structures, is innervated by the ophthalmic branch of the trigeminal nerve (V1). However, because of the absence of replicable neurobiological evidence, a general acceptance of the involvement of the trigeminal nerve in magnetoreception is lacking in birds. Using an antibody to ZENK protein to indicate neuronal activation, we here document reliable magnetic activation of neurons in and near the principal (PrV) and spinal tract (SpV) nuclei of the trigeminal brainstem complex, which represent the two brain regions known to receive primary input from the trigeminal nerve. Significantly more neurons were activated in PrV and in medial SpV when European robins (Erithacus rubecula) experienced a magnetic field changing every 30 seconds for a period of 3 h (CMF) than when robins experienced a compensated, zero magnetic field condition (ZMF). No such differences in numbers of activated neurons were found in comparison structures. Under CMF conditions, sectioning of V1 significantly reduced the number of activated neurons in and near PrV and medial SpV, but not in lateral SpV or in the optic tectum. Tract tracing of V1 showed spatial proximity and regional overlap of V1 nerve endings and ZENK-positive (activated) neurons in SpV, and partly in PrV, under CMF conditions. Together, these results suggest that magnetic field changes activate neurons in and near the trigeminal brainstem complex and that V1 is necessary for this activation. We therefore suggest that V1 transmits magnetic information to the brain in this migratory passerine bird.bird migration | magnetic sense | magnetite | magnetoperception | magnetoreception

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Section: Discussionsupporting

confidence: 70%

mentioning

confidence: 99%

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

Heyers

Zapka

Hoffmeister

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

117

124

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“…Both types of magnetite particles have been described in birds, with single domains suggested to be present in the ethmoid region and the nasal cavity (e.g. Beason & Nichols 1984;Williams & Wild 2001) and superparamagnetic particles reported in distinct structures in the skin of the upper beak (Hanzlik et al 2000;Winklhofer et al 2001;Fleissner et al 2003Fleissner et al , 2007Tian et al 2007). Behavioural responses of birds to a strong, brief magnetic pulse, designed to alter the magnetization of magnetite, support the involvement of magnetite-based receptors in magnetoreception (e.g.…”

Section: Introductionmentioning

confidence: 98%

Directional orientation of birds by the magnetic field under different light conditions

Wiltschko

Stapput

Thalau

et al. 2009

J. R. Soc. Interface.

158

205

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This paper reviews the directional orientation of birds with the help of the geomagnetic field under various light conditions. Two fundamentally different types of response can be distinguished. (i) Compass orientation controlled by the inclination compass that allows birds to locate courses of different origin. This is restricted to a narrow functional window around the total intensity of the local geomagnetic field and requires light from the short-wavelength part of the spectrum. The compass is based on radical-pair processes in the right eye; magnetite-based receptors in the beak are not involved. Compass orientation is observed under 'white' and low-level monochromatic light from ultraviolet (UV) to about 565 nm green light. (ii) 'Fixed direction' responses occur under artificial light conditions such as more intense monochromatic light, when 590 nm yellow light is added to short-wavelength light, and in total darkness. The manifestation of these responses depends on the ambient light regime and is 'fixed' in the sense of not showing the normal change between spring and autumn; their biological significance is unclear. In contrast to compass orientation, fixed-direction responses are polar magnetic responses and occur within a wide range of magnetic intensities. They are disrupted by local anaesthesia of the upper beak, which indicates that the respective magnetic information is mediated by iron-based receptors located there. The influence of light conditions on the two types of response suggests complex interactions between magnetoreceptors in the right eye, those in the upper beak and the visual system.

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“…Several groups have attempted to identify the primary sensory cells associated with an iron oxide-based magnetoreceptor (19)(20)(21)(22)(23)(24). Most have used the Prussian Blue reaction which labels ferric iron.…”

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confidence: 99%

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

Edelman

Fritz

Nimpf

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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The cellular basis of the magnetic sense remains an unsolved scientific mystery. One theory that aims to explain how animals detect the magnetic field is the magnetite hypothesis. It argues that intracellular crystals of the iron oxide magnetite (Fe3O4) are coupled to mechanosensitive channels that elicit neuronal activity in specialized sensory cells. Attempts to find these primary sensors have largely relied on the Prussian Blue stain that labels cells rich in ferric iron. 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. We report the identification of a small number of cells (1 in 476,000) with large magnetic moments (8–106 fAm2) from various tissues. The development of single-cell correlative light and electron microscopy (CLEM) coupled with electron energy loss spectroscopy (EELS) and energy-filtered transmission electron microscopy (EFTEM) permitted subcellular analysis of magnetic cells. This revealed the presence of extracellular structures composed of iron, titanium, and chromium accounting for the magnetic properties of these cells. Application of single-cell CLEM to magnetic cells from the trout failed to identify any intracellular structures consistent with biogenically derived magnetite. Our work illustrates the need for new methods to test the magnetite hypothesis of magnetosensation.

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Trigeminally innervated iron-containing structures in the beak of homing pigeons, and other birds

Cited by 69 publications

References 18 publications

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

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

Directional orientation of birds by the magnetic field under different light conditions

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

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