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

Heyers, Dominik; Zapka, Manuela; Hoffmeister, Mara; Wild, J. Martin; Mouritsen, Henrik

doi:10.1073/pnas.0907068107

Cited by 117 publications

(139 citation statements)

References 41 publications

(71 reference statements)

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“…In addition, do they necessarily have to be magnetite based? Regions innervated by the ophthalmic branch of the trigeminal nerve, along with the vestibular system remain the most promising anatomical locations for the magnetosensors (16,33). Although a trigeminal-based magnetoreceptor need not necessarily be iron dependent, the vestibular recordings performed by Dickman and colleague (17) in the absence of light provide the best evidence for a magnetite-based magnetoreceptor in the pigeon inner ear.…”

Section: Discussionmentioning

confidence: 87%

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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Section: Discussionmentioning

confidence: 87%

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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“…There is evidence that this light-based magnetic system is at least to some extent a part of the imageforming visual pathway [48]. In addition, the ophthalmic branch of the trigeminal nerve is activated by a changing magnetic-field stimulus and relays this information to the bird brainstem [49]. It is likely that also pigeons sense the magnetic field in terms of a magnetic compass and/or local magnetic deviations [25,50,51].…”

Section: Mri Of Awake Pigeonsmentioning

confidence: 99%

Functional MRI and functional connectivity of the visual system of awake pigeons

Groof

Jonckers

Güntürkün

et al. 2013

Behavioural Brain Research

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h i g h l i g h t sFirst study to image the whole brain of awake pigeons. We show a habituation program for MR-sessions under awake and head-fixed conditions. Movement under these conditions is minimal. First measurement of functional connectivity in a non-mammalian species. Analyses of BOLD-response and functional connectivity are feasible. a r t i c l e i n f o b s t r a c tAt present, functional MRI (fMRI) is increasingly used in animal research but the disadvantage is that the majority of the imaging is applied in anaesthetized animals. Only a few articles present results obtained in awake rodents. In this study both traditional fMRI and resting state (rsfMRI) were applied to four pigeons, that were trained to remain still while being imaged, removing the need for anesthesia. This is the first time functional connectivity measurements are performed in a non-mammalian species. Since the visual system of pigeons is a well-known model for brain asymmetry, the focus of the study was on the neural substrate of the visual system. For fMRI a visual stimulus was used and functional connectivity measurements were done with the entopallium (E; analog for the primary visual cortex) as a seed region. Interestingly in awake pigeons the left E was significantly functionally connected to the right E. Moreover we compared connectivity maps for a seed region in both hemispheres resulting in a stronger bilateral connectivity starting from left E then from right E. These results could be used as a starting point for further imaging studies in awake birds and also provide a new window into the analysis of hemispheric dominance in the pigeon.

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“…The spectral purity of the radiofrequency field and its spatial homogeneity in the test sites were controlled with a passive H-field probe (6 cm diameter, Rhode & Schwarz, probe set HZ-11), connected to a spectrum analyser with 1 Hz resolution (HP 89410A). -To temporarily deactivate a putative magnetite-based magnetoreception pathway associated with the ophthalmic branch of the trigeminal nerve [14][15][16] (for review, see [17]), the upper beak of the birds was locally anaesthetized with Xylocaine 2 per cent (Astra Zeneca GmbH, Wedel, Germany; active substance: lydocainhydrochlorid 1 H 2 O). The anaesthetic was applied externally by gently rubbing a soaked cotton plug along the edges of the upper beak about 5 min before tests began, a procedure that had been shown to disrupt responses that do not originate from the radical pair processes in the eye; yet it does not affect normal compass orientation (see earlier studies [18,19] for details).…”

Section: (B) Test Conditionsmentioning

confidence: 99%

Avian magnetic compass can be tuned to anomalously low magnetic intensities

Winklhofer

Dylda²,

Thalau³

et al. 2013

Proc. R. Soc. B.

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The avian magnetic compass works in a fairly narrow functional window around the intensity of the local geomagnetic field, but adjusts to intensities outside this range when birds experience these new intensities for a certain time. In the past, the geomagnetic field has often been much weaker than at present. To find out whether birds can obtain directional information from a weak magnetic field, we studied spontaneous orientation preferences of migratory robins in a 4 mT field (i.e. a field of less than 10 per cent of the local intensity of 47 mT). Birds can adjust to this low intensity: they turned out to be disoriented under 4 mT after a pre-exposure time of 8 h to 4 mT, but were able to orient in this field after a total exposure time of 17 h. This demonstrates a considerable plasticity of the avian magnetic compass. Orientation in the 4 mT field was not affected by local anaesthesia of the upper beak, but was disrupted by a radiofrequency magnetic field of 1.315 MHz, 480 nT, suggesting that a radical-pair mechanism still provides the directional information in the low magnetic field. This is in agreement with the idea that the avian magnetic compass may have developed already in the Mesozoic in the common ancestor of modern birds.

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

Cited by 117 publications

References 41 publications

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

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

Functional MRI and functional connectivity of the visual system of awake pigeons

Avian magnetic compass can be tuned to anomalously low magnetic intensities

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