The neural substrate subserving magnetoreception and magnetic orientation in mammals is largely unknown. Previous experiments have demonstrated that the processing of magnetic sensory information takes place in the superior colliculus. Here, the effects of magnetic field conditions on neuronal activity in the rodent navigation circuit were assessed by quantifying c-Fos expression. Ansell's mole-rats (Fukomys anselli), a mammalian model to study the mechanisms of magnetic compass orientation, were subjected to natural, periodically changing, and shielded magnetic fields while exploring an unfamiliar circular arena. In the undisturbed local geomagnetic field, the exploration of the novel environment and/or nesting behaviour induced c-Fos expression throughout the head direction system and the entorhinal-hippocampal spatial representation system. This induction was significantly suppressed by exposure to periodically changing and/or shielded magnetic fields; discrete decreases in c-Fos were seen in the dorsal tegmental nucleus, the anterodorsal and the laterodorsal thalamic nuclei, the postsubiculum, the retrosplenial and entorhinal cortices, and the hippocampus. Moreover, in inactive animals, magnetic field intensity manipulation suppressed c-Fos expression in the CA1 and CA3 fields of the hippocampus and the dorsal subiculum, but induced expression in the polymorph layer of the dentate gyrus. These findings suggest that key constituents of the rodent navigation circuit contain populations of neurons responsive to magnetic stimuli. Thus, magnetic information may be integrated with multimodal sensory and motor information into a common spatial representation of allocentric space within this circuit.

Department of Zoology Faculty of Science Charles University Prague Vinicna 7 CZ 12844 Praha 2 Czech Republic

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Aggleton J. P., Pearce J. M. 2001. Neural systems underlying episodic memory: insights from animal research. Phil. Trans. R. Soc. Lond. B 356, 1467–1482. (10.1098/rstb.2001.0946) PubMed DOI PMC

Amin E., Pearce J. M., Brown M. W., Aggleton J. P. 2006. Novel temporal configurations of stimuli produce discrete changes in immediate-early gene expression in the rat hippocampus. Eur. J. Neurosci. 24, 2611–2621. (10.1111/j.1460-9568.2006.05131.x) PubMed DOI

Avni R., Tzvaigrach Y., Eilam D. 2008. Exploration and navigation in the blind mole rat (Spalax ehrenbergi): global calibration as a primer of spatial representation. J. Exp. Biol. 211, 2817–2826. (10.1242/jeb.019927) PubMed DOI

Barry C., Hayman R., Burgerss N., Jeffery K. J. 2007. Experience-dependent rescaling of entorhinal grids. Nat. Neurosci. 10, 682–684. (10.1038/nn1905) PubMed DOI

Begall S., Cerveny J., Neef J., Vojtech O., Burda H. 2008. Magnetic alignment in grazing and resting cattle and deer. Proc. Natl Acad. Sci. USA 105, 17 206 (10.1073/pnas.0809028105) PubMed DOI PMC

Benhamou S., Sauve J. P., Bovet P. 1990. Spatial memory in large-scale movements—efficiency and limitations of the egocentric coding process. J. Theor. Biol. 145, 1–12. (10.1016/S0022-5193(05)80531-4) DOI

Best P. J., White A. M., Minai A. 2001. Spatial processing in the brain: the activity of hippocampal place cells. Annu. Rev. Neurosci. 24, 459–486. (10.1146/annurev.neuro.24.1.459) PubMed DOI

Blair H. T., Sharp P. E. 2002. Functional organization of the rat head-direction circuit. In The neural basis of navigation: evidence from single cell recording (ed. Sharp P. E.), pp. 163–182. Dordrecht, The Netherlands: Kluwer Academic Publishers.

Burda H., Marhold S., Westenberger T., Wiltschko R., Wiltschko R. 1990. Magnetic compass orientation in the subterranean rodent Cryptomys hottentotus (Bathyergidae). Experientia 46, 528–530. (10.1007/BF01954256) PubMed DOI

Burda H., Beiles A., Marhold S., Simson S., Nevo E., Wiltschko W. 1991. Magnetic orientation in subterranean mole rats of the superspecies Spalax ehrenbergi: experiments, patterns and memory. Isr. J. Zool. 37, 182–183.

Burda H., Begall S., Cerveny J., Neef J., Němec P. 2009. Extremely low-frequency electromagnetic fields disrupt magnetic alignment of ruminants. Proc. Natl Acad. Sci. USA 106, 5708–5713. (10.1073/pnas.0811194106) PubMed DOI PMC

Cain S., Boles L. C., Wang J. H., Lohmann K. J. 2005. Magnetic orientation in marine turtles, lobsters, and molluscs: concepts and conundrums. Integr. Comput. Biol. 45, 539–546. (10.1093/icb/45.3.539) PubMed DOI

Colombo P. J. 2004. Learning-included activation of transcription factors among multiple memory systems. Neurobiol. Learn. Mem. 82, 268–277. (10.1016/j.nlm.2004.07.005) PubMed DOI

Colombo P. J., Brightwell J. J., Countryman R. A. 2003. Cognitive strategy-specific increases in phosphorylated cAMP response element-binding protein and c-Fos in the hippocampus and dorsal striatum. J. Neurosci. 23, 3547–3554. PubMed PMC

Dammann P., Burda H. 2006. Sexual activity and reproduction delay ageing in a mammal. Curr. Biol. 16, R117–R118. (10.1016/j.cub.2006.02.012) PubMed DOI

Davila A. F., Fleissner G., Winklhofer M., Petersen N. 2003. A new model for a magnetoreceptor in homing pigeons based on interacting clusters of superparamagnetic magnetite. Phys. Chem. Earth 28, 647–652. (10.1016/S1474-7065(03)00118-9) DOI

Deutschlander M. E., Freake M. J., Borland S. C. H., Phillips J. B., Madden R. C., Anderson L. E., Wilson B. W. 2003. Learned magnetic compass orientation by the Siberian hamster Phodopus sungorus. Anim. Behav. 65, 779–786. (10.1006/anbe.2003.2111) DOI

de Vries J. L., Oosthuizen M. K., Sichilima A. M., Bennett N. C. 2008. Circadian rhythms of locomotor activity in Ansell's mole-rat: are mole-rat's clocks ticking? J. Zool. 276, 343–349. (10.1111/j.1469-7998.2008.00496.x) DOI

Etienne A. S., Jeffery K. J. 2004. Path integration in mammals. Hippocampus 14, 180–192. (10.1002/hipo.10173) PubMed DOI

Etiene A. S., Maurer R., Saucy F. 1988. Limitations in the assessment of path dependent information. Behaviour 106, 81–111. (10.1163/156853988X00106) DOI

Ferbinteanu J., Shapiro M. L. 2003. Prospective and retrospective memory coding in the hippocampus. Neuron 40, 1227–1239. (10.1016/S0896-6273(03)00752-9) PubMed DOI

Fleischmann A., et al. 2003. Impaired long-term memory and NR2A-type NMDA receptor-dependent synaptic plasticity in mice lacking c-Fos in the CNS. J. Neurosci. 23, 9116–9122. PubMed PMC

Fleissner G., Stahl B., Thalau P., Falkenberg G., Fleissner G. 2007. A novel concept of Fe-mineral-based magnetoreception: histological and physicochemical data from the upper beak of homing pigeons. Naturwissenschaften 94, 631–642. (10.1007/s00114-007-0236-0) PubMed DOI

Freake M. J., Muheim R., Phillips J. B. 2006. Magnetic maps in animals: a theory comes of age? Q. Rev. Biol. 81, 327–347. (10.1086/511528) PubMed DOI

Frost B. J., Mouritsen H. 2006. The neural mechanisms of long distance animal navigation. Curr. Opin. Neurobiol. 16, 481–488. (10.1016/j.conb.2006.06.005) PubMed DOI

Fyhn M., Molden S., Witter M. P., Moser E. I., Moser B. 2004. Spatial representation in the enthorhinal cortex. Science 305, 1258–1264. (10.1126/science.1099901) PubMed DOI

Goodridge J. P., Dudchenko P. A., Worboys K. A., Golob E. J., Taube J. S. 1998. Cue control and head direction cells. Behav. Neurosci. 112, 749–761. (10.1037/0735-7044.112.4.749) PubMed DOI

Guzowski J. F., Setlow B., Wagner E. K., McGaugh J. L. 2001. Experience-dependent gene expression in the rat hippocampus after spatial learning: a comparison of the immediate-early genes Arc, c-Fos, and zif268. J. Neurosci. 21, 5089–5098. PubMed PMC

Hafting T., Fyhn M., Molden S., Moser M. B., Moser E. I. 2005. Microstructure of a spatial map in the entorhinal cortex. Nature 436, 801–806. (10.1038/nature03721) PubMed DOI

Handa R. J., Nunley K. M., Bollnow M. R. 1993. Induction of c-Fos messenger-RNA in the brain and anterior-pituitary gland by a novel environment. Neuroreport 4, 1079–1082. PubMed

Herdegen T., Leah J. D. 1998. Inducible and constitutive transcription factors in the mammalian nervous system: control of gene expression by Jun, Fos and Krox, and CREB/ATF proteins. Brain Res. Rev. 28, 370–490. (doi:10.1016/S0165-0173(98)00018-6). PubMed

Herdegen T., Kovary K., Buhl A., Bravo R., Zimmermann M., Gass P. 1995. Basal expression of the inducible transcription factors c-Jun, JunB, JunD, c-Fos, FosB, and Krox-24 in the adult-rat brain. J. Comp. Neurol. 354, 39–56. (10.1002/cne.903540105) PubMed DOI

Hess U. S., Lynch G., Gall C. M. 1995. Regional patterns of c-Fos mRNA expression in rat hippocampus following exploration of a novel environment versus performance of a well-learned discrimination. J. Neurosci. 15, 7796–7809. PubMed PMC

Heyers D., Manns M., Luksch H., Gunturkun O., Mouritsen H. 2007. A visual pathway links brain structures active during magnetic compass orientation in migratory birds. PLoS ONE 2, e937 (10.1371/journal.pone.0000937) PubMed DOI PMC

Holland R. A., Thorup K., Vonhof M. J., Cochran W. W., Wikelski M. 2006. Navigation—bat orientation using Earth's magnetic field. Nature 444, 702 (10.1038/444702b) PubMed DOI

Hughes P., Lawlor P., Dragunow M. 1992. Basal expression of Fos, Fos-related, Jun, and Krox 24 proteins in rat hippocampus. Mol. Brain Res. 13, 355–357. PubMed

Jeffery K. J. 2003. The neurobiology of spatial behaviour. New York, NY: Oxford University Press.

Jenkins T. A., Amin E., Pearce J. M., Brown M. W., Aggleton J. P. 2004. Novel spatial arrangements of familiar visual stimuli promote activity in the rat hippocampal formation but not the parahippocampal cortices: a c-Fos expression study. Neuroscience 124, 43–52. (10.1016/j.neuroscience.2003.11.024) PubMed DOI

Johnsen S., Lohmann K. J. 2005. The physics and neurobiology of magnetoreception. Nat. Rev. Neurosci. 6, 703–712. (10.1038/nrn1745) PubMed DOI

Johnsen S., Lohmann K. J. 2008. Magnetoreception in animals. Phys. Today 61, 29–35. (10.1063/1.2897947) DOI

Kimchi T., Terkel J. 2001. Magnetic compass orientation in the blind mole rat Spalax ehrenbergi. J. Exp. Biol. 204, 751–758. PubMed

Kimchi T., Terkel J. 2004. Comparison of the role of somatosensory stimuli in maze learning in a blind subterranean rodent and a sighted surface-dwelling rodent. Behav. Brain Res. 153, 389–395. (10.1016/j.bbr.2003.12.015) PubMed DOI

Kimchi T., Etienne A. S., Terkel J. 2004. A subterranean mammal uses the magnetic compass for path integration. Proc. Natl Acad. Sci. USA 101, 1105–1109. (10.1073/pnas.0307560100) PubMed DOI PMC

Knierim J. J. 2002. The path-integration properties of hippocampal place cells. In The neural basis of navigation: evidence from single cell recording (ed. Sharp P. E.), pp. 41–58. Dordrecht, The Netherlands: Kluwer Academic Publishers.

Kristofikova Z., Cermak M., Benesova O., Klaschka J., Zach P. 2005. Exposure of postnatal rats to a static magnetic field of 0.14 T influences functional laterality of the hippocampal high-affinity choline uptake system in adulthood; in vitro test with magnetic nanoparticles. Neurochem. Res. 30, 253–262. (10.1007/s11064-005-2448-z) PubMed DOI

Kubik S., Miyashita T., Guzowski J. F. 2007. Using immediate-early genes to map hippocampal subregional functions. Learn. Mem. 14, 758–770. (10.1101/lm.698107) PubMed DOI

Lai H. 1996. Spatial learning deficit in the rat after exposure to a 60 Hz magnetic field. Bioelectromagnetics 17, 494–496. (10.1002/(SICI)1521-186X(1996)17:6%3C494::AID-BEM9%3E3.0.CO;2-Z) PubMed DOI

Lai H., Carino M. 1999. 60 Hz magnetic fields and central cholinergic activity: effects of exposure intensity and duration. Bioelectromagnetics 20, 284–289. (10.1002/(SICI)1521-186X(1999)20:5<284::AID-BEM4>3.0.CO;2-Z) PubMed DOI

Lai H., Carino M., Horita A., Guy A. W. 1993. Effects of a 60 Hz magnetic field on central cholinergic systems of the rat. Bioelectromagnetics 14, 5–15. (10.1002/bem.2250140104) PubMed DOI

Leutgeb S., Leutgeb J. K., Barnes C. A., Moser E. I., McNaughton B. L., Moser M. B. 2005. Independent codes for spatial and episodic memory in hippocampal neuronal ensembles. Science 309, 619–623. (10.1126/science.1114037) PubMed DOI

Liedvogel M., Maeda K., Henbest K., Schleicher E., Simon T., Timmel C. R., Hore P. J., Mouritsen H. 2007. Chemical magnetoreception: bird cryptochrome 1a is excited by blue light and forms long-lived pair radicals. PLoS One 2, e1106 (10.1371/journal.pone.0001106) PubMed DOI PMC

Lohmann K. J., Lohmann C. M. F., Putman N. F. 2007. Magnetic maps in animals: nature’s GPS. J. Exp. Biol. 210, 3697–3705. (10.1242/jeb.001313) PubMed DOI

Maaswinkel H., Whishaw I. Q. 1999. Homing with locale, taxon, and dead reckoning strategies by foraging rats: sensory hierarchy in spatial navigation. Behav. Brain Res. 99, 143–152. (10.1016/S0166-4328(98)00100-4) PubMed DOI

Mai J. K., Semm P. 1990. Pattern of brain glucose utilization following magnetic stimulation. J. Hirnforsch. 31, 331–336. PubMed

Marhold S., Burda H., Kreilos I., Wiltschko W. 1997a. Magnetic orientation in common mole-rats from Zambia. In Orientation and navigation—birds, humans and other animals. Paper no. 5 Oxford, UK: Royal Institute of Navigation.

Marhold S., Wiltschko W., Burda H. 1997b. A magnetic polarity compass for direction finding in a subterranean mammal. Naturwissenschaften 84, 421–423. (10.1007/s001140050422) DOI

Marhold S., Beiles A., Burda H. 2000. Spontaneous directional preference in a subterranean rodent, the blind mole rat Spalax ehrenberghi. Folia Zool. 49, 7–18.

McNaughton B. L., Battaglia F. P., Jensen O., Moser E. I., Moser B. 2006. Path integration and the neural basis of the ‘cognitive map’. Nat. Rev. Neurosci. 7, 663–678. (10.1038/nrn1932) PubMed DOI

Mehlhorn J., Rehkämper G. 2009. Neurobiology of the homing pigeon—a review. Naturwissenschaften 96, 1011–1025. (10.1007/s00114-009-0560-7) PubMed DOI

Miyashita T., Kubik S., Lewandowski G., Guzowski J. F. 2008. Networks of neurons, networks of genes: an integrated view of memory consolidation. Neurobiol. Learn. Mem. 89, 269.–284 (10.1016/j.nlm.2007.08.012) PubMed DOI PMC

Mizumori S. J., Williams J. D. 1993. Directionally selective mnemonic properties of neurons in the lateral dorsal nucleus of the thalamus of rats. J. Neurosci. 13, 4015–4028. PubMed PMC

Moita M. A. P., Rosis S., Zhou Y., LeDoux J. E., Blair H. T. 2003. Hippocampal place cells acquire location-specific responses to the conditioned stimulus during auditory fear conditioning. Neuron 37, 485–497. (10.1016/S0896-6273(03)00033-3) PubMed DOI

Montero V. M. 1997. C-Fos induction in sensory pathways of rats exploring a novel complex environment: shifts of active thalamic reticular sectors by predominant sensory cues. Neuroscience 76, 1069–1081. (10.1016/S0306-4522(96)00417-4) PubMed DOI

Moritz R. E., Burda H., Begall S., Němec P. 2007. Magnetic compass: a useful tool underground. In Subterranean rodents: news from underground (eds Begall S., Burda H.), pp. 161–174. Heidelberg, Germany: Springer.

Moser E. I., Kropff E., Moser B. 2008. Place cells, grid cells, and the brain’s spatial representation system. Annu. Rev. Neurosci. 31, 69–89. (10.1146/annurev.neuro.31.061307.090723) PubMed DOI

Mouritsen H., Ritz T. 2005. Magnetoreception in bird navigation. Curr. Opin. Neurobiol. 15, 406–414. (10.1016/j.conb.2005.06.003) PubMed DOI

Mouritsen H., Feenders G., Liedvogel M., Wada K., Jarvis E. D. 2005. Night-vision brain area in migratory songbirds. Proc. Natl Acad. Sci. USA 102, 8339–8344. (10.1073/pnas.0409575102) PubMed DOI PMC

Muheim R., Edgar N. M., Sloan K. A., Phillips J. B. 2006. Magnetic compass orientation in C57BL/6J mice. Learn. Behav. 34, 366–373. PubMed

Muller R. U., Poucet B., Rivard B. 2002. Sensory determinants of hippocampal place cell firing fields. In The neural basis of navigation: evidence from single cell recording (ed. Sharp P. E.), pp. 2–22. Dordrecht, The Netherlands: Kluwer Academic Publishers.

Němec P., Altmann J., Marhold S., Burda H., Oelschläger H. H. A. 2001. Neuroanatomy of magnetoreception: the superior colliculus involved in magnetic orientation in a mammal. Science 294, 366–368. (10.1126/science.1063351) PubMed DOI

Němec P., Burda H., Peichl L. 2004. Subcortical visual system of the African mole-rat Cryptomys anselli: to see or not to see? Eur. J. Neurosci. 20, 757–768. (10.1111/j.1460-9568.2004.03510.x) PubMed DOI

Němec P., Burda H., Oelschläger H. H. A. 2005. Towards the neural basis of magnetoreception: a neuroanatomical approach. Naturwissenschaften 92, 151–157. (10.1007/s00114-005-0612-6) PubMed DOI

Němec P., Cvekova P., Burda H., Benada O., Peichl L. 2007. Visual systems and the role of vision in subterranean rodents: diversity of retinal properties and visual system designs. In Subterranean rodents—news from underground (eds Begall S., Burda H., Schleich C. E.), pp. 129–160. Heidelberg, Germany: Springer.

Němec P., Cvekova P., Benada O., Wielkopolska E., Olkowitcz S., Turlejski K., Burda H., Bennett N. C., Peichl L. 2008. The visual system in subterranean African mole-rats (Rodentia, Bathyergidae): retina, subcortical visual nuclei and primary visual cortex. Brain Res. Bull. 75, 356–364. (10.1016/j.brainresbull.2007.10.055) PubMed DOI

Oelschläger H. H. A., Nakamura M., Herzog M., Burda H. 2000. Visual system labeled by c-Fos immunohistochemistry after light exposure in the ‘blind’ subterranean Zambian mole-rat (Cryptomys anselli). Brain Behav. Evol. 55, 209–220. (10.1159/000006653) PubMed DOI

O'Keeffe J. 1976. Place units in the hippocampus of the freely moving rat. Exp. Neurol. 51, 78–109. (10.1016/0014-4886(76)90055-8) PubMed DOI

O'Keeffe J., Dostrovsky J. 1971. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 34, 171–175. PubMed

O'Keefe J., Nadel L. 1978. The hippocampus as a cognitive map. Oxford, UK: Clarendon.

Park J. T., Kenneth C. C., Samaan D., Comer C. H. 2007. Adaptive neural organization of naked mole-rat somatosensation (and those similarly challenged). In Subterranean rodents: news from underground (eds Begall S., Burda H., Schleich C. H. E.), pp. 175–193. Heidelberg, Germany: Springer.

Paxinos G., Watson C. 2005. The rat brain in stereotaxic coordinates. Amsterdam, The Netherlands: Elsevier Academic Press.

Quirk G. J., Muller R. U., Kubie J. L. 1990. The firing of hippocampal place cells in the dark reflects the rat's recent experience. J. Neurosci. 10, 2008–2017. PubMed PMC

Ranck J. B., Jr 1984. Head direction cells in the deep layer of dorsal presubiculum in freely moving rats. Soc. Neurosci. Abstr. 10, 599.

Rodgers C. H. T., Hore P. J. 2009. Chemical magnetoreception in birds: the radical pair mechanism. Proc. Natl Acad. Sci. USA 106, 353–360. (10.1073/pnas.0711968106) PubMed DOI PMC

Samu D., Eros P., Ujfalussy B., Kiss T. 2009. Robust path integration in the entorhinal grid cell system with hippocampal feed-back. Biol. Cybern. 101, 19–34. (10.1007/s00422-009-0311-z) PubMed DOI

Semm P., Demaine C. 1986. Neurophysiological properties of the magnetic cells in the pigeon’s visual system. J. Comp. Physiol. A 159, 619–625. (10.1007/BF00612035) PubMed DOI

Semm P., Nohr D., Demaine C., Wiltschko W. 1984. Neural basis of the magnetic compass: interactions of visual, magnetic and vestibular inputs in the pigeon’s brain. J. Comp. Physiol. A 155, 283–288. (10.1007/BF00610581) DOI

Sharp P. E. 2002. The neural basis of navigation: evidence from single cell recording. Dordrecht, The Netherlands: Kluwer Academic Publishers.

Sharp P. E., Blair H. T., Cho J. 2001. The anatomical and computational basis of the rat head-direction cell signal. Trends Neurosci. 24, 289–294. (10.1016/S0166-2236(00)01797-5) PubMed DOI

Shcherbakov V. P., Winklhofer M. 1999. The osmotic magnetometer: a new model for magnetite-based magnetoreceptors in animals. Eur. Biophys. J. 28, 380–392. (10.1007/s002490050222) DOI

Shimizu T., Bowers A. N., Budzynski C. A., Kahn M. C., Bingman V. P. 2004. What does a pigeon (Columba livia) brain look like during homing? Selective examination of ZENK expression. Behav. Neurosci. 118, 845–851. (10.1037/0735-7044.118.4.845) PubMed DOI

Stuchlik A., Fenton A. A., Bures J. 2001. Substratal idiothetic navigation of rats is impaired by removal or devaluation of extramaze and intramaze cues. Proc. Natl Acad. Sci. USA 98, 3537–3542. (10.1073/pnas.051630498) PubMed DOI PMC

Taube J. S. 2002. Sensory determinants of head direction. In The neural basis of navigation: evidence from single cell recording (ed. Sharp P. E.), pp. 141–161. Dordrecht, The Netherlands: Kluwer Academic Publishers.

Taube J. S. 2007. The head direction signal: origins and sensory-motor integration. Annu. Rev. Neurosci. 30, 181–207. (10.1146/annurev.neuro.29.051605.112854) PubMed DOI

Taube J. S., Muller R. U., Ranck J. B., Jr 1990. Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J. Neurosci. 10, 420–435. PubMed PMC

Thalau P., Ritz T., Burda H., Wegner R., Wiltschko R. 2006. The magnetic compass mechanisms of birds and rodents are based on different physical principles. J. R. Soc. Interface 3, 583–587. (10.1098/rsif.2006.0130) PubMed DOI PMC

Touretzky D. S. 2002. The rodent navigation circuit. In The neural basis of navigation: evidence from single cell recording (ed. Sharp P. E.), pp. 217–234. Dordrecht, The Netherlands: Kluwer Academic Publishers.

Vann S. D., Brown M. W., Erichsen J. T., Aggleton J. P. 2000. Fos imaging reveals differential patterns of hippocampal and parahippocampal subfield activation in rats in response to different spatial memory tests. J. Neurosci. 20, 2711–2718. PubMed PMC

Vargas J. P., Siegel J. J., Bingman V. P. 2006. The effects of a changing ambient magnetic field on single-unit activity in the homing pigeon hippocampus. Brain Res. Rev. 70, 158–164. (10.1016/j.brainresbull.2006.03.018) PubMed DOI

Wang Y., Pan Y., Parsons S., Walker M. M., Zhang S. 2007. Bats respond to polarity of a magnetic field. Proc. R. Soc. B 274, 2901–2905. (10.1098/rspb.2007.0904) PubMed DOI PMC

Wegner R. E., Begall S., Burda H. 2006. Magnetic compass in the cornea: local anaesthesia impairs orientation in a mammal. J. Exp. Biol. 209, 4747–4750. (10.1242/jeb.02573) PubMed DOI

Wiener S. I., Taube J. S. 2005. Head direction cells and the neural mechanisms of spatial orientation. Cambridge, MA: MIT Press.

Wiltschko R., Wiltschko W. 2006. Magnetoreception. BioEssays 28, 157–168. (10.1002/bies.20363) PubMed DOI

Wiltschko W., Wiltschko R. 2005. Magnetic orientation and magnetoreception in birds and other animals. J. Comp. Physiol. A 191, 675–693. (10.1007/s00359-005-0627-7) PubMed DOI

Wirtshafter D. 2005. Cholinergic involvement in the cortical and hippocampal Fos expression induced in the rat by placement in a novel environment. Brain Res. 1051, 57–65. (10.1016/j.brainres.2005.05.052) PubMed DOI

Witter M. P., Amaral D. G. 2004. Hippocampal formation. In The rat nervous system (ed. Paxinos G.), pp. 635–704. San Diego, CA: Elsevier Academic Press.

Wood E. R., Dudchenko P. A., Robitsek R. J., Eichenbaum H. 2000. Hippocampal neurons encode information about different types of memory episodes occurring in the same location. Neuron 27, 623–633. (10.1016/S0896-6273(00)00071-4) PubMed DOI

Xiao J., Levitt J. B., Buffenstein R. 2006. A stereotaxic atlas of the brain of the naked mole-rat (Heterocephalus glaber). Neuroscience 141, 1415–1435. (10.1016/j.neuroscience.2006.03.077) PubMed DOI

Zapka M., et al. 2009. Visual but not trigeminal mediation of magnetic compass information in a migratory bird. Nature 461, 1274–1277. (10.1038/nature08528) PubMed DOI

Eyes are essential for magnetoreception in a mammal

Brain atlas of the African mole-rat Fukomys anselli

Spontaneous expression of magnetic compass orientation in an epigeic rodent: the bank vole, Clethrionomys glareolus

Odours stimulate neuronal activity in the dorsolateral area of the hippocampal formation during path integration