Diverse animal species perceive Earth's magnetism and use their magnetic sense to orientate and navigate. Even non-migrating insects such as fruit flies and cockroaches have been shown to exploit the flavoprotein Cryptochrome (Cry) as a likely magnetic direction sensor; however, the transduction mechanism remains unknown. In order to work as a system to steer insect flight or control locomotion, the magnetic sense must transmit the signal from the receptor cells to the brain at a similar speed to other sensory systems, presumably within hundreds of milliseconds or less. So far, no electrophysiological or behavioral study has tackled the problem of the transduction delay in case of Cry-mediated magnetoreception specifically. Here, using a novel aversive conditioning assay on an American cockroach, we show that magnetic transduction is executed within a sub-second time span. A series of inter-stimulus intervals between conditioned stimuli (magnetic North rotation) and unconditioned aversive stimuli (hot air flow) provides original evidence that Cry-mediated magnetic transduction is sufficiently rapid to mediate insect orientation.

Faculty of Science Institute of Experimental Biology Masaryk University Brno Czechia

Zobrazit více v PubMed

Bae J.-E., Bang S., Min S., Lee S.-H., Kwon S.-H., Lee Y., et al. . (2016). Positive geotactic behaviors induced by geomagnetic field in Drosophila. Mol. Brain 9:55. 10.1186/s13041-016-0235-1 PubMed DOI PMC

Baik L. S., Fogle K. J., Roberts L., Galschiodt A. M., Chevez J. A., Recinos Y., et al. . (2017). CRYPTOCHROME mediates behavioral executive choice in response to UV light. Proc. Natl. Acad. Sci. U S A 114, 776–781. 10.1073/pnas.1607989114 PubMed DOI PMC

Bazalova O., Kvicalova M., Damulewicz M., Valkova T., Slaby P., Bartos P., et al. . (2016). Cryptochrome 2 mediates directional magnetoreception in cockroaches. Proc. Natl. Acad. Sci. U S A 113, 1660–1665. 10.1073/pnas.1518622113 PubMed DOI PMC

Bhavsar M. B., Stumpner A., Heinrich R. (2017). Brain regions for sound processing and song release in a small grasshopper. J. Insect Physiol. 99, 15–24. 10.1016/j.jinsphys.2017.03.006 PubMed DOI

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

Clark G. A., Hawkins R. D., Kandel E. R. (1994). Activity-dependent enhancement of presynaptic facilitation provides a cellular mechanism for the temporal specificity of classical conditioning in aplysia. Learn. Mem. 1, 243–257. PubMed

Engel J. E., Hoy R. R. (1999). Experience-dependent modification of ultrasound auditory processing in a cricket escape response. J. Exp. Biol. 202, 2797–2806. PubMed

Fan R.-J., Anderson P., Hansson B. S. (1997). Behavioural analysis of olfactory conditioning in the moth Spodoptera littoralis (Boisd.) (Lepidoptera: Noctuidae). J. Exp. Biol. 200, 2969–2976. PubMed

Fogle K. J., Baik L. S., Houl J. H., Tran T. T., Roberts L., Dahm N. A., et al. . (2015). CRYPTOCHROME-mediated phototransduction by modulation of the potassium ion channel β-subunit redox sensor. Proc. Natl. Acad. Sci. U S A 112, 2245–2250. 10.1073/pnas.1416586112 PubMed DOI PMC

Fogle K. J., Parson K. G., Dahm N. A., Holmes T. C. (2011). CRYPTOCHROME is a blue-light sensor that regulates neuronal firing rate. Science 331, 1409–1413. 10.1126/science.1199702 PubMed DOI PMC

Galili D. S., Lüdke A., Galizia C. G., Szyszka P., Tanimoto H. (2011). Olfactory trace conditioning in Drosophila. J. Neurosci. 31, 7240–7248. 10.1523/JNEUROSCI.6667-10.2011 PubMed DOI PMC

Gegear R. J., Casselman A., Waddell S., Reppert S. M. (2008). Cryptochrome mediates light-dependent magnetosensitivity in Drosophila. Nature 454, 1014–1018. 10.1038/nature07183 PubMed DOI PMC

Giachello C. N. G., Scrutton N. S., Jones A. R., Baines R. A. (2016). Magnetic fields modulate blue-light-dependent regulation of neuronal firing by cryptochrome. J. Neurosci. 36, 10742–10749. 10.1523/JNEUROSCI.2140-16.2016 PubMed DOI PMC

Gibson W. T., Gonzalez C. R., Fernandez C., Ramasamy L., Tabachnik T., Du R. R., et al. . (2015). Behavioral responses to a repetitive visual threat stimulus express a persistent state of defensive arousal in Drosophila. Curr. Biol. 25, 1401–1415. 10.1016/j.cub.2015.03.058 PubMed DOI PMC

Giurfa M., Fabre E., Flaven-Pouchon J., Groll H., Oberwallner B., Vergoz V., et al. . (2009). Olfactory conditioning of the sting extension reflex in honeybees: memory dependence on trial number, interstimulus interval, intertrial interval, and protein synthesis. Learn. Mem. 16, 761–765. 10.1101/lm.1603009 PubMed DOI

Giurfa M., Malun D. (2004). Associative mechanosensory conditioning of the proboscis extension reflex in honeybees. Learn. Mem. 11, 294–302. 10.1101/lm.63604 PubMed DOI PMC

Hardie R., Raghu P. (2001). Visual transduction in Drosophila. Nature 413, 186–193. 10.1038/35093002 PubMed DOI

Heyers D., Zapka M., Hoffmeister M., Wild J. M., Mouritsen H. (2010). Magnetic field changes activate the trigeminal brainstem complex in a migratory bird. Proc. Natl. Acad. Sci. U S A 107, 9394–9399. 10.1073/pnas.0907068107 PubMed DOI PMC

Hiscock H. G., Worster S., Kattnig D. R., Steers C., Jin Y., Manolopoulos D. E., et al. . (2016). The quantum needle of the avian magnetic compass. Proc. Natl. Acad. Sci. U S A 113, 4634–4639. 10.1073/pnas.1600341113 PubMed DOI PMC

Hore P. J., Mouritsen H. (2016). The radical-pair mechanism of magnetoreception. Annu. Rev. Biophys. 45, 299–344. 10.1146/annurev-biophys-032116-094545 PubMed DOI

Lau J. C. S., Rodgers C. T., Hore P. J. (2012). Compass magnetoreception in birds arising from photo-induced radical pairs in rotationally disordered cryptochromes. J. R. Soc. Interface 9, 3329–3337. 10.1098/rsif.2012.0374 PubMed DOI PMC

Lent D. D., Kwon H.-W. (2004). Antennal movements reveal associative learning in the American cockroach Periplaneta americana. J. Exp. Biol. 207, 369–375. 10.1242/jeb.00736 PubMed DOI

Leucht T., Martin H. (1990). Interactions between E-vector orientation and weak, steady magnetic-fields in the honeybee, apis mellifica. Naturwissenschaften 77, 130–133. 10.1007/bf01134475 DOI

Liang C.-H., Chuang C.-L., Jiang J.-A., Yang E.-C. (2016). Magnetic sensing through the abdomen of the honey bee. Sci. Rep. 6:23657. 10.1038/srep23657 PubMed DOI PMC

Liedvogel M., Mouritsen H. (2010). Cryptochromes—a potential magnetoreceptor: what do we know and what do we want to know? J. R. Soc. Interface 7, S147–S162. 10.1098/rsif.2009.0411.focus 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

Lohmann K. J., Pentcheff N. D., Nevitt G. A., Stetten G. D., Zimmerfaust R. K., Jarrard H. E., et al. . (1995). Magnetic orientation of spiny lobsters in the ocean: experiments with undersea coil systems. J. Exp. Biol. 198, 2041–2048. PubMed

Lohmann K. J., Willows A. O., Pinter R. B. (1991). An identifiable molluscan neuron responds to changes in earth-strength magnetic fields. J. Exp. Biol. 161, 1–24. PubMed

Maeda K., Henbest K. B., Cintolesi F., Kuprov I., Rodgers C. T., Liddell P. A., et al. . (2008). Chemical compass model of avian magnetoreception. Nature 453, U387–U390. 10.1038/nature06834 PubMed DOI

Matsumoto Y., Mizunami M. (2002). Temporal determinants of long-term retention of olfactory memory in the cricket Gryllus bimaculatus. J. Exp. Biol. 205, 1429–1437. PubMed

Mizunami M., Matsumoto Y., Watanabe H., Nishino H. (2013). “Olfactory and visual learning in cockroaches and crickets,” in Handbook of Behavioral Neuroscience, (Vol. 22) eds Menzel R., Benjamin P. R. (San Diego, CA: Elsevier Academic Press Inc.), 549–560.

Mongeau J.-M., Sponberg S. N., Miller J. P., Full R. J. (2015). Sensory processing within cockroach antenna enables rapid implementation of feedback control for high-speed running maneuvers. J. Exp. Biol. 218, 2344–2354. 10.1242/jeb.118604 PubMed DOI

Mouritsen H., Hore P. J. (2012). The magnetic retina: light-dependent and trigeminal magnetoreception in migratory birds. Curr. Opin. Neurobiol. 22, 343–352. 10.1016/j.conb.2012.01.005 PubMed DOI

Murakami S., Dan C., Zagaeski B., Maeyama Y., Kunes S., Tabata T. (2010). Optimizing Drosophila olfactory learning with a semi-automated training device. J. Neurosci. Methods 188, 195–204. 10.1016/j.jneumeth.2010.02.007 PubMed DOI PMC

Ozturk N., Selby C. P., Annayev Y., Zhong D., Sancar A. (2011). Reaction mechanism of Drosophila cryptochrome. Proc. Natl. Acad. Sci. U S A 108, 516–521. 10.1073/pnas.1017093108 PubMed DOI PMC

Pavlova G. A., Glantz R. M., Willows A. O. D. (2011). Responses to magnetic stimuli recorded in peripheral nerves in the marine nudibranch mollusk Tritonia diomedea. J. Comp. Physiol. A 197, 979–986. 10.1007/s00359-011-0659-0 PubMed DOI

Popescu I. R., Willows A. O. D. (1999). Sources of magnetic sensory input to identified neurons active during crawling in the marine mollusc Tritonia diomedea. J. Exp. Biol. 202, 3029–3036. PubMed

Sato K., Pellegrino M., Nakagawa T., Nakagawa T., Vosshall L. B., Touhara K. (2008). Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature 452, 1002–1006. 10.1038/nature06850 PubMed DOI

Shaw J., Boyd A., House M., Woodward R., Mathes F., Cowin G., et al. . (2015). Magnetic particle-mediated magnetoreception. J. R. Soc. Interface 12:0499. 10.1098/rsif.2015.0499 PubMed DOI PMC

Szyszka P., Gerkin R. C., Galizia C. G., Smith B. H. (2014). High-speed odor transduction and pulse tracking by insect olfactory receptor neurons. Proc. Natl. Acad. Sci. U S A 111, 16925–16930. 10.1073/pnas.1412051111 PubMed DOI PMC

Takanashi T., Fukaya M., Nakamuta K., Skals N., Nishino H. (2016). Substrate vibrations mediate behavioral responses via femoral chordotonal organs in a cerambycid beetle. Zoological Lett. 2:18. 10.1186/s40851-016-0053-4 PubMed DOI PMC

Tanimoto H., Heisenberg M., Gerber B. (2004). Experimental psychology: event timing turns punishment to reward. Nature 430:983. 10.1038/430983a PubMed DOI

Vácha M. (2006). Laboratory behavioural assay of insect magnetoreception: magnetosensitivity of Periplaneta americana. J. Exp. Biol. 209, 3882–3886. 10.1242/jeb.02456 PubMed DOI

Vacha M. (2017). “Magnetoreception of invertebrates,” in The Oxford Handbook of Invertebrate Neurobiology, ed. Byrne J. H. (Oxford: Oxford University Press; ). 10.1093/oxfordhb/9780190456757.013.16 DOI

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. Bull. 70, 158–164. 10.1016/j.brainresbull.2006.03.018 PubMed DOI

Vidal-Gadea A., Ward K., Beron C., Ghorashian N., Gokce S., Russell J., et al. . (2015). Magnetosensitive neurons mediate geomagnetic orientation in Caenorhabditis elegans. Elife 4:e07493. 10.7554/eLife.07493 PubMed DOI PMC

Vogt K., Yarali A., Tanimoto H. (2015). Reversing stimulus timing in visual conditioning leads to memories with opposite valence in Drosophila. PLoS One 10:e0139797. 10.1371/journal.pone.0139797 PubMed DOI PMC

Walker M. M., Diebel C. E., Haugh C. V., Pankhurst P. M., Montgomery J. C., Green C. R. (1997). Structure and function of the vertebrate magnetic sense. Nature 390, 371–376. 10.1038/37057 PubMed DOI

Wang J. H., Cain S. D., Lohmann K. J. (2004). Identifiable neurons inhibited by Earth-strength magnetic stimuli in the mollusc Tritonia diomedea. J. Exp. Biol. 207, 1043–1049. 10.1242/jeb.00864 PubMed DOI

Wasserman E. A., Miller R. R. (1997). What’s elementary about assocative learning? Annu. Rev. Psychol. 48, 573–607. 10.1146/annurev.psych.48.1.573 PubMed DOI

Wiltschko W., Weindler P., Wiltschko R. (1998). Interaction of magnetic and celestial cues in the migratory orientation of passerines. J. Avian Biol. 29, 606–617. 10.2307/3677181 DOI

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

Wu L.-Q., Dickman J. D. (2012). Neural correlates of a magnetic sense. Science 336, 1054–1057. 10.1126/science.1216567 PubMed DOI

Wyeth R. C. (2010). Should animals navigating over short distances switch to a magnetic compass sense? Front. Behav. Neurosci. 4:42. 10.3389/fnbeh.2010.00042 PubMed DOI PMC

Yarali A., Nehrkorn J., Tanimoto H., Herz A. V. M. (2012). Event timing in associative learning: from biochemical reaction dynamics to behavioural observations. PLoS One 7:e32885. 10.1371/journal.pone.0032885 PubMed DOI PMC