Molecular basis of infrared detection by snakes

Article metrics

Abstract

Snakes possess a unique sensory system for detecting infrared radiation, enabling them to generate a ‘thermal image’ of predators or prey. Infrared signals are initially received by the pit organ, a highly specialized facial structure that is innervated by nerve fibres of the somatosensory system. How this organ detects and transduces infrared signals into nerve impulses is not known. Here we use an unbiased transcriptional profiling approach to identify TRPA1 channels as infrared receptors on sensory nerve fibres that innervate the pit organ. TRPA1 orthologues from pit-bearing snakes (vipers, pythons and boas) are the most heat-sensitive vertebrate ion channels thus far identified, consistent with their role as primary transducers of infrared stimuli. Thus, snakes detect infrared signals through a mechanism involving radiant heating of the pit organ, rather than photochemical transduction. These findings illustrate the broad evolutionary tuning of transient receptor potential (TRP) channels as thermosensors in the vertebrate nervous system.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Anatomy of the pit organ and comparison of gene expression in snake sensory ganglia.
Figure 2: Expression of TRPA1 and TRPV1 in rattlesnake sensory ganglia.
Figure 3: Functional analysis of snake TRPA1 channels.
Figure 4: Analysis of TRPA1 from python and boa.
Figure 5: Functional analysis of snake sensory neurons.

Accession codes

Primary accessions

Gene Expression Omnibus

Data deposits

Deep sequencing data are archived under GEO accession number GSE19911. GenBank accession numbers are GU562965 (Python regius TRPA1), GU562966 (Elaphe obsoleta lindheimeri TRPA1), GU562967 (Crotalus atrox TRPA1), GU562968 (Crotalus atrox TRPV1), and GU562969 (Corallus hortulanus TRPA1).

Change history

  • 15 April 2010

    A correction was made to the spelling of an author name (N.T.I.) on 15 April.

References

  1. 1

    Bullock, T. H. & Cowles, R. B. Physiology of an infrared receptor: the facial pit of pit vipers. Science 115, 541–543 (1952)

  2. 2

    Campbell, A. L., Naik, R. R., Sowards, L. & Stone, M. O. Biological infrared imaging and sensing. Micron 33, 211–225 (2002)

  3. 3

    Ebert, J. Infrared Sense in Snakes – Behavioural and Anatomical Examinations (Crotalus atrox, Python regius, Corallus hortulanus). Dr rer. nat. thesis, Rheinische Friedrich Wilhelms Univ. Bonn. (2007)

  4. 4

    Barrett, R., Maderson, P. F. A. & Meszler, R. M. in Biology of Reptilia (ed. Parsons, T. S.) Ch. 4 277–300 (Academic Press, 1970)

  5. 5

    Ebert, J. & Schmitz, A. in Herpetologia Bonnensis II (eds Vences, M. Kohler, J., Ziegler T. & Bohme, W.) 215–217 (2006)

  6. 6

    Terashima, S. & Liang, Y. F. Temperature neurons in the crotaline trigeminal ganglia. J. Neurophysiol. 66, 623–634 (1991)

  7. 7

    Amemiya, F., Ushiki, T., Goris, R. C., Atobe, Y. & Kusunoki, T. Ultrastructure of the crotaline snake infrared pit receptors: SEM confirmation of TEM findings. Anat. Rec. 246, 135–146 (1996)

  8. 8

    Bleichmar, H. & De Robertis, E. Submicroscopic morphology of the infrared receptor of pit vipers. Z. Zellforsch. Mikrosk. Anat. 56, 748–761 (1962)

  9. 9

    Hartline, P. H., Kass, L. & Loop, M. S. Merging of modalities in the optic tectum: infrared and visual integration in rattlesnakes. Science 199, 1225–1229 (1978)

  10. 10

    Newman, E. A. & Hartline, P. H. Integration of visual and infrared information in bimodal neurons in the rattlesnake optic tectum. Science 213, 789–791 (1981)

  11. 11

    Molenaar, G. J. The sensory trigeminal system of a snake in the possession of infrared receptors. II. The central projections of the trigeminal nerve. J. Comp. Neurol. 179, 137–151 (1978)

  12. 12

    de Cock Buning, T., Terashima, S. & Goris, R. C. Python pit organs analyzed as warm python pit organs analyzed as warm receptors. Cell. Mol. Neurobiol. 1, 271–278 (1981)

  13. 13

    Warren, J. W. & Proske, U. Infrared receptors in the facial pits of the Australian python Morelia spilotes. Science 159, 439–441 (1968)

  14. 14

    Kishida, R., Amemiya, F., Kusunoki, T. & Terashima, S. A new tectal afferent nucleus of the infrared sensory system in the medulla oblongata of Crotaline snakes. Brain Res. 195, 271–279 (1980)

  15. 15

    Kishida, R., de Cock Buning, T. & Dubbeldam, J. L. Primary vagal nerve projections to the lateral descending trigeminal nucleus in boidae (Python molurus and Boa constrictor). Brain Res. 263, 132–136 (1983)

  16. 16

    Noble, G. K. & Schmidt, A. The structure and function of facial and labial pits of snakes. Proc. Am. Phil. Soc. 77, 263–288 (1937)

  17. 17

    Pappas, T. C., Motamedi, M. & Christensen, B. N. Unique temperature-activated neurons from pit viper thermosensors. Am. J. Physiol. Cell Physiol. 287, C1219–C1228 (2004)

  18. 18

    Bautista, D. M. et al. TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 124, 1269–1282 (2006)

  19. 19

    Julius, D. & Basbaum, A. I. Molecular mechanisms of nociception. Nature 413, 203–210 (2001)

  20. 20

    Molenaar, G. J. An additional trigeminal system in certain snakes possessing infrared receptors. Brain Res. 78, 340–344 (1974)

  21. 21

    Schroeder, D. M. & Loop, M. S. Trigeminal projections in snakes possessing infrared sensitivity. J. Comp. Neurol. 169, 1–13 (1976)

  22. 22

    Eng, S. R., Dykes, I. M., Lanier, J., Fedtsova, N. & Turner, E. E. POU-domain factor Brn3a regulates both distinct and common programs of gene expression in the spinal and trigeminal sensory ganglia. Neural Dev. 2, 3 (2007)

  23. 23

    Su, A. I. et al. A gene atlas of the mouse and human protein-encoding transcriptomes. Proc. Natl Acad. Sci. USA 101, 6062–6067 (2004)

  24. 24

    Woolf, C. J. & Ma, Q. Nociceptors–noxious stimulus detectors. Neuron 55, 353–364 (2007)

  25. 25

    Jordt, S. E. et al. Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427, 260–265 (2004)

  26. 26

    Kobayashi, K. et al. Distinct expression of TRPM8, TRPA1, and TRPV1 mRNAs in rat primary afferent neurons with aδ/c-fibers and colocalization with trk receptors. J. Comp. Neurol. 493, 596–606 (2005)

  27. 27

    Tominaga, M. et al. The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 21, 531–543 (1998)

  28. 28

    Bandell, M. et al. Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin. Neuron 41, 849–857 (2004)

  29. 29

    Macpherson, L. J. et al. Noxious compounds activate TRPA1 ion channels through covalent modification of cysteines. Nature 445, 541–545 (2007)

  30. 30

    Hinman, A., Chuang, H. H., Bautista, D. M. & Julius, D. TRP channel activation by reversible covalent modification. Proc. Natl Acad. Sci. USA 103, 19564–19568 (2006)

  31. 31

    Prober, D. A. et al. Zebrafish TRPA1 channels are required for chemosensation but not for thermosensation or mechanosensory hair cell function. J. Neurosci. 28, 10102–10110 (2008)

  32. 32

    Hamada, F. N. et al. An internal thermal sensor controlling temperature preference in Drosophila . Nature 454, 217–220 (2008)

  33. 33

    Viswanath, V. et al. Opposite thermosensor in fruitfly and mouse. Nature 423, 822–823 (2003)

  34. 34

    Krochmal, A. R., Bakken, G. S. & LaDuc, T. J. Heat in evolution’s kitchen: evolutionary perspectives on the functions and origin of the facial pit of pitvipers (Viperidae: Crotalinae). J. Exp. Biol. 207, 4231–4238 (2004)

  35. 35

    Safer, A. B. & Grace, M. S. Infrared imaging in vipers: differential responses of crotaline and viperine snakes to paired thermal targets. Behav. Brain Res. 154, 55–61 (2004)

  36. 36

    Kishida, R., Goris, R. C., Terashima, S. & Dubbeldam, J. L. A suspected infrared-recipient nucleus in the brainstem of the vampire bat, Desmodus rotundus . Brain Res. 322, 351–355 (1984)

  37. 37

    Jordt, S. E., McKemy, D. D. & Julius, D. Lessons from peppers and peppermint: the molecular logic of thermosensation. Curr. Opin. Neurobiol. 13, 487–492 (2003)

  38. 38

    Komatsu, H., Mori, I., Rhee, J. S., Akaike, N. & Ohshima, Y. Mutations in a cyclic nucleotide-gated channel lead to abnormal thermosensation and chemosensation in C. elegans . Neuron 17, 707–718 (1996)

  39. 39

    Ramot, D., MacInnis, B. L. & Goodman, M. B. Bidirectional temperature-sensing by a single thermosensory neuron in C. elegans . Nature Neurosci. 11, 908–915 (2008)

  40. 40

    Story, G. M. et al. ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112, 819–829 (2003)

  41. 41

    Caspani, O. & Heppenstall, P. A. TRPA1 and cold transduction: an unresolved issue? J. Gen. Physiol. 133, 245–249 (2009)

  42. 42

    Wang, G. et al. Anopheles gambiae TRPA1 is a heat-activated channel expressed in thermosensitive sensilla of female antennae. Eur. J. Neurosci. 30, 967–974 (2009)

  43. 43

    Matsuura, H., Sokabe, T., Kohno, K., Tominaga, M. & Kadowaki, T. Evolutionary conservation and changes in insect TRP channels. BMC Evol. Biol. 9, 228 (2009)

  44. 44

    Dong, S. & Kumazawa, Y. Complete mitochondrial DNA sequences of six snakes: phylogenetic relationships and molecular evolution of genomic features. J. Mol. Evol. 61, 1432 (2005)

  45. 45

    Liman, E. R. Use it or lose it: molecular evolution of sensory signaling in primates. Pflugers Arch. 453, 125–131 (2006)

  46. 46

    Myers, B. R., Sigal, Y. M. & Julius, D. Evolution of thermal response properties in a cold-activated TRP channel. PLoS One 4, e5741 (2009)

  47. 47

    Chuang, H. H., Neuhausser, W. M. & Julius, D. The super-cooling agent icilin reveals a mechanism of coincidence detection by a temperature-sensitive TRP channel. Neuron 43, 859–869 (2004)

  48. 48

    DeCoursey, T. E. & Cherny, V. V. Temperature dependence of voltage-gated H+ currents in human neutrophils, rat alveolar epithelial cells, and mammalian phagocytes. J. Gen. Physiol. 112, 503–522 (1998)

Download references

Acknowledgements

We thank A. Priel for advice and assistance with calcium imaging and electrophysiology, C. Chu for help with sequencing, J. Poblete for technical assistance, and the staff of the Natural Toxins Research Center serpentarium for animal husbandry. We thank P. Garrity for providing the dTrpA1 cDNA. This work was supported by a Ruth L. Kirschstein National Research Service Award (GM080853) (N.T.I.), a NIH Institutional Research Service Award in Molecular and Cellular Basis of Cardiovascular Disease (A.T.C.), the Howard Hughes Medical Institute (J.S.W.), and grants from the National Institutes of Health, including NCRR Viper grant P40 RR018300-06 (E.E.S. and J.C.P.), P01 AG010770 (J.S.W.) and NS047723 and NS055299 (D.J.).

Author Contributions E.O.G., J.F.C.-M. and N.T.I. designed and performed experiments and analysed data. N.T.I. and J.S.W. developed analytical tools and analysed data. Y.M.K., G.H. and A.T.C. performed experiments and/or provided reagents and analysed data. E.E.S. and J.C.P. supervised snake husbandry and handling. E.O.G., Y.M.K., J.F.C.-M. and D.J. wrote the manuscript with discussion and contributions from all authors. J.S.W. and D.J. provided advice and guidance throughout. D.J. initiated and supervised the project.

Author information

Correspondence to David Julius.

Supplementary information

Supplementary Figures

This file contains Supplementary Figures 1-8 with legends. (PDF 9759 kb)

PowerPoint slides

PowerPoint slide for Fig. 1

PowerPoint slide for Fig. 2

PowerPoint slide for Fig. 3

PowerPoint slide for Fig. 4

PowerPoint slide for Fig. 5

Rights and permissions

Reprints and Permissions

About this article

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.