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Responses of infrared-sensitive tectal units of the pit viper Crotalus atrox to moving objects

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Abstract

Rattlesnakes perceive IR radiation with their pit organs. This enables them to detect and strike towards warm-blooded prey even in the dark. In addition, the IR sense allows rattlesnakes to find places for thermoregulation. Animate objects (e.g., prey) tend to move and thus cause moving IR images across the pit membrane. Even when an object is stationary, scanning head movements of rattlesnakes will result in moving IR images across the pit membrane. We recorded the neuronal activity of IR-sensitive tectal neurons of the rattlesnake Crotalus atrox while stimulating the snakes with an IR source that moved horizontally at various velocities. As long as object velocity was low (angular velocity of ~5°/s) IR-sensitive tectal neurons hardly showed any responses. With increasing object velocity though, neuronal activity reached a maximum at ~50°/s. A further increase in object velocity up to ~120°/s resulted in a slight decrease of neuronal activity. Our results demonstrate the importance of moving stimuli for the snake’s IR detection abilities: in contrast to fast moving objects, stationary or slowly moving objects will not be detected when the snake is motionless, but might be detected by scanning head movements.

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Abbreviations

IR:

Infrared

LTTD:

Nucleus descendens lateralis nervi trigemini

RC:

Nucleus reticularis caloris

RF:

Receptive field

References

  • Bakken GS, Colayori SE, Duong T (2012) Analytical methods for the geometric optics of thermal vision illustrated with four species of pitvipers. J Exp Biol 215:2621–2629

    Article  PubMed  Google Scholar 

  • Beavers RA (1976) Food habits of the western diamondback rattlesnake, Crotalus atrox, in Texas (Viperidae). Southwest Nat 20:503–515

    Article  Google Scholar 

  • Blum B, Auker CR, Carpenter DO (1978) A head holder and stereotaxic device for the rattlesnake. Brain Res Bull 3:271–274

    Article  CAS  PubMed  Google Scholar 

  • Borst A, Euler T (2011) Seeing things in motion: models, circuits, and mechanisms. Neuron 71:974–994

    Article  CAS  PubMed  Google Scholar 

  • Bullock TH, Diecke F (1956) Properties of an infra-red receptor. J Physiol 134:47–87

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bullock TH, Fox W (1957) The anatomy of the infra-red sense organ in the facial pit of pit vipers. J Cell Sci 3:219–234

    Google Scholar 

  • Chen Q, Deng H, Brauth SE et al (2012) Reduced performance of prey targeting in pit vipers with contralaterally occluded infrared and visual senses. PLoS ONE 7:e34989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Cock Buning T (1983) Thresholds of infrared sensitive tectal neurons in Python reticulatus, Boa constrictor and Agkistrodon rhodostoma. J Comp Physiol A 151:461–467

    Article  Google Scholar 

  • De Cock Buning T, Terashima S, Goris RC (1981a) Crotaline pit organs analyzed as warm receptors. Cell Mol Neurobiol 1:69–85

    Article  PubMed  Google Scholar 

  • De Cock Buning T, Terashima S, Goris RC (1981b) Python pit organs analyzed as warm receptors. Cell Mol Neurobiol 1:271–278

    Article  PubMed  Google Scholar 

  • Djawdan M (1988) Maximal running speeds of bipedal and quadrupedal rodents. J Mammal 69:765–772

    Article  Google Scholar 

  • Ebert J, Westhoff G (2006) Behavioural examination of the infrared sensitivity of rattlesnakes (Crotalus atrox). J Comp Physiol A 192:941–947

    Article  CAS  Google Scholar 

  • Eskew EA, Willson JD, Winne CT (2009) Ambush site selection and ontogenetic shifts in foraging strategy in a semi-aquatic pit viper, the Eastern cottonmouth. J Zool 277:179–186

    Article  Google Scholar 

  • Goris RC, Nomoto M (1967) Infrared reception in oriental crotaline snakes. Comp Biochem Physiol 23:879–892

    Article  CAS  PubMed  Google Scholar 

  • Goris RC, Terashima S (1973) Central response to infra-red stimulation of the pit receptors in a crotaline snake, Trimeresurus flavoviridis. J Exp Biol 58:59–76

    CAS  PubMed  Google Scholar 

  • Gracheva EO, Ingolia NT, Kelly YM et al (2010) Molecular basis of infrared detection by snakes. Nature 464:1006–1011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gruberg ER, Kicliter E, Newman EA et al (1979) Connections of the tectum of the rattlesnake Crotalus viridis: an HRP study. J Comp Neurol 188:31–41

    Article  CAS  PubMed  Google Scholar 

  • Harris JF, Gamow RI (1971) Snake infrared receptors: thermal or photochemical mechanism? Science 172:1252–1253

    Article  CAS  PubMed  Google Scholar 

  • Hartline PH, Kass L, Loop MS (1978) Merging of modalities in the optic tectum: infrared and visual integration in rattlesnakes. Science 199:1225–1229

    Article  CAS  PubMed  Google Scholar 

  • Heiligenberg W, Rose GJ (1987) The optic tectum of the gymnotiform electric fish, Eigenmannia: labeling of physiologically identified cells. Neuroscience 22:331–340

    Article  CAS  PubMed  Google Scholar 

  • Kardong, Bels (1998) Rattlesnake strike behavior: kinematics. J Exp Biol 201:837–850

    PubMed  Google Scholar 

  • Kardong KV, Mackessy SP (1991) The strike behavior of a congenitally blind rattlesnake. J Herpetol 25:208–211

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kohl T, Colayori SE, Westhoff G, Bakken GS, Young BA (2012) Directional sensitivity in the thermal response of the facial pit in western diamondback rattlesnakes (Crotalus atrox). J Exp Biol 215:2630–2636

    Article  PubMed  Google Scholar 

  • Kohl T, Bothe MS, Luksch H, Straka H, Westhoff G (2014) Organotopic organization of the primary infrared sensitive nucleus (LTTD) in the western diamondback rattlesnake (Crotalus atrox). J Comp Neurol 522(18):3943–3959

    Article  PubMed  Google Scholar 

  • Krochmal AR, Bakken GS (2003) Thermoregulation in the pits: use of thermal radiation for retreat site selection by rattlesnakes. J Exp Biol 206:2539–2545

    Article  PubMed  Google Scholar 

  • Lynn WG (1931) The structure and function of the facial pit of the pit vipers. Am J Anat 49:97–139

    Article  Google Scholar 

  • Marasco PD, Catania KC (2007) Response properties of primary afferents supplying Eimer’s organ. J Exp Biol 210:765–780

    Article  PubMed  Google Scholar 

  • Moiseenkova V, Bell B, Motamedi M, Wozniak E, Christensen B (2003) Wide-band spectral tuning of heat receptors in the pit organ of the copperhead snake (Crotalinae). Am J Physiol Integr Comp Physiol 284:598–606

    Article  Google Scholar 

  • Molenaar GJ (1974) An additional trigeminal system in certain snakes possessing infrared receptors. Brain Res 78:340–344

    Article  CAS  PubMed  Google Scholar 

  • Newman EA, Hartline PH (1981) Integration of visual and infrared information in bimodal neurons in the rattlesnake optic tectum. Science 213:789–791

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Newman EA, Gruberg ER, Hartline PH (1980) The infrared trigemino-tectal pathway in the rattlesnake and in the python. J Comp Neurol 191:465–477

    Article  CAS  PubMed  Google Scholar 

  • Noble GK, Schmidt A (1937) The structure and function of the facial and labial pits of snakes. Proc Am Phil Soc 77:263–288

    Google Scholar 

  • Schroeder DM, Loop MS (1976) Trigeminal projections in snakes possessing infrared sensitivity. J Comp Neurol 169:1–11

    Article  CAS  PubMed  Google Scholar 

  • Shine R, Li-Xin S (2002) Arboreal ambush site selection by pit-vipers Gloydius shedaoensis. Anim Behav 63:565–576

    Article  Google Scholar 

  • Shine R, Sun L, Kearney M, Fitzgerald M (2002) Why do Juvenile Chinese pit-vipers (Gloydius shedaoensis) select arboreal ambush sites? Ethology 108:897–910

    Article  Google Scholar 

  • Shine R, Sun L, Kearney M, Fitzgerald M (2006) Thermal correlates of foraging-site selection by Chinese pit-vipers (Gloydius shedaoensis, Viperidae). J Therm Biol 27:405–412

    Article  Google Scholar 

  • Terashima S, Goris RC (1976) Receptive area of an infrared tectal unit. Brain Res 101:155–159

    Article  CAS  PubMed  Google Scholar 

  • Terashima S, Goris RC (1979) Receptive areas of primary infrared afferent neurons in crotaline snakes. Neuroscience 4:1137–1144

    Article  CAS  PubMed  Google Scholar 

  • Terashima S, Goris RC, Katsuki Y (1968) Generator potential of crotaline snake infrared receptor. J Neurophysiol 31:682–688

    CAS  PubMed  Google Scholar 

  • Van Dyke JU, Grace MS (2010) The role of thermal contrast in infrared-based defensive targeting by the copperhead, Agkistrodon contortrix. Anim Behav 79:993–999

    Article  Google Scholar 

  • Wagner H, Takahashi T (1990) Neurons in the midbrain of the barn owl are sensitive to the direction of apparent acoustic motion. Naturwissenschaften 77:439–442

    Article  CAS  PubMed  Google Scholar 

  • Zittlau KE, Class B, Münz H (1986) Directional sensitivity of lateral line units in the clawed toad Xenopus laevis Daudin. J Comp Physiol A 158:469–477

    Article  Google Scholar 

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Acknowledgments

We thank Slawa Braun for animal care and Joachim Mogdans and Vera Schlüssel for critical reading of the manuscript. We also thank two anonymous reviewers for carefully reading and commenting on the manuscript. The authors acknowledge the financial support provided by the DFG (KO4835/1-1). Care and maintenance of experimental animals followed the guidelines for reptiles and venomous snakes. Animal housing and experiments were approved by the LANUVNRW (50.203.2-BN 7, 5/03).

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Authors and Affiliations

  1. Institute of Zoology, Rheinische Friedrich-Wilhelms-University Bonn, Poppelsdorfer Schloss, Meckenheimer Allee 169, 53115, Bonn, Germany

    Felix Kaldenbach & Horst Bleckmann

  2. Chair of Zoology, Technical University of Munich, Liesel-Beckmann-Str. 4, 85354, Freising-Weihenstephan, Germany

    Tobias Kohl

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  1. Felix Kaldenbach
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  2. Horst Bleckmann
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  3. Tobias Kohl
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Correspondence to Tobias Kohl.

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Kaldenbach, F., Bleckmann, H. & Kohl, T. Responses of infrared-sensitive tectal units of the pit viper Crotalus atrox to moving objects. J Comp Physiol A 202, 389–398 (2016). https://doi.org/10.1007/s00359-016-1076-1

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  • DOI: https://doi.org/10.1007/s00359-016-1076-1

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