Neurophilosophy

SNAKES have a unique sensory system for detecting infrared radiation, with which they can visualize temperature changes within their immediate environment. Using this special sense, they can image the body heat radiating from warm-blooded animals nearby. This enables them to track their prey quickly and with great accuracy, even in the dark, and to target the most vulnerable parts of the prey’s body when they strike. It also warns them of the presence of predators, and may be used to find appropriate locations for building dens.

Infrared detection is known to be mediated by a specialized sensory apparatus called the pit organ, but several important questions about the detection mechanisms remain. It is still unclear, for example, where in the pit organ the infrared sensor is located, and whether it detects light particles directly, in a similar way to the eye, or heat energy. These questions have now been answered by a group of researchers from the University of California in San Francisco. In an advance online publication in the journal Nature, they report the identification of the sensor: it is an ancient protein called TRPA1, which has been adapted for this purpose in snakes, but not in other vertebrates.

The pit organ (indicated by the red arrow in the photograph below) is the distinguishing feature of the subfamily of snakes commonly referred to as the pit vipers, which includes rattlesnakes and lanceheads. It is a hollow cavity located between the eye and the nostril (black arrow), which works in much the same way as a pinhole camera. At the back of the cavity is a thin membrane which is densely packed with nerve endings and blood vessels, and which serves as the infrared sensor. Radiation heats the membrane and it detects the tiny changes in temperature. The information is then sent to the optic tectum in the midbrain, where the thermal and visual images are superimposed.

One snake species, the western diamondback rattlesnake (Crotalus atrox), has an unrivalled ability to detect infrared radiation. Its pit organs are exquisitely sensitive to heat, detecting temperature changes of 0.003°C, so that the diamondback is able to image other animals from distances of up to 1 meter. Two factors contribute to the sensitivity of the rattlesnake’s pit organ. The membrane is supplied with 6,000 – 7,000 sensory nerves, each of which branches repeatedly at the membrane, with the branches bending towards the outer surface of the membrane. The membrane divides the cavity into two chambers, and so is insulated by air on both sides. This increases the sensitivity further by reducing heat escape. By contrast, the pit organs of pythons and boas have fewer nerve endings and consist of just one chamber, with the membrane against the back. As a result, they are 5-10 times less sensitive to heat than the rattlesnake organ.

rattlesnake pit organ diagram.jpg Being excitable, aggressive and highly venomous, rattlesnakes are, as the researchers put it, “inconvenient subjects for physiological and behavioral studies”. The researchers therefore used a large-scale molecular biological technique called transcriptional profiling to indirectly measure the expression levels of all the genes in three different snake species, and to compare the activity levels of the same genes in different tissues. Specifically, they compared gene expression in the trigeminal and dorsal root ganglia of the rattlesnake and two species of non-pit snakes (the Texas Rat snake and the Western Coachwhip). The trigeminal ganglion is a cluster of nerve cell bodies in the face; in pit snakes it is enlarged, and sends a large bundle of nerve fibres to the pit organ. The dorsal root ganglia are located on either side of the spinal cord, and contain clusters of cells that carry sensory information from the trunk.

A gene encoding the infrared sensor should be expressed in the trigeminal, but not the dorsal root ganglia, of the rattlesnake, and should also be absent from the trigeminal ganglia of non-pit snakes. The researchers found one gene that matched this profile perfectly – TRPA1, which was found to be enriched 400-fold in the rattlesnake trigeminal ganglion. Further investigation revealed that the protein is inactive at room temperature, but responds to temperatures of 27.6°C and above. TRPA1 from pythons, boas and rat snakes were also activated by heat, but with higher thresholds: the python and boa protein are less sensitive to heat than the rattlesnake protein, and the rat snake protein is the least sensitive of all. And like their mammalian equivalents, the proteins from all three snakes were also found to be weakly activated by allyl isothiocyanate, a pungent compound found in wasabe and other mustard plants.

TRPA1 is a member of the transient receptor potential family of proteins, which in the vertebrates are primarily involved in temperature sensation. Most of these proteins were first identified by the same group of researchers who carried out this study. In 1996, they described TRPV1, which is activated by temperatures of 43°C, and which also contains a binding site for capsaicin, a molecule found in chili peppers. Subsequently, they identified the cold receptor TRPM8, which is activated by temperatures below approximately 26°C and also by menthol and peppermint. Interestingly, TRPA1 is activated by heat in fruit flies but not in the vertebrates. In this sense, the pit viper TRPA1 gene resembles that of the fruit fly more closely than that of mammals – not only is it heat-sensitive, but it is more sensitive to heat than any other known TRP protein, making it well-suited to its role as an infrared sensor. By contrast the version found in non-pit snakes is far less sensitive to heat, and is likely only useful for detecting changes in body surface temperature.

Evidently, TRPA1 has been adapted during the course of evolution, for use as an infrared sensor in some snake species. This adaptation would have involved changes in the DNA seqeunce of the gene, which led to a massive increase in the protein’s abundance within the pit viper trigeminal ganglion, and greater heat sensitivity. Both modern (pit vipers) and ancient (pythons and boas) snakes use TRPA1 for this purpose, even though they are separated from their common ancestor by some 30 million years, and have pit organs with very different sensitivities and architecture. This suggests that the ability to detect infrared radiation evolved independently in these two groups of snakes, by a process called convergent evolution.

Related:


Gracheva, E., et al. (2010). Molecular basis of infrared detection by snakes. Nature. DOI: 10.1038/nature08943.

Campbell, A. L. et al. (2002). Biological infrared sensing and imaging. Micron 33: 211-225. [PDF]

Comments

  1. #1 peacay
    March 17, 2010

    Thanks Mo, that’s fascinating stuff. The transcriptional profiling sounds to be an elegant strategy. I remember years ago hearing a talk from toxicologists describing their use of reverse bead chromotography to isolate target proteins of snake or spider neurotoxins and having a similar feeling about their (then) innovative approach to problem solving.