The Python pit organ: imaging and immunocytochemical analysis of an extremely sensitive natural infrared detector¹

Abstract

The Python infrared-sensitive pit organ is a natural infrared imager that combines high sensitivity, ambient temperature function, microscopic dimensions, and self-repair. We are investigating the spectral sensitivity and signal transduction process in snake infrared-sensitive neurons, neither of which is understood. For example, it is unknown whether infrared receptor neurons function on a thermal or a photic mechanism. We imaged pit organs in living Python molurus and Python regius using infrared-sensitive digital video cameras. Pit organs were significantly more absorptive and/or emissive than surrounding tissues in both 3–5 μm and 8–12 μm wavelength ranges. Pit organs exhibited greater absorption/emissivity in the 8–12 μm range than in the 3–5 μm range. To directly test the relationship between photoreceptors and pit organ infrared-sensitive neurons, we performed immunocytochemistry using antisera directed against retinal photoreceptor opsins. Retinal photoreceptors were labeled with antisera specific for retinal opsins, but these antisera failed to label terminals of infrared-sensitive neurons in the pit organ. Infrared-receptive neurons were also distinguished from retinal photoreceptors on the basis of their calcium-binding protein content. These results indicate that the pit organ absorbs infrared radiation in two major atmospheric transmission windows, one of which (8–12 μm) matches emission of targeted prey, and that infrared receptors are biochemically distinct from retinal photoreceptors. These results also provide the first identification of prospective biochemical components of infrared signal transduction in pit organ receptor neurons.

Introduction

Artificial infrared image-forming devices have many applications. While artificial infrared (IR)-sensing technology has improved dramatically in recent years (Wolfe and Zissis, 1985), there are many reasons to seek even greater improvements in this technology. Highly sensitive image-forming IR detectors are bulky, complicated (often necessitating frequent repair or modification), and costly to maintain. In order to function with reasonable sensitivity they often must be supercooled, adding to the their bulk, cost, and potential failure. Natural infrared detectors, however, are microscopic in dimensions, self-repairing, and function at normal ambient temperatures. Perhaps most importantly, snake infrared detectors may be an order of magnitude more sensitive than the best artificial ones (Bullock and Diecke, 1956). The system reportedly distinguishes as little as a 0.003°C change in temperature of water flowing over the pit organ (Bullock and Diecke, 1956). An analysis of the extremely sensitive snake image-forming IR detector should provide insight for the development of new technologies that will result in greater sensitivity, operation at higher temperatures, and reductions in size and weight.

Snakes of the families Boidae (boas and pythons) and Viperidae (pitvipers, including the rattlesnakes) form spatial images of their thermal environments (Hartline et al., 1978) using highly sensitive infrared receptors which form an array of infrared-sensitive neuronal terminals just beneath the epidermis of the pit organ (Fig. 1). Both the infrared and visual systems (along with chemical and tactile cues) are involved in prey detection by boids and pitvipers, but prey detection and localization do not require the eyes. A congenitally blind rattlesnake accurately targeted prey with an efficiency and precision comparable to sighted animals of the same species (Kardong and Mackessey, 1991). When this snake's pit organs were covered, the snake struck prey with much less frequency and accuracy, indicating that the infrared detectors play an important role in prey detection and localization.

The spectral sensitivity of pit organ infrared receptors has never been investigated. Previous studies have employed a variety of stimulation devices, including the human hand, visible light sources, and lasers of various wavelengths and intensities (sometimes of very high intensity; see for example Terashima and Goris, 1977). Furthermore, essentially nothing is known about the mechanism of IR signal transduction. A better understanding of the properties of these cells may lead to the development of smaller and more sensitive artificial infrared-sensing devices.

We report here that the Python pit organ absorbs both in the 3–5 and 8–12 μm windows of atmospheric infrared transmission, and that absorption may be greater in the 8–12 μm region. We also show that pit organ infrared receptor cells are biochemically distinct from retinal photoreceptors, and identify two potential components of infrared signal transduction.