Microvasculature of crotaline snake pit organs: Possible function as a heat exchange mechanism

Abstract

The infrared sensory membranes of the pit organs of pit vipers have an extremely rich capillary vasculature, which has been noted passim in the literature, but never illustrated or studied in detail. We rendered the pit vasculature visible in various ways, namely, by microinjection of India ink, by a combination of ink and succinate dehydroge-nase staining, and by making resin casts for scanning electron microscope study. We also used transmission electron microscopy for identifying the types (arterioles, venules, capillaries) of blood vessels. Then we compared the pit vasculature with that of the retina and the dermis. Good visualization of the vasculature was obtained with both ink and resin injection. Arterioles, venules, and capillaries could be distinguished with all methods used. The monolayer vasculature was denser in the pit membrane than in the retina or skin. Each loop of the network enclosed a small number of infrared receptors so that all receptors were in contact with a capillary on at least one side. The forward-looking areas of the pit had a denser network than side-looking areas. Since infrared rays cause nerve impulses by raising the temperature of individual receptors, the capillary network functions not only as a supplier of energy but also as a cooling mechanism to reduce afterimages. Thus the denser network in the forward-looking areas causes these areas to be more sensitive and have better image resolution than the rest of the membrane.

The imaging properties and sensitivity of the facial pits of pitvipers as determined by optical and heat-transfer analysis

“…10° in the forward direction (see also DeSalvo and Hartline, 1978). The importance of forward imaging is indicated by a higher density of receptors and associated blood vessels on the portion of the membrane corresponding to objects directly in front of the head (Amemiya et al, 1999;Goris and Nomoto, 1967;Goris and Terishima, 1973). Viewed from the forward direction, the external aperture is higher than it is wide (Fig.·1A) and the optical spread function is therefore subelliptical.…”

Directional sensitivity in the thermal response of the facial pit in western diamondback rattlesnakes (Crotalus atrox)

“…In Crotalus the receptors in the facial pit's sensory membrane contribute to three branches of the trigeminal nerve (Fig.3); our anatomical results suggest that C. atrox is similar to other pit vipers in both the position and minimal overlap of the three respective fields on the sensory membrane (Bullock and Fox, 1957;Amemiya et al, 1999). This study recorded from only one (the superficial maxillary) of these three branches.…”

“…Though we cannot provide a definitive explanation for this discrepancy, we hypothesize that it is due to heterogeneous distribution of receptor organs in the posterior portion of the sensory membrane. The spread functions were created assuming a homogeneous spatial distribution of receptors; previous workers have suggested that there is an area of increased receptor density in the posterior portion of the membrane (Amemiya et al, 1999). A localized cluster of increased receptor density could function like a thermal fovea; in any case it would increase local sensitivity that could skew the experimental results relative to the biophysical predictions.…”

Respiratory cooling in rattlesnakes

“…Although an entire class of infrared imaging cameras employs cryogenic elements, de Cock Buning (1984) has argued that cooling of the pit organs would not increase their thermal resolution. However, a complex network of capillaries on the pit membrane is at least suggestive of a heat exchanger, in which case temporal resolution of the pit organ may depend on the periodic influx of cooled blood to ''erase'' thermal afterimages (Amemiya et al, 1999). A second possible function of cool pits relates to their operational temperature range.…”