Nervous control of blood flow microkinetics in the infrared organs of pit vipers

Goris, Richard C.; Nakano, Masato; Atobe, Yoshitoshi; Kadota, Tetsuo; Funakoshi, Kengo; Hisajima, Tatsuya; Kishida, Reiji

doi:10.1016/s1566-0702(00)00195-8

Cited by 17 publications

(29 citation statements)

References 17 publications

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“…We used minimum estimates of heat loss from the pit membrane; higher heat loss rates (e.g. due to perfusion of the pit membrane) (Goris et al, 2000) result in a faster response, but require increased receptor temperature sensitivity as a given stimulus creates a smaller membrane temperature change. The color scale steps correspond to a contrast of 0.001°C, equal to the most sensitive discrimination suggested in a neurophysiological study (Bullock and Diecke, 1956).…”

Section: Pit Membrane Images Of Field and Laboratory Scenesmentioning

confidence: 99%

“…The color scale steps correspond to a contrast of 0.001°C, equal to the most sensitive discrimination suggested in a neurophysiological study (Bullock and Diecke, 1956). For comparison of our results with published laboratory estimates of distances at which a mouse can be detected (Ebert and Westhoff, 2006;Goris et al, 2000;Kardong, 1986;Safer and Grace, 2004;Stanford and Hartline, 1984), we generated slow-frame 60degϫ160deg thermographic source movies using Matlab scripts. These simulate, first, a high-temperature quasi-point source such as a soldering iron or cigarette (e.g.…”

Section: Pit Membrane Images Of Field and Laboratory Scenesmentioning

confidence: 99%

“…These simulate, first, a high-temperature quasi-point source such as a soldering iron or cigarette (e.g. Goris et al, 2000;Stanford and Hartline, 1984) passing right to left in front of the snake. Second, we simulated BALB/c mice at various distances in a room temperature environment (e.g.…”

Section: Pit Membrane Images Of Field and Laboratory Scenesmentioning

confidence: 99%

“…The 60degϫ160deg source thermograms first simulate a high-temperature quasi-point source (e.g. Goris et al, 2000;Stanford and Hartline, 1984) passing right to left in front of the snake. As expected, the image of the quasi-point source is distinct and approximates the spread function.…”

Section: Image-forming Characteristics Laboratory Environments With Umentioning

confidence: 99%

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Analytical methods for the geometric optics of thermal vision illustrated with four species of pitvipers

Bakken

Colayori

Duong

2012

Journal of Experimental Biology

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SUMMARYThe pitviper facial pit is a pinhole camera-like sensory organ consisting of a flask-shaped cavity divided into two chambers by a suspended membrane. Neurophysiological studies and simplified optical models suggest that facial pits detect thermal radiation and form an image that is combined with visual input in the optic tectum to form a single multispectral image. External pit anatomy varies markedly among taxonomic groups. However, optical function depends on unknown internal anatomy. Therefore, we developed methods for relating anatomy to optical performance. To illustrate, we constructed detailed anatomical models of the internal anatomy of the facial pits of four individuals of four pitviper species using X-ray tomography sections of fresh material. We used these models to define the point spread function, i.e. the distribution of radiation from a point source over the pit membrane, for each species. We then used optical physics, heat transfer physics and computational image processing to define the thermal image formed on the pit membrane for each species. Our computed pit membrane images are consistent with behavioral observations if the sensitivity of membrane receptors equals the most sensitive (ca. 0.001°C) laboratory estimates. Vignetting (variation in optical aperture size with view angle) and differences between body and environmental temperatures can create temperature variation across the membrane that greatly exceeds image temperature contrasts, potentially impairing imaging. Spread functions plotted versus source point azimuth and elevation show distinct patterns that suggest new research directions into the relationships among the optical anatomy, ecology, behavior and sensory neurophysiology of pitvipers. Supplementary material available online at

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Section: Pit Membrane Images Of Field and Laboratory Scenesmentioning

confidence: 99%

Section: Pit Membrane Images Of Field and Laboratory Scenesmentioning

confidence: 99%

Section: Pit Membrane Images Of Field and Laboratory Scenesmentioning

confidence: 99%

Section: Image-forming Characteristics Laboratory Environments With Umentioning

confidence: 99%

See 2 more Smart Citations

Analytical methods for the geometric optics of thermal vision illustrated with four species of pitvipers

Bakken

Colayori

Duong

2012

Journal of Experimental Biology

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“…There is evidence of multispectral image formation; neural signals from the facial pit are integrated with those from the visual system (Hartline et al, 1978). Workers have explored aspects of this sensory system ranging from the molecular activation (Gracheva et al, 2010), the role of the vascular system (Goris et al, 2000) and the mechanics of neural integration within the trigeminal system (Stanford and Hartline, 1984). Despite these advances, little is known about the adaptive role of this system in the behavioral ecology of the snake.…”

Section: Introductionmentioning

confidence: 99%

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

Kohl

Colayori

Westhoff

et al. 2012

Journal of Experimental Biology

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SUMMARYRecent work published in the accompanying paper used a combination of 3D morphological reconstruction to define optical spread functions and heat transfer physics to study how external heat energy would reach the sensory membrane within the facial pit of pitvipers. The results from all of the species examined indicated asymmetric directional sensitivity, e.g. the pit would preferentially respond to stimuli located below and behind the snake. The present study was intended as a test of these findings through a quantitative neurophysiological analysis of directional sensitivity in the facial pit of the western diamondback rattlesnake, Crotalus atrox. An infrared emitter was positioned through a coordinate system (with varying angular orientations and distances) and the response it evoked measured through neurophysiological recordings of a trigeminal nerve branch composed of the afferents from the sensory membrane of the facial pit. Significant differences were found in the strength of the membraneʼs neural response to a constant stimulus presented at different orientations (relative to the facial pit opening) and over different distances. The peak sensitivity (at 12deg above and 20deg in front of the facial pit opening) was in good agreement with the predicted directional sensitivities based on optical spread functions and 3D topography. These findings support the hypothesis that the topography, and functional performance, of the facial pit has undergone an adaptive radiation within the pit vipers, and that differences in the behavioral ecology of the pit vipers (i.e. terrestrial versus arboreal) are reflected within the facial pits.

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Ultrastructure of the capillary pericytes and the expression of smooth muscle α-actin and desmin in the snake infrared sensory organs

et al. 2000

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The infrared sensory membranes of pit organs of pit vipers have an extremely rich capillary vasculature that forms many vascular loops, each serving a small number of infrared nerve terminals. We clarified the ultrastructure of capillary pericytes in the pit membranes by scanning and transmission electron microscopy, and examined the immunoreactivity in their cytoplasm to two contractile proteins: smooth muscle α‐actin (SM α‐actin) and desmin. The capillary pericytes had two major cytoplasmic processes: thickened primary processes that radiate to embrace the endothelial tube and flattened secondary processes that are distributed widely on the endothelium. Coexpression of SM α‐actin and desmin was observed in the pericytes of entire capillary segments, and SM α‐actin was characterized by prominent filament bundles directed mainly at right angles to the capillary long axis. This expression pattern was different from that of capillary pericytes of the scales, where SM α‐actin was expressed diffusely in the cytoplasm. In a series of electron microscopic sections, we often observed the pericyte processes depressing the endothelial wall. We also observed a close relationship of the pericytes with inter‐endothelial cell junctions, and pericyte processes connected with the endothelial cells via gap junctions. From these findings, we surmised that capillary pericytes in the pit membrane have a close functional relationship with the endothelium, and through their contractile and relaxing activity regulate capillary bloodflow to stabilize production of infrared nerve impulses. Anat Rec 260:299–307, 2000. © 2000 Wiley‐Liss, Inc.

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Nervous control of blood flow microkinetics in the infrared organs of pit vipers

Cited by 17 publications

References 17 publications

Analytical methods for the geometric optics of thermal vision illustrated with four species of pitvipers

Analytical methods for the geometric optics of thermal vision illustrated with four species of pitvipers

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

Ultrastructure of the capillary pericytes and the expression of smooth muscle α-actin and desmin in the snake infrared sensory organs

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