I.R. Image of a small dog

1. Thermoreception Some general points: • Like other radiation, objects can reflect or emit IR waves. Temperature determines spectrum of emission. • Since absorption of I.R. by biological tissues leads to heating, I.R. can be associated with ‘light’ or ‘heat’. • A great deal of information available in I.R. I.R. Image of a small dog

2. From Wikipedia: The infrared part of the electromagnetic spectrum covers the range from roughly 300 GHz (1 mm) to 400 THz (750 nm). It can be divided into three parts: Far-infrared, from 300 GHz (1 mm) to 30 THz (10 μm). The lower part of this range may also be called microwaves. This radiation is typically absorbed by so-called rotational modes in gas-phase molecules, by molecular motions in liquids, and by phonons in solids. The water in the Earth's atmosphere absorbs so strongly in this range that it renders the atmosphere effectively opaque. However, there are certain wavelength ranges ("windows") within the opaque range which allow partial transmission, and can be used for astronomy. The wavelength range from approximately 200 μm up to a few mm is often referred to as “sub-millimeter” in astronomy reserving far infrared for wavelengths below 200 μm. Mid-infrared, from 30 to 120 THz (10 to 2.5 μm). Hot objects (black-body radiators) can radiate strongly in this range. It is absorbed by molecular vibrations, that is, when the different atoms in a molecule vibrate around their equilibrium positions. This range is sometimes called the fingerprint region since the mid-infrared absorption spectrum of a compound is very specific for that compound. Near-infrared, from 120 to 400 THz (2,500 to 750 nm). Physical processes that are relevant for this range are similar to those for visible light.

3. Can partition thermoreception into submodalities: distance cutaneous/contact internal … for both invertebrates & vertebrates

4. First example of invertebrate distance thermoreception: The Jewel Beetle, Melanophila acuminata Jewel Beetles fly from many miles following the infrared radiation of forest fires to join a mating frenzy. Beetles mate while the fire is burning, then females oviposit in smoldering bark. The burnt trees no longer have defense mechanisms, so larvae have ample food supply.

5. M. acriminata has two metathoracic pit organs next to the coxal cavities on the metathoracic legs. During flight, beetles raise their legs exposing the pit organs to the I.R. source.

6. The ideal wavelength to attract M. acuminata is the same wavelength radiated from forest fires.

7. How it works… Jewel beetle pit organs contain densely packed sensilla ( approx. 60 domed sensilla), each associated with a wax gland. Therefore the pit is filled with wax filaments. The sensilla absorb I.R. radiation at the peak emission wavelength of forest fires (2.4 - 4.0 µm). Infrared sensilla resemble and are surrounded by hair mechanoreceptors, which they may have derived from. Each sensillum consists of a mesocuticular sphere, an endocuticular stalk, and an epidermal sensory neuron. Every sphere (approx. 50-100 per sensillum) is innervated by a single bipolar neuron (lots of convergence!). Axons project to the beetle’s ventral nerve cord. The spherule is filled with a highly concentrated solution of organic molecules containing particular CH-CO bonds. The bond structure absorbs strongly in the I.R. When IR radiation is absorbed the whole structure vibrates, and the vibration warms the solution. The conversion of radiation into heat causes a small change in the volume of the spherule. Only 60 µW/cm2 is enough energy to cause a volume change of 1.0 nm. The volume change then deforms the dendritic tip and triggers a nerve impulse. The source of IR radiation can be up to 50 miles away… and the beetle only needs 1.0 ms of radiation to determine azimuth! (data next slide)

8. Only a very brief exposure is necessary to achieve a neural response.

9. How spectral sensitivity is measured

10. Invertebrate distance thermoreception example 2: Australian Fire Beetles Merimna atrata & Acanthocnemus nigricans (M. atrata and A. nigricans are not studied as extensively as M. acuminata, but are known to posses organs capable of detecting I.R. radiation.) . M. atrata has four abdominal receptors each innervated by a thermosensitive multipolar neuron. The organs are analogous to labial thermosensor organs in boid snakes. The primary dendrite branches into more than 800 closely packed terminal endings which contain large a number of mitochondria. Warming causes increased receptor activity. Lowest threshold was found at 40mW-cm-2, latencies of 47 ms. M. atrata is unique among insects for these receptors.

11. A. Nigerians • A. nigricans I.R. organs act as thermoreceptors; include an air-filled inner chamber similar to pit vipers. Thermoreceptor organ

13. Invertebrate distance thermoreception example 3: Triatoma infestans (major vector of Chagras disease)

14. Haematophagus insects such as Triatoma infestans use I.R. radiation combined with olfaction to target prey. • T. infestans leave refuge at night to seek blood. • Thermal senses reside mainly in antennae. • Dominant role is for short distance orientation. • Over short distance warmth stimulates active (not at rest) insect. • Warmth is the major cause of extension of proboscis.

15. Invertebrate “distance” thermosense example 4: Pachliopta aristolochiae • Pachliopta aristolochiae (butterfly) • Sensitive to heat damage while sunbathing • thermoreceptors located on darkly colored wings and antennae used for behavioral thermoregulation: • Wing orientation adjustment • Movement to shade • Warm receptors compute slope of warming (rate). • Above a set-point, warming rate elicits an initial response of slow wing closing movements. • Higher rate of warming rates, (solar radiation exposure > 100mW/cm2 , elicit violent wing fluttering movements.

16. Absorption spectrum of butterfly thermoreceptors

17. References H. Schmitz, H. Bleckmann, J Comp Physiol A (1998) 182: 647-657 E. Gigl, H. Tichy, J Comp Physiol A (2001) 187: 467-475 Gretchen Jehle jehle@lamar.colostate.edu http://web.neurobio.arizona.edu/gronenberg/nrsc581/thermo/thermoreception.htm

18. Vertebrate Distance Thermoreception I.R. detectors of pit vipers

21. Vertebrate thermoreception NOT associated with thermoregulaton: Snake pit organ Minimal thickness!

23. Performance of pit organ

25. Vampire Bats Vampire bats – members of the New World Leaf-nosed bats, the Phyllostomidae. • 3 species of living vampire bats - Desmodus rotundus  the Common Vampire bats • Found in South and Central America. • Fossils of three other species show they were more widespread historically but still confined to the New World. Unique characteristic of vampire bats – they are “sanguinary” (meaning – blood thirsty, or, blood sucking) A hairy-legged vampire bat. One of the three species of vampire bats, it has a relatively short, stout jaw useful in administering a slicing wound to its prey. (Wilson, Don E. Bats in Question: The Smithsonian Answer Book. Washington and London: Smithsonian Institution P, 1997. p. 8)

26. The gloved hand gives an excellent impression of the relative size of this female Common Vampire Bat. (Fenton, Brock M. Bats. Oxford & NY: Facts on File, 1992. p.150) Misc Info on Desmodus rotundus • Physical Characteristics: • Dark grayish-brown fur color with a paler underside. • Pointed ears, larger thumb and 20 teeth. • No tail • Size – length: 6.6 – 8.8 cm; weight: ~40 grams • Approximate life span: ~9 years (wild) • up to 19 years (captivity) • Reproduction: • sexual maturity: 9-10 months • gestation: 205 - 214 days • usually single births • feed on regurgitated blood at 2 months, forage for blood themselves at 4 months • Habitat: • Arid and humid regions of the tropics and subtropics; • Usually reside in caves, but might also occupy hollow trees, old wells, mine shafts, abandoned buildings Though larger than most of bats of the world temperate zones, vampire bats are much smaller than frugiverous Flying Foxes (1.5kg). Horror movie depictions of vampire bats often use flying foxes as models because larger bats are easier to photograph. This contributes to the public perception of vampire bats as large, terrifying animals. But animals that feed on blood, whether they are insects, leeches or bats, tend to be small because blood is a precious commodity and hard to obtain in large amounts.

27. Diet and Behavior of Desmodus rotundus Vampire bats fly low, only about 3 feet off the ground, probably to improve thermodetection of terrestrial mammalian prey: horses, burros, cattle, occasionally humans It takes up to two hours to fill up one bat! Process: • selection of animal (IR + echolocation… plus chemo?) • (ii) licking site with tongue • (iii) shaving or shearing of hair • (iv) biting off a circular piece of skin A profile picture of a Common Vampire Bat. The sloping face and muzzle that make it easy for the bat to approach and bite its prey. (Fenton, Brock M. Bats. Oxford and NY: Facts on File, 1992. p. 153)

28. So do Desmodus rotundus have IR sensory mechanism? Thermosensory organs in bats very similar in gross morphology to structure to the pit organs in rattlesnakes (Kurten and Schmidt, 1982)…. See next slide for more detail. Desmodus rotundus: the details of the face and nose-leaf. The bat's heat detecting system is located on the nose-leaf. Also evident are the tips of the upper incisors, the teeth used to make the feeding wound. (Fenton, Brock M. Bats. Oxford and NY: Facts on File, 1992. p. 152)

29. Front view: Arrows indicate the three nasal pits. Nasal structure of Desmodus rotundus have noticeable depressions – resembling the pit organs of rattlesnakes. The Nasal Structure – A Description • The nasal structure have two distinct parts • (i) central nose leaf with nostrils, and, • (ii) a separate semicircular ring of pads – the pit organs are situated here. • There are a total of 3 pit organs • one apical and two lateral pits Lateral pits – 1mm wide, 1mm deep; at 45° angle right and left of the median plane of the animal. Apical pit – slightly raised towards the nose leaf; directed upward and forward. The position of the pit organs likely to give stereoscopic sense of IR information. Additional advantages in the nasal structure to help in prey detection: The nose leaf is also very flexible and can be made to orient towards the direction of the prey for better detection. The bat can change the apertures of the nasal pits by altering the shape of the central nose (controls the amount IR entering through the aperture)

30. Accessory structures for thermodetection? • The nose leaf and the pits are hairless – less interference with I.R. detection? • Very distinct glandular and gland-free zone from pad to pit floor. Significance? • Nose leaf has a striated muscle and connective tissue layer all around right underneath the skin but the pit regions have only a dense layer of connective tissue – direct pit toward I.R. source? • Not many blood vessels in the connective tissue region; none in the pit floor – reduce thermal background noise • (see Campbell A L, et al.,2002 for ultrastructure)

31. facial thermogram The picture here (Kurten and Schmidt, 1982) shows facial surface temperature differences of a vampire bat. The region surrounding the eyes appear to be the warmest region. The pit area is about 9°C lower in temperature than that around the nose, and the nose cooler than the surrounding face! The nose and the pit organs are thermally isolated – allows the pit organs to detect temperature changes in the environment without any possibility of being affected by body temperature. • Excellent insulation from body heat • pre-requisite for an efficient sense of thermal radiation (the lower the temperature of the sensory organ, the better the detector).

32. Behavioral experiments with vampire bats Train bats to respond to artificial I.R. sources (fly to side 1 or side 2 of a room to get a food reward. To measure the bat’s thermo-detection threshold the radiation level was lowered each day in a gradual manner. Behavioral threshold of 0.3x10-4 W/cm2 (Kurten and Schmidt, 1982)

33. Smallest amount of radiation detected by the vampire bats  0.5 × 10-4 W/cm2 Humans radiate about 0.8 × 10-4 W/cm2 (approx) at a distance of 8 cm The threshold distance for a vampire bat to recognize humans is between 13 and 16 cm = very close range!! So what is the Vampire Bat’s Thermo-detection Range and Threshold?

34. A comparison between different species with IR imaging & sensory organs and thermo-receptors [Campbell A L, Naik R R, Soward L and, Stone M O. Biological Infrared Imaging and Sensing. Micron 33:211-225]

35. Possible region within the brain of the vampire bats for processing infra-red information A comparative study of the brain of different species of bats (vampire bats and others), reveals a specific brain stem nucleus in Desmodus rotundus not found in other species of bats. Kishida R, Goris R C, Terashima S, Dubbeldam J L (1984) The morphological organization of the nucleus is similar to the infrared sensing region of the brain of infrared sensitive snakes. This nucleus in the bats is… • situated in the descending trigeminal tract • crescent shaped along the tranverse section • clearly demarcated within the brain by the myelinated fiber bundle of the descending trigeminal tract and of the tractus spiro cerebelarris (sc) (snakes: The lateral descending trigeminal system (tract and nucleus), which is situated lateral to the common descending tract in the medulla, receive trigeminal fibers from the infra-red sensory organs) So far, however, no direct link has been demonstrated between the special vampire bat nucleus and their infrared sensory nasal pit organs

36. Schematic diagram showing the transverse section of a vampire bat brain. The red-circled areas depict the special nucleus by the descending trigeminal tract (DV). Tractus spiro cerebelarris SC (in diagram)

37. Vertebrate cutaneous thermoreception Some general points… • All neurons are thermosensitive to some degree • For example, mechanoreceptors are weakly activated by cold, giving cold objects the illusion of greater mass. • Neurons specialized for thermoreception have greater change in firing rate for a given temperature change compared with non-thermoreceptors • Warm- and cold-sensitive neurons • No specific histological specialization; undifferentiated nerve endings • No accessory organs • Size differential in thermoreceptive neurons • Warm: C-fibers - unmyelinated, 1 m dia. or less • Cold: A fibers - myelinated, 1.5 - 3 m dia.