Identification and function of thermosensory neurons in Drosophila larvae

Abstract

Although the ability to sense temperature is critical for many organisms, the underlying mechanisms are poorly understood. Using the calcium reporter yellow cameleon 2.1 and electrophysiological recordings, we identified thermosensitive neurons and examined their physiologic response in Drosophila melanogaster larvae. In the head, terminal sensory organ neurons showed increased activity in response to cooling by < or =1 degrees C, heating reduced their basal activity, and different units showed distinct response patterns. Neither cooling nor heating affected dorsal organ neurons. Body wall neurons showed a variety of distinct response patterns to both heating and cooling; the diverse thermal responses were strikingly similar to those described in mammals. These data establish a functional map of thermoresponsive neurons in Drosophila larvae and provide a foundation for understanding mechanisms of thermoreception in both insects and mammals.

Temperature sensing across species

“…Sayeed and Benzer [30] found that when adult flies are placed upon a linear thermal gradient (18 to 31.5°C), these animals show a strong preference for ~24° C. However, unlike nematodes, flies cultivated or acclimatized at temperatures either above or below 24°C (29 or 18° C) still retain this partiality and thus do not reset their preferences based upon experience. Moreover, in a two-temperature choice paradigm, adult flies prefer 22 over 30° C. Similarly, Liu et al [31] showed that Drosophila larvae prefer to reside at 18°C when given the choice of this temperature versus either 11 or 30°C. In another experimental paradigm, larvae placed upon a thermal gradient from 27 to 41°C were shown to thermotax to the coolest temperatures, avoiding those above their optimal growth temperature [32].…”

“…Like in C. elegans, peripheral sensory neurons in larvae have been mapped anatomically and structurally and can be observed optically as they lie at the surface of the semi-transparent cuticular layer [31]. Sensory neurons fall into two classes: type I, which terminates in a single ciliated dendrite, and type II, which lack sensory cilia and extend multiple dendrites [23].…”

“…In larvae, distinct thermosensory responses have been observed in type I neurons in the terminal sensory organ and in type II multidendritic (md) neurons in the abdominal body wall [31,33,35]. Using transgenic larvae expressing the Ca 2+ reporter cameleon, Liu et al [31] observed increased intracellular Ca 2+ in only the terminal organ upon cooling from 18 to 10°C but not when temperatures were raised to 40°C.…”

“…Using transgenic larvae expressing the Ca 2+ reporter cameleon, Liu et al [31] observed increased intracellular Ca 2+ in only the terminal organ upon cooling from 18 to 10°C but not when temperatures were raised to 40°C. Extracellular electrical recordings in the terminal organ also uncovered substantial basal activity at room temperature, which increased with cooling and decreased when the larvae were warmed.…”

“…Extracellular electrical recordings in the terminal organ also uncovered substantial basal activity at room temperature, which increased with cooling and decreased when the larvae were warmed. In contrast, intracellular Ca 2+ largely decreased in type II md neurons upon cooling, whereas heating produced a mixed result with some cells exhibiting increased intracellular Ca 2+ , whereas others had no changes at all [31]. Using suction-electrode recordings from sectioned abdominal nerves, Tracey et al [33] observed increased spiking at temperature thresholds of ~28 and 38°C, suggesting the existence of at least two functionally distinct md thermoceptors in the abdominal wall.…”