Temperature Integration at the AC Thermosensory Neurons inDrosophila

Abstract

Temperature sensation has a strong impact on animal behavior and is necessary for animals to avoid exposure to harmful temperatures. It is now well known that thermoTRP (Transient Receptor Potential) channels in thermosensory neurons detect a variable range of temperature stimuli. However, little is known about how a range of temperature information is relayed and integrated in the neural circuits. Here, we show novel temperature integration between two warm inputs via Drosophila TRPA channels, TRPA1 and Pyrexia (Pyx). The internal AC (Anterior Cell) thermosensory neurons, which express TRPA1, detect warm temperatures and mediate temperature preference behavior. We found that the AC neurons were activated twice when subjected to increasing temperatures. The first response was at ~25°C via TRPA1 channel, which is expressed in the AC neurons. The second response was at ~27°C via the 2nd antennal segments, indicating that the 2nd antennal segments are involved in the detection of warm temperatures. Further analysis reveals that pyx-Gal4 expressing neurons have synapses on the AC neurons and that mutation of pyx eliminates the second response of the AC neurons. These data suggest that AC neurons integrate both their own TRPA1-dependent temperature responses and a Pyx-dependent temperature response from the 2nd antennal segments. Our data reveal the first identification of temperature integration, which combines warm temperature information from peripheral to central neurons and provides the possibility that temperature integration is involved in the plasticity of behavioral outputs.

The Pyrexia transient receptor potential channel mediates circadian clock synchronization to low temperature cycles in Drosophila melanogaster

“…While pyx mutants do show a sharp activity increase after the temperature drop, they lack a synchronized activity peak in the warm phase, and their activity levels are evenly distributed over the cold and warm phase. Next, we tried to rescue the pyx 3 mutation by introducing a pyx-encoding transgene ( pyxGe pyx 3 ) that rescues both the pyx 3 heat-induced paralysis, as well as the AC neuron response at 278C [17,19]. Although pyx 3 rescue flies were still active during the cold phase, clear activity peaks are present towards the middle of the warm phase, indicating at least partial rescue of the temperature entrainment phenotype (figure 1d).…”

“…The TRP channel encoded by the pyrexia ( pyx) gene is directly activated by temperatures above 388C and protects flies from high temperature stress [17]. Surprisingly, pyx is also responsible for the response of temperature-sensitive anterior cell (AC) brain neurons, which regulate the temperature preference behaviour of adult fruitflies [18,19]. Pyx mediates the AC neuron response between 278C and 338C, suggesting that the Pyx channel may also be activated indirectly as has been shown for dTRPA1 [19,20].…”

“…Surprisingly, pyx is also responsible for the response of temperature-sensitive anterior cell (AC) brain neurons, which regulate the temperature preference behaviour of adult fruitflies [18,19]. Pyx mediates the AC neuron response between 278C and 338C, suggesting that the Pyx channel may also be activated indirectly as has been shown for dTRPA1 [19,20]. Here, we investigated the possibility that Pyx contributes to temperature entrainment of the fly clock.…”

Drosophila circadian rhythms in seminatural environments: Summer afternoon component is not an artifact and requires TrpA1 channels

“…Two pairs of AC neurons expressing TrpA1 appear to be the main internal thermosensors, but they also integrate temperature information from peripheral sensors (28). The AC sensors are activated by TrpA1 at ∼25°C, but a second response is observed at 27°C, which is generated by pyrexia-expressing neurons located in the second antennal segment and which synapse onto the AC neurons (28).…”

“…Two pairs of AC neurons expressing TrpA1 appear to be the main internal thermosensors, but they also integrate temperature information from peripheral sensors (28). The AC sensors are activated by TrpA1 at ∼25°C, but a second response is observed at 27°C, which is generated by pyrexia-expressing neurons located in the second antennal segment and which synapse onto the AC neurons (28). Interestingly, when we used the pyx mutant in our behavioral assay, we found no effect on the A component, mirroring the observation that pyx is also not required in a temperature preference assay (28), but we did observe a significant suppression of M and E. Painless is also expressed in the antennae, but again we did not observe any effect on the A component in pain mutants.…”