Temperature sensing across species

Abstract

The ability to detect changes in temperature is a fundamental sensory mechanism for every species and provides organisms with a detailed view of the environment. This review focuses on what is known of the neuronal and molecular substrates for thermosensation across species, focusing on the three robust model systems extensively used to study sensory signaling, the nematode Caenorhabditis elegans, the fruit fly Drosophila melanogaster, and the laboratory mouse. Nematodes migrate to thermal climes that are amenable to their survival, a behavior that is regulated primarily through a single sensory neuron. Additionally, nematodes "learn" to seek out this temperate zone based upon their prior experience, a robust model of learning and memory. Drosophila larvae also prefer select thermal zones that are optimal for growth and have also developed vigorous mechanisms to avoid unfavorable conditions. In mammals, the transduction mechanisms for thermosensation have been identified primarily due to the fact that naturally occurring plant products evoke distinct psychophysical sensation of temperature change. More remarkably, the elucidation of the molecular sensors in mammals, along with those in Drosophila, has demonstrated conservation in the molecular mediators of temperature sensation across diverse species.

Fig 1

The model for a C. elegans thermosensory neural circuit. Temperature-evoked activation of AFD stimulates the interneuron AIY, which in turn activates the integrating interneuron RIA. An unknown thermosensitive sensory neuron (X) activates AIZ, which in turn inhibits RIA. However, AIZ activity is reduced by AIY activation in this model circuit. The identity of genes known to be expressed in, and regulate the function of, the neurons in this circuit are labeled. Modified from Mori and Ohshima [5]

Fig 2

Drosophila TRP ion channels drive both larvae and adult flies to thermotax towards the optimum growth temperature or provide aversive signals from noxious stimuli. dTRPA1 and an unknown thermosensor drive animals towards the optimum clime, whereas Painless allows them to avoid noxious heat. dTRPA2 provides thermotolerance for temperatures near the noxious range. Aversive responses to high intensity noxious heat (>50°C) is mediated by an unknown thermosensor

Fig 3

Mammalian TRP ion channels detect a broad range of temperatures and their in vitro properties predict the thermal zones each channel potentially mediates. Moreover, many of these channels are activated by plant derivatives, which provide distinct sensations of temperature. Mouse models have shown that TRPV1, TRPV3, and TRPV4 are involved in thermosensing in vivo, whereas analyses of cold response in TRPA1-null mice are controversial