You’re Hot and You’re Cold

By Elizabeth Marin

Anyone who has reached for an extra jumper on a cold morning or sought the shade of a tree on a hot afternoon realises that even warm-blooded animals prefer fairly narrow ranges of temperature and humidity. Mammals have sensory neurons that innervate the skin, among other organs, and express specific temperature-sensitive members of the TRP (transient receptor potential) ion channel family. These include TRPM8, which is crucial for detecting cool to cold environmental temperatures as well as evaporative cooling of the cornea, and TRPV1, which appears to be involved in acute heat sensation as well as maintenance of appropriate core body temperature [1]. However, like many other animals, humans appear to lack hygroreceptors – that is, specific sensory organs to detect humidity. Instead, information appears to be integrated from various classes of sensory neurons in the skin that respond to evaporative cooling and mechanical pressure and friction [2].

Small poikilothermic (cold-blooded) organisms, such as the fruit fly, are especially vulnerable to environmental temperature and humidity because of their high surface area-to-volume ratio. In particular, they are at serious risk of desiccation when it’s hot and dry and of immobilisation when it’s too cold. They exhibit clear species-specific preferences [3,4] and have dedicated thermoreceptors and hygroreceptors which enable them to navigate away from dangerous extremes. Like the olfactory sensory neurons discussed in an earlier post, these thermosensitive and hygrosensitive neurons have dendrites in tiny structures called sensilla. However, these sensilla have a different shape than olfactory sensilla and are located in specialised structures of the third antennal segment. In flies, three thermosensory sensilla, each containing one hot-responsive and one cold-responsive sensory neuron, are housed in each protruding arista [5], while hygrosensory sensilla containing triads of neurons sensitive to dry, moist, or cooling air line the protected chambers of an invagination called the sacculus [6,7] (Fig. 1).

Figure 1: Peripheral anatomy of the thermosensory and hygrosensory systems in Drosophila. Three hot-responsive and three cold-responsive sensory neurons are housed in each arista at the base of the third antennal segment. A three-chambered invagination called the sacculus contains specialised sensilla that house combinations of hygrosensory neurons, including triads of cooling-, dry-, and moist air-responsive cells. EM image credit: CSIRO

Insect olfactory sensory neurons typically express just one of many possible odorant receptors (ORs), seven transmembrane proteins that likely form heteromers with a broadly expressed family member, ORCO. Unlike vertebrate olfactory GPCRs, insects ORs do not feature conventional binding sites for G proteins, but their ability to trigger depolarisation (firing) of the sensory neurons may still involve a second messenger cascade [8]. Alternatively, ligand-gated ionotropic receptors (IRs) are used in some chemosensory neurons in the taste and olfactory systems [9,10,11]. The molecular mechanisms underlying thermosensation and hygrosensation are currently less clear but generally involve the co-expression of multiple IRs, a couple of which are likely to function as co-receptors while the others provide specificity [11,12,13,4,6,7]. Ligands have not yet been identified for the IRs that are narrowly expressed in antennal thermosensory and hygrosensory neurons [11]; perhaps changes in temperature or humidity are sufficient to alter neuronal excitability via sensillar swelling and dendrite expansion/compression, as has been suggested for cockroach hygroreceptors [14]. Two TRP ion channel genes, nanchung and water witch, have also been implicated in neuronal responses to dry and moist air, respectively [15].

Like olfactory sensory neurons, thermosensory and hygrosensory neurons send their axons through the antennal nerve to the antennal lobe, where they converge in one of five ventral posterior (VP) glomeruli dedicated to hot-, cold-, dry-, moist-, or cooling air [5,11] (Fig. 2A). There they synapse on the dendrites of projection neurons (PNs) that relay information to higher brain centres. As for olfactory neurons, these target regions include the mushroom body calyx and lateral horn, but also additional brain neuropils such as the posterior lateral protocerebrum and the posterior slope [16,17] (Fig. 2B). In particular, at least one thermosensory PN relays information from VP3 (the cold glomerulus) to a substructure of the mushroom body called the lateral accessory calyx, which appears to be specialised for thermosensory information [18,17,19]. Furthermore, several PNs appear to integrate information from two or more VP glomeruli [17,7].

Figure 2: A. Reconstructions from EM traces of thermosensory and hygrosensory neurons revealing five ventroposterior glomeruli in the antennal lobe: VP1 (cooling), VP2 (hot), VP3 (cold), VP4 (dry), and VP5 (moist). B. Brain neuropils innervated by thermosensory and hygrosensory PNs: antennal lobe (AL), mushroom body calyx (MB), lateral accessory calyx (LAC), lateral horn (LH), posterior lateral protocerebrum (PLP), posterior slope (PS). The black trace represents a cold-activated PN that relays information from VP3 to the LAC.

What happens next? At this time, little has been published regarding the targets of these PN classes in the adult fly. It seems plausible that, similar to the olfactory system, Kenyon cells receiving inputs from these PNs function with MBONs (Mushroom Body Output Neurons) and DANs (dopaminergic neurons) to enable the association of specific levels of temperature and humidity (or changes in those levels) with other experiences. In the lateral horn, there may be specific regions that receive thermosensory and hygrosensory inputs, perhaps integrating them with other sensory cues, and ultimately facilitate appropriate behavioural responses. Using a connectomic approach to identify the synaptic partners of thermosensory and hygrosensory PNs, we aim to reconstruct these circuits and develop testable models for their function.

A more detailed synthesis of our current knowledge concerning insect thermosensation and hygrosensation can be found here.

References

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