Converting Drosophobia into Drosophila

Abstract

Fruit flies seek water, but only when they are thirsty. And imbibing is rewarding only to water-deprived individuals. The effects of thirst on water seeking and on formation of associative memories of drinking water each are mediated by distinct sets of dopamine neurons that innervate restricted zones of the mushroom bodies in the fly brain.The name of the genus of small flies Drosophila has an etymological root in the Greek words drosos, meaning dew or moisture, and philia, meaning loving. Drosophila melanogaster has a long and storied history in the fields of genetics and behavioral neuroscience. Ironically, Drosophila under standard laboratory conditions innately avoid water and prefer a dry environment. In this issue of Nature Neuroscience, Lin et al. 1 uncover some of the key neurobiological underpinnings that cause D. melanogaster to seek water when thirsty-showing behavioral signs of liking water instead of avoiding it, thereby living up to their nameand to remember odors that were informative about where to quench their thirst. Notably, these neural mechanisms tap into the highly conserved dopamine system. Moreover, the naive water seeking and rewarding behaviors are each modulated by anatomically distinct and dedicated sets of dopaminergic neurons whose processes label different substructures of the mushroom body (MB), a known olfactory association center in insects 2,3 .In laboratory conditions, wild-type adult fruit flies exhibit a strong innate preference for dry conditions over wet 4 . This is likely an adaptation to avoid becoming caught in sticky food substrates. Lin et al. 1 demonstrated, however, that a 6-h deprivation, which makes the animals thirsty enough to seek water, will overcome this moisture avoidance. Investigation of the neural circuits under lying this simple plasticity in responses to water provides insight into mechanisms by which past experience and internal state modulate behavioral choices.The effect of thirst on water seeking is reminiscent of those of satiety on associative memory of sugar reward 3,5,6 . With sugar reward learning, hungry animals learn which odors were present during sugar presentation. And hungry animals are able to retrieve and express such memories. In contrast, well-fed animals don't remember which odors where present when food was offered 7,8 .The known mechanisms by which satiety modulates sugar learning provided an entry point to uncover neural mechanisms regulating naive and conditioned water-seeking preferences. Both aversive and appetitive olfactory memory in flies relies on the MB brain structure 3 , and specific sets of dopamine neurons provide instructive signals to MB both for aversive (electric shock reinforced) and appetitive (sugar reinforced) olfactory memory 9 . Lin et al. 1 decided to use water as a reward in place of sugar, with the assumption that this would likewise engage the MB olfactory learning center.In the conventional sugar reward-learning task, hungry flies are sequentially exposed to two different odorants, one of which is paired...