Dehydrated Drosophila melanogaster track a water plume in tethered flight.

Perception of sensory stimuli can be modulated by changes in internal state to drive contextually appropriate behavior. For example, dehydration is a threat to terrestrial animals, especially to Drosophila melanogaster due to their large surface area to volume ratio, particularly under the energy demands of flight. While hydrated D. melanogaster avoid water cues, while walking, dehydration leads to water-seeking behavior. We show that in tethered flight, hydrated flies ignore a water stimulus, whereas dehydrated flies track a water plume. Antennal occlusions eliminate odor and water plume tracking, whereas inactivation of moist sensing neurons in the antennae disrupts water tracking only upon starvation and dehydration. Elimination of the olfactory coreceptor eradicates odor tracking while leaving water-seeking behavior intact in dehydrated flies. Our results suggest that while similar hygrosensory receptors may be used for walking and in-flight hygrotaxis, the temporal dynamics of modulating the perception of water vary with behavioral state.

Acuity and summation strategies differ in vinegar and desert fruit flies.

An animal's vision depends on terrain features that limit the amount and distribution of available light. Approximately 10,000 years ago, vinegar flies (Drosophila melanogaster) transitioned from a single plant specialist into a cosmopolitan generalist. Much earlier, desert flies (D. mojavensis) colonized the New World, specializing on rotting cactuses in southwest North America. Their desert habitats are characteristically flat, bright, and barren, implying environmental differences in light availability. Here, we demonstrate differences in eye morphology and visual motion perception under three ambient light levels. Reducing ambient light from 35 to 18 cd/m2 causes sensitivity loss in desert but not vinegar flies. However, at 3 cd/m2, desert flies sacrifice spatial and temporal acuity more severely than vinegar flies to maintain contrast sensitivity. These visual differences help vinegar flies navigate under variably lit habitats around the world and desert flies brave the harsh desert while accommodating their crepuscular lifestyle.

Diversity of visuomotor reflexes in two Drosophila species.

For adaptive behavior, an organism must identify and assign subjective value to salient sensory information, but what stimuli are salient could change depending upon the local features of the environment. Insects such as fruit flies (Drosophila), for example, rely on olfactory cues to locate food and oviposition sites. But not all Drosophila species find the same stimuli to be salient: for example, four geographically isolated populations of Drosophila mojavensis, which feed and oviposit on necrotic cacti, show olfactory-driven behavioral preferences for host cacti specific to the local environment of each population [1,2]. We wondered whether visual features specific to certain environments could drive divergent visuomotor responses. We compared the visuomotor reflexes of D. melanogaster, a cosmopolitan generalist found in moderately dense visual environments, with D. mojavensis, a cactophilic specialist found in comparatively sparse visual landscapes. We found that, like D. melanogaster, D. mojavensis steer towards long vertical stripes, such as landscape features [3], but in contrast to D. melanogaster's aversion to small objects [3], D. mojavensis find small objects attractive or of neutral value.

Group behavior: social context modulates behavioral responses to sensory stimuli.

A new study reveals an unanticipated role for social context in driving group behavior of a solitary species to a sensory stimulus and is mediated by mechanosensory neurons signaling touch interactions among individuals.

Olfactory neuromodulation of motion vision circuitry in Drosophila.

It is well established that perception is largely multisensory; often served by modalities such as touch, vision, and hearing that detect stimuli emanating from a common point in space; and processed by brain tissue maps that are spatially aligned. However, the neural interactions among modalities that share no spatial stimulus domain yet are essential for robust perception within noisy environments remain uncharacterized. Drosophila melanogaster makes its living navigating food odor plumes. Odor acts to increase the strength of gaze-stabilizing optomotor reflexes to keep the animal aligned within an invisible plume, facilitating odor localization in free flight. Here, we investigate the cellular mechanism for cross-modal behavioral interactions. We characterize a wide-field motion-selective interneuron of the lobula plate that shares anatomical and physiological similarities with the "Hx" neuron identified in larger flies. Drosophila Hx exhibits cross-modal enhancement of visual responses by paired odor, and presynaptic inputs to the lobula plate are required for behavioral odor tracking but are not themselves the target of odor modulation, nor is the neighboring wide-field "HSE" neuron. Octopaminergic neurons mediating increased visual responses upon flight initiation also show odor-evoked calcium modulations and form connections with Hx dendrites. Finally, restoring synaptic vesicle trafficking within the octopaminergic neurons of animals carrying a null mutation for all aminergic signaling is sufficient to restore odor-tracking behavior. These results are the first to demonstrate cellular mechanisms underlying visual-olfactory integration required for odor localization in fruit flies, which may be representative of adaptive multisensory interactions across taxa.

Regulation of response properties and operating range of the AFD thermosensory neurons by cGMP signaling.

BACKGROUND: The neuronal mechanisms that encode specific stimulus features in order to elicit defined behavioral responses are poorly understood. C. elegans forms a memory of its cultivation temperature (T(c)) and exhibits distinct behaviors in different temperature ranges relative to T(c). In particular, C. elegans tracks isotherms only in a narrow temperature band near T(c). T(c) memory is in part encoded by the threshold of responsiveness (T∗(AFD)) of the AFD thermosensory neuron pair to temperature stimuli. However, because AFD thermosensory responses appear to be similar at all examined temperatures above T∗(AFD), the mechanisms that generate specific behaviors in defined temperature ranges remain to be determined. RESULTS: Here, we show that the AFD neurons respond to the sinusoidal variations in thermal stimuli followed by animals during isothermal tracking (IT) behavior only in a narrow temperature range near T(c). We find that mutations in the AFD-expressed gcy-8 receptor guanylyl cyclase (rGC) gene result in defects in the execution of IT behavior and are associated with defects in the responses of the AFD neurons to oscillating thermal stimuli. In contrast, mutations in the gcy-18 or gcy-23 rGCs alter the temperature range in which IT behavior is exhibited. Alteration of intracellular cGMP levels via rGC mutations or addition of cGMP analogs shift the lower and upper ranges of the temperature range of IT behavior in part via alteration in T∗(AFD). CONCLUSIONS: Our observations provide insights into the mechanisms by which a single sensory neuron type encodes features of a given stimulus to generate different behaviors in defined zones.

A diacylglycerol kinase modulates long-term thermotactic behavioral plasticity in C. elegans.

A memory of prior thermal experience governs Caenorhabditis elegans thermotactic behavior. On a spatial thermal gradient, C. elegans tracks isotherms near a remembered temperature we call the thermotactic set-point (T(S)). The T(S) corresponds to the previous cultivation temperature and can be reset by sustained exposure to a new temperature. The mechanisms underlying this behavioral plasticity are unknown, partly because sensory and experience-dependent components of thermotactic behavior have been difficult to separate. Using newly developed quantitative behavioral analyses, we demonstrate that the T(S) represents a weighted average of a worm's temperature history. We identify the DGK-3 diacylglycerol kinase as a thermal memory molecule that regulates the rate of T(S) resetting by modulating the temperature range of synaptic output, but not temperature sensitivity, of the AFD thermosensory neurons. These results provide the first mechanistic insight into the basis of experience-dependent plasticity in this complex behavior.