Fruit flies exhibit robust attraction to food odors, which usually excite multiple glomeruli. To understand how the representation of such odors leads to behavior, we used genetic tools to dissect the contribution of each activated glomerulus. Apple cider vinegar triggers robust innate attraction at a relatively low concentration, which activates six glomeruli. By silencing individual glomeruli, we found that the absence of activity in two glomeruli, DM1 and VA2, markedly reduced attraction. Conversely, when each of these two glomeruli was selectively activated, flies exhibited as robust an attraction to vinegar as wild type flies. Notably, a higher concentration of vinegar excites an additional glomerulus and is less attractive to flies. Here we show that the activation of the additional glomerulus is necessary and sufficient to mediate the behavioral switch. Together, these results indicate that individual glomeruli, rather than the entire pattern of active glomeruli, mediate innate behavioral output.

Avoiding the strike of an approaching predator requires rapid visual detection of a looming object, followed by a directed escape maneuver. While looming-sensitive neurons have been discovered in various animal species, the relative importance of stimulus features that are extracted by the visual system is still unclear. Furthermore, the neural mechanisms that compute object approach are largely unknown. We found that a virtual looming stimulus, i.e., a dark expanding disk on a bright background, reliably evoked rapid escape movements. Related stimuli, such as dimming, receding, or bright looming objects, were substantially less effective, and angular size was a critical determinant of escape initiation. Two-photon calcium imaging in retinal ganglion cell (RGC) axons revealed three retinorecipient areas that responded robustly to looming stimuli. One of these areas, the optic tectum, is innervated by a subset of RGC axons that respond selectively to looming stimuli. Laser-induced lesions of the tectal neuropil impaired the behavior. Our findings demonstrate a visually mediated escape behavior in zebrafish larvae exposed to objects approaching on a collision course. This response is sensitive to spatiotemporal parameters of the looming stimulus. Our data indicate that a subset of RGC axons within the tectum responds selectively to features of looming stimuli and that this input is necessary for visually evoked escape.

Zebrafish larvae show characteristic prey capture behavior in response to small moving objects. The neural mechanism used to recognize objects as prey remains largely unknown. We devised a machine learning behavior classification system to quantify hunting kinematics in semi-restrained animals exposed to a range of virtual stimuli. Two-photon calcium imaging revealed a small visual area, AF7, that was activated specifically by the optimal prey stimulus. This pretectal region is innervated by two types of retinal ganglion cells, which also send collaterals to the optic tectum. Laser ablation of AF7 markedly reduced prey capture behavior. We identified neurons with arbors in AF7 and found that they projected to multiple sensory and premotor areas: the optic tectum, the nucleus of the medial longitudinal fasciculus (nMLF) and the hindbrain. These findings indicate that computations in the retina give rise to a visual stream which transforms sensory information into a directed prey capture response.DOI: http://dx.doi.org/10.7554/eLife.04878.001

SummaryIn a process called quorum sensing, bacteria communicate with one another using secreted chemical signalling molecules termed autoinducers. A novel autoinducer called AI-2, originally discovered in the quorum-sensing bacterium Vibrio harveyi, is made by many species of Gram-negative and Grampositive bacteria. In every case, production of AI-2 is dependent on the LuxS autoinducer synthase. The genes regulated by AI-2 in most of these luxS-containing species of bacteria are not known. Here, we describe the identification and characterization of AI-2-regulated genes in Salmonella typhimurium. We find that LuxS and AI-2 regulate the expression of a previously unidentified operon encoding an ATP binding cassette (ABC)-type transporter. We have named this operon the lsr (luxS regulated) operon. The Lsr transporter has homology to the ribose transporter of Escherichia coli and S. typhimurium. A gene encoding a DNA-binding protein that is located adjacent to the Lsr transporter structural operon is required to link AI-2 detection to operon expression. This gene, which we have named lsrR, encodes a protein that represses lsr operon expression in the absence of AI-2. Mutations in the lsr operon render S. typhimurium unable to eliminate AI-2 from the extracellular environment, suggesting that the role of the Lsr apparatus is to transport AI-2 into the cells. It is intriguing that an operon regulated by AI-2 encodes functions resembling the ribose transporter, given recent findings that AI-2 is derived from the ribosyl moiety of S-ribosylhomocysteine.

Investigating how information propagates between layers in the olfactory system is an important step toward understanding the olfactory code. Each glomerular output projection neuron (PN) receives two sources of input: the olfactory receptor neurons (ORNs) of the same glomerulus and interneurons that innervate many glomeruli. We therefore asked how these inputs interact to produce PN output. We used receptor gene mutations to silence all of the ORNs innervating a specific glomerulus and recorded PN activity with two-photon calcium imaging and electrophysiology. We found evidence for balanced excitatory and inhibitory synaptic inputs but saw little or no response in the absence of direct ORN input. We next asked whether any transformation of activity occurs at successive layers of the antennal lobe. We found a strong link between PN firing and dendritic calcium elevation, the latter of which is tightly correlated with calcium activity in ORN axons, supporting the idea of glomerular propagation of olfactory information. Finally, we showed that odors are represented by a sparse population of PNs. Together, these results are consistent with the idea that direct receptor input provides the main excitatory drive to PNs, whereas interneurons modulate PN output. Balanced excitatory and inhibitory interneuron input may provide a mechanism to adjust PN sensitivity.antennal lobe ͉ gain modulation ͉ olfaction ͉ smell ͉ sparse code S ensory systems have the difficult task of encoding the identity and intensity of behaviorally relevant stimuli in the environment. The question of how these stimuli are encoded and propagated from the periphery to higher brain centers is central to systems neuroscience. The stereotypic organization of the Drosophila olfactory system and the identification of the odorant receptor genes make the fly an attractive model system in which to study the successive processing of sensory information.Drosophila olfactory receptor neurons (ORNs) in the antennae detect odors and relay neural activity to the antennal lobe in the brain. An adult fly expresses Ϸ50 odorant receptor genes (1-6). In the antennal lobe, axons of ORNs expressing the same receptor gene project with precision to spatially invariant glomeruli (4-7). Most second-order projection neurons (PNs) send dendrites to individual glomeruli in the antennal lobe and send axons to the mushroom body and the lateral horn of the protocerebrum (8-11).Imaging experiments in the insect antennal lobe (12-14) reveal a spatial map of glomerular activity. It has been hypothesized that each glomerulus is a functional unit and that the pattern of glomerular activity encodes the quality of odors (15). However, the Drosophila antennal lobe contains many GABAergic inhibitory interneurons (10,16,17), as well as a group of recently identified cholinergic excitatory interneurons (18). These two classes of interneurons apparently have opposing effects on PNs, and the extent to which they contribute to PN output is unknown. There are two general models for the function...