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Animals adapt their behaviors to specific ecological niches, but the genetic and cellular basis of nervous system evolution is poorly understood. We have compared the olfactory circuits of the specialist Drosophila sechellia-which feeds exclusively on Morinda citrifolia fruit-with its generalist cousins D. melanogaster and D. simulans. We show that D. sechellia exhibits derived odor-evoked attraction and physiological sensitivity to the abundant Morinda volatile hexanoic acid and characterize how the responsible sensory receptor (the variant ionotropic glutamate receptor IR75b) and attraction-mediating circuit have evolved. A single amino acid change in IR75b is sufficient to recode it as a hexanoic acid detector. Expanded representation of this sensory pathway in the brain relies on additional changes in the IR75b promoter and trans-acting loci. By contrast, higher-order circuit adaptations are not apparent, suggesting conserved central processing. Our work links olfactory ecology to structural and regulatory genetic changes influencing nervous system anatomy and function., (Copyright © 2017 Elsevier Inc. All rights reserved.)

Trace conditioning is a form of classical conditioning, where a neutral stimulus (conditioned stimulus, CS) is associated with a following appetitive or aversive stimulus (unconditioned stimulus, US). Unlike classical delay conditioning, in trace conditioning there is a stimulus-free gap between CS and US, and thus a poststimulus neural representation (trace) of the CS is required to bridge the gap until its association with the US. The properties of such stimulus traces are not well understood, nor are their underlying physiological mechanisms. Using behavioral and physiological approaches, we studied appetitive olfactory trace conditioning in honeybees. We found that single-odor presentation created a trace containing information about odor identity. This trace conveyed odor information about the initial stimulus and was robust against interference by other odors. Memory acquisition decreased with increasing CS-US gap length. The maximum learnable CS-US gap length could be extended by previous trace-conditioning experience. Furthermore, acquisition improved when an additional odor was presented during the CS-US gap. Using calcium imaging, we tested whether projection neurons in the primary olfactory brain area, the antennal lobe, contain a CS trace. We found odor-specific persistent responses after stimulus offset. These post-odor responses, however, did not encode the CS trace, and perceived odor quality could be predicted by the initial but not by the post-odor response. Our data suggest that olfactory trace conditioning is a less reflexive form of learning than classical delay conditioning, indicating that odor traces might involve higher-level cognitive processes.

When an animal smells an odor, olfactory sensory neurons generate an activity pattern across olfactory glomeruli of the first sensory neuropil, the insect antennal lobe or the vertebrate olfactory bulb. Here, several networks of local neurons interact with sensory neurons and with output neurons--insect projection neurons, or vertebrate mitral/tufted cells. The extent and form of information processing taking place in these local networks has been subject of controversy. To investigate the role of local neurons in odor information processing we have used the calcium sensor G-CaMP to perform in vivo recordings of odor-evoked spatiotemporal activity patterns in five genetically defined neuron populations of the antennal lobe of Drosophila melanogaster: three distinct populations of local neurons (two GABAergic and one cholinergic), as well as sensory neurons and projection neurons. Odor-specific and concentration dependent spatiotemporal response patterns varied among neuron populations. Activity transfer differed along the olfactory pathway for different glomerulus-odor combinations: we found cases of profile broadening and of linear and complex transfer. Moreover, the discriminability between the odors also varied across neuron populations and was maximal in projection neurons. Discriminatory power increased with higher odor concentrations over a wide dynamic range, but decreased at the highest concentration. These results show the complexity and diversity of odor information processing mechanisms across olfactory glomeruli in the fly antennal lobe.

To understand how odor information is represented and processed in the antennal lobe (AL) of Drosophila melanogaster, we have optically recorded glomerular calcium responses to single odors and odor mixtures from olfactory sensory neurons (OSNs) and projection neurons (PNs). Odor mixtures offer a good tool to analyze odor processing because experimental results can be tested against clear predictions. At the level of the OSNs, the representation of odor mixtures could be predicted from the response patterns of the components in most cases. PN responses to mixtures, however, provide evidences of interglomerular inhibition. Application of picrotoxin (PTX), an antagonist of GABA(A)-like receptors, enhanced odor responses, modified their temporal course, and eliminated mixture suppression at the PN level. Our results can be best explained by postulating the existence of at least two local networks in the fly AL: a glomerulus specific network, which includes excitatory and inhibitory connections and a PTX sensitive inhibitory global network that acts on all glomeruli with proportional strength to the global AL input.