Person: Paoli, Marco
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Social modulation of individual preferences in cockroaches
In social species, decision-making is both influenced by, and in turn influences, the social context. This reciprocal feedback introduces coupling across scales, from the neural basis of sensing, to individual and collective decision-making. Here, we adopt an integrative approach investigating decision-making in dynamical social contexts. When choosing shelters, isolated cockroaches prefer vanillin-scented (food-associated) shelters over unscented ones, yet in groups, this preference is inverted. We demonstrate that this inversion can be replicated by replacing the full social context with social odors: presented alone food and social odors are attractive, yet when presented as a mixture they are avoided. Via antennal lobe calcium imaging, we show that neural activity in vanillin-responsive regions reduces as social odor concentration increases. Thus, we suggest that the mixture is evaluated as a distinct olfactory object with opposite valence, providing a mechanism that would naturally result in individuals avoiding what they perceive as recently exploited resources.
Coding of odour and space in the hemimetabolous insect Periplaneta americana
The general architecture of the olfactory system is highly conserved from insects to humans, but neuroanatomical and physiological differences can be observed across species. The American cockroach, inhabiting dark shelters with a rather stable olfactory landscape, is equipped with long antennae used for sampling the surrounding air-space for orientation and navigation. The antennae's exceptional length provides a wide spatial working range for odour detection; however, it is still largely unknown whether and how this is also used for mapping the structure of the olfactory environment. By selectively labelling antennal lobe projection neurons with a calcium-sensitive dye, we investigated the logic of olfactory coding in this hemimetabolous insect. We show that odour responses are stimulus specific and concentration dependent, and that structurally related odorants evoke physiologically similar responses. By using spatially confined stimuli, we show that proximal stimulations induce stronger and faster responses than distal ones. Spatially confined stimuli of the female pheromone periplanone B activate a subregion of the male macroglomerulus. Thus, we report that the combinatorial logic of odour coding deduced from holometabolous insects applies also to this hemimetabolous species. Furthermore, a fast decrease in sensitivity along the antenna, not supported by a proportionate decrease in sensillar density, suggests a neural architecture that strongly emphasizes neuronal inputs from the proximal portion of the antenna.
In Vivo Two-Photon Imaging of the Olfactory System in Insects
This chapter describes how to apply two-photon neuroimaging to study the insect olfactory system in vivo. It provides a complete protocol for insect brain functional imaging, with some additional remarks on the acquisition of morphological information from the living brain. We discuss the most important choices to make when buying or building a two-photon laser-scanning microscope. We illustrate different possibilities of animal preparation and brain tissue labeling for in vivo imaging. Finally, we give an overview of the main methods of image data processing and analysis, followed by a short description of pioneering applications of this imaging modality.
Olfactory coding in honeybees
With less than a million neurons, the western honeybee Apis mellifera is capable of complex olfactory behaviors and provides an ideal model for investigating the neurophysiology of the olfactory circuit and the basis of olfactory perception and learning. Here, we review the most fundamental aspects of honeybee's olfaction: first, we discuss which odorants dominate its environment, and how bees use them to communicate and regulate colony homeostasis; then, we describe the neuroanatomy and the neurophysiology of the olfactory circuit; finally, we explore the cellular and molecular mechanisms leading to olfactory memory formation. The vastity of histological, neurophysiological, and behavioral data collected during the last century, together with new technological advancements, including genetic tools, confirm the honeybee as an attractive research model for understanding olfactory coding and learning.
Spatial Receptive Fields for Odor Localization
Animals rely on olfaction to navigate through complex olfactory landscapes, but the mechanisms that allow an animal to encode the spatial structure of an odorous environment remain unclear. To acquire information about the spatial distribution of an odorant, animals may rely on bilateral olfactory organs and compare side differences of odor intensity and timing [1-6] or may perform spatial and temporal signal integration of subsequent samplings [7]. The American cockroach can efficiently locate a source of sex pheromone even after the removal of one antenna, suggesting that bilateral comparison is not a prerequisite for odor localization in this species [8, 9]. Cognate olfactory sensory neurons (OSNs) originating from different locations on the flagellum, but bearing the same olfactory receptor, converge onto the same glomerulus within the antennal lobe, which is thought to result in a loss of spatial information. Here, we identified 12 types of pheromone-responsive projection neurons (PNs), each with spatially tuned receptive field. The combination of (1) the antennotopic organization of OSNs terminals and (2) the stereotyped compartmentalization of PNs' dendritic arborization within the macroglomerulus (MG), allows encoding the spatial position of the pheromone. Furthermore, each PN type innervates a different compartment of the mushroom body, providing the means for encoding spatial olfactory information along the olfactory circuit. Finally, MG PNs exhibit both excitatory and inhibitory spatial receptive fields and modulate their responses based on changes in stimulus geometry. In conclusion, we propose a mechanism for encoding information on the spatial distribution of a pheromone, expanding both our understanding of odor coding and of the strategies insects adopt to localize a sexual mate.
Minute Impurities Contribute Significantly to Olfactory Receptor Ligand Studies : Tales from Testing the Vibration Theory
Several studies have attempted to test the vibrational hypothesis of odorant receptor activation in behavioral and physiological studies using deuterated compounds as odorants. The results have been mixed. Here, we attempted to test how deuterated compounds activate odorant receptors using calcium imaging of the fruit fly antennal lobe. We found specific activation of one area of the antennal lobe corresponding to inputs from a specific receptor. However, upon more detailed analysis, we discovered that an impurity of 0.0006% ethyl acetate in a chemical sample of benzaldehyde-d5 was entirely responsible for a sizable odorant-evoked response in Drosophila melanogaster olfactory receptor cells expressing dOr42b. Without gas chromatographic purification within the experimental setup, this impurity would have created a difference in the responses of deuterated and nondeuterated benzaldehyde, suggesting that dOr42b be a vibration sensitive receptor, which we show here not to be the case. Our results point to a broad problem in the literature on use of non-GC-pure compounds to test receptor selectivity, and we suggest how the limitations can be overcome in future studies.
Structural and transcriptional evidence of mechanotransduction in the Drosophila suzukii ovipositor
Drosophila suzukii is an invasive pest that prefers to lay eggs in ripening fruits, whereas most closely related Drosophila species exclusively use rotten fruit as oviposition site. This behaviour is allowed by an enlarged and serrated ovipositor that can pierce intact fruit skin, and by multiple contact sensory systems (mechanosensation and taste) that detect the optimal egg-laying substrates. Here, we tested the hypothesis that bristles present in the D. suzukii ovipositor tip contribute to these sensory modalities. Analysis of the bristle ultrastructure revealed that four different types of cuticular elements (conical pegs type 1 and 2, chaetic and trichoid sensilla) are present on the tip of each ovipositor plate. All of them have a poreless shaft and are innervated at their base by a single neuron that ends in a distal tubular body, thus resembling mechanosensitive structures. Fluorescent labelling in D. suzukii and D. melanogaster revealed that pegs located on the ventral side of the ovipositor tip are innervated by a single neuron in both species. RNA-sequencing profiled gene expression, notably sensory receptor genes of the terminalia of D. suzukii and of three other Drosophila species with changes in their ovipositor structure (from serrated to blunt ovipositor: Drosophila subpulchrella, Drosophila biarmipes and D. melanogaster). Our results revealed few species-specific transcripts and an overlapping expression of candidate mechanosensitive genes as well as the presence of some chemoreceptor transcripts. These experimental evidences suggest a mechanosensitive function for the D. suzukii ovipositor, which might be crucial across Drosophila species independently from ovipositor shape.
Neuronal Response Latencies Encode First Odor Identity Information across Subjects
Odorants are coded in the primary olfactory processing centers by spatially and temporally distributed patterns of glomerular activity. Whereas the spatial distribution of odorant-induced responses is known to be conserved across individuals, the universality of its temporal structure is still debated. Via fast two-photon calcium imaging, we analyzed the early phase of neuronal responses in the form of the activity onset latencies in the antennal lobe projection neurons of honeybee foragers. We show that each odorant evokes a stimulus-specific response latency pattern across the glomerular coding space. Moreover, we investigate these early response features for the first time across animals, revealing that the order of glomerular firing onsets is conserved across individuals and allows them to reliably predict odorant identity, but not concentration. These results suggest that the neuronal response latencies provide the first available code for fast odor identification.
SIGNIFICANCE STATEMENT
Here, we studied early temporal coding in the primary olfactory processing centers of the honeybee brain by fast imaging of glomerular responses to different odorants across glomeruli and across individuals. Regarding the elusive role of rapid response dynamics in olfactory coding, we were able to clarify the following aspects: (1) the rank of glomerular activation is conserved across individuals, (2) its stimulus prediction accuracy is equal to that of the response amplitude code, and (3) it contains complementary information. Our findings suggest a substantial role of response latencies in odor identification, anticipating the static response amplitude code.