Mikael A. Carlsson

An artificial moth: Chemical source localization using a robot based neuronal model of moth optomotor anemotactic search

Robots have been used to model nature, while nature in turn can contribute to the real-world artifacts we construct. One particular domain of interest is chemical search where a number of efforts are underway to construct mobile chemical search and localization systems. We report on a project that aims at constructing such a system based on our understanding of the pheromone communication system of the moth. Based on an overview of the peripheral processing of chemical cues by the moth and its role in the organization of behavior we emphasize the multimodal aspects of chemical search, i.e. optomotor anemotactic chemical search. We present a model of this behavior that we test in combination with a novel thin metal oxide sensor and custom build mobile robots. We show that the sensor is able to detect the odor cue, ethanol, under varying flow conditions. Subsequently we show that the standard model of insect chemical search, consisting of a surge and cast phases, provides for robust search and localization performance. The same holds when it is augmented with an optomotor collision avoidance model based on the Lobula Giant Movement Detector (LGMD) neuron of the locust. We compare our results to others who have used the moth as inspiration for the construction of odor robots.

Olfactory activation patterns in the antennal lobe of the sphinx moth, Manduca sexta.

The sphinx moth Manduca sexta is a well-studied insect with regard to central olfactory functions. Until now, the innervation patterns of olfactory receptor neurons into the array of olfactory glomeruli in the antennal lobe have, however, been unclear. Using optical imaging to visualize calcium dynamics within the antennal lobe we demonstrate specific patterns elicited by sex pheromone components and plant-derived odours. These patterns mainly reflect receptor neuron activity. Within the male-specific macroglomerular complex the two major pheromone components evoke stereotyped activity in either of two macroglomerular complex glomeruli. Based on previous knowledge of output neuron specificity, our results suggest a matching of information between input and output in the macroglomerular complex. Plant odours evoked activity in the sexually isomorphic glomeruli. Two major results were obtained: (1) terpenes and aromatic compounds activate different clusters of glomeruli with only minor overlapping, and (2) the position of certain key glomeruli is fixed in both males and females, which suggests that host-plant related odorants are processed in a similar way in both sexes.

Odorant-Evoked Nitric Oxide Signals in the Antennal Lobe of Manduca sexta

The gaseous signaling molecule nitric oxide (NO) can affect the activities of neurons and neural networks in many different systems. The strong expression of NO synthase (NOS) in the primary synaptic neuropil (the antennal lobe in insects and the olfactory bulb in vertebrates) of the olfactory system of most organisms, and the unique spheroidal geometry of olfactory glomeruli in those neuropils, have led to suggestions that NO signaling is important for processing olfactory information. No direct evidence exists, however, that NO signals are produced in olfactory glomeruli. We investigated the production of NO in the antennal lobe of the moth, Manduca sexta, by using immunocytochemistry and real-time optical imaging with a NO-sensitive fluorescent marker, diaminofluorescein diacetate. We confirmed that NOS was expressed in the axons of olfactory receptor neurons projecting to all glomeruli. Soluble guanylyl cyclase, the best characterized target of NO, was found in a subset of postsynaptic antennal lobe neurons that included projection neurons, a small number of GABA-immunoreactive neurons, and a serotonin-immunoreactive neuron. We found that odorant stimulation evoked NO signals that were reproducible and spatially focused. Different odorants evoked spatially distinct patterns of NO production. Increased concentrations of pheromone and plant odorants caused increases in peak signal intensity. Increased concentrations of plant odorants also evoked a dramatic increase in signal area. The results of these experiments show clearly that odorant stimulation can evoke NO production in the olfactory system. The NO signals produced are likely to play an important role in processing olfactory information.

The Neuropeptide Allatostatin A Regulates Metabolism and Feeding Decisions in Drosophila

Coordinating metabolism and feeding is important to avoid obesity and metabolic diseases, yet the underlying mechanisms, balancing nutrient intake and metabolic expenditure, are poorly understood. Several mechanisms controlling these processes are conserved in Drosophila, where homeostasis and energy mobilization are regulated by the glucagon-related adipokinetic hormone (AKH) and the Drosophila insulin-like peptides (DILPs). Here, we provide evidence that the Drosophila neuropeptide Allatostatin A (AstA) regulates AKH and DILP signaling. The AstA receptor gene, Dar-2, is expressed in both the insulin and AKH producing cells. Silencing of Dar-2 in these cells results in changes in gene expression and physiology associated with reduced DILP and AKH signaling and animals lacking AstA accumulate high lipid levels. This suggests that AstA is regulating the balance between DILP and AKH, believed to be important for the maintenance of nutrient homeostasis in response to changing ratios of dietary sugar and protein. Furthermore, AstA and Dar-2 are regulated differentially by dietary carbohydrates and protein and AstA-neuronal activity modulates feeding choices between these types of nutrients. Our results suggest that AstA is involved in assigning value to these nutrients to coordinate metabolic and feeding decisions, responses that are important to balance food intake according to metabolic needs.

Spatio-temporal Ca2+ dynamics of moth olfactory projection neurones

We studied the Ca2+ dynamics of odour‐evoked glomerular patterns in the antennal lobe of the moth Spodoptera littoralis using optical imaging. Here we selectively stained a large population of antennal lobe output neurones, projection neurones, by retrograde filling with FURA‐dextran from the inner antennocerebral tract in the protocerebrum. Different plant‐associated odorants evoked distributed patterns of activated glomeruli that were odour dependent and repeatable. These patterns were, however, dynamic during the period of odour exposure. Temporal responses differed across glomeruli and were stimulus dependent. Next we examined how the correlations between patterns evoked by different odorants changed with time. Initially, responses to structurally similar compounds were highly correlated, whereas responses to structurally different compounds differed. Within the period of odour exposure (1 s) we found a significant reduction in similarity of responses evoked by different odours, irrespective of initial similarity, whereas trial‐to‐trial correlations remained high. Our results suggested an ability for coarse classification at the initial encounter with an odour source. With time, however, the discrimination ability increases and structurally similar odours can be distinguished.

Spatial representation of odorant structure in the moth antennal lobe: A study of structure-response relationships at low doses

How odorant structure and concentration are spatially represented within the primary olfactory integration center, the antennal lobe (AL) or olfactory bulb (OB) in invertebrates and vertebrates, respectively, is currently a topic of high interest. Here, we show the spatial representation of odorant structure in the antennal lobe of the moth Spodoptera littoralis by imaging calcium activity evoked by straight chain aliphatic alcohols and aldehydes at low doses. Activity patterns of a given odor were most similar to compounds with the same functional group, differing in chain length by only one carbon atom. A chain length dependency was present as the most activated glomerulus in the lobe shifted from a medial to a lateral position with increasing chain length of the molecule. Statistical analysis revealed that in both classes of chemicals the chain length of the molecule was represented in a similar way. No topographically fixed domains were observed for any of the classes. However, activity patterns evoked by lower chain length molecules were spatially more distinct than patterns evoked by higher chain length molecules. The number of activated glomeruli for both classes of chemicals increased with increasing chain length to reach a maximum at eight or nine C atoms followed by a decrease as the chain length further increased. J. Comp. Neurol. 467:11–21, 2003.

Responses in highly selective sensory neurons to blends of pheromone components in the moth Agrotis segetum

Pheromone detecting sensory neurons in moths are known to be highly sensitive and selective. Female-emitted sexual pheromones are normally mixtures of a few to several components. However, not much is known about how receptor neurons respond to blends of compounds. In the present study we investigated how four physiological types of pheromone component-selective neurons responded to binary mixtures or to the complete blend in the turnip moth Agrotis segetum. We found that responses to mixtures only rarely differed from that to the excitatory component alone. The mixture interactions were exclusively suppressive and occurred only at high concentrations. Therefore we conclude that the, in A. segetum, commonly observed mixture interactions observed in higher brain centra are mainly the result of central nervous processing and that information about the pheromone components reaches the antennal lobes virtually unaltered. In addition, we found a physiological type of receptor neuron, responding selectively to one of the female-emitted pheromone components, that has previously not been observed in the Swedish population.

Antennal lobe projection destinations of Helicoverpa zea male olfactory receptor neurons responsive to heliothine sex pheromone components.

We used single sensillum recordings to define male Helicoverpa zea olfactory receptor neuron physiology followed by cobalt staining to trace the axons to destination glomeruli of the antennal lobe. Receptor neurons in type A sensilla that respond to the major pheromone component, (Z)-11-hexadecenal, projected axons to the cumulus of the macroglomerular complex (MGC). In approximately 40% of these sensilla a second receptor neuron was stained that projected consistently to a specific glomerulus residing in a previously unrecognized glomerular complex with six other glomeruli stationed immediately posterior to the MGC. Cobalt staining corroborated by calcium imaging showed that receptor neurons in type C sensilla sensitive to (Z)-9-hexadecenal projected to the dorsomedial posterior glomerulus of the MGC, whereas the co-compartmentalized antagonist-sensitive neurons projected to the dorsomedial anterior glomerulus. We also discovered that the olfactory receptor neurons in type B sensilla exhibit the same axonal projections as those in type C sensilla. Thus, it seems that type B sensilla are anatomically type C with regard to the projection destinations of the two receptor neurons, but physiologically one of the receptor neurons is now unresponsive to everything except (Z)-9-tetradecenal, and the other responds to none of the pheromone-related odorants tested.

Feeding regulates sex pheromone attraction and courtship in Drosophila females.

In Drosophila melanogaster, gender-specific behavioural responses to the male-produced sex pheromone cis-vaccenyl acetate (cVA) rely on sexually dimorphic, third-order neural circuits. We show that nutritional state in female flies modulates cVA perception in first-order olfactory neurons. Starvation increases, and feeding reduces attraction to food odour, in both sexes. Adding cVA to food odour, however, maintains attraction in fed females, while it has no effect in males. Upregulation of sensitivity and behavioural responsiveness to cVA in fed females is paralleled by a strong increase in receptivity to male courtship. Functional imaging of the antennal lobe (AL), the olfactory centre in the insect brain, shows that olfactory input to DA1 and VM2 glomeruli is also modulated by starvation. Knocking down insulin receptors in neurons converging onto the DA1 glomerulus suggests that insulin-signalling partly controls pheromone perception in the AL, and adjusts cVA attraction according to nutritional state and sexual receptivity in Drosophila females.

Olfactory coding in five moth species from two families

SUMMARY The aim of the present study was to determine what impact phylogeny and life history might have on the coding of odours in the brain. Using three species of hawk moths (Sphingidae) and two species of owlet moths (Noctuidae), we visualized neural activity patterns in the antennal lobe, the first olfactory neuropil in insects, evoked by a set of ecologically relevant plant volatiles. Our results suggest that even between the two phylogenetically distant moth families, basic olfactory coding features are similar. But we also found different coding strategies in the moths’ antennal lobe; namely, more specific patterns for chemically similar odorants in the two noctuid species than in the three sphingid species tested. This difference demonstrates the impact of the phylogenetic distance between species from different families despite some parallel life history traits found in both families. Furthermore, pronounced differences in larval and adult diet among the sphingids did not translate into differences in the olfactory code; instead, the three species had almost identical coding patterns.