Multimodal interactions in insect navigation

Animals travelling through the world receive input from multiple sensory modalities that could be important for the guidance of their journeys. Given the availability of a rich array of cues, from idiothetic information to input from sky compasses and visual information through to olfactory and other cues (e.g. gustatory, magnetic, anemotactic or thermal) it is no surprise to see multimodality in most aspects of navigation. In this review, we present the current knowledge of multimodal cue use during orientation and navigation in insects. Multimodal cue use is adapted to a species’ sensory ecology and shapes navigation behaviour both during the learning of environmental cues and when performing complex foraging journeys. The simultaneous use of multiple cues is beneficial because it provides redundant navigational information, and in general, multimodality increases robustness, accuracy and overall foraging success. We use examples from sensorimotor behaviours in mosquitoes and flies as well as from large scale navigation in ants, bees and insects that migrate seasonally over large distances, asking at each stage how multiple cues are combined behaviourally and what insects gain from using different modalities

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 robot

Dopaminergic Modulation Shapes Sensorimotor Processing in the Drosophila Mushroom Body

To survive in a complex and dynamic environment, animals must adapt their behavior based on their current needs and prior experiences. This flexibility is often mediated by neuromodulation within neural circuits that link sensory representations to alternative behavioral responses depending on contextual cues and learned associations. In Drosophila, the mushroom body is a prominent neural structure essential for olfactory learning. Dopaminergic neurons convey salient information about reward and punishment to the mushroom body in order to adjust synaptic connectivity between Kenyon cells, the neurons representing olfactory stimuli, and the mushroom body output neurons that ultimately influence behavior. However, we still lack a mechanistic understanding of how the dopaminergic neurons represent the moment-tomoment experience of a fly and drive changes in this sensory-to-motor transformation. Furthermore, very little is known about how the output neuron pathways lead to the execution of appropriate odor-related behaviors. We took advantage of the mushroom body’s modular circuit organization to investigate how the dopaminergic neuron population encodes different contextual cues. In vivo functional imaging of the dopaminergic neurons reveals that they represent both external reinforcement stimuli, like sugar rewards or punitive electric shock, as well as the fly’s motor state, through coordinated and partially antagonistic activity patterns across the population. This multiplexing of motor and reward signals by the dopaminergic neurons parallels the dual roles of dopaminergic inputs to the vertebrate basal ganglia, thus demonstrating a conserved link between these distantly related neural circuits. We proceed to demonstrate that this dopaminergic signal in the mushroom body modifies neurotransmission with synaptic specificity and temporal precision to coordinately regulate the propagation of sensory signals through the output neurons. To explore how these output pathways ultimately influence olfactory navigation we have developed a closed loop olfactory paradigm in which we can monitor and manipulate the mushroom body output neurons as a fly navigates in a virtual olfactory environment. We have begun to probe the mushroom body circuitry in the context of olfactory navigation. These preliminary investigations have led to the identification of putative pathways for linking mushroom body output with the circuits that implement odor-tracking behavior and the characterization of the complex sensorimotor representations in the dopaminergic network. Our work reveals that the Drosophila dopaminergic system modulates mushroom body output at both acute and enduring timescales to guide immediate behaviors and learned responses

Roles of Aminergic Neurons in Formation and Recall of Associative Memory in Crickets

We review recent progress in the study of roles of octopaminergic (OA-ergic) and dopaminergic (DA-ergic) signaling in insect classical conditioning, focusing on our studies on crickets. Studies on olfactory learning in honey bees and fruit-flies have suggested that OA-ergic and DA-ergic neurons convey reinforcing signals of appetitive unconditioned stimulus (US) and aversive US, respectively. Our work suggested that this is applicable to olfactory, visual pattern, and color learning in crickets, indicating that this feature is ubiquitous in learning of various sensory stimuli. We also showed that aversive memory decayed much faster than did appetitive memory, and we proposed that this feature is common in insects and humans. Our study also suggested that activation of OA- or DA-ergic neurons is needed for appetitive or aversive memory recall, respectively. To account for this finding, we proposed a model in which it is assumed that two types of synaptic connections are strengthened by conditioning and are activated during memory recall, one type being connections from neurons representing conditioned stimulus (CS) to neurons inducing conditioned response and the other being connections from neurons representing CS to OA- or DA-ergic neurons representing appetitive or aversive US, respectively. The former is called stimulus–response (S–R) connection and the latter is called stimulus–stimulus (S–S) connection by theorists studying classical conditioning in vertebrates. Results of our studies using a second-order conditioning procedure supported our model. We propose that insect classical conditioning involves the formation of S–S connection and its activation for memory recall, which are often called cognitive processes

Octopaminergic neurons have multiple targets in Drosophila larval mushroom body calyx and can modulate behavioral odor discrimination.

Discrimination of sensory signals is essential for an organism to form and retrieve memories of relevance in a given behavioral context. Sensory representations are modified dynamically by changes in behavioral state, facilitating context-dependent selection of behavior, through signals carried by noradrenergic input in mammals, or octopamine (OA) in insects. To understand the circuit mechanisms of this signaling, we characterized the function of two OA neurons, sVUM1 neurons, that originate in the subesophageal zone (SEZ) and target the input region of the memory center, the mushroom body (MB) calyx, in larval Drosophila We found that sVUM1 neurons target multiple neurons, including olfactory projection neurons (PNs), the inhibitory neuron APL, and a pair of extrinsic output neurons, but relatively few mushroom body intrinsic neurons, Kenyon cells. PN terminals carried the OA receptor Oamb, a Drosophila α1-adrenergic receptor ortholog. Using an odor discrimination learning paradigm, we showed that optogenetic activation of OA neurons compromised discrimination of similar odors but not learning ability. Our results suggest that sVUM1 neurons modify odor representations via multiple extrinsic inputs at the sensory input area to the MB olfactory learning circuit.MRC studentship, UK Genetics Society Summer scholarship, BBSRC DTP summer placement, Isaac Newton Trust

Progress in the use of genetic methods to study insect behavior outside Drosophila

In the span of a decade we have seen a rapid progress in the application of genetic tools and genome editing approaches in ‘non-model’ insects. It is now possible to target sensory receptor genes and neurons, explore their functional roles and manipulate behavioral responses in these insects. In this review, we focus on the latest examples from Diptera, Lepidoptera and Hymenoptera of how applications of genetic tools advanced our understanding of diverse behavioral phenomena. We further discuss genetic methods that could be applied to study insect behavior in the future

Neurofly 2008 abstracts : the 12th European Drosophila neurobiology conference 6-10 September 2008 Wuerzburg, Germany

This volume consists of a collection of conference abstracts

Spatial information from the odour environment in mammalian olfaction

The sense of smell is an essential modality for many species, in particular nocturnal and crepuscular mammals, to gather information about their environment. Olfactory cues provide information over a large range of distances, allowing behaviours ranging from simple detection and recognition of objects, to tracking trails and navigating using odour plumes from afar. In this review, we discuss the features of the natural olfactory environment and provide a brief overview of how odour information can be sampled and might be represented and processed by the mammalian olfactory system. Finally, we discuss recent behavioural approaches that address how mammals extract spatial information from the environment in three diferent contexts: odour trail tracking, odour plume tracking and, more general, olfactory-guided navigation. Recent technological developments have seen the spatiotemporal aspect of mammalian olfaction gain signifcant attention, and we discuss both the promising aspects of rapidly developing paradigms and stimulus control technologies as well as their limitations. We conclude that, while still in its beginnings, research on the odour environment ofers an entry point into understanding the mechanisms how mammals extract information about space

匂い源探索における状態依存的な複数感覚統合に関する研究

学位の種別: 課程博士審査委員会委員 : （主査）東京大学教授 神崎 亮平, 東京大学教授 下山 勲, 東京大学教授 竹内 昌治, 東京大学特任講師 安藤 規泰, 総合研究大学院大学講師 木下 充代University of Tokyo(東京大学