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A bio-hybrid odor-guided autonomous palm-sized air vehicle

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Abstract

Biohybrid systems integrate living materials with synthetic devices, exploiting their respective advantages to solve challenging engineering problems. One challenge of critical importance to society is detecting and localizing airborne volatile chemicals. Many flying animals depend their ability to detect and locate the source of aerial chemical plumes for finding mates and food sources. A robot with comparable capability could reduce human hazard and drastically improve performance on tasks such as locating disaster survivors, hazardous gas leaks, incipient fires, or explosives. Three advances are needed before they can rival their biological counterparts: 1) a chemical sensor with a much faster response time that nevertheless satisfies the size, weight, and power (SWaP) constraints of flight, 2) a design, sensor suite, and control system that allows it to move toward the source of a plume fully autonomously while navigating obstacles, and 3) the ability to detect the plume with high specificity and sensitivity among the assortment of chemicals that invariably exist in the air. Here we address the first two, introducing a human-safe palm-sized air vehicle equipped with the odor-sensing antenna of an insect, the first odor-sensing biohybrid robot system to fly. Using this sensor along with a suite of additional navigational sensors, as well as passive wind fins, our robot orients upwind and navigates autonomously toward the source of airborne plumes. Our robot is the first flying biohybrid system to successfully perform odor localization in a confined space, and it is able to do so while detecting and avoiding obstacles in its flight path. We show that insect antennae respond more quickly than metal oxide gas sensors, enabling the fastest odor localization ever demonstrated by a flying robot. By using the insect chemosensory apparatus, we anticipate a feasible path toward improved chemical specificity and sensitivity by leveraging recent advances in gene editing.

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... Furthermore, although inverted and vertical climbing was demonstrated (Chen et al. 2020;de Rivaz et al. 2018), maneuvering across complex terrains is still a conundrum for these artificial robots. However, the answers to these challenges might be found in the emerging ideas of biohybrid systems, which utilize the advantages of organic components in robotics applications (Anderson et al. 2020;Lee et al. 2022;Nitta et al. 2021;Webster-Wood et al. 2017;Yalikun et al. 2019). While bio-inspired and biomimetic systems seek insights from living materials, biohybrid systems incorporate them with synthetic devices (Anderson et al. 2020;Webster-Wood et al. 2017). ...
... However, the answers to these challenges might be found in the emerging ideas of biohybrid systems, which utilize the advantages of organic components in robotics applications (Anderson et al. 2020;Lee et al. 2022;Nitta et al. 2021;Webster-Wood et al. 2017;Yalikun et al. 2019). While bio-inspired and biomimetic systems seek insights from living materials, biohybrid systems incorporate them with synthetic devices (Anderson et al. 2020;Webster-Wood et al. 2017). This approach allows the hybrid systems to exploit both organic and artificial benefits from their two facets (Anderson et al. 2020;Webster-Wood et al. 2017). ...
... While bio-inspired and biomimetic systems seek insights from living materials, biohybrid systems incorporate them with synthetic devices (Anderson et al. 2020;Webster-Wood et al. 2017). This approach allows the hybrid systems to exploit both organic and artificial benefits from their two facets (Anderson et al. 2020;Webster-Wood et al. 2017). These systems were widely demonstrated in the forms of millimeter-scale actuators or aquatic/airborne miniature robots (Anderson et al. 2020;Lee et al. 2022;Nitta et al. 2021;Yalikun et al. 2019). ...
Article
While bio-inspired and biomimetic systems draw inspiration from living materials, biohybrid systems incorporate them with synthetic devices, allowing the exploitation of both organic and artificial advantages inside a single entity. In the challenging development of centimeter-scaled mobile robots serving unstructured territory navigations, biohybrid systems appear as a potential solution in the forms of terrestrial insect-machine hybrid systems, which are the fusion of living ambulatory insects and miniature electronic devices. Although their maneuver can be deliberately controlled via artificial electrical stimulation, these hybrid systems still inherit the insects’ outstanding locomotory skills, orchestrated by a sophisticated central nervous system and various sensory organs, favoring their maneuvers in complex terrains. However, efficient autonomous navigation of these hybrid systems is challenging. The struggle to optimize the stimulation parameters for individual insects limits the reliability and accuracy of navigation control. This study overcomes this problem by implementing a feedback control system with an insight view of tunable navigation control for an insect-machine hybrid system based on a living darkling beetle. Via a thrust controller for acceleration and a proportional controller for turning, the system regulates the stimulation parameters based on the instantaneous status of the hybrid robot. While the system can provide an overall success rate of ~71% for path-following navigations, fine-tuning its control parameters could further improve the outcome’s reliability and precision to up to ~94% success rate and ~1/2 body length accuracy, respectively. Such tunable performance of the feedback control system provides flexibility to navigation applications of insect-machine hybrid systems.
... These robots were intended for a multitude of applications, including drug loading, delivery, and screening, as well as fluid actuation, bioimaging, cardiac tissue repair, and object manipulation. In biohybrid robots, cells can be used for sensing, communication, integration, or as a power supply, but, thus far, they have been predominantly used for actuation (2,(16)(17)(18)(19). In cell-based actuation, two main approaches are possible. ...
... In Fig. 2, we illustrate the potential of microfluidics in the future evolution of biohybrid robots-a combination of tissue engineering and robotics. Even if most biohybrid robotic research has thus far focused on bioactuation, the interest in other biofunctionalities is increasing, as demonstrated by recent publications concerning the sensing of the environment and control of movements (16,18,19,47). Microfluidics will play a crucial role in well-established biofunctionalities, as well as in the emergent ones. ...
... Recognizing biochemicals in the surroundings, whether they are liquid media or air, is a typical use for biosensors, and it can be exploited to create experiences of "taste" or "olfaction" in robots, in which the biochemical detection communicates with the robot control system to affect motion (18). Nevertheless, the perception of other types of stimuli remains widely unexplored. ...
Article
The next robotics frontier will be led by biohybrids. Capable biohybrid robots require microfluidics to sustain, improve, and scale the architectural complexity of their core ingredient: biological tissues. Advances in microfluidics have already revolutionized disease modeling and drug development, and are positioned to impact regenerative medicine but have yet to apply to biohybrids. Fusing microfluidics with living materials will improve tissue perfusion and maturation, and enable precise patterning of sensing, processing, and control elements. This perspective suggests future developments in advanced biohybrids.
... Furthermore, although inverted and vertical climbing was demonstrated [1,4], maneuvering across complex terrains is still a conundrum for these artificial robots. However, the answers to these challenges might be found in the emerging ideas of biohybrid systems, which utilize the advantages of organic components in robotics applications [6][7][8][9][10]. While bio-inspired and biomimetic systems seek insights from living materials, biohybrid systems incorporate them with synthetics devices [6,8]. ...
... However, the answers to these challenges might be found in the emerging ideas of biohybrid systems, which utilize the advantages of organic components in robotics applications [6][7][8][9][10]. While bio-inspired and biomimetic systems seek insights from living materials, biohybrid systems incorporate them with synthetics devices [6,8]. This approach allows the hybrid systems to exploit both organic and artificial benefits from their two facets [6,8]. ...
... While bio-inspired and biomimetic systems seek insights from living materials, biohybrid systems incorporate them with synthetics devices [6,8]. This approach allows the hybrid systems to exploit both organic and artificial benefits from their two facets [6,8]. These systems were successfully and widely demonstrated in the form of millimeter-scale actuators or aquatic/airborne miniature robots [7][8][9][10]. ...
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Preprint
Terrestrial cyborg insects were long discussed as potential complements for insect-scale mobile robots. These cyborgs inherit the insects' outstanding locomotory skills, orchestrated by a sophisticated central nervous system and various sensory organs, favoring their maneuvers in complex terrains. However, the autonomous navigation of these cyborgs was not yet comprehensively studied. The struggle to select optimal stimuli for individual insects hinders reliable and accurate navigations. This study overcomes this problem and provides a detailed look at the terrestrial navigation of cyborg insects (darkling beetle) by implementing a feedback control system. Via a thrust controller for acceleration and a proportional controller for turning, the system regulates the stimulation parameters depending on the beetle's instantaneous status. Adjusting the system's control parameters allows reliable and precise path-following navigations (i.e., up to ~94% success rate, ~1/2 body length accuracy). Also, the system's performance can be tuned, providing flexibility to navigation applications of terrestrial cyborg insects. Video: https://youtu.be/p00mfxFo7VY
... New sensors based on piezoelectric and pyroelectric effects [31] can be applied to environmental monitoring by measuring temperature and pressure. Olfactory sensors consisting of insect tentacles combined with mechanical devices can be used to track down the source of gas leaks or fires, thus identifying explosives, disaster prevention, and disaster relief [32]. An intracortical brain-computer interface enables paralyzed people to gain typing speed comparable to that of normal people by decoding neural activity [33]. ...
... electric effects [31] can be applied to environmental monitoring by measuring temperature and pressure. Olfactory sensors consisting of insect tentacles combined with mechanical devices can be used to track down the source of gas leaks or fires, thus identifying explosives, disaster prevention, and disaster relief [32]. An intracortical brain-computer interface enables paralyzed people to gain typing speed comparable to that of normal people by decoding neural activity [33]. ...
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Intelligent unmanned systems for ground, sea, aviation, and aerospace application are important research directions for the new generation of artificial intelligence in China. Intelligent unmanned systems are also important carriers of interactive mapping between physical space and cyberspace in the process of the digitization of human society. Based on the current domestic and overseas development status of unmanned systems for ground, sea, aviation, and aerospace application, this paper reviewed the theoretical problems and research trends of multi-agent cross-domain cooperative perception. The scenarios of multi-agent cooperative perception tasks in different areas were deeply investigated and analyzed, the scientific problems of cooperative perception were analyzed, and the development direction of multi-agent cooperative perception theory research for solving the challenges of the complex environment, interactive communication, and cross-domain tasks was expounded.
... This is mostly due to the complex spreading of gas in cluttered environments. Moreover, current sensors have poor quality compared to animals' smelling capabilities [7], which is further complicated by the propellers' own down-wash [8]. ...
... Hence, we replace the gas-seeking part of Sniffy Bug (PSO) by two other well-known strategies, leading to (i) Sniffy Bug with anemotaxis, and (ii) Sniffy Bug with chemotaxis. In the case of anemotaxis, inspired by [7], waypoints are placed randomly when no gas is present, and upwind when gas is detected. Then, when the agent loses track of the plume, it generates random waypoints around the last point it has seen inside the plume, until it finds the plume again. ...
... This is mostly due to the complex spreading of gas in cluttered environments. Moreover, current sensors have poor quality compared to animals' smelling capabilities [7], which is further complicated by the propellers' own down-wash [8]. ...
... Hence, we replace the gas-seeking part of Sniffy Bug (PSO) by two other well-known strategies, leading to (i) Sniffy Bug with anemotaxis, and (ii) Sniffy Bug with chemotaxis. In the case of anemotaxis, inspired by [7], waypoints are placed randomly when no gas is present, and upwind when gas is detected. Then, when the agent loses track of the plume, it generates random waypoints around the last point it has seen inside the plume, until it finds the plume again. ...
Full-text available
Preprint
Nano quadcopters are ideal for gas source localization (GSL) as they are safe, agile and inexpensive. However, their extremely restricted sensors and computational resources make GSL a daunting challenge. In this work, we propose a novel bug algorithm named `Sniffy Bug', which allows a fully autonomous swarm of gas-seeking nano quadcopters to localize a gas source in an unknown, cluttered and GPS-denied environments. The computationally efficient, mapless algorithm foresees in the avoidance of obstacles and other swarm members, while pursuing desired waypoints. The waypoints are first set for exploration, and, when a single swarm member has sensed the gas, by a particle swarm optimization-based procedure. We evolve all the parameters of the bug (and PSO) algorithm, using our novel simulation pipeline, `AutoGDM'. It builds on and expands open source tools in order to enable fully automated end-to-end environment generation and gas dispersion modeling, allowing for learning in simulation. Flight tests show that Sniffy Bug with evolved parameters outperforms manually selected parameters in cluttered, real-world environments.
... Moreover, Martinez et al. [102] incorporated entire olfactory systems of the insects into the robotic systems to control the robots and localize odour via intact signals form insect antenna. Recently, Adnerson et al. [104,105] patented bio-hybrid odour-guided autonomous palm-sized air vehicle equipped with the odoursensing antenna of an insect. They demonstrated that insect antennae respond more quickly than metal oxide gas sensors, enabling odour localization at an improved speed over previous flying robots [105]. ...
... Recently, Adnerson et al. [104,105] patented bio-hybrid odour-guided autonomous palm-sized air vehicle equipped with the odoursensing antenna of an insect. They demonstrated that insect antennae respond more quickly than metal oxide gas sensors, enabling odour localization at an improved speed over previous flying robots [105]. Recently, Saha et al. [25] proposed a hybrid device based on the olfactory sensors and sophisticated neural computational framework available in an insect olfactory system ( Fig. 6.3). ...
Article
Due to unique abilities of the animals regarding analysis of complex gas substances, they still remain a gold standard in analysis of explosives. Unusual capabilities of biological chemosensory systems, including both vertebrates and invertebrates, stimulate elaboration of the devices mimicking their activity and operation parameters as precisely as possible. The electronic analogues are a subject of investigation in many research centres, which brings their successful commercialization closer. They are believed to substitute or to complement animals in the analysis of gas substances, including explosive and hazardous ones. The limitations of classic gas sensors can be overcome using the strategies inspired by the solutions known from biological systems. Apart from high selectivity and sensitivity desired for analysis of the explosives, mimicking biological systems allows overcoming other problems connected mainly with effective sampling and odour localization. Presented review is focused on the biomimetic devices, which mimic the sense of smell in a direct way and which are the inspiration to design the devices used for detection of the explosives. Potential of biosensors and bioelectronic noses (B-ENs) to mimic the incredibly accurate and versatile "biological noses" was evaluated. A summary of the strategies inspired by biological olfactory systems should facilitate the approach to the problem of artificial instruments design and to development of the strategy aimed at analysis of the explosives with these systems.
... In addition, we will develop a quadcopter system that can operate as intended in a space with multiple odor sources by incorporating an algorithm that discriminates between the target and background odors. Moreover, we will enhance our system to be a practical system by incorporating the proposed wind direction estimation method [41] or a mechanism that physically faces upwind by attaching fins [42] into the system, because this experiment was conducted assuming an upwind direction. ...
Article
In this study, we designed and experimentally verified the placement of odor sensors and an algorithm using the aero-olfactory effect of a palm-sized quadcopter to solve the three-dimensional chemical plume tracking (3D-CPT) problem. Solving 3D-CPT is important in engineering as it helps perform rescue operations during disasters and identify sources of harmful substances. Moreover, the odor sensors must be properly located and a CPT algorithm be applied to improve the tracking performance of a chemical. However, studies regarding the use of quadcopters for solving the 3D-CPT problem are scarce, and the relationship between the odor sensor location and algorithm is debatable. Hence, we utilized particle image velocimetry, an airflow visualization technology, to evaluate the arrival direction of chemicals at different heights. The results showed that odor sensors must be placed on the upper and front surfaces of a quadcopter to monitor the chemicals three-dimensionally. Additionally, we designed a 3D surge-casting algorithm, which is an extension of the CPT strategy of a flying moth, that is, surge casting, to accommodate the proposed odor sensor placement. By conducting 3D-CPT experiments based on different heights of odor sources using the proposed system, we discovered that even in an environment with significant changes in the wind direction the CPT performance is better than that of the conventional 3D-CPT algorithm. Thus, 3D-CPT should be further improved to enable its application in unknown and cluttered environments. In this study, we improved the 3D-CPT performance of a palm-sized quadcopter by designing an appropriate sensor arrangement and algorithm balance.
... In terms of olfactory, a low-cost gas sensor has been deployed [23] on a robot to search for the gas source in a turbulent and diffusive environment. Even circuits or robots have been equipped with insects' odor-sensing antennae to perform specific tasks [24]- [27]. Thus, olfactory is feasible for robots. ...
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Preprint
Searching in a denied environment is challenging for swarm robots as no assistance from GNSS, mapping, data sharing, and central processing are allowed. However, using olfactory and auditory to cooperate like animals could be an important way to improve the collaboration of swarm robots. In this paper, an Olfactory-Auditory augmented Bug algorithm (OA-Bug) is proposed for a swarm of autonomous robots to explore a denied environment. A simulation environment is built to measure the performance of OA-Bug. The coverage of the search task using OA-Bug can reach 96.93%, with the most significant improvement of 40.55% compared with a similar algorithm, SGBA. Furthermore, experiments are conducted on real swarm robots to prove the validity of OA-Bug. Results show that OA-Bug can improve the performance of swarm robots in a denied environment.
... An even bigger limitation in this field is the impending explosion in the prevalence of truly unusual living creatures and distributed systems [30]. Novel living beings produced by engineering and hybrid approaches (such as evolutionary design) include ex vivo constructs such as embryoids, organoids, and assembloids [31,32], cyborgs of animals and plants [3,4,[33][34][35][36][37][38] resulting from living tissue tightly integrated with designed inorganic interfaces [39,40] and with closed-loop control systems [41], biological robots such as computer-controlled invertebrates [42][43][44], and hybrots consisting of living brains instrumentized to control artificial new bodies [1,43,[45][46][47][48][49]. Without any familiar phylogenetic guideposts (e.g., "it's a kind of fish so we expect a fish-like range of behaviors"), it may be extremely difficult to place the intelligence of novel, synthetic creatures with respect to the familiar examples. ...
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Intelligence is a central feature of human beings’ primary and interpersonal experience. Understanding how intelligence originated and scaled during evolution is a key challenge for modern biology. Some of the most important approaches to understanding intelligence are the ongoing efforts to build new intelligences in computer science (AI) and bioengineering. However, progress has been stymied by a lack of multidisciplinary consensus on what is central about intelligence regardless of the details of its material composition or origin (evolved vs. engineered). We show that Buddhist concepts offer a unique perspective and facilitate a consilience of biology, cognitive science, and computer science toward understanding intelligence in truly diverse embodiments. In coming decades, chimeric and bioengineering technologies will produce a wide variety of novel beings that look nothing like familiar natural life forms; how shall we gauge their moral responsibility and our own moral obligations toward them, without the familiar touchstones of standard evolved forms as comparison? Such decisions cannot be based on what the agent is made of or how much design vs. natural evolution was involved in their origin. We propose that the scope of our potential relationship with, and so also our moral duty toward, any being can be considered in the light of Care—a robust, practical, and dynamic lynchpin that formalizes the concepts of goal-directedness, stress, and the scaling of intelligence; it provides a rubric that, unlike other current concepts, is likely to not only survive but thrive in the coming advances of AI and bioengineering. We review relevant concepts in basal cognition and Buddhist thought, focusing on the size of an agent’s goal space (its cognitive light cone) as an invariant that tightly links intelligence and compassion. Implications range across interpersonal psychology, regenerative medicine, and machine learning. The Bodhisattva’s vow (“for the sake of all sentient life, I shall achieve awakening”) is a practical design principle for advancing intelligence in our novel creations and in ourselves.
... The second-order question is, what's it like to be a caterpillar, slowly changing into a butterfly as its brain is largely dissolved and reassembled into a different architecture for an animal whose sense organs, effectors, and perhaps overall Umwelt is completely different. All of this raises fascinating issues of first person experience not only in purely biological metamorphoses (such as human patients undergoing stem cell implants into their brains), but also technological hybrids such as brains instrumentized with novel sensory arrays, robotic bodies, software information systems, or brains functionally linked to other brains (Warwick et al., 1998;Demarse et al., 2001;Potter et al., 2003;Bakkum et al., 2007a,b;Tsuda et al., 2009;Cohen-Karni et al., 2012;Giselbrecht et al., 2013;Aaser et al., 2017;Ricotti et al., 2017;Ding et al., 2018;Mehrali et al., 2018;Anderson et al., 2020;Ando and Kanzaki, 2020;Merritt et al., 2020;Orive et al., 2020;Saha et al., 2020;Dong et al., 2021;Li et al., 2021;Pio-Lopez, 2021). The developmental approach to the emergence of consciousness on short, ontogenetic timescales complements the related question on phylogenetic timescales, and is likely to be a key component of mature theories in this field. ...
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Synthetic biology and bioengineering provide the opportunity to create novel embodied cognitive systems (otherwise known as minds) in a very wide variety of chimeric architectures combining evolved and designed material and software. These advances are disrupting familiar concepts in the philosophy of mind, and require new ways of thinking about and comparing truly diverse intelligences, whose composition and origin are not like any of the available natural model species. In this Perspective, I introduce TAME—Technological Approach to Mind Everywhere—a framework for understanding and manipulating cognition in unconventional substrates. TAME formalizes a non-binary (continuous), empirically-based approach to strongly embodied agency. TAME provides a natural way to think about animal sentience as an instance of collective intelligence of cell groups, arising from dynamics that manifest in similar ways in numerous other substrates. When applied to regenerating/developmental systems, TAME suggests a perspective on morphogenesis as an example of basal cognition. The deep symmetry between problem-solving in anatomical, physiological, transcriptional, and 3D (traditional behavioral) spaces drives specific hypotheses by which cognitive capacities can increase during evolution. An important medium exploited by evolution for joining active subunits into greater agents is developmental bioelectricity, implemented by pre-neural use of ion channels and gap junctions to scale up cell-level feedback loops into anatomical homeostasis. This architecture of multi-scale competency of biological systems has important implications for plasticity of bodies and minds, greatly potentiating evolvability. Considering classical and recent data from the perspectives of computational science, evolutionary biology, and basal cognition, reveals a rich research program with many implications for cognitive science, evolutionary biology, regenerative medicine, and artificial intelligence.
... For a motion planning approach using chemical-sensing drones see Bourne et al. (2020). Nano drone chemical-sensing approaches have been demonstrated (Burgués et al., 2019;Anderson et al., 2020). However short flight times make them impractical for the larger-scale volcano surveys we target. ...
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We present methods for autonomous collaborative surveying of volcanic CO2 emissions using aerial robots. CO2 is a useful predictor of volcanic eruptions and an influential greenhouse gas. However, current CO2 mapping methods are hazardous and inefficient, as a result, only a small fraction of CO2 emitting volcanoes have been surveyed. We develop algorithms and a platform to measure volcanic CO2 emissions. The Dragonfly Unpiloted Aerial Vehicle (UAV) platform is capable of long-duration CO2 collection flights in harsh environments. We implement two survey algorithms on teams of Dragonfly robots and demonstrate that they effectively map gas emissions and locate the highest gas concentrations. Our experiments culminate in a successful field test of collaborative rasterization and gradient descent algorithms in a challenging real-world environment at the edge of the Valles Caldera supervolcano. Both algorithms treat multiple flocking UAVs as a distributed flexible instrument. Simultaneous sensing in multiple UAVs gives scientists greater confidence in estimates of gas concentrations and the locations of sources of those emissions. These methods are also applicable to a range of other airborne concentration mapping tasks, such as pipeline leak detection and contaminant localization.
... (18)(19)(20) Furthermore, insect antennae have also been used as olfactory sensors for mobile robots to evaluate searching algorithms in actual odor environments. (21)(22)(23)(24) However, EAG measurement has the disadvantage of being susceptible to electrical and mechanical noise. (25,26) In particular, when EAG measurement is performed using mobile robots, the odor response decreases over time if isolated antennae are used. ...
Article
Extremely sensitive odor sensors are required for odor searching in mobile robots. The male silkmoth (Bombyx mori) is a candidate biosensor because of its high sensitivity to the conspecific sex pheromone with stereotypic searching behavior. Furthermore, the odor preferences of silkmoths can be modified using genetic tools. Therefore, techniques that can easily detect the odor response of silkmoths with high sensitivity have become important for odor detection and searching. In recent years, machine learning has been used to classify the behaviors of silkmoths to estimate the timing of odor reception. Therefore, it is possible to utilize a silkmoth’s behavioral response as an olfactory sensor for robotic odor searching. In this work, we developed an odor-searching mobile robot with an odor sensing device based on a silkmoth’s walking pattern. First, we collected behavioral data with and without odor stimuli. Then, we predicted the presence of an odor using a support vector machine. Finally, we implemented the sensing device in an odor-searching robot and demonstrated that the classifier performance was sufficient for a robot to localize an odor source by utilizing artificial searching algorithms. These results indicated the feasibility of an insect-behavior-based olfactory sensor for robotic odor searching.
... Flying insects have emerged as excellent model systems for studying how organisms track chemical plumes in moving fluids [16], [17], serving as inspiration for small robotic systems [18]. One strategy proposed to explain insects' ability to orient with respect to ambient wind, called visual anemotaxis [19], allows them to orient upwind by turning until the angle of perceived apparent wind is aligned with the angle of motion. ...
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Preprint
Estimating the direction of ambient fluid flow is key for many flying or swimming animals and robots, but can only be accomplished through indirect measurements and active control. Recent work with tethered flying insects indicates that their sensory representation of orientation, apparent flow, direction of movement, and control is represented by a 2-dimensional angular encoding in the central brain. This representation simplifies sensory integration by projecting the direction (but not scale) of measurements with different units onto a universal polar coordinate frame. To align these angular measurements with one another and the motor system does, however, require a calibration of angular gain and offset for each sensor. This calibration could change with time due to changes in the environment or physical structure. The circumstances under which small robots and animals with angular sensors and changing calibrations could self-calibrate and estimate the direction of ambient fluid flow while moving remains an open question. Here, a methodical nonlinear observability analysis is presented to address this. The analysis shows that it is mathematically feasible to continuously estimate flow direction and perform regular self-calibrations by adopting frequent changes in course (or active prevention thereof) and orientation, and requires fusion and temporal differentiation of three sensory measurements: apparent flow, orientation (or its derivative), and direction of motion (or its derivative). These conclusions are consistent with the zigzagging trajectories exhibited by many plume tracking organisms, suggesting that perhaps flow estimation is a secondary driver of their trajectory structure.
... For example, pixels in EB cameras can signal brightness changes exceeding some threshold; microphones in EB audio sensors can react to sound intensity variations in certain frequency ranges (Li et al., 2012;Liu et al., 2014;Inilabs.com, 2020); EB chemical or olfactory sensor arrays or bio-hybrid sensors can fire as a result of chemical element concentration deviations (Koickal et al., 2007;Chiu and Tang, 2013;Vanarse et al., 2017;Anderson et al., 2020); EB tactile sensors respond to changes in force and movement (Kim et al., 2018;Baghaei Naeini et al., 2020). ...
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Autonomous flight for large aircraft appears to be within our reach. However, launching autonomous systems for everyday missions still requires an immense interdisciplinary research effort supported by pointed policies and funding. We believe that concerted endeavors in the fields of neuroscience, mathematics, sensor physics, robotics, and computer science are needed to address remaining crucial scientific challenges. In this paper, we argue for a bio-inspired approach to solve autonomous flying challenges, outline the frontier of sensing, data processing, and flight control within a neuromorphic paradigm, and chart directions of research needed to achieve operational capabilities comparable to those we observe in nature. One central problem of neuromorphic computing is learning. In biological systems, learning is achieved by adaptive and relativistic information acquisition characterized by near-continuous information retrieval with variable rates and sparsity. This results in both energy and computational resource savings being an inspiration for autonomous systems. We consider pertinent features of insect, bat and bird flight behavior as examples to address various vital aspects of autonomous flight. Insects exhibit sophisticated flight dynamics with comparatively reduced complexity of the brain. They represent excellent objects for the study of navigation and flight control. Bats and birds enable more complex models of attention and point to the importance of active sensing for conducting more complex missions. The implementation of neuromorphic paradigms for autonomous flight will require fundamental changes in both traditional hardware and software. We provide recommendations for sensor hardware and processing algorithm development to enable energy efficient and computationally effective flight control.
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Tiny “gnat robots,” weighing just a few milligrams, were first conjectured in the 1980s. How to stabilize one if it were to hover like a small insect has not been answered. Challenges include the requirement that sensors be both low mass and high bandwidth and that silicon-micromachined rate gyroscopes are too heavy. The smallest robot to perform controlled hovering uses a sensor suite weighing hundreds of milligrams. Here, we demonstrate that an accelerometer represents perhaps the most direct way to stabilize flight while satisfying the extreme size, speed, weight, and power constraints of a flying robot even as it scales down to just a few milligrams. As aircraft scale reduces, scaling physics dictates that the ratio of aerodynamic drag to mass increases. This results in reduced noise in an accelerometer’s airspeed measurement. We show through simulation and experiment on a 30-gram robot that a 2-milligram off-the-shelf accelerometer is able in principle to stabilize a 10-milligram robot despite high noise in the sensor itself. Inspired by wind-vision sensory fusion in the flight controller of the fruit fly Drosophila melanogaster , we then added a tiny camera and efficient, fly-inspired autocorrelation-based visual processing to allow the robot to estimate and reject wind as well as control its attitude and flight velocity using a Kalman filter. Our biology-inspired approach, validated on a small flying helicopter, has a wind gust response comparable to the fruit fly and is small and efficient enough for a 10-milligram flying vehicle (weighing less than a grain of rice).
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The past ten years have seen the rapid expansion of the field of biohybrid robotics. By combining engineered, synthetic components with living biological materials, new robotics solutions have been developed that harness the adaptability of living muscles, the sensitivity of living sensory cells, and even the computational abilities of living neurons. Biohybrid robotics has taken the popular and scientific media by storm with advances in the field, moving biohybrid robotics out of science fiction and into real science and engineering. So how did we get here, and where should the field of biohybrid robotics go next? In this perspective, we first provide the historical context of crucial subareas of biohybrid robotics by reviewing the past 10+ years of advances in microorganism-bots and sperm-bots, cyborgs, and tissue-based robots. We then present critical challenges facing the field and provide our perspectives on the vital future steps towards creating autonomous living machines.
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Flying insects encounter turbulent environments, where chemotaxis along a concentration gradient makes little sense. Detection of the onset and offset of discrete odor pulses is then expected to become crucial for navigation, but it is not well understood how the olfactory system encodes the offset of the odor pulse. Previous works indicated that the duration of a male moth olfactory receptor neuron's (ORN) spike firing response to pheromone stimuli greatly exceeds the pulse duration. However, these works were based on imprecise odor delivery systems. We built an odor delivery system capable of delivering much sharper pheromone stimuli. The stimuli evoked ORN firing responses that faithfully tracked the stimulus duration, provided the stimulus lasted at least 200 ms. A transient inhibition marked the termination of such stimuli. Shorter stimuli produced a firing response exceeding the stimulus duration. The response shapes could be explained by adaptation of the ORN on only two time scales. With simulations, we showed that the observed limits in stimulus offset detection propagate to the antennal lobe and are likely to be behaviorally significant. Our results increase the understanding of the mechanisms necessary for male moths to navigate through pheromone plumes.
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The rich variety of biological forms and behaviours results from one evolutionary history on Earth, via frozen accidents and selection in specific environments. This ubiquitous baggage in natural, familiar model species obscures the plasticity and swarm intelligence of cellular collectives. Significant gaps exist in our understanding of the origin of anatomical novelty, of the relationship between genome and form, and of strategies for control of large-scale structure and function in regenerative medicine and bioengineering. Analysis of living forms that have never existed before is necessary to reveal deep design principles of life as it can be. We briefly review existing examples of chimaeras, cyborgs, hybrots and other beings along the spectrum containing evolved and designed systems. To drive experimental progress in multicellular synthetic morphology, we propose teleonomic (goal-seeking, problem-solving) behaviour in diverse problem spaces as a powerful invariant across possible beings regardless of composition or origin. Cybernetic perspectives on chimaeric morphogenesis erase artificial distinctions established by past limitations of technology and imagination. We suggest that a multi-scale competency architecture facilitates evolution of robust problem-solving, living machines. Creation and analysis of novel living forms will be an essential testbed for the emerging field of diverse intelligence, with numerous implications across regenerative medicine, robotics and ethics.
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Autonomous robots are expected to perform a wide range of sophisticated tasks in complex, unknown environments. However, available onboard computing capabilities and algorithms represent a considerable obstacle to reaching higher levels of autonomy, especially as robots get smaller and the end of Moore's law approaches. Here, we argue that inspiration from insect intelligence is a promising alternative to classic methods in robotics for the artificial intelligence (AI) needed for the autonomy of small, mobile robots. The advantage of insect intelligence stems from its resource efficiency (or parsimony) especially in terms of power and mass. First, we discuss the main aspects of insect intelligence underlying this parsimony: embodiment, sensory-motor coordination, and swarming. Then, we take stock of where insect-inspired AI stands as an alternative to other approaches to important robotic tasks such as navigation and identify open challenges on the road to its more widespread adoption. Last, we reflect on the types of processors that are suitable for implementing insect-inspired AI, from more traditional ones such as microcontrollers and field-programmable gate arrays to unconventional neuromorphic processors. We argue that even for neuromorphic processors, one should not simply apply existing AI algorithms but exploit insights from natural insect intelligence to get maximally efficient AI for robot autonomy.
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Among small rotorcraft, the use of multiple compact rotors in a mechanically simple design leads to impressive agility and maneuverability but inevitably results in high energetic demand and acutely restricted endurance. Small spinning propellers used in these vehicles contrast with large lifting surfaces of winged seeds, which spontaneously gyrate into stable autorotation upon falling. The pronounced aerodynamic surfaces and delayed stalls are believed key to efficient unpowered flight. Here, the bioinspired principles are adopted to notably reduce the power consumption of small aerial vehicles by means of a samara-inspired robot. We report a dual-wing 35.1-gram aircraft capable of hovering flight via powered gyration. Equipped with two rotors, the underactuated robot with oversized revolving wings, designed to leverage unsteady aerodynamics, was optimized for boosted flight efficiency. Through the analysis of flight dynamics and stability, the vehicle was designed for passive attitude stability, eliminating the need for fast feedback to stay upright. To this end, the drone demonstrates flight with a twofold decrease in power consumption when compared with benchmark multirotor robots. Exhibiting the power loading of 8.0 grams per watt, the vehicle recorded a flight time of 14.9 minutes and up to 24.5 minutes when equipped with a larger battery. Taking advantage of the fast revolving motion to overcome the severe underactuation, we also realized position-controlled flight and illustrated examples of mapping and surveillance applications with a 21.5-gram payload.
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In recent years, there has been a great deal of research on olfaction in organisms at the molecular level, and a database of responses to various odorants has been compiled. Insects, in particular, have an excellent ability to detect odorants, and their olfactory mechanisms have been remarkably elucidated based on genetic engineering methods. Therefore, we are focusing on the olfactory system of insects and investigating the use of insect olfactory receptors and organisms for the application of odorant sensors. In this article, we describe the use of the insect olfactory receptor expression system in heterologous cells and the production of transgenic silkmoths for development of odorant biosensors.
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Small drones with chemical or biosensor devices that can detect airborne odorant molecules have attracted considerable attention owing to their applicability in environmental and security monitoring and search-and-rescue operations. Small drones with commercial metal-oxide-semiconductor (MOX) gas sensors have been developed for odor source localization; however, their real-time-odor-detection performance has proven inadequate. However, biosensing technologies based on insect olfactory systems exhibit relatively high sensitivity, selectivity, and real-time response with respect to odorant molecules compared to commercial MOX gas sensors. In such devices, excised insect antennae function as portable odorant biosensor elements and have been found to deliver excellent sensing performance. This study presents experimental protocols for odorant-molecule detection in the air using a small autonomous bio-hybrid drone based on a mountable electroantennography (EAG) device incorporating silkmoth antennae. We developed a mountable EAG device including sensing/processing parts with a Wi-Fi module. The device was equipped with a simple sensor enclosure to enhance the sensor directivity. Thus, odor source localization was conducted using the spiral-surge algorithm, which does not assume an upwind direction. The experimental bio-hybrid odor-detecting drone identified real-time odorant-concentration differences in a pseudo-open environment (outside a wind tunnel) and localized the source. The developed drone and associated system can serve as an efficient odorant molecule-detection tool and a suitable flight platform for developing odor source localization algorithms owing to its high programmability. © 2021 JoVE Creative Commons Attribution-NonCommercial-NoDerivs 3.0 Unported License.
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Small drones with biosensor devices have great potential for detecting odorant molecules in air and can be applied to environmental and security monitoring. To realize these applications, two important factors are considered: first, development of highly sensitive, selective, and real-time odorant sensor devices, and second, construction of a highly maneuverable platform with efficient odor source localization. Previously, small drones with commercial gas sensors or biosensors based on insect antennas have been developed. However, the performance of gas sensors proved to be inadequate for real-time sensing; the flight performance of a bio-hybrid drone was limited because the yaw turn was not considered and flight tests were conducted in a wind tunnel. In this study, we developed a fully autonomous small drone with a portable electroantennogram (EAG) based on silkmoth antennae mounted on it. The EAG device was also equipped with a sensor enclosure to enhance sensor directivity. The bio-hybrid drone can recognize real-time odorant concentration differences in a pseudo-open environment (outside the wind tunnel). We also developed an enclosure for enhancing the sensor directivity of EAG. Owing to the enclosure, the drone could distinguish the front-back direction in the odor plume without a wind direction sensor. Based on these results, the drone recognized the maximum value of odorant concentration during an over 360° yaw turn and localized the odor source using the spiral-surge algorithm without any assumption of the upwind direction. This study proposes an efficient flight platform for detecting odorant molecules in air and localizing their sources.
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Artificial control of animal locomotion has the potential to simultaneously address longstanding challenges to actuation, control, and power requirements in soft robotics. Robotic manipulation of locomotion can also address previously inaccessible questions about organismal biology otherwise limited to observations of naturally occurring behaviors. Here, we present a biohybrid robot that uses onboard microelectronics to induce swimming in live jellyfish. Measurements demonstrate that propulsion can be substantially enhanced by driving body contractions at an optimal frequency range faster than natural behavior. Swimming speed can be enhanced nearly threefold, with only a twofold increase in metabolic expenditure of the animal and 10 mW of external power input to the microelectronics. Thus, this biohybrid robot uses 10 to 1000 times less external power per mass than other aquatic robots reported in literature. This capability can expand the performance envelope of biohybrid robots relative to natural animals for applications such as ocean monitoring.
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Mosquitoes are important vectors of disease and require sources of carbohydrates for reproduction and survival. Unlike host-related behaviors of mosquitoes, comparatively less is understood about the mechanisms involved in nectar-feeding decisions, or how this sensory information is processed in the mosquito brain. Here we show that Aedes spp. mosquitoes, including Aedes aegypti , are effective pollinators of the Platanthera obtusata orchid, and demonstrate this mutualism is mediated by the orchid’s scent and the balance of excitation and inhibition in the mosquito’s antennal lobe (AL). The P. obtusata orchid emits an attractive, nonanal-rich scent, whereas related Platanthera species—not visited by mosquitoes—emit scents dominated by lilac aldehyde. Calcium imaging experiments in the mosquito AL revealed that nonanal and lilac aldehyde each respectively activate the LC2 and AM2 glomerulus, and remarkably, the AM2 glomerulus is also sensitive to N,N-diethyl-meta-toluamide (DEET), a mosquito repellent. Lateral inhibition between these 2 glomeruli reflects the level of attraction to the orchid scents. Whereas the enriched nonanal scent of P. obtusata activates the LC2 and suppresses AM2, the high level of lilac aldehyde in the other orchid scents inverts this pattern of glomerular activity, and behavioral attraction is lost. These results demonstrate the ecological importance of mosquitoes beyond operating as disease vectors and open the door toward understanding the neural basis of mosquito nectar-seeking behaviors.
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The electroantennogram (EAG) is a technique used for measuring electrical signals from the antenna of an insect. Its rapid response time, quick recovery speed, and high sensitivity make it suitable for odour-tracking tasks employing mobile robots. However, its application to flying robots has not been extensively studied owing to the electrical and mechanical noises generated. In this study, we investigated the characteristics of the EAG mounted on a tethered flying quadcopter and developed a special counter-based algorithm for detecting the odour-generated responses. As the EAG response is negative, the algorithm creates a window and compares the values inside it. Once a value is smaller than the first one, the counter will increase by one and finally turns the whole signal into a clearer odour stimulated result. By experimental evaluation, the new algorithm gives a higher cross-correlation coefficient when compared with the fixed-threshold method. The result shows that the accuracy of this novel algorithm for recognising odour-evoked EAG signals from noise exceeds that of the traditional method; furthermore, the use of insect antennae as odour sensors for flying robots is demonstrated to be feasible.
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We have designed a bio-hybrid Fly-Robot Interface (FRI) to study sensorimotor control in insects. The FRI consists of a miniaturized recording platform mounted on a 2-wheeled robot and is controlled by the neuronal spiking activity of an identified visual interneuron, the blowfly H1-cell. For a given turning radius of the robot, we found a proportional relationship between the spike rate of the H1-cell and the relative distance of the FRI from the patterned wall of an experimental arena. Under closed-loop conditions during oscillatory forward movements biased towards the wall, collision avoidance manoeuvres were triggered whenever the H1-cell spike rate exceeded a certain threshold value. We also investigated the FRI behaviour in corners of the arena. The ultimate goal is to enable autonomous and energy-efficient manoeuvrings of the FRI within arbitrary visual environments.
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The hawkmoth Manduca sexta and one of its preferred hosts in the North American Southwest, Datura wrightii , share a model insect–plant relationship based on mutualistic and antagonistic life-history traits. D. wrightii is the innately preferred nectar source and oviposition host for M. sexta . Hence, the hawkmoth is an important pollinator while the M. sexta larvae are specialized herbivores of the plant. Olfactory detection of plant volatiles plays a crucial role in the behavior of the hawkmoth. In vivo, the odorant receptor coreceptor (Orco) is an obligatory component for the function of odorant receptors (ORs), a major receptor family involved in insect olfaction. We used CRISPR-Cas9 targeted mutagenesis to knock out (KO) the MsexOrco gene to test the consequences of a loss of OR-mediated olfaction in an insect–plant relationship. Neurophysiological characterization revealed severely reduced antennal and antennal lobe responses to representative odorants emitted by D. wrightii . In a wind-tunnel setting with a flowering plant, Orco KO hawkmoths showed disrupted flight orientation and an ablated proboscis extension response to the natural stimulus. The Orco KO gravid female displayed reduced attraction toward a nonflowering plant. However, more than half of hawkmoths were able to use characteristic odor-directed flight orientation and oviposit on the host plant. Overall, OR-mediated olfaction is essential for foraging and pollination behaviors, but plant-seeking and oviposition behaviors are sustained through additional OR-independent sensory cues.
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This paper describes the development and validation of the currently smallest aerial platform with olfaction capabilities. The developed Smelling Nano Aerial Vehicle (SNAV) is based on a lightweight commercial nano-quadcopter (27 g) equipped with a custom gas sensing board that can host up to two in situ metal oxide semiconductor (MOX) gas sensors. Due to its small form-factor, the SNAV is not a hazard for humans, enabling its use in public areas or inside buildings. It can autonomously carry out gas sensing missions of hazardous environments inaccessible to terrestrial robots and bigger drones, for example searching for victims and hazardous gas leaks inside pockets that form within the wreckage of collapsed buildings in the aftermath of an earthquake or explosion. The first contribution of this work is assessing the impact of the nano-propellers on the MOX sensor signals at different distances to a gas source. A second contribution is adapting the ‘bout’ detection algorithm, proposed by Schmuker et al. (2016) to extract specific features from the derivative of the MOX sensor response, for real-time operation. The third and main contribution is the experimental validation of the SNAV for gas source localization (GSL) and mapping in a large indoor environment (160 m2) with a gas source placed in challenging positions for the drone, for example hidden in the ceiling of the room or inside a power outlet box. Two GSL strategies are compared, one based on the instantaneous gas sensor response and the other one based on the bout frequency. From the measurements collected (in motion) along a predefined sweeping path we built (in less than 3 min) a 3D map of the gas distribution and identified the most likely source location. Using the bout frequency yielded on average a higher localization accuracy than using the instantaneous gas sensor response (1.38 m versus 2.05 m error), however accurate tuning of an additional parameter (the noise threshold) is required in the former case. The main conclusion of this paper is that a nano-drone has the potential to perform gas sensing tasks in complex environments.
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In this study, we design and verify an intake system using the wake of a pocket-sized quadcopter for the chemical plume tracing (CPT) problem. Solving CPT represents an important technique in the field of engineering because it can be used to perform rescue operations at the time of a disaster and to identify sources of harmful substances. An appropriate intake of air when sensing odors plays an important role in performing CPT. Hence, we used the air flow generated by a quadcopter itself to intake chemical particles into two alcohol sensors. By experimental evaluation, we verified that the quadcopter wake intake method has good directivity and can be used to realize CPT. Concretely, even at various odor source heights, the quadcopter had a three-dimensional CPT success rate of at least 70%. These results imply that, although a further development of three-dimensional CPT is necessary in order to conduct it in unknown and cluttered environments, the intake method proposed in this paper enables a pocket-sized quadcopter to perform three-dimensional CPT.
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Actuation is essential for artificial machines to interact with their surrounding environment and to accomplish the functions for which they are designed. Over the past few decades, there has been considerable progress in developing new actuation technologies. However, controlled motion still represents a considerable bottleneck for many applications and hampers the development of advanced robots, especially at small length scales. Nature has solved this problem using molecular motors that, through living cells, are assembled into multiscale ensembles with integrated control systems. These systems can scale force production from piconewtons up to kilonewtons. By leveraging the performance of living cells and tissues and directly interfacing them with artificial components, it should be possible to exploit the intricacy and metabolic efficiency of biological actuation within artificial machines. We provide a survey of important advances in this biohybrid actuation paradigm.
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Natural genetic circuits enable cells to make sophisticated digital decisions. Building equally complex synthetic circuits in eukaryotes remains difficult, however, because commonly used components leak transcriptionally, do not arbitrarily interconnect or do not have digital responses. Here, we designed dCas9-Mxi1-based NOR gates in Saccharomyces cerevisiae that allow arbitrary connectivity and large genetic circuits. Because we used the chromatin remodeller Mxi1, our gates showed minimal leak and digital responses. We built a combinatorial library of NOR gates that directly convert guide RNA (gRNA) inputs into gRNA outputs, enabling the gates to be € wired' together. We constructed logic circuits with up to seven gRNAs, including repression cascades with up to seven layers. Modelling predicted the NOR gates have effectively zero transcriptional leak explaining the limited signal degradation in the circuits. Our approach enabled the largest, eukaryotic gene circuits to date and will form the basis for large, synthetic, cellular decision-making systems.
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Male moths aiming to locate pheromone-releasing females rely on stimulus-adapted search maneuvers complicated by a discontinuous distribution of pheromone patches. They alternate sequences of upwind surge when perceiving the pheromone and cross- or downwind casting when the odor is lost. We compare four search strategies: three reactive versus one cognitive. The former consist of pre-programmed movement sequences triggered by pheromone detections while the latter uses Bayesian inference to build spatial probability maps. Based on the analysis of triphasic responses of antennal lobe neurons (On, inhibition, Off), we propose three reactive strategies. One combines upwind surge (representing the On response to a pheromone detection) and spiral casting, only. The other two additionally include crosswind (zigzag) casting representing the Off phase. As cognitive strategy we use the infotaxis algorithm which was developed for searching in a turbulent medium. Detection events in the electroantennogram of a moth attached to a robot indirectly control this cyborg, depending on the strategy in use. The recorded trajectories are analyzed with regard to success rates, efficiency, and other features. In addition, we qualitatively compare our robotic trajectories to behavioral search paths. Reactive searching is more efficient (yielding shorter trajectories) for higher pheromone doses whereas cognitive searching works better for lower doses. With respect to our experimental conditions (2 m from starting position to pheromone source), reactive searching with crosswind zigzag yields the shortest trajectories (for comparable success rates). Assuming that the neuronal Off response represents a short-term memory, zigzagging is an efficient movement to relocate a recently lost pheromone plume. Accordingly, such reactive strategies offer an interesting alternative to complex cognitive searching.
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Robots designed to track chemical leaks in hazardous industrial facilities1 or explosive traces in landmine fields2 face the same problem as insects foraging for food or searching for mates3: the olfactory search is constrained by the physics of turbulent transport4. The concentration landscape of wind borne odors is discontinuous and consists of sporadically located patches. A pre-requisite to olfactory search is that intermittent odor patches are detected. Because of its high speed and sensitivity5-6, the olfactory organ of insects provides a unique opportunity for detection. Insect antennae have been used in the past to detect not only sex pheromones7 but also chemicals that are relevant to humans, e.g., volatile compounds emanating from cancer cells8 or toxic and illicit substances9-11. We describe here a protocol for using insect antennae on autonomous robots and present a proof of concept for tracking odor plumes to their source. The global response of olfactory neurons is recorded in situ in the form of electroantennograms (EAGs). Our experimental design, based on a whole insect preparation, allows stable recordings within a working day. In comparison, EAGs on excised antennae have a lifetime of 2 hr. A custom hardware/software interface was developed between the EAG electrodes and a robot. The measurement system resolves individual odor patches up to 10 Hz, which exceeds the time scale of artificial chemical sensors12. The efficiency of EAG sensors for olfactory searches is further demonstrated in driving the robot toward a source of pheromone. By using identical olfactory stimuli and sensors as in real animals, our robotic platform provides a direct means for testing biological hypotheses about olfactory coding and search strategies13. It may also prove beneficial for detecting other odorants of interests by combining EAGs from different insect species in a bioelectronic nose configuration14 or using nanostructured gas sensors that mimic insect antennae15.
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Gas source localization (GSL) with mobile robots is a challenging task due to the unpredictable nature of gas dispersion, the limitations of the currents sensing technologies, and the mobility constraints of ground-based robots. This work proposes an integral solution for the GSL task, including source declaration. We present a novel pseudo-gradient-based plume tracking algorithm and a particle filter-based source declaration approach, and apply it on a gas-sensitive micro-drone. We compare the performance of the proposed system in simulations and real-world experiments against two commonly used tracking algorithms adapted for aerial exploration missions.
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Significance Insects are widely appreciated for their aerial agility, but the organization of their control system is not well understood. In particular, it is not known how they rapidly integrate information from different sensory systems—such as their eyes and antennae—to regulate flight speed. Although vision may provide an estimate of the true groundspeed in the presence of wind, delays inherent in visual processing compromise the performance of the flight speed regulator and make the animal unstable. Mechanoreceptors on the antennae of flies cannot measure groundspeed directly, but can detect changes in airspeed more quickly. By integrating information from both senses, flies achieve stable regulation of flight speed that is robust to perturbations such as gusts of wind.
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IN studies of moths flying upwind to a pheromone source, attention has focused on the influence on flight orientation of the composition1,2 and concentration3,4 of the chemical message, and of changes in the visual environment5,6 and in wind speeds7-9. The chemical signal must be intermittent for moths to fly upwind10-12, when they usually follow a zigzag track, the evident expression of a self-steered counterturning programme13,14. The integration of counterturning and optomotor anemotaxis allows insects to polarize the zigzags upwind in odour plumes10,15. Not all moths, however, zigzag along a plume16,17. It has been suggested that the propensity to zigzag or to fly straight upwind is related to the frequency at which males encounter pheromone filaments that comprise the plume, as well as the male's latency of response, characteristic for each moth species, to both the onset and loss of contact with filaments18. Here we present evidence that flight manoeuvres are dictated by the interactions of the male with individual odour pulses. We use Cadra cautella, the almond moth, to show how the structure of an odour plume19,20 can greatly modify the flight track. Males following either turbulent or mechanically pulsed plumes fly faster and straighter upwind, and locate sources more frequently than males following continuous narrow plumes. Males also fly straighter upwind to fast-pulsed plumes than to slow-pulsed plumes. The temporally modulated interplay between counterturning and optomotor anemotaxis that is induced by the plume's structure therefore seems to explain the manoeuvres and resultant flight track shapes made by C. cautella males when flying upwind towards a pheromone source.
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In Southwestern USA, the jimsonweed Datura wrightii and the nocturnal sphinx moth Manduca sexta form a pollinator-plant and herbivore-plant association. While certain plant volatile organic compounds (VOCs) attract moths for oviposition, it is likely that other host-derived olfactory cues, such as herbivore-induced VOCs, repel moths for oviposition. Here, we studied the oviposition preference of female M. sexta towards intact and damaged host plants of three species: D. wrightii, D. discolor (a less preferred feeding resource but also used by females for oviposition), and Solanum lycopersicum-tomato-(used by moths as an oviposition resource only). Damage was inflicted to the plants either by larval feeding or artificial damage. Mated females were exposed to an intact plant and a damaged plant and allowed to lay eggs for 10 min. Oviposition preferences of females were highly heterogeneous in all cases, but a larger proportion of moths laid significantly fewer eggs on feeding-damaged and artificially damaged plants of S. lycopersicum. Many females also avoided feeding-damaged D. discolor and D. wrightii plants induced by treatment with methyl jasmonate. Chemical analyses showed a significant increase in the total amount of VOCs released by vegetative tissues of feeding-damaged plants, as well as species-specific increases in emission of certain VOCs. In particular, feeding-damaged S. lycopersicum plants emitted (-)-linalool, an odorant that repels moths for oviposition. Finally, the emission of D. wrightii floral VOCs, which are important in mediating feeding by adult moths (and hence pollination), did not change in plants damaged by larval feeding. We propose that the observed differential effects of herbivory on oviposition choice are due to different characteristics (i.e., mutually beneficial or parasitic) of the insect-plant interaction.
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A 2.5 mW wireless flight control system for cyborg moths is presented, consisting of a 3-to-5 GHz non-coherent pulsed ultra-wideband receiver system-on-chip with an integrated 4-channel pulse-width modulation stimulator mounted on a 1.5 cm by 2.6 cm printed circuit board. The highly duty cycled, energy detection receiver requires 0.5-to-1.4 nJ/bit and achieves a sensitivity of -76 dBm at a data rate of 16 Mb/s (10<sup>-3</sup> BER). A multi-stage inverter-based RF front end with resonant load and differential signal chain allow for robust, low energy operation. Digital calibration is used in the baseband amplifier, ADC and DLL to cancel voltage and timing offsets. Through the use of a flexible PCB and 3-D die stacking, the total weight of the electronics is kept to 1 g, within the carrying capacity of an adult Manduca sexta moth. Preliminary wireless flight control of a moth in a wind tunnel is demonstrated.
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Over time, leg prostheses have improved in design, but have been incapable of actively adapting to different walking velocities in a manner comparable to a biological limb. People with a leg amputation using such commercially available passive-elastic prostheses require significantly more metabolic energy to walk at the same velocities, prefer to walk slower and have abnormal biomechanics compared with non-amputees. A bionic prosthesis has been developed that emulates the function of a biological ankle during level-ground walking, specifically providing the net positive work required for a range of walking velocities. We compared metabolic energy costs, preferred velocities and biomechanical patterns of seven people with a unilateral transtibial amputation using the bionic prosthesis and using their own passive-elastic prosthesis to those of seven non-amputees during level-ground walking. Compared with using a passive-elastic prosthesis, using the bionic prosthesis decreased metabolic cost by 8 per cent, increased trailing prosthetic leg mechanical work by 57 per cent and decreased the leading biological leg mechanical work by 10 per cent, on average, across walking velocities of 0.75-1.75 m s(-1) and increased preferred walking velocity by 23 per cent. Using the bionic prosthesis resulted in metabolic energy costs, preferred walking velocities and biomechanical patterns that were not significantly different from people without an amputation.
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Sensing the chemical environment is critical for all organisms. Diverse animals from insects to mammals utilize highly organized olfactory system to detect, encode, and process chemostimuli that may carry important information critical for health, survival, social interactions and reproduction. Therefore, for animals to properly interpret and react to their environment it is imperative that the olfactory system recognizes chemical stimuli with appropriate selectivity and sensitivity. Because olfactory receptor proteins play such an essential role in the specific recognition of diverse stimuli, understanding how they interact with and transduce their cognate ligands is a high priority. In the nearly two decades since the discovery that the mammalian odorant receptor gene family constitutes the largest group of G protein-coupled receptor (GPCR) genes, much attention has been focused on the roles of GPCRs in vertebrate and invertebrate olfaction. However, is has become clear that the 'family' of olfactory receptors is highly diverse, with roles for enzymes and ligand-gated ion channels as well as GPCRs in the primary detection of olfactory stimuli.
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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.
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Coupled gas chromatography with electroantennographic detection (GC-EAD) using antennae of adult female Manduca sexta was employed to screen for olfactory stimulants present in headspace collections from four species of larval host plants belonging to two families: Solanaceae--Lycopersicon esculentum (tomato), Capiscum annuum (bell pepper), and Datura wrightii; and Martyniaceae--Pronboscideaparviflora. Headspace volatiles were collected from undamaged foliage of potted, living plants. GC-EAD revealed 23 EAD-active compounds, of which 15 were identified by GC-mass spectrometry. Identified compounds included aliphatic, aromatic, and terpenoid compounds bearing a range of functional groups. Nine EAD-active compounds were common to all four host plant species: (Z)-3-hexenyl acetate, nonanal, decanal, phenylacetaldehyde, methyl salicylate, benzyl alcohol, geranyl acetone, (E)-nerolidol, and one unidentified compound. Behavioral responses of female moths to an eight-component synthetic blend of selected tomato headspace volatiles were tested in a laboratory wind tunnel. Females were attracted to the blend. A comparison of responses from antennae of males and females to bell pepper headspace volatiles revealed that males responded to the same suite of volatiles as females, except for (Z)-3-hexenyl benzoate. EAD responses of males also were lower for (Z)-and (E)-nerolidol and one unidentified compound. Electroantennogram EAG dose-response curves for the 15 identified EAD-active volatiles were recorded. At the higher test doses (10-100 microg), female antennae yielded larger EAG responses to terpenoids and to aliphatic and aromatic esters. Male antennae did respond to the higher doses of (Z)-3-hexenyl benzoate, indicating that they can detect this compound. On the basis of ubiquity of the EAD-active volatiles identified to date in host plant headspace collections, we suggest that M. sexta uses a suite of volatiles to locate and identify appropriate host plants.
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The flapping wings of insects and birds induce a strong flow over their body during flight. Although this flow influences the sensory biology and physiology of a flying animal, there are very little data on the characteristics of this self-generated flow field or its biological consequences. A model proposed in the companion paper estimated the induced flow over flying insects. In this study, we used a pair of hot wire anemometers to measure this flow at two locations near the body of a tethered flapping hawk moth, Manduca sexta. The axial inflow anemometer measured the airflow prior to its entry into the stroke plane, whereas the radial outflow anemometer measured the airflow after it crossed the stroke plane. The high temporal resolution of the hot wire anemometers allowed us to measure not only the mean induced flow but also subtle higher frequency disturbances occurring at 1-4 times the wing beat frequency. These data provide evidence for the predictions of a mathematical model proposed in the companion paper. Specifically, the absolute value of the measured induced flow matches the estimate of the model. Also, as predicted by the model, the induced flow varies linearly with wing beat frequency. Our experiments also show that wing flexion contributes significantly to the observed higher frequency disturbances. Thus, the hot wire anemometry technique provides a useful means to quantify the aerodynamic signature of wing flexion. The phasic and tonic components of induced flow influence several physiological processes such as convective heat loss and gas exchange in endothermic insects, as well as alter the nature of mechanosensory and olfactory stimuli to the sensory organs of a flying insect.
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Flying insects have evolved sophisticated sensory capabilities to achieve rapid course control during aerial maneuvers. Among two-winged insects such as houseflies and their relatives, the hind wings are modified into club-shaped, mechanosensory halteres, which detect Coriolis forces and thereby mediate flight stability during maneuvers. Here, we show that mechanosensory input from the antennae serves a similar role during flight in hawk moths, which are four-winged insects. The antennae of flying moths vibrate and experience Coriolis forces during aerial maneuvers. The antennal vibrations are transduced by individual units of Johnston's organs at the base of their antennae in a frequency range characteristic of the Coriolis input. Reduction of the mechanical input to Johnston's organs by removing the antennal flagellum of these moths severely disrupted their flight stability, but reattachment of the flagellum restored their flight control. The antennae thus play a crucial role in maintaining flight stability of moths.
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Odor-mediated insect navigation in airborne chemical plumes is vital to many ecological interactions, including mate finding, flower nectaring, and host locating (where disease transmission or herbivory may begin). After emission, volatile chemicals become rapidly mixed and diluted through physical processes that create a dynamic olfactory environment. This review examines those physical processes and some of the analytical technologies available to characterize those behavior-inducing chemical signals at temporal scales equivalent to the olfactory processing in insects. In particular, we focus on two areas of research that together may further our understanding of olfactory signal dynamics and its processing and perception by insects. First, measurement of physical atmospheric processes in the field can provide insight into the spatiotemporal dynamics of the odor signal available to insects. Field measurements in turn permit aspects of the physical environment to be simulated in the laboratory, thereby allowing careful investigation into the links between odor signal dynamics and insect behavior. Second, emerging analytical technologies with high recording frequencies and field-friendly inlet systems may offer new opportunities to characterize natural odors at spatiotemporal scales relevant to insect perception and behavior. Characterization of the chemical signal environment allows the determination of when and where olfactory-mediated behaviors may control ecological interactions. Finally, we argue that coupling of these two research areas will foster increased understanding of the physicochemical environment and enable researchers to determine how olfactory environments shape insect behaviors and sensory systems.
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In this research, we aim to model an adaptive behavior of an animal and implement it to an autonomous robot. The conventional bio-inspired algorithm is difficult to demonstrate the ability as much as the animal because it models without considering dynamic characteristics of the robot. Therefore, in this study, we constructed an animal-in-the-loop system, which is a novel experimental system for identifying the adaptive behavior of the animal in a form that considers the dynamic characteristics of the robot to be implemented.
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This study reports the first ever demonstration of the aero navigation of a free-flying insect based on feedback control. Instead of imitating the complicated kinetics and mechanisms of insect locomotion, a live insect can be directly transformed into a soft robot by embedding it with artificial devices. Since many insects can perform acrobatics aerially, thereby exhibiting far greater flexibility than current man-made flyers, correctly commanding the internal structures of an insect to perform based on the instructions would be a breakthrough. Herein, beetles (Mecynorrhina torquata) were chosen as the flying platform, and an inertial measurement unit-implemented electronic backpack was designed and manufactured to remotely command the beetles. To achieve horizontal flight control, multiple flight muscles of the beetles, that is, the basalar and third axillary muscles were stimulated to control the flight directions. However, the beetles were found to gradually adapt to the electrical stimulation, and the flight corrections were elicited by generating compensatory flight forces during a long-lasting stimulation (>300 ms), which were revealed by the decrease in induced lateral force. Based on this finding, a proportional derivative feedback controller was designed to navigate the flying beetles based on the predetermined path using frequency-dependent electrical pulses. To avoid a continuous stimulation, we proposed a stimulation protocol which separated two stimulations with a 50-ms rest. Compared to long stimulations (>300 ms), a 150-ms stimulation with 200-ms update interval was more efficient in correcting the flight direction of the beetles.
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The design of a flying odor compass is proposed for the localization of gas source. The compass is built on a quad-rotor helicopter and contains three gas sensors. A data processing method is proposed to estimate the direction which the odor comes from. The method adopts continuous wavelet transform and modulus maxima approaches to uncover the time difference information hidden in the gas sensor signals. Experiments have demonstrated the effectiveness of this design.
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The use of mobile robots is an effective method of validating sensory-motor models of animals in a real environment. The well-identified insect sensory-motor systems have been the major targets for modeling. Furthermore, mobile robots implemented with such insect models attract engineers who aim to avail advantages from organisms. However, directly comparing the robots with real insects is still difficult even if we successfully model the biological systems, because of the physical differences between them. We developed a hybrid robot to bridge the gap. This hybrid robot is an insect-controlled robot, in which a tethered male silkmoth (Bombyx mori) drives the robot in order to localize an odor source. This robot has the following three advantages: 1) from a biomimetic perspective, the robot enables us to evaluate the potential performance of future insect-mimetic robots; 2) from a biological perspective, the robot enables us to manipulate the closed-loop of an onboard insect for further understanding of its sensory-motor system; and 3) the robot enables comparison with insect models as a reference biological system. In this paper, we review the recent works regarding insect-controlled robots and discuss the significance for both engineering and biology.
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Males of the hawkmoth, Manduca sexta, track wind-borne plumes of female sex pheromone by flying upwind, while continuously turning from side-to-side and changing altitude. Their characteristic "zigzagging" trajectory has long been thought to result from the interaction of two mechanisms, an odor-modulated orientation to wind and a built-in central nervous system turning program. An interesting and as of yet unanswered question about this tracking behavior is how the cross-section of an odor plume or its clean-air "edges" affects moths' odor tracking behavior. This study attempts to address this question by video recording and analyzing the behavior of freely flying M. sexta males tracking plumes from pheromone sources of different lengths and orientations with equal odor concentration per unit area. Our results showed that moths generated significantly wider tracks in wide plumes from the longest horizontally-oriented sources as compared to narrower point-source plumes, but had relatively unaltered tracks when orienting to plumes from the same length sources oriented vertically. This suggests that in addition to wind and the presence of pheromones, the area of the plume's cross section or its edges may also play an important role in the plume tracking mechanisms of M. sexta.
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Antennal lobe interneurons of male Spodoptera littoralis (Boisd.) were investigated by using intracellular recording and staining techniques. Physiological and morphological characteristics of local interneurons and projection neurons responding to sex pheromone and plant-associated volatiles are described. The interneurons identified were divided into three groups, depending on their physiological response characteristics. Both types of interneurons, local interneurons and projection neurons, were described in all three groups. 1. Interneurons responding exclusively to sex pheromone stimuli, displayed different degrees of specificity. These neurons responded to either one, two, three or all four of the single sex pheromone or sex pheromone-like compounds tested. Most of these neurons also responded to a mixture of the two pheromone components present in the female S. littoralis blend. Two local interneurons and one projection neuron were identified as blend specialists, not responding to the single female produced sex pheromone components, but only to their mixture. Five pheromone specific projection neurons arborized in one or more subcompartments of the macroglomercular complex (MGC) and some of them had axonal branches in the calyces of the mushroom body and in different parts of the lateral protocerebrum. 2. Interneurons responding only to plant-associated volatiles varied highly in specificity. Neurons responding to only one of the stimuli, neurons responding to a variety of different odours and one neuron responding to all stimuli tested, were found. Three specialized local interneurons had arborizations only in ordinary glomeruli. One specialized and three less specialized local interneurons had arborizations within the MGC and the ordinary glomeruli. The projection neurons responding only to plant-associated volatiles had mostly uni- or multiglomerular arborizations within the ordinary glomeruli. 3. Interneurons responding to both sex pheromones and plant-associated stimuli varied in specificity. Individual interneurons that responded to few plant-associated odours mostly responded to several pheromone stimuli as well. Projection neurons responding to most of the plant-associated volatiles also responded to all pheromone stimuli. Two local interneurons responding to both stimulus groups, arborized within the MGC and the ordinary glomeruli. Projection neurons mostly arborized in only one ordinary glomerulus or in one compartment of the MGC. The variation in specificity and sensitivity of antennal lobe interneurons and structure-function correlations are discussed.
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The authors have studied the emergent mechanism in insect behavior by using a robotic system. Since insects have a simpler nervous system than humans, it is an appropriate model for clarifying the above mechanism. In this study, the pheromone oriented behavior of male silkworm moths was shown by a pheromone-guided mobile robot which had male moth antennae that can detect sex pheromones. This study focuses on the pheromone sensor that used antennae from a living moth. Since the antennae of silkworm moths are very sensitive as compared to artificial gas sensors, they can be used as living gas sensors that can detect pheromone molecules.
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We developed microfabricated flexible neural probes (FNPs) to provide a bi-directional electrical link to the moth Manduca sexta. These FNPs can deliver electrical stimuli to, and capture neural activity from, the insect's central nervous system. They are comprised of two layers of polyimide with gold sandwiched in between in a split-ring geometry that incorporates the bi-cylindrical anatomical structure of the insect's ventral nerve cord. The FNPs provide consistent left and right abdominal stimulation both across animals and within an individual animal. The features of the stimulation (direction, threshold charge) are aligned with anatomical features of the moth. We also have used these FNPs to record neuronal activity in the ventral nerve cord of the moth. Finally, by integrating carbon nanotube (CNT)-Au nanocomposites into the FNPs we have reduced the interfacial impedance between the probe and the neural tissue, thus reducing the magnitude of stimulation voltage. This in turn allows use of the FNPs with a wireless stimulator, enabling stimulation and flight biasing of freely flying moths. Together, these FNPs present a potent new platform for manipulating and measuring the neural circuitry of insects, and for other nerves in humans and other animals with similar dimensions as the ventral nerve cord of the moth.
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Distribution and neuronal organization of sensilla on the surface of the annulate flagellar segment of the antenna of the male Manduca sexta were studied by scanning and transmission electron microscopy. Nine types of sensilla were identified and their bipolar neurons ascribed to specific sensory modalities on the basis of their cuticular and dendritic morphology. Cuticle morphology identifies two types of sensilla trichodea, two types of sensilla basiconica and one type of sensillum coeloconicum. Certain of these olfactory sensilla are further subdivided on the basis of their dendritic structures. One type of sensillum chaeticum was interpreted as a contact chemoreceptor. A second type of sensillum coeloconicum and a styliform sensilla complex were interpreted as bimodal hygro- and thermosensilla. A second species of sensillum chaeticum serves mechanosensation. Counts from annuli situated about midway along the flagellum revealed a total of about 2200 sensilla supplied by approximately 5160 sensory neurons. A conservative estimate suggests that a male antenna with 85-90 annuli provides the flagellar nerve with at least 3.6 x 10(5) receptor axons, a number that exceeds previous estimates by almost 50% Each species of receptor has a characteristic location on the annulus. Of the 2100 or so sensilla situated on the dorsal, ventral and the leading edge surfaces, about 800 consist of male-specific type-I trichoids containing pheromone-sensitive receptors. Arciform arrays of these sensilla on the upper and lower surfaces of each annulus presumably optimize the capture and absorption of odour molecules. The trailing edge of the flagellum, which is thickly covered by scales and was assumed until now to lack receptors, contains both mechanosensitive and contact chemoreceptors. The modality of non-olfactory receptors is considered with respect to similar elements that have been functionally identified in other species. The coexistence of non-olfactory sensilla with olfactory elements is discussed with respect to current knowledge of the organization of olfactory centres in the brain.
Article
Extracellular electrophysiological recordings were made from individual type-A trichoid sensilla on the antenna of the female sphinx moth Manduca sexta. A single annulus of the antenna bears about 1,100 of these sensilla, and each is innervated by two olfactory receptor cells. We tested the responses of these receptor cells to a panel of 102 volatile compounds, as well as three plant-derived odor mixtures, and could discern three different functional types of type-A trichoid sensilla. One subset of receptor cells exhibited an apparently narrow molecular receptive range, responding strongly to only one or two terpenoid odorants. The second subset was activated exclusively by aromatics and responded strongly to two to seven odorants. The third subset had a broad molecular receptive range and responded strongly to odorants belonging to several chemical classes. We also found receptor cells that did not respond to any of the odorants tested but were spontaneously active. Certain odorants elicited excitatory responses in some sensilla but inhibitory responses in others, and some receptor cells were strongly excited by certain odorants but inhibited by others. Impregnation of groups of receptor cells in type-A trichoid sensilla with rhodamine-dextran demonstrated that their axons project mainly to the large female glomeruli of the antennal lobe.
Article
Many motile organisms localize the source of attractive odorants by following plumes upwind. In the case of D. melanogaster, little is known of how individuals alter their flight trajectories after encountering and losing a plume of an attractive odorant. We have characterized the three-dimensional flight behavior of D. melanogaster in a wind tunnel under a variety of odor conditions. In the absence of olfactory cues, hungry flies initiate flight and display anemotactic orientation. Following contact with a narrow ribbon plume of an attractive odor, flies reduce their crosswind velocity while flying faster upwind, resulting in a surge directed toward the odor source. Following loss of odor contact due to plume truncation, flies frequently initiate a stereotyped crosswind casting response, a behavior rarely observed in a continuous odor plume. Similarly, within a homogeneous odor cloud, flies move fast while maintaining an upwind heading. These results indicate both similarities and differences between the behavior of D. melanogaster and the responses of male moths to pheromone plumes, suggesting possible differences in underlying neural mechanisms.
Article
Four chemical plume-tracking algorithms have been compared using a mobile robot. These algorithms are based upon hypotheses proposed to explain the plume-tracking behavior of flying insects. They all use information from a wind sensor and a single chemical sensor to determine how the agent should move to locate the source of the chemical plume. The performance of the robot using each of the algorithms was tested in a wind tunnel under a range of wind speeds (0.55, 0.95, and 1.4 m/s) using a model chemical (ionized air). The robot was capable of tracking the ion plume to its source effectively with each algorithm, having an overall success rate of over 85%. The simplest implemented algorithm, surge anemotaxis, was found to be the fastest. However, the shape of the tracking paths observed indicated that this simple algorithm may not explain the plume-tracking behavior of certain insects as well as the other algorithms tested. Further tests are required to see if the surge anemotaxis algorithm remains the most efficient under more realistic wind conditions.
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