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Sensorimotor ecology of the insect antenna: Active sampling by a multimodal sensory organ
Abstract
Insect antennae are actively moveable, multimodal sensory organs: they are sensorimotor systems. As such they are key to a wide range of different behaviours, ranging from spatial orientation, search and exploration to communication. The role of active movement in antennal sensory function has received increasing attention over the past decades. For example, modern tracking techniques revealed different antennal sampling strategies and action ranges, along with their dependence on behavioural context or sensory environment. At the same time, research on species with different antennal morphology now allow comparisons across insect orders, highlighting the significance of structural and motor constraints on antennal function. Finally, studies on sensory acquisition and processing have contributed a wealth of knowledge on distinct submodalities of mechano- and chemoreception. This includes the mechanosensation of posture, movement, gravity, contact location and surface texture, as well as chemosensation of smell and taste. Here, we review our current understanding of insect antennae as sensorimotor systems. In particular, we discuss how their behavioural function (A) depends on active movement, (B) how it is shaped by structural and motor constraints, and (C) how this relates to mechano- and chemoreception. Based on an overview of antennal function and structure we propose a major functional distinction into contact antennae as opposed to non-contact antennae. Focussing on contact antennae, we then address questions about (i) distinct antennal exploration and sampling patterns, (ii) whether and how they change with behavioural context, and (iii) whether and how they differ between sensory modality.
... Mainly, these organs demonstrate proficiency in mechano-sensation related to pressure and vibration, utilizing spatiotemporal encoding methods to interpret somatosensory information obtained from various mechanoreceptors. These intricate systems endow a refined perception of textures, profiles, and shapes during both tactile interaction and active exploration [1][2][3] . Inspired by nature, artificial tactile sensory systems, including e-skin and e-whisker, have been reported, contributing to the ongoing development of skin electronics and epidermal electronics [4][5][6][7] . ...
... Insects' tactile sensory organs, despite their diminutive scale and paucity of neurons compared to mammals, exhibit efficient processing and multimodal sensory functions encompassing mechano-perception, magneto-perception, audio-perception, and chemoperception 2,16,17 . These capabilities could serve as blueprints for the development of biomimetic sensory platforms. ...
... The exquisite antennal structures, densely innervated with sensory receptors and neurons, emit spatiotemporally-encoded neural spike sequences, allowing for the detection of vibrotactile and magnetic stimuli. The perceptual acuity is comparable to, or even surpasses, that of human skin, thereby enabling insects to execute complex tasks, including foraging, object identification, and navigation 2,22,28,29 . Nevertheless, tactile sensory systems inspired by insect antennae (antennal sensillum as well) are yet to be fully explored. ...
Insect antennae facilitate the nuanced detection of vibrations and deflections, and the non-contact perception of magnetic or chemical stimuli, capabilities not found in mammalian skin. Here, we report a neuromorphic antennal sensory system that emulates the structural, functional, and neuronal characteristics of ant antennae. Our system comprises electronic antennae sensor with three-dimensional flexible structures that detects tactile and magnetic stimuli. The integration of artificial synaptic devices adsorbed with solution-processable MoS2 nanoflakes enables synaptic processing of sensory information. By emulating the architecture of receptor-neuron pathway, our system realizes hardware-level, spatiotemporal perception of tactile contact, surface pattern, and magnetic field (detection limits: 1.3 mN, 50 μm, 9.4 mT). Vibrotactile-perception tasks involving profile and texture classifications were accomplished with high accuracy (> 90%), surpassing human performance in “blind” tactile explorations. Magneto-perception tasks including magnetic navigation and touchless interaction were successfully completed. Our work represents a milestone for neuromorphic sensory systems and biomimetic perceptual intelligence.
... Based on our investigations, the antennae of adult P. maha are clavate in form, with no significant sexual dimorphism. Considering that insect antennae are known to contribute to stability and orientation during flight [34], the absence of sexual dimorphism in the overall antennal morphology suggests that both sexes might have similar flight capabilities. This uniformity may be essential for navigating diverse habitats such as ...
... Based on our investigations, the antennae of adult P. maha are clavate in form, with no significant sexual dimorphism. Considering that insect antennae are known to contribute to stability and orientation during flight [34], the absence of sexual dimorphism in the overall antennal morphology suggests that both sexes might have similar flight capabilities. This uniformity may be essential for navigating diverse habitats such as grasslands, gardens, agricultural fields, and urban areas. ...
The pale grass blue, Pseudozizeeria maha, is a small lycaenid butterfly widely distributed across Asia. Due to its exclusively diurnal lifestyle and conspicuous sexual dimorphism in wing coloration, vision has traditionally been regarded as the primary sensory system driving various behaviors. However, non-visual sensory systems related to sex-specific behavioral responses, such as antennae, have received far less attention. This study investigated the morphological characteristics and sensilla types of the antennae in adult P. maha using scanning electron microscopy, with a focus on potential sexual dimorphism. The antennae of adult P. maha are clavate, with no significant sexual differences in overall morphology. Six types of antennal sensilla were identified: Böhm bristles, sensilla squamiformia, sensilla trichodea, sensilla chaetica, sensilla basiconica, and sensilla coeloconica, with no sexual dimorphism observed in their morphological types or dimensions. Remarkably, the sensilla coeloconica exhibit significant sexual dimorphism, with a more prominent presence in females. This finding suggests that female P. maha may rely more on olfactory cues for some sex-specific behaviors, such as oviposition site selection.
... Recent research has observed that when insects land on odour sources, they actively vibrate their antennae to enhance sensory sampling (Schneider 1964;Loudon 2009;Dürr, Berendes & Strube-Bloss 2022). We speculate that this antennal movement can induce fluctuations in the air, affecting the distribution of odour plumes. ...
Flying insects exhibit remarkable capabilities in coordinating their olfactory sensory system and flapping wings during odour plume-tracking flights. While observations have indicated that their flapping wing motion can ‘sniff’ up the incoming plumes for better odour sampling range, how flapping motion impacts the odour concentration field around the antennae is unknown. Here, we reconstruct the body and wing kinematics of a forwards-flying butterfly based on high-speed images. Using an in-house computational fluid dynamics solver, we simulate the unsteady flow field and odourant transport process by solving the Navier–Stokes and odourant advection-diffusion equations. Our results show that, during flapping flight, the interaction between wing leading-edge vortices and antenna vortices strengthens the circulation of antenna vortices by over two-fold compared with cases without flapping motion, leading to a significant increase in odour intensity fluctuation along the antennae. Specifically, the interaction between the wings and antennae amplifies odour intensity fluctuations on the antennae by up to 8.4 fold. This enhancement is critical in preventing odour fatigue during odour-tracking flights. Further analysis reveals that this interaction is influenced by the inter-antennal angle. Adjusting this angle allows insects to balance between resistance to odour fatigue and the breadth of odour sampling. Narrower inter-antennal angles enhance fatigue resistance, while wider angles extend the sampling range but reduce resistance. Additionally, our findings suggest that while the flexibility of the wings and the thorax's pitching motion in butterflies do influence odour fluctuation, their impact is relatively secondary to that of the wing–antenna interaction.
... Depending on the connection to other structures, different mechanical stimuli can activate the sensory organs: the mechanical coupling determines how mechanical stimuli reach the sensilla and thus how the sensory organ is activated [18]. Resulting from the different connections, chordotonal organs can detect external stimuli such as substrate vibrations and sound or stimuli generated by body movements such as stretching or bending [1,17,19,20]. ...
The subgenual organ complex of stick insects has a unique neuroanatomical organisation with two elaborate chordotonal organs, the subgenual organ and the distal organ. These organs are present in all leg pairs and are already developed in newly hatched stick insects. The present study analyses for the first time the morphology of sensory organs in the subgenual organ complex for a membrane connecting the two sensory organs in newly hatched insects (Sipyloidea chlorotica (Audinet-Serville 1838)). The stick insect legs were analysed following hatching by axonal tracing and light microscopy. The subgenual organ complex in first juvenile instars shows the sensory organs and a thin membrane connecting the sensory organs resembling the morphology of adult animals. Rarely was this membrane not detected, where it is assumed as not developed during embryogenesis. The connection appears to influence the shape of the subgenual organ, with one end extending towards the distal organ as under tension. These findings are discussed for the following functional implications: (1) the physiological responses of the subgenual organ complex to mechanical stimuli after hatching, (2) the influence of the membrane on the displacement of the sensory organs, and (3) the connection between the subgenual organ and distal organ as a possible functional coupling.
... This behaviours and their underlying neural mechanisms can be studied relatively straight forward in different insect species. Besides receiving stimuli at the insect antenna, which in itself represents an actively movable, multisensory organ (Dürr et al., 2022), beetles and ants integrate antennal information with visual stimuli to enhance their performance during short and long distance navigation (Dacke et al., 2019;Buehlmann et al., 2020a;Buehlmann et al., 2020b). ...
To obtain accurate information about the outside world and to make appropriate decisions, animals often combine information from different sensory pathways to form a comprehensive representation of their environment. This process of multimodal integration is poorly understood, but it is common view that the single elements of a multimodal stimulus influence each other’s perception by enhancing or suppressing their neural representation. The neuronal level of interference might be manifold, for instance, an enhancement might increase, whereas suppression might decrease behavioural response times. In order to investigate this in an insect behavioural model, the Western honeybee, we trained individual bees to associate a sugar reward with an odour, a light, or a combined olfactory-visual stimulus, using the proboscis extension response (PER). We precisely monitored the PER latency (the time between stimulus onset and the first response of the proboscis) by recording the muscle M17, which innervates the proboscis. We found that odours evoked a fast response, whereas visual stimuli elicited a delayed PER. Interestingly, the combined stimulus showed a response time in between the unimodal stimuli, suggesting that olfactory-visual integration accelerates visual responses but decelerates the olfactory response time.
Fipronil, a pesticide widely used to control agricultural and household insect pests, blocks insect GABAA and glutamate (GluCl) ionotropic receptors, resulting in uncontrolled hyperexcitation and paralysis that eventually leads to death. The use of fipronil is controversial because unintentional exposure to this compound may contribute to the ongoing global decline of insect pollinator populations. Although the sublethal effects of fipronil have been linked to aberrant behavior and impaired olfactory learning in insects, the precise mechanisms involved in these responses remain unclear. In this article, we highlight recent studies that have investigated the interaction among different pathways involved in the ability of fipronil to modulate insect behavior, with particular emphasis on the role of GABAergic neurotransmission in fine-tuning the integration of sensorial responses and insect behavior. Recent findings suggest that fipronil can also cause functional alterations that affect synaptic organization and the availability of metal ions in the brain.
Animals form a behavioral decision by evaluating sensory evidence on the background of past experiences and the momentary motivational state. In insects, we still lack understanding of how and at which stage of the recurrent sensory-motor pathway behavioral decisions are formed. The mushroom body (MB), a central brain structure in insects1 and crustaceans,2,3 integrates sensory input of different modalities4,5,6 with the internal state, the behavioral state, and external sensory context7,8,9,10 through a large number of recurrent, mostly neuromodulatory inputs,11,12 implicating a functional role for MBs in state-dependent sensory-motor transformation.13,14 A number of classical conditioning studies in honeybees15,16 and fruit flies17,18,19 have provided accumulated evidence that at its output, the MB encodes the valence of a sensory stimulus with respect to its behavioral relevance. Recent work has extended this notion of valence encoding to the context of innate behaviors.8,20,21,22 Here, we co-analyzed a defined feeding behavior and simultaneous extracellular single-unit recordings from MB output neurons (MBONs) in the cockroach in response to timed sensory stimulation with odors. We show that clear neuronal responses occurred almost exclusively during behaviorally responded trials. Early MBON responses to the sensory stimulus preceded the feeding behavior and predicted its occurrence or non-occurrence from the single-trial population activity. Our results therefore suggest that at its output, the MB does not merely encode sensory stimulus valence. We hypothesize instead that the MB output represents an integrated signal of internal state, momentary environmental conditions, and experience-dependent memory to encode a behavioral decision.
Overall body proportions and relative limb length are highly characteristic for most insect taxa. In case of the legs, limb length has mostly been discussed with regard to parameters of locomotor performance and, in particular cases, as an adaptation to environmental factors or to the mating system. Here, we compare three species of stick and leaf insects (Phasmatodea) that differ strongly in the length ratio between antennae and walking legs, with the antennae of Medauroidea extradentata being much shorter than its legs, nearly equal length of antennae and legs in Carausius morosus , and considerably longer antennae than front legs in Aretaon asperrimus . We show that that relative limb length is directly related to the near-range exploration effort, with complementary function of the antennae and front legs irrespective of their length ratio. Assuming that these inter-species differences hold for both sexes and all developmental stages, we further explore how relative limb length differs between sexes and how it changes throughout postembryonic development. We show that the pattern of limb-to-body proportions is species-characteristic despite sexual dimorphism, and find that the change in sexual dimorphism is strongest during the last two moults. Finally, we show that antennal growth rate is consistently higher than that of front legs, but differs categorically between the species investigated. Whereas antennal growth rate is constant in Carausius , the antennae grow exponentially in Medauroidea and with a sudden boost during the last moult in Aretaon .
The fact that honey bees have a relatively simple nervous system that allows complex behaviors has made them an outstanding model for studying neurobiological processes. Studies on learning and memory routinely use appetitive and aversive learning paradigms that involve recording of the proboscis or the sting extension. However, these protocols are based on all-or-none responses, which has the disadvantage of occluding intermediate and more elaborated behaviors. Nowadays, the great advances in tracking software and data analysis, combined with affordable video recording systems, have made it possible to extract very detailed information about animal behavior. Here we describe antennal movements that are elicited by odor that have no, positive or negative valence. We show that animals orient their antennae towards the source of the odor when it is positive, and orient them in the opposite direction when the odor is negative. Moreover, we found that this behavior was modified between animals that had been trained based on protocols of different strength. Since this procedure allows a more accurate description of the behavioral outcome using a relatively small number of animals, it represents a great tool for studying different cognitive processes and olfactory perception.
The study of sensory systems in insects has a long-spanning history of almost an entire century. Olfaction, vision, and gustation are thoroughly researched in several robust insect models and new discoveries are made every day on the more elusive thermo- and mechano-sensory systems. Few specialized senses such as hygro- and magneto-reception are also identified in some insects. In light of recent advancements in the scientific investigation of insect behavior, it is not only important to study sensory modalities individually, but also as a combination of multimodal inputs. This is of particular significance, as a combinatorial approach to study sensory behaviors mimics the real-time environment of an insect with a wide spectrum of information available to it. As a fascinating field that is recently gaining new insight, multimodal integration in insects serves as a fundamental basis to understand complex insect behaviors including, but not limited to navigation, foraging, learning, and memory. In this review, we have summarized various studies that investigated sensory integration across modalities, with emphasis on three insect models (honeybees, ants and flies), their behaviors, and the corresponding neuronal underpinnings.
Animals perceive their surroundings by using various modalities of sensory inputs to guide their locomotion. Nocturnal insects such as crickets use mechanosensory inputs mediated by their antennae to orient in darkness. Spatial information is acquired via voluntary antennal contacts with surrounding objects, but it remains unclear whether the insects modulate behaviors mediated by other sensory organs based on that information. Crickets exhibit escape behavior in response to a short air-puff, which is detected by the abdominal mechanosensory organs called cerci and is perceived as a “predator approach” signal. We placed objects of different shapes at different locations with which the cricket actively made contact using its antenna. We then examined the effects on wind-elicited escape behavior. The crickets changed their movement trajectory in response to nearby objects like walls so that they could avoid collision with these obstacles even during the cercal-mediated behavior. For instance, when a wall was placed in front of the crickets so that it was detected by one antenna, the escape trajectory in response to a stimulus from behind was significantly biased toward the side opposite the wall. Even when the antenna on the free side without the wall was ablated, this collision avoidance was also observed, suggesting that the mechanosensory inputs from one antenna detecting an object edge would be sufficient to perceive the location of obstacle in front. This study demonstrated that crickets were able to use the spatial information acquired with their antennal system to modify their behavior mediated by other sensory organs.
Significance
Surface-bound odor trail tracking is critical for the survival of terrestrial animals dependent on olfaction. Little is known about how animals track trails at the algorithmic level. In the present study, we propose that a tracking animal maintains a noisy estimate of where the trail is headed based on its past contacts with the trail. We show that virtual agents trained to exploit this strategy reproduce the tracking patterns of ants and rodents. The observed patterns emerge simply as a consequence of common geometric constraints, which also impose fundamental limits on how quickly an animal can track trails. A series of experiments is proposed to quantify how past experience and trail statistics shape tracking behavior.
Significance
Almost all animals must make decisions on the move. Here, employing an approach that integrates theory and high-throughput experiments (using state-of-the-art virtual reality), we reveal that there exist fundamental geometrical principles that result from the inherent interplay between movement and organisms’ internal representation of space. Specifically, we find that animals spontaneously reduce the world into a series of sequential binary decisions, a response that facilitates effective decision-making and is robust both to the number of options available and to context, such as whether options are static (e.g., refuges) or mobile (e.g., other animals). We present evidence that these same principles, hitherto overlooked, apply across scales of biological organization, from individual to collective decision-making.
Most animals survive and thrive due to navigational behavior to reach their destinations. In order to navigate, it is important for animals to integrate information obtained from multisensory inputs and use that information to modulate their behavior. In this study, by using a virtual reality (VR) system for an insect, we investigated how the adult silkmoth integrates visual and wind direction information during female search behavior (olfactory behavior). According to the behavioral experiments using a VR system, the silkmoth had the highest navigational success rate when odor, vision, and wind information were correctly provided. However, the success rate of the search was reduced if the wind direction information provided was different from the direction actually detected. This indicates that it is important to acquire not only odor information but also wind direction information correctly. When the wind is received from the same direction as the odor, the silkmoth takes positive behavior; if the odor is detected but the wind direction is not in the same direction as the odor, the silkmoth behaves more carefully. This corresponds to a modulation of behavior according to the degree of complexity (turbulence) of the environment. We mathematically modeled the modulation of behavior using multisensory information and evaluated it using simulations. The mathematical model not only succeeded in reproducing the actual silkmoth search behavior but also improved the search success relative to the conventional odor-source search algorithm.
Highly interconnected neural networks perform olfactory signal processing in the central nervous system. In insects, the first synaptic processing of the olfactory input from the antennae occurs in the antennal lobe, the functional equivalent of the olfactory bulb in vertebrates. Key components of the olfactory network in the antennal lobe are two main types of neurons: the local interneurons and the projection (output) neurons. Both neuron types have different physiological tasks during olfactory processing, which accordingly require specialized functional phenotypes. This review gives an overview of important cell type-specific functional properties of the different types of projection neurons and local interneurons in the antennal lobe of the cockroach Periplaneta americana , which is an experimental system that has elucidated many important biophysical and cellular bases of intrinsic physiological properties of these neurons.
Sensing olfactory signals in the environment represents a crucial and significant task of sensory systems in almost all organisms to facilitate survival and reproduction. Notably, the olfactory system of diverse animal phyla shares astonishingly many fundamental principles with regard to anatomical and functional properties. Binding of odor ligands by chemosensory receptors present in the olfactory peripheral organs leads to a neuronal activity that is conveyed to first and higher-order brain centers leading to a subsequent odor-guided behavioral decision. One of the key centers for integrating and processing innate olfactory behavior is the lateral horn (LH) of the protocerebrum in insects. In recent years the LH of Drosophila has garnered increasing attention and many studies have been dedicated to elucidate its circuitry. In this review we will summarize the recent advances in mapping and characterizing LH-specific cell types, their functional properties with respect to odor tuning, their neurotransmitter profiles, their connectivity to pre-synaptic and post-synaptic partner neurons as well as their impact for olfactory behavior as known so far.
In social species, decision-making is both influenced by, and in turn influences, the social context. This reciprocal feedback introduces coupling across scales, from the neural basis of sensing, to individual and collective decision-making. Here, we adopt an integrative approach investigating decision-making in dynamical social contexts. When choosing shelters, isolated cockroaches prefer vanillin-scented (food-associated) shelters over unscented ones, yet in groups, this preference is inverted. We demonstrate that this inversion can be replicated by replacing the full social context with social odours: presented alone food and social odours are attractive, yet when presented as a mixture they are avoided. Via antennal lobe calcium imaging, we show that neural activity in vanillin-responsive regions reduces as social odour concentration increases. Thus, we suggest that the mixture is evaluated as a distinct olfactory object with opposite valence, providing a mechanism that would naturally result in individuals avoiding what they perceive as recently exploited resources.
The Johnston’s organ (JO) in the insect antenna is a multisensory organ involved in several navigational tasks including wind-compass orientation, flight control, graviception, and, possibly, magnetoreception. Here we investigate the three dimensional anatomy of the JO and its neuronal projections into the brain of the desert ant Cataglyphis, a marvelous longdistance
navigator. The JO of C. nodus workers consists of 40 scolopidia comprising three sensory neurons each. The numbers of scolopidia slightly vary between different sexes (female/male) and castes (worker/queen). Individual scolopidia attach to the intersegmental
membrane between pedicel and flagellum of the antenna and line up in a ring-like organization. Three JO nerves project along the two antennal nerve branches into the brain. Anterograde double staining of the antennal afferents revealed that JO receptor neurons
project to several distinct neuropils in the central brain. The T5 tract projects into the antennal mechanosensory and motor center (AMMC), while the T6 tract bypasses the AMMC via the saddle and forms collaterals terminating in the posterior slope (PS) (T6I), the
ventral complex (T6II), and the ventrolateral protocerebrum (T6III). Double labeling of JO and ocellar afferents revealed that input from the JO and visual information from the ocelli converge in tight apposition in the PS. The general JO anatomy and its central projection patterns resemble situations in honeybees and Drosophila. The multisensory nature of the JO together with its projections to multisensory neuropils in the ant brain likely serves synchronization and calibration of different sensory modalities during the ontogeny of
navigation in Cataglyphis.
The general architecture of the olfactory system is highly conserved from insects to humans, but neuroanatomical and physiological differences can be observed across species. The American cockroach, inhabiting dark shelters with a rather stable olfactory landscape, is equipped with long antennae used for sampling the surrounding air-space for orientation and navigation. The antennae's exceptional length provides a wide spatial working range for odour detection; however, it is still largely unknown whether and how this is also used for mapping the structure of the olfactory environment. By selective labelling antennal lobe projection neurons with a calcium sensitive dye, we investigated the logic of olfactory coding in this hemimetabolous insect. We show that odour responses are stimulus-specific and concentration-dependent, and that structurally related odorants evoke physiologically similar responses. By using spatially confined stimuli, we show that proximal stimulations induce stronger and faster responses than distal ones. Spatially confined stimuli of the female pheromone periplanone-B activate sub-region of the male macroglomerulus. Thus, we report that the combinatorial logic of odour coding deduced from holometabolous insects applies also to this hemimetabolous species. Furthermore, a fast decrease in sensitivity along the antenna, not supported by a proportionate decrease in sensillar density, suggests a neural architecture that strongly emphasizes neuronal inputs from the proximal portion of the antenna.
Mushroom bodies (MBs) are multisensory integration centers in the insect brain involved in learning and memory formation. In the honeybee, the main sensory input region (calyx) of MBs is comparatively large and receives input from mainly olfactory and visual senses, but also from gustatory/tactile modalities. Behavioral plasticity following differential brood care, changes in sensory exposure or the formation of associative long-term memory (LTM) was shown to be associated with structural plasticity in synaptic microcircuits (microglomeruli) within olfactory and visual compartments of the MB calyx. In the same line, physiological studies have demonstrated that MB-calyx microcircuits change response properties after associative learning. The aim of this review is to provide an update and synthesis of recent research on the plasticity of microcircuits in the MB calyx of the honeybee, specifically looking at the synaptic connectivity between sensory projection neurons (PNs) and MB intrinsic neurons (Kenyon cells). We focus on the honeybee as a favorable experimental insect for studying neuronal mechanisms underlying complex social behavior, but also compare it with other insect species for certain aspects. This review concludes by highlighting open questions and promising routes for future research aimed at understanding the causal relationships between neuronal and behavioral plasticity in this charismatic social insect.
Complex behaviours may be viewed as sequences of modular actions, each elicited by specific sensory cues in their characteristic timescales. From this perspective, we can construct models in which unitary behavioural modules are hierarchically placed in context of related actions. Here, we analyse antennal positioning reflex in hawkmoths as a tuneable behavioural unit. Mechanosensory feedback from two antennal structures, Böhm’s bristles (BB) and Johnston’s organs (JO), determines antennal position. At flight onset, antennae attain a specific position, which is maintained by feedback from BB. Simultaneously, JO senses deflections in flagellum-pedicel joint due to frontal airflow, to modulate its steady-state position. Restricting JO abolishes positional modulation but maintains stability against perturbations. Linear feedback models are sufficient to predict antennal dynamics at various set-points. We modelled antennal positioning as a hierarchical neural-circuit in which fast BB feedback maintains instantaneous set-point, but slow JO feedback modulates it, thereby elucidating mechanisms underlying its robustness and flexibility. Flying insects position their antennae by integrating multisensory inputs across different timescales. This study describes an underlying hierarchical neural circuit that maintains antennal position in a fast and robust manner, whilst retaining flexibility to incorporate slower feedback to modulate position.
It is believed that long-term memory (LTM) cannot be formed immediately because it must go through a protein synthesis-dependent consolidation process. However, the current study uses Drosophila aversive olfactory conditioning to show that such processes are dispensable for context-dependent LTM (cLTM). Single-trial conditioning yields cLTM that is formed immediately in a protein-synthesis independent manner and is sustained over 14 days without decay. Unlike retrieval of traditional LTM, which requires only the conditioned odour and is mediated by mushroom-body neurons, cLTM recall requires both the conditioned odour and reinstatement of the training-environmental context. It is mediated through lateral-horn neurons that connect to multiple sensory brain regions. The cLTM cannot be retrieved if synaptic transmission from any one of these centres is blocked, with effects similar to those of altered encoding context during retrieval. The present study provides strong evidence that long-term memory can be formed easily without the need for consolidation.
Olfaction is an essential sensory modality for insects and their olfactory environment is mostly made up of plant-emitted volatiles. The terrestrial vegetation produces an amazing diversity of volatile compounds, which are then transported, mixed, and degraded in the atmosphere. Each insect species expresses a set of olfactory receptors that bind part of the volatile compounds present in its habitat. Insect odorscapes are thus defined as species-specific olfactory spaces, dependent on the local habitat, and dynamic in time. Manipulations of pest-insect odorscapes are a promising approach to answer the strong demand for pesticide-free plant-protection strategies. Moreover, understanding their olfactory environment becomes a major concern in the context of global change and environmental stresses to insect populations. A considerable amount of information is available on the identity of volatiles mediating biotic interactions that involve insects. However, in the large body of research devoted to understanding how insects use olfaction to locate resources, an integrative vision of the olfactory environment has rarely been reached. This article aims to better apprehend the nature of the insect odorscape and its importance to insect behavioral ecology by reviewing the literature specific to different disciplines from plant ecophysiology to insect neuroethology. First, we discuss the determinants of odorscape composition, from the production of volatiles by plants (section “Plant Metabolism and Volatile Emissions”) to their filtering during detection by the olfactory system of insects (section “Insect Olfaction: How Volatile Plant Compounds Are Encoded and Integrated by the Olfactory System”). We then summarize the physical and chemical processes by which volatile chemicals distribute in space (section “Transportation of Volatile Plant Compounds and Spatial Aspects of the Odorscape”) and time (section “Temporal Aspects: The Dynamics of the Odorscape”) in the atmosphere. The following sections consider the ecological importance of background odors in odorscapes and how insects adapt to their olfactory environment. Habitat provides an odor background and a sensory context that modulate the responses of insects to pheromones and other olfactory signals (section “Ecological Importance of Odorscapes”). In addition, insects do not respond inflexibly to single elements in their odorscape but integrate several components of their environment (section “Plasticity and Adaptation to Complex and Variable Odorscapes”). We finally discuss existing methods of odorscape manipulation for sustainable pest insect control and potential future developments in the context of agroecology (section “Odorscapes in Plant Protection and Agroecology”).
Significance
We show that South African dung beetles use a multimodal orientation compass based on celestial cues and wind cues to steer across the savanna. The cue preference between these 2 modalities is set in a flexible manner: at low sun elevations, the beetles use a celestially driven compass, but switch to a wind-dominated compass at high sun elevations. This switch allows the beetles to orient with high precision even when the midday sky no longer provides reliable directional input. Moreover, our data suggest that the wind and celestial cues converge in the same memory network in the brain. This spatial memory based on both modalities allows the animal to rely on the most reliable cue at any moment in time.
Animals exhibit innate behaviours to a variety of sensory stimuli including olfactory cues. In Drosophila, one higher olfactory centre, the lateral horn (LH), is implicated in innate behaviour. However, our structural and functional understanding of the LH is scant, in large part due to a lack of sparse neurogenetic tools for this region. We generate a collection of split-GAL4 driver lines providing genetic access to 82 LH cell types. We use these to create an anatomical and neurotransmitter map of the LH and link this to EM connectomics data. We find ~30% of LH projections converge with outputs from the mushroom body, site of olfactory learning and memory. Using optogenetic activation, we identify LH cell types that drive changes in valence behavior or specific locomotor programs. In summary, we have generated a resource for manipulating and mapping LH neurons, providing new insights into the circuit basis of innate and learned olfactory behavior.
Honeybees use visual and olfactory cues to detect flowers during foraging trips. Hence, the reward association of a nectar source is a multimodal construct which has at least two major components – olfactory and visual cues. How both sensory modalities are integrated to form a common reward association and whether and how they may interfere, is an open question. The present study used stimulation with UV, blue and green light to evoke distinct photoreceptor activities in the compound eye and two odour components (Geraniol, Citronellol). To test if a compound of both modalities is perceived as the sum of its elements (elemental processing) or as a unique cue (configural processing) we combined monochromatic light with single odour components in positive (PP) and negative patterning (NP) experiments. During PP, the compound of two modalities was rewarded, whereas the single elements were not. For NP, stimuli comprising a single modality were rewarded, whereas the olfactory-visual compound was not. Furthermore, we compared the differentiation abilities between two light stimuli with and without being part of an olfactory-visual compound. Interestingly, the behavioural performances revealed a prominent case of configural processing, but only in those cases when UV light was an element of an olfactory-visual compound. Instead, learning with green- and blue-containing compounds rather supports elemental processing theory.
Like all animals, bees need to consume essential amino acids to maintain their body’s protein synthesis. Perception and discrimination of amino acids are, however, still poorly understood in bees (and insects in general). We used chemotactile conditioning of the proboscis extension response (PER) to examine (1) whether Bombus terrestris workers are able to perceive amino acids by means of their antennae and (if so) which ones, (2) whether they are able to differentiate between different amino acids, and (3) whether they are able to differentiate between different concentrations of the same amino acid. We found that workers perceived asparagine, cysteine, hydroxyproline, glutamic acid, lysine, phenylalanine, and serine, but not alanine, leucine, proline, or valine by means of their antennae. Surprisingly, they were unable to differentiate between different (perceivable) amino acids, but they distinguished between different concentrations of lysine. Consequently, bumblebees seem to possess amino acid receptors at the tip of their antennae, which enable a general perception of those solute amino acids that have an additional functional group (besides the common amino and carboxylic groups). They may thus have the ability to assess the overall amino acid content of pollen and nectar prior to ingestion.
The antennal lobe of the moth brain is the primary olfactory center processing information concerning pheromones and plant odors. Plutella xylostella is a major worldwide pest of cruciferous vegetables and its behavior is highly dependent on their olfactory system. However, detailed knowledge of the anatomy and function of the P. xylostella olfactory system remains limited. In the present study, we present the 3-Dimentional (3-D) map of the antennal lobe of P. xylostella, based on confocal microscopic analysis of glomerular segmentation and Neurobiotin backfills of Olfactory Receptor Neurons (ORNs). We identified 74–76 ordinary glomeruli and a macroglomerular complex (MGC) situated at the entrance of the antennal nerve in males. The MGC contained three glomeruli. The volumes of glomeruli in males ranged from 305.83 ± 129.53 to 25440.00 ± 1377.67 μm3. In females, 74–77 glomeruli were found, with the largest glomerulus ELG being situated at the entrance of the antennal nerve. The volumes of glomeruli in females ranged from 802.17 ± 95.68 to 8142.17 ± 509.46 μm3. Sexual dimorphism was observed in anomalous supernumerary, anomalous missing, shape, size, and array of several of the identified glomeruli in both sexes. All glomeruli, except one in the antennal lobe (AL), received projections of antennal ORNs. The glomeruli PV1 in both sexes received input from the labial palp nerve and was assumed as the labial pit organ glomerulus (LPOG). These results provide a foundation for better understanding of coding mechanisms of odors in this important pest insect.
Chemical communication involves the production, transmission, and perception of odors. Most adult insects rely on chemical signals and cues to locate food resources, oviposition sites or reproductive partners and, consequently, numerous odors provide a vital source of information. Insects detect these odors with receptors mostly located on the antennae, and the diverse shapes and sizes of these antennae (and sensilla) are both astonishing and puzzling: what selective pressures are responsible for these different solutions to the same problem-to perceive signals and cues? This review describes the selection pressures derived from chemical communication that are responsible for shaping the diversity of insect antennal morphology. In particular, we highlight new technologies and techniques that offer exciting opportunities for addressing this surprisingly neglected and yet crucial component of chemical communication.
Internal representation of far-range space in insects is well established, as it is necessary for navigation behavior. Although it is likely that insects also have an internal representation of near-range space, the behavioral evidence for the latter is much less evident. Here, we estimate the size and shape of the spatial equivalent of a near-range representation that is constituted by somatosensory sampling events. To do so, we use a large set of experimental whole-body motion capture data on unrestrained walking, climbing and searching behavior in stick insects of the species Carausius morosus to delineate ‘action volumes’ and ‘contact volumes’ for both antennae and all six legs. As these volumes are derived from recorded sampling events, they comprise a volume equivalent to a representation of coinciding somatosensory and motor activity. Accordingly, we define this volume as the peripersonal space of an insect. It is of immediate behavioral relevance, because it comprises all potential external object locations within the action range of the body. In a next step, we introduce the notion of an affordance space as that part of peripersonal space within which contact-induced spatial estimates lie within the action ranges of more than one limb. Because the action volumes of limbs overlap in this affordance space, spatial information from one limb can be used to control the movement of another limb. Thus, it gives rise to an affordance as known for contact-induced reaching movements and spatial coordination of footfall patterns in stick insects. Finally, we probe the computational properties of the experimentally derived affordance space for pairs of neighboring legs. This is done by use of artificial neural networks that map the posture of one leg into a target posture of another leg with identical foot position.
Studies of sexual selection that occurs prior to mating have focussed on either the role of armaments in intra-sexual selection, or extravagant signals for inter-sexual selection. However, Darwin suggested that sexual selection may also act on ‘organs of sense’, an idea that seems to have been largely overlooked. Here, we refine this idea in the context of the release of sex pheromones by female insects: females that lower the release of sex pheromones may benefit by mating with high-quality males, if their signalling investment results in sexual selection favouring males with larger or more sensitive antennae that are costly to develop and maintain.
Hearing is essential for the courtship of one of the major carriers of human disease, the mosquito. Males locate females through flight-tone recognition and both sexes engage in mid-air acoustic communications, which can take place within swarms containing thousands of individuals. Despite the importance of hearing for mosquitoes, its mechanisms are still largely unclear. We here report a multilevel analysis of auditory function across three disease-transmitting mosquitoes (Aedes aegypti, Anopheles gambiae and Culex quinquefasciatus). All ears tested display transduction-dependent power gain. Quantitative analyses of mechanotransducer function reveal sex-specific and species-specific variations, including male-specific, highly sensitive transducer populations. Systemic blocks of neurotransmission result in large-amplitude oscillations only in male flagellar receivers, indicating sexually dimorphic auditory gain control mechanisms. Our findings identify modifications of auditory function as a key feature in mosquito evolution. We propose that intra-swarm communication has been a driving force behind the observed sex-specific and species-specific diversity.
In natural environments, stimuli and events learned by animals usually occur in a combination of more than one sensory modality. An important problem in experimental psychology has been thus to understand how organisms learn about multimodal compounds and how they discriminate this compounds from their unimodal constituents. Here we tested the ability of honey bees to learn bimodal patterning discriminations in which a visual-olfactory compound (AB) should be differentiated from its visual (A) and olfactory (B) elements. We found that harnessed bees trained in classical conditioning of the proboscis extension reflex (PER) are able to solve bimodal positive and negative patterning (NP) tasks. In positive patterning (PP), bees learned to respond significantly more to a bimodal reinforced compound (AB+) than to non-reinforced presentations of single visual (A-) or olfactory (B-) elements. In NP, bees learned to suppress their responses to a non-reinforced compound (AB-) and increase their responses to reinforced presentations of visual (A+) or olfactory (B+) elements alone. We compared the effect of two different inter-trial intervals (ITI) in our conditioning approaches. Whereas an ITI of 8 min allowed solving both PP and NP, only PP could be solved with a shorter ITI of 3 min. In all successful cases of bimodal PP and NP, bees were still able to discriminate between reinforced and non-reinforced stimuli in memory tests performed one hour after conditioning. The analysis of individual performances in PP and NP revealed that different learning strategies emerged in distinct individuals. Both in PP and NP, high levels of generalization were found between elements and compound at the individual level, suggesting a similar difficulty for bees to solve these bimodal patterning tasks. We discuss our results in light of elemental and configural learning theories that may support the strategies adopted by honey bees to solve bimodal PP or NP discriminations.
Odor attraction in walking Drosophila melanogaster is commonly used to relate neural function to behavior, but the algorithms underlying attraction are unclear. Here, we develop a high-throughput assay to measure olfactory behavior in response to well-controlled sensory stimuli. We show that odor evokes two behaviors: an upwind run during odor (ON response), and a local search at odor offset (OFF response). Wind orientation requires antennal mechanoreceptors, but search is driven solely by odor. Using dynamic odor stimuli, we measure the dependence of these two behaviors on odor intensity and history. Based on these data, we develop a navigation model that recapitulates the behavior of flies in our apparatus, and generates realistic trajectories when run in a turbulent boundary layer plume. The ability to parse olfactory navigation into quantifiable elementary sensori-motor transformations provides a foundation for dissecting neural circuits that govern olfactory behavior.
In the insect brain, the mushroom body is a higher order brain area that is key to memory formation and sensory processing. Mushroom body (MB) extrinsic neurons leaving the output region of the MB, the lobes and the peduncle, are thought to be especially important in these processes. In the honeybee brain, a distinct class of MB extrinsic neurons, A3 neurons, are implicated in playing a role in learning. Their MB arborisations are either restricted to the lobes and the peduncle, here called A3 lobe connecting neurons, or they provide feedback information from the lobes to the input region of the MB, the calyces, here called A3 feedback neurons. In this study, we analyzed the morphology of individual A3 lobe connecting and feedback neurons using confocal imaging. A3 feedback neurons were previously assumed to innervate each lip compartment homogenously. We demonstrate here that A3 feedback neurons do not innervate whole subcompartments, but rather innervate zones of varying sizes in the MB lip, collar, and basal ring. We describe for the first time the anatomical details of A3 lobe connecting neurons and show that their connection pattern in the lobes resemble those of A3 feedback cells. Previous studies showed that A3 feedback neurons mostly connect zones of the vertical lobe that receive input from Kenyon cells of distinct calycal subcompartments with the corresponding subcompartments of the calyces. We can show that this also applies to the neck of the peduncle and the medial lobe, where both types of A3 neurons arborize only in corresponding zones in the calycal subcompartments. Some A3 lobe connecting neurons however connect multiple vertical lobe areas. Contrarily, in the medial lobe, the A3 neurons only innervate one division. We found evidence for both input and output areas in the vertical lobe. Thus, A3 neurons are more diverse than previously thought. The understanding of their detailed anatomy might enable us to derive circuit models for learning and memory and test physiological data.
Active tactile exploration behaviour is constrained to a large extent by the morphological and biomechanical properties of the animal's somatosensory system. In the model organism Carausius morosus, the main tactile sensory organs are long, thin, seemingly delicate, but very robust antennae. Previous studies have shown that these antennae are compliant under contact, yet stiff enough to maintain a straight shape during active exploration. Overcritical damping of the flagellum, on the other hand, allows for a rapid return to the straight shape after release of contact. Which roles do the morphological and biomechanical adaptations of the flagellum play in determining these special mechanical properties? To investigate this question, we used a combination of biomechanical experiments and numerical modelling. A set of four finite-element (FE) model variants was derived to investigate the effect of the distinct geometrical and material properties of the flagellum on its static (bending) and dynamic (damping) characteristics. The results of our numerical simulations show that the tapered shape of the flagellum had the strongest influence on its static biomechanical behaviour. The annulated structure and thickness gradient affected the deformability of the flagellum to a lesser degree. The inner endocuticle layer of the flagellum was confirmed to be essential for explaining the strongly damped return behaviour of the antenna. By highlighting the significance of two out of the four main structural features of the insect flagellum, our study provides a basis for mechanical design of biomimetic touch sensors tuned to become maximally flexible while quickly resuming a straight shape after contact.
Learning visual cues is an essential capability of bees for vital behaviors such as orientation in space and recognition of nest sites, food sources and mating partners. To study learning and memory in bees under controlled conditions, the proboscis extension response (PER) provides a well-established behavioral paradigm. While many studies have used the PER paradigm to test olfactory learning in bees because of its robustness and reproducibility, studies on PER conditioning of visual stimuli are rare. In this study, we designed a new setup to test the learning performance of restrained honey bees and the impact of several parameters: stimulus presentation length, stimulus size (i.e. visual angle) and ambient illumination. Intact honey bee workers could successfully discriminate between two monochromatic lights when the color stimulus was presented for 4, 7 and 10 s before a sugar reward was offered, reaching similar performance levels to those for olfactory conditioning. However, bees did not learn at shorter presentation durations. Similar to free-flying honey bees, harnessed bees were able to associate a visual stimulus with a reward at small visual angles (5 deg) but failed to utilize the chromatic information to discriminate the learned stimulus from a novel color. Finally, ambient light had no effect on acquisition performance. We discuss possible reasons for the distinct differences between olfactory and visual PER conditioning.
Insect antennae are sensory organs of great importance because they can sense diverse environmental stimuli. In addition to serving as primary olfactory organs of insects, antennae also sense a wide variety of mechanosensory stimuli, ranging from low‐frequency airflow or gravity cues to high‐frequency antennal vibrations due to sound, flight or touch. The basal segments of the antennae house multiple types of mechanosensory structures that prominently include the sensory hair plates, or Böhm's bristles, which measure the gross extent of antennal movement, and a ring of highly sensitive scolopidial neurons, collectively called the Johnston's organs, which record subtle flagellar vibrations. To fulfil their multifunctional mechanosensory role, the antennae of insects must actively move thereby enhancing their ability to sense various cues in the surrounding environment. This tight coupling between antennal mechanosensory function and antennal movements means that the underlying mechanosensory‐motor apparatus constitutes a highly tuned feedback‐controlled system. Our study aims to explore how the sensory and motor components of this system are configured to enable such functional versatility. We describe antennal mechanosensory neurons, their central projections in the brain relative to antennal motor neurons and the internal morphology of various antennal muscles that actuate the basal segments of the antenna. We studied these in the Oleander hawk moth (Daphnis nerii) using a combination of techniques such as neural dye fills, confocal microscopy, scanning electron microscopy and X‐Ray tomography. Our study thus provides a detailed anatomical picture of the antennal mechanosensory‐motor apparatus, which in turn provides key insights into its multifunctional role. This article is protected by copyright. All rights reserved.
When sampling odors, many insects are moving their antennae in a complex but repeatable fashion. Previous studies with bees have tracked antennal movements in only two dimensions, with a low sampling rate and with relatively few odorants. A detailed characterization of the multimodal antennal movement patterns as function of olfactory stimuli is thus wanted. The aim of this study is to test for a relationship between the scanning movements and the properties of the odor molecule.
We tracked several key locations on the antennae of bumblebees at high frequency and in three dimensions while stimulating the insect with puffs of 11 common odorants released in a low-speed continuous flow. Water and paraffin were used as negative controls. Movement analysis was done with the neural network Deeplabcut.
Bees use a stereotypical oscillating motion of their antennae when smelling odors, similar across all bees, independently of the identity of the odors and hence their diffusivity and vapor pressure. The variability in the movement amplitude among odors is as large as between individuals. The main type of oscillation at low frequencies and large amplitude is triggered by the presence of an odor and is in line with previous work, as is the speed of movement. The second oscillation mode at higher frequencies and smaller amplitude is constantly present. Antennae are quickly deployed when a stimulus is perceived, decorrelate their movement trajectories rapidly and oscillate vertically with a large amplitude and laterally with a smaller one. The cone of air space thus sampled was identified through the 3D understanding of the motion patterns.
The amplitude and speed of antennal scanning movements seem to be function of the internal state of the animal, rather than determined by the odorant. Still, bees display an active olfactory sampling strategy. First, they deploy their antennae when perceiving an odor. Second, fast vertical scanning movements further increase the odorant capture rate. Finally, lateral movements might enhance the likelihood to locate the source of odor, similarly to the lateral scanning movement of insects at odor plume boundaries.
Desert ants, Cataglyphis fortis, search for a repeatedly visited food source by employing a combined olfactory and anemotactic orientation strategy (in addition to their visually based path-integration scheme). This behaviour was investigated by video-tracking consecutive foraging trips of individually marked ants under a variety of experimental conditions, including manipulations of the olfactory and wind-detecting systems of the ants. If the wind blows from a constant direction, ants familiar with the feeding site follow outbound paths that lead them into an area 0.5–2.5 m downwind of the feeding station. Here, the ants apparently pick up odour plumes emanating from the food source and follow these by steering an upwind course until they reach the feeder. If the food is removed, foragers usually concentrate their search movements within the area downwind of the feeding site. Only when the wind happens to subside or when tail-wind conditions prevail do the ants steer direct courses towards the food.
Elimination of olfactory input by clipping the antennal flagella, or of wind perception by immobilising the bases of the antennae, altered the foraging behaviour of the ants in ways that supported these interpretations. Ants with clipped flagella were never observed to collect food items.
Insect antennae are hollow, blood-filled fibers with complex shape. Muscles in the two basal segments control antennal movement, but the rest (flagellum) is muscle-free. The insect can controllably flex, twist, and maneuver its antennae laterally. To explain this behavior, we performed a comparative study of structural and tensile properties of the antennae of Periplaneta americana (American cockroach), Manduca sexta (Carolina hawkmoth), and Vanessa cardui (painted lady butterfly). These antennae demonstrate a range of distinguishable tensile properties, responding either as brittle or strain-adaptive fibers that stiffen when stretched. Scanning electron microscopy and high-speed imaging of antennal breakup during stretching revealed complex coupling of blood pressure and cuticle deformation in antennae. A generalized Lamé theory of solid mechanics was developed to include the force-driven deformation of blood-filled antennal tubes. We validated the theory against experiments with artificial antennae with no adjustable parameters. Blood pressure increased when the insect inflated its antennae or decreased below ambient pressure when an external tensile load was applied to the antenna. The pressure–cuticle coupling can be controlled through changes of the blood volume in the antennal lumen. In insects that do not fill the antennal lumen with blood, this blood pressure control is lacking, and the antennae react only by muscular activation. We suggest that the principles we have discovered for insect antennae apply to other appendages that share a leg-derived ancestry. Our work offers promising new applications for multifunctional fiber-based microfluidics that could transport fluids and be manipulated by the same fluid on demand.
Statement of Significance
Insect antennae are blood-filled, segmented fibers with muscles in the two basal segments. The long terminal segment is muscle-free but can be flexed. To explain this behavior, we examined structure-function relationships of antennae of cockroaches, hawkmoths, and butterflies. Hawkmoth antennae behave as brittle fibers, but butterfly and cockroach antennae showed strain-adaptive behavior like fibers that stiffen when stretched. Videomicroscopy of antennal breakup during stretching revealed complex coupling of blood pressure and cuticle deformation. Our solid mechanics model explains this behavior. Because antennae are leg-derived appendages, we suggest that the principles we found apply to other appendages of leg-derived ancestry. Our work offers new applications for multifunctional fiber-based microfluidics that could transport fluids and be manipulated by the fluid on demand.
Many animals use their tactile sense for active exploration and tactually guided behaviors like near-range orientation. In insects, tactile sensing is often intimately linked to locomotion, resulting in the orchestration of several concurrent active movements, including turning of the entire body, rotation of the head, and searching or sampling movements of the antennae. The present study aims at linking the sequence of tactile contact events to associated changes of all three kinds of these active movements (body, head and antennae). To do so, we chose the Indian stick insect Carausius morosus, a common organism to study sensory control of locomotion. Methodologically, we combined recordings of walking speed, heading, whole-body kinematics and antennal contact sequences during stationary, tethered walking and controlled presentation of an “artificial twig” for tactile exploration.
Our results show that object presentation episodes as brief as five seconds are sufficient to allow for a systematic investigation of tactually-induced turning behavior in walking stick insects. Animals began antennating the artificial twig within 0.5 s. and altered the beating-fields of both antennae in a position-dependent manner. This change was mainly carried by a systematic shift of the head-scape joint movement and accompanied by associated changes in contact likelihood, contact location and sampling direction of the antennae. The turning tendency of the insect also depended on stimulus position, whereas the active, rhythmic head rotation remained un-affected by stimulus presentation. We conclude that the azimuth of contact location is a key parameter of active tactile exploration and tactually-induced turning in stick insects.
In insects the tactile sense is important for near-range orientation and is involved in various behaviors. Nocturnal insects such as the stick insect Carausius morosus continuously explore their surroundings by actively moving their antennae when walking. Upon antennal contact with objects, stick insects show a targeted front-leg movement. As this reaction occurs within 40 ms, descending transfer of information from the brain to the thorax needs to be fast. So far, a number of descending interneurons have been described that may be involved in this reach-to-grasp behavior. One of these is the contralateral ON-type velocity-sensitive neuron (cONv). cONv was found to encode antennal joint-angle velocity during passive movement. Here, we characterize the transient response properties of cONv, including its dependence on joint angle range and direction. Since antennal hair field afferent terminals were shown to arborize close to cONv dendrites, we test whether antennal hair fields contribute to the joint-angle velocity encoding of cONv. To do so, we conducted bilateral extracellular recordings of both cONv interneurons per animal before and after hair field ablations. Our results show that cONv responses are highly transient, with velocity-dependent differences in delay and response magnitude. As yet, the steady state activity level was maintained until the stop of antennal movement, irrespective of movement velocity. Hair field ablation caused a moderate but significant reduction of movement-induced cONv firing rate by up to 40 %. We conclude that antennal proprioceptive hair fields contribute to the velocity-tuning of cONv, though further antennal mechanoreceptors must be involved, too.
Wind can act as an external cue to control an animal’s heading. A new study reveals the neural mechanisms behind the wind information pathway in the insect brain.
Many walking insects use vision for long-distance navigation, but the influence of vision on rapid walking performance that requires close-range obstacle detection and directing the limbs towards stable footholds remains largely untested. We compared Argentine ant ( Linepithema humile ) workers in light versus darkness while traversing flat and uneven terrain. In darkness, ants reduced flat-ground walking speeds by only 5%. Similarly, the approach speed and time to cross a step obstacle were not significantly affected by lack of lighting. To determine whether tactile sensing might compensate for vision loss, we tracked antennal motion and observed shifts in spatiotemporal activity as a result of terrain structure but not illumination. Together, these findings suggest that vision does not impact walking performance in Argentine ant workers. Our results help contextualize eye variation across ants, including subterranean, nocturnal and eyeless species that walk in complete darkness. More broadly, our findings highlight the importance of integrating vision, proprioception and tactile sensing for robust locomotion in unstructured environments.
Spatial maps in the brain are most accurate when they are linked to external sensory cues. Here, we show that the compass in the Drosophila brain is linked to the direction of the wind. Shifting the wind rightward rotates the compass as if the fly were turning leftward, and vice versa. We describe the mechanisms of several computations that integrate wind information into the compass. First, an intensity-invariant representation of wind direction is computed by comparing left-right mechanosensory signals. Then, signals are reformatted to reduce the coding biases inherent in peripheral mechanics, and wind cues are brought into the same circular coordinate system that represents visual cues and self-motion signals. Because the compass incorporates both mechanosensory and visual cues, it should enable navigation under conditions where no single cue is consistently reliable. These results show how local sensory signals can be transformed into a global, multimodal, abstract representation of space.
In pursuit of food, hungry animals mobilize significant energy resources and overcome exhaustion and fear. How need and motivation control the decision to continue or change behavior is not understood. Using a single fly treadmill, we show that hungry flies persistently track a food odor and increase their effort over repeated trials in the absence of reward suggesting that need dominates negative experience. We further show that odor tracking is regulated by two mushroom body output neurons (MBONs) connecting the MB to the lateral horn. These MBONs, together with dopaminergic neurons and Dop1R2 signaling, control behavioral persistence. Conversely, an octopaminergic neuron, VPM4, which directly innervates one of the MBONs, acts as a brake on odor tracking by connecting feeding and olfaction. Together, our data suggest a function for the MB in internal state-dependent expression of behavior that can be suppressed by external inputs conveying a competing behavioral drive.
Wind is a major navigational cue for insects, but how wind direction is decoded by central neurons in the insect brain is unknown. Here we find that walking flies combine signals from both antennae to orient to wind during olfactory search behavior. Movements of single antennae are ambiguous with respect to wind direction, but the difference between left and right antennal displacements yields a linear code for wind direction in azimuth. Second-order mechanosensory neurons share the ambiguous responses of a single antenna and receive input primarily from the ipsilateral antenna. Finally, we identify novel “wedge projection neurons” that integrate signals across the two antennae and receive input from at least three classes of second-order neurons to produce a more linear representation of wind direction. This study establishes how a feature of the sensory environment—wind direction—is decoded by neurons that compare information across two sensors. Suver et al. describe how walking flies use their two antennae to measure wind direction. They describe a mechanosensory pathway that encodes antennal movements, with higher-order neurons combining information from the two antennae to linearly encode wind direction.
For many insects, celestial compass cues play an important role in keeping track of their directional headings. One well-investigated group of celestial orientating insects are the African ball-rolling dung beetles. After finding a dung pile, these insects detach a piece, form it into a ball and roll it away along a straight path while facing backwards. A brain region, termed the central complex, acts as an internal compass that constantly updates the ball-rolling dung beetle about its heading. In this review, we give insights into the compass network behind straight-line orientation in dung beetles and place it in the context of the orientation mechanisms and neural networks of other insects. We find that the neuronal network behind straight-line orientation in dung beetles has strong similarities to the ones described in path-integrating and migrating insects, with the central complex being the key control point for this behavior. We conclude that, despite substantial differences in behavior and navigational challenges, dung beetles encode compass information in a similar way to other insects.
Hemipteroid insects (Paraneoptera), with over 10% of all known insect diversity, are a major component of terrestrial and aquatic ecosystems. Previous phylogenetic analyses have not consistently resolved the relationships among major hemipteroid lineages. We provide maximum likelihood-based phylogenomic analyses of a taxonomically comprehensive dataset comprising sequences of 2,395 single-copy, protein-coding genes for 193 samples of hemipteroid insects and outgroups. These analyses yield a well-supported phylogeny for hemipteroid insects. Monophyly of each of the three hemipteroid orders (Psocodea, Thysanoptera, and Hemiptera) is strongly supported, as are most relationships among suborders and families. Thysanoptera (thrips) is strongly supported as sister to Hemiptera. However, as in a recent large-scale analysis sampling all insect orders, trees from our data matrices support Psocodea (bark lice and parasitic lice) as the sister group to the holometabolous insects (those with complete metamorphosis). In contrast, four-cluster likelihood mapping of these data does not support this result. A molecular dating analysis using 23 fossil calibration points suggests hemipteroid insects began diversifying before the Carboniferous, over 365 million years ago. We also explore implications for understanding the timing of diversification, the evolution of morphological traits, and the evolution of mitochondrial genome organization. These results provide a phylogenetic framework for future studies of the group.
Directed and meaningful animal behavior depends on the ability to sense key features in the environment. Among the different environmental signals, olfactory cues are critically important for foraging, navigation, and social communication in many species, including ants. Ants use their two antennae to explore the olfactory world, but how they do so remains largely unknown. In this study, we use high resolution videography to characterize the antennae dynamics of carpenter ants (Camponotus pennsylvanicus). Antennae are highly active during both odor tracking and exploratory behavior. When tracking, ants used several distinct behavioral strategies with stereotyped antennae sampling patterns (which we call Sinusoidal, Probing, and Trail Following). In all behaviors, left and right antennae movements were anti-correlated, and tracking ants exhibited biases in the use of left vs right antenna to sample the odor trail. These results suggest non-redundant roles for the two antennae. In one of the behavioral modules (Trail Following), ants used both antennae to detect trail edges and direct subsequent turns, suggesting a specialized form of tropotaxis. Lastly, removal of an antenna resulted not only in less accurate tracking but also in changes in the sampling pattern of the remaining antenna. Our quantitative characterization of odor trail tracking lays a foundation to build better models of olfactory sensory processing and sensorimotor behavior in terrestrial insects.
Despite their tiny brains, insects show impressive abilities when navigating over short distances during path integration or during migration over thousands of kilometers across entire continents. Celestial compass cues often play an important role as references during navigation. In contrast to many other insects, South African dung beetles rely exclusively on celestial cues for visual reference during orientation. After finding a dung pile, these animals cut off a piece of dung from the pat, shape it into a ball and roll it away along a straight path until a suitable place for underground consumption is found. To maintain a constant bearing, a brain region in the beetle's brain, called the central complex, is crucially involved in the processing of skylight cues, similar to what has already been shown for path‐integrating and migrating insects.
In this study, we characterized the neuroanatomy of the sky‐compass network and the central complex in the dung beetle brain in detail. Using tracer injections, combined with imaging and 3D modelling, we describe the anatomy of the possible sky‐compass network in the central brain. We used a quantitative approach to study the central‐complex network and found that several types of neuron exhibit a highly organized connectivity pattern. The architecture of the sky‐compass network and central complex is similar to that described in insects that perform path integration or are migratory. This suggests that, despite their different orientation behaviors, this neural circuity for compass orientation is highly conserved across the insects.
This article is protected by copyright. All rights reserved.
Like several other arthropod species, stick insects use their antennae for tactile exploration of the near-range environment and for spatial localisation of touched objects. More specifically, Carausius morosus continuously moves its antennae during locomotion and reliably responds to antennal contact events with directed movements of a front leg. Here we investigate the afferent projection patterns of antennal hair fields (aHF), proprioceptors known to encode antennal posture and movement, and to be involved in antennal movement control. We show that afferents of all seven aHF of C. morosus have terminal arborisations in the dorsal lobe (DL) of the cerebral (=supraoesophageal) ganglion, and descending collaterals that terminate in a characteristic part of the gnathal (=suboesophageal) ganglion. Despite differences of functional roles among aHF, terminal arborisation patterns show no topological arrangement according to segment specificity or direction of movement. In the DL, antennal motoneuron neurites show arborizations in proximity to aHF afferent terminals. Despite the morphological similarity of single mechanoreceptors of aHF and adjacent tactile hairs on the pedicel and flagellum, we find a clear separation of proprioceptive and exteroceptive mechanosensory neuropils in the cerebral ganglion. Moreover, we also find this functional separation in the gnathal ganglion.
Insect antennae have been repeatedly proposed as paragons of active tactile sensors for biomimetic robots. A challenging aspect of using insect-like feelers for tactile localisation concerns the compliance of the long and slender structure of insect antennae. Other than in a rigid sensory probe, where the contact location in space may be estimated from the pointing direction and contact distance along the probe (polar coordinates), the strong compliance of insect antennae during contact events raises the question how insects can localise contact positions in space. Here we study the stick insect antenna to address this question. Our main objective was to test whether and how the bending properties of the insect antenna may allow reliable estimation of spatial contact locations through an array of bending sensors. During walking and climbing, the stick insect Carausius morosus executes cyclic antennal movements to explore the ambient space ahead. When the antenna touches an obstacle, it often bends strongly. Nevertheless, the insect can reliably reach for the contacted obstacle. Here, we systematically deflected insect antennae with an industrial robot to mimic an array of static contact locations. Then, we measured the resulting curvature of the flagellum, assuming that campanifom sensilla distributed along the flagellum could encode the corresponding bending profile. We found that we could train an artificial neural network to estimate the contact positions in 3D space with an accuracy of 0.5 mm or less from a given set of curvature data. This suggests that the bending characteristics of a tactile sensory probe could be tuned to aid spatial localisation by contact-site-dependent, compliant deformation.