Antennal Position Research Articles

Dynamic antennal positioning allows honeybee followers to decode the dance

The honeybee waggle dance has been widely studied as a communication system, yet we know little about how nestmates assimilate the information needed to navigate toward the signaled resource. They are required to detect the dancer's orientation relative to gravity and duration of the waggle phase and translate this into a flight vector with a direction relative to the sun1 and distance from the hive.2,3 Moreover, they appear capable of doing so from varied, dynamically changing positions around the dancer. Using high-speed, high-resolution video, we have uncovered a previously unremarked correlation between antennal position and the relative body axes of dancer and follower bees. Combined with new information about antennal inputs4,5 and spatial encoding in the insect central complex,6,7 we show how a neural circuit first proposed to underlie path integration could be adapted to decoding the dance and acquiring the signaled information as a flight vector that can be followed to the resource. This provides the first plausible account of how the bee brain could support the interpretation of its dance language.

Triple electroantennography captures the range and spatial arrangement of olfactory sensory neuron response on an insect antenna

BackgroundElectroantennography (EAG) is a basic neuroscientific tool that is widely used to measure olfactory responses in insects. It is particularly adapted to probing the olfactory systems of non-model insect species in chemical ecology and evolutionary biology. As currently practiced, EAG measures have varying degrees of correlation with olfactory responses, especially for insects whose olfactory sensory neurons (OSNs) are arranged in zones on the antennae. This limitation was shown to be partly due to the fact that only a single antennal position was recorded. New methodsWe describe a setup using triple electroantennography (EAG3), whereby three antennal positions are recorded simultaneously. The spatial arrangement of the electrodes ensures the mechanical stability of the assembly. The EAG3 detector was coupled to a gas chromatograph (GC-EAD3), customized using a Dean’s switch to improve the EAG signals by chopper modulation. EAG3 signals were analysed through a current point model to estimate olfactory responses across the antenna. ResultsRecordings were performed on Tephritidae and Drosophila species, which have antennae of different shapes and sizes. We confirmed that the spatio-temporal pattern of antennal activation was stimulus dependent and allowed us to quantify the antennal olfactory response. Comparisons with existing methodCompared to typical single-probe EAG, we show that EAG3 improves response quantification and increases the range of compounds for which a sensory response is detected. ConclusionsOur EAG3 setup is an original low-cost and easy-to-use method. It offers a useful bridge between comprehensive neurophysiological investigations and the broader themes explored in chemical ecology.

Active antennal movements in Drosophila can tune wind encoding

Insects use their antennae to smell odors,1,2 detect auditory cues,3,4 and sense mechanosensory stimuli such as wind5 and objects,6,7,8 frequently by combining sensory processing with active movements. Genetic access to antennal motor systems would therefore provide a powerful tool for dissecting the circuit mechanisms underlying active sensing, but little is known about how the most genetically tractable insect, Drosophila melanogaster, moves its antennae. Here, we use deep learning to measure how tethered Drosophila move their antennae in the presence of sensory stimuli and identify genetic reagents for controlling antennal movement. We find that flies perform both slow adaptive movements and fast flicking movements in response to wind-induced deflections, but not the attractive odor apple cider vinegar. Next, we describe four muscles in the first antennal segment that control antennal movements and identify genetic driver lines that provide access to two groups of antennal motor neurons and an antennal muscle. Through optogenetic inactivation, we provide evidence that antennal motor neurons contribute to active movements with different time courses. Finally, we show that activation of antennal motor neurons and muscles can adjust the gain and acuity of wind direction encoding by antennal displacement. Together, our experiments provide insight into the neural control of antennal movement and suggest that active antennal positioning in Drosophila may tune the precision of wind encoding.

Antenna movements as a function of odorants’ biological value in honeybees (Apis mellifera L.)

In honeybees, the antennae are highly mobile sensory organs that express scanning movements in various behavioral contexts and toward many stimuli, especially odorants. The rules underlying these movements are still unclear. Using a motion-capture system, we analyzed bees’ antennal responses to a panel of pheromonal and other biologically relevant odorants. We observed clear differences in bees’ antennal responses, with opposite movements to stimuli related to opposite contexts: slow backward movements were expressed in response to alarm pheromones, while fast forward movements were elicited by food related cues as well as brood and queen related pheromones. These responses are reproducible, as a similar pattern of odor-specific responses was observed in bees from different colonies, on different years. We then tested whether odorants’ attractiveness for bees, measured using an original olfactory orientation setup, may predict antenna movements. This simple measure of odorants’ valence did however not correlate with either antennal position or velocity measures, showing that more complex rules than simple hedonics underlie bees’ antennal responses to odorants. Lastly, we show that newly-emerged bees express only limited antennal responses compared to older bees, suggesting that a significant part of the observed responses are acquired during bees’ behavioral development.

The Space-Time Variation of Phase Imbalance for GF-3 Azimuth Multichannel Mode

Azimuth multichannel (AMC) synthetic aperture radar (SAR) is an advanced technology that can prevent the minimum antenna area constraint and provide high-resolution and wide-swath SAR images. The calibration of phase imbalance is an important topic in the AMC SAR signal processing since it has a significant impact on the image quality. For one SAR image, the phase imbalance is usually considered as a constant. However, because of the attitude errors, antenna position errors, target elevation, target motion, and phase mismatch of the antenna pattern, the actual phase imbalance is time-varying in azimuth and space-varying in range. Although the space-time variation of phase imbalances is too tiny to make a little effect on the product quality, it is still meaning to study the variation. On the one hand, it is possible to quickly estimate the phase imbalance of the whole observing operation and eliminate the influences of target motion, on the phase imbalance. On the other hand, some parameters, such as motion, can be retrieved by the phase imbalance. This article first establishes the signal models between phase imbalances and attitude errors, antennal position errors, and target elevation. Then, the signal model is verified by some simulations based on the parameters of Gaofen-3 (GF-3). In addition, the phase imbalance of the real data acquired by GF-3 is processed. Finally, based on the procession results of GF-3 real data, this article makes some discussions and points out the direction for the future work.

Tuneable reflexes control antennal positioning in flying hawkmoths

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.

Current Source Density Analysis of Electroantennogram Recordings: A Tool for Mapping the Olfactory Response in an Insect Antenna.

The set of chemosensory receptors expressed by the olfactory receptor neurons lying in an insect's antennae and maxillary palps define the ability of this insect to perceive the volatile chemicals of its environment. The main two electrophysiological methods of antennal recordings for studying the range of chemicals that activate chemosensory receptors have limitations. Single-sensillum recording (SSR) samples a subset of olfactory receptor neurons and therefore does not reveal the full capacity of an insect to perceive an odor. Electroantennography (EAG), even if less resolutive than SSRs, is sometimes preferred since it samples the activity of a large number of the olfactory receptor neurons. But, at least in flies, the amplitude of the EAG signal is not directly correlated with the degree of sensitivity of the insect to the olfactory compound. Such dual methodology was also used to study mammalian brains, and the current source density (CSD) analysis was developed to bridge the gap between the cellular and the population recordings. This paper details the use of a similar approach adapted to the study of olfactory responses within insects with bulbous antennae. The EAG was recorded at multiple antennal positions and the CSD that generates the EAG potentials were estimated. The method measures the activation of olfactory receptor neurons (ORNs) across the antennae and thus it quantifies the olfactory sensitivity of the insect. It allows a rapid mapping of olfactory responses and thus can be used to guide further SSRs or to determine that two chemicals are detected by independent ORNs. This study further explored biases resulting from a limited number of recording positions or from an approximation of the antennal geometry that should be considered for interpreting the CSD maps. It also shows that the CSD analysis of EAGs is compatible with a gas chromatograph stimulator for analyzing the response to complex odors. Finally, I discuss the origin of the EAG signal in light of the CSD theory.

Fast intensity adaptation enhances the encoding of sound in Drosophila

To faithfully encode complex stimuli, sensory neurons should correct, via adaptation, for stimulus properties that corrupt pattern recognition. Here we investigate sound intensity adaptation in the Drosophila auditory system, which is largely devoted to processing courtship song. Mechanosensory neurons (JONs) in the antenna are sensitive not only to sound-induced antennal vibrations, but also to wind or gravity, which affect the antenna’s mean position. Song pattern recognition, therefore, requires adaptation to antennal position (stimulus mean) in addition to sound intensity (stimulus variance). We discover fast variance adaptation in Drosophila JONs, which corrects for background noise over the behaviorally relevant intensity range. We determine where mean and variance adaptation arises and how they interact. A computational model explains our results using a sequence of subtractive and divisive adaptation modules, interleaved by rectification. These results lay the foundation for identifying the molecular and biophysical implementation of adaptation to the statistics of natural sensory stimuli.

Airflow and optic flow mediate antennal positioning in flying honeybees.

To maintain their speeds during navigation, insects rely on feedback from their visual and mechanosensory modalities. Although optic flow plays an essential role in speed determination, it is less reliable under conditions of low light or sparse landmarks. Under such conditions, insects rely on feedback from antennal mechanosensors but it is not clear how these inputs combine to elicit flight-related antennal behaviours. We here show that antennal movements of the honeybee, Apis mellifera, are governed by combined visual and antennal mechanosensory inputs. Frontal airflow, as experienced during forward flight, causes antennae to actively move forward as a sigmoidal function of absolute airspeed values. However, corresponding front-to-back optic flow causes antennae to move backward, as a linear function of relative optic flow, opposite the airspeed response. When combined, these inputs maintain antennal position in a state of dynamic equilibrium.

A Computational Model of a Descending Mechanosensory Pathway Involved in Active Tactile Sensing.

Many animals, including humans, rely on active tactile sensing to explore the environment and negotiate obstacles, especially in the dark. Here, we model a descending neural pathway that mediates short-latency proprioceptive information from a tactile sensor on the head to thoracic neural networks. We studied the nocturnal stick insect Carausius morosus, a model organism for the study of adaptive locomotion, including tactually mediated reaching movements. Like mammals, insects need to move their tactile sensors for probing the environment. Cues about sensor position and motion are therefore crucial for the spatial localization of tactile contacts and the coordination of fast, adaptive motor responses. Our model explains how proprioceptive information about motion and position of the antennae, the main tactile sensors in insects, can be encoded by a single type of mechanosensory afferents. Moreover, it explains how this information is integrated and mediated to thoracic neural networks by a diverse population of descending interneurons (DINs). First, we quantified responses of a DIN population to changes in antennal position, motion and direction of movement. Using principal component (PC) analysis, we find that only two PCs account for a large fraction of the variance in the DIN response properties. We call the two-dimensional space spanned by these PCs ‘coding-space’ because it captures essential features of the entire DIN population. Second, we model the mechanoreceptive input elements of this descending pathway, a population of proprioceptive mechanosensory hairs monitoring deflection of the antennal joints. Finally, we propose a computational framework that can model the response properties of all important DIN types, using the hair field model as its only input. This DIN model is validated by comparison of tuning characteristics, and by mapping the modelled neurons into the two-dimensional coding-space of the real DIN population. This reveals the versatility of the framework for modelling a complete descending neural pathway.

Visual feedback influences antennal positioning in flying hawk moths

Insect antennae serve a variety of sensory functions including tactile sensing, olfaction and flight control. For all of these functions, the precise positioning of the antenna is essential to ensure the proper acquisition of sensory feedback. Although antennal movements in diverse insects may be elicited or influenced by multimodal sensory stimuli, the relative effects of these cues and their integration in the context of antennal positioning responses are not well understood. In previous studies, we have shown that fields of Böhm's bristles located at the base of the antennae provide crucial mechanosensory input for antennal positioning in flying hawk moths. Here, we present electrophysiological and behavioral evidence to show that, in addition to the Böhm's bristles, antennal muscles of hawk moths also respond to bilateral visual input. Moreover, in contrast to the mechanosensory-motor circuit, which is entirely contained within the ipsilateral side, visual feedback influences antennal positioning on both contralateral and ipsilateral sides. Electromyograms recorded from antennal muscles show that the latency of muscle responses to visual stimulation ranged from 35 to 60 ms, considerably slower than their responses to mechanosensory stimuli (<10 ms). Additionally, the visual inputs received by antennal muscles are both motion-sensitive and direction-selective. We characterized the influence of visual feedback on antennal positioning by presenting open-loop translational and rotational visual stimuli to tethered flying moths. During rotational stimuli, we observed that the antenna contralateral to the direction of the turn moved forward through larger angles than the ipsilateral antenna. These observations suggest that whereas input from the Böhm's bristles mediates rapid corrections of antennal position, visual feedback may be involved in slower, bilaterally coordinated movements of the antenna during visually guided flight maneuvers. Thus, visual feedback can modulate the set point at which the antenna is held during flight in hawk moths.

The neural mechanisms of antennal positioning in flying moths

In diverse insects, the forward positioning of the antenna is often among the first behavioral indicators of the onset of flight. This behavior may be important for the proper acquisition of the mechanosensory and olfactory inputs by the antennae during flight. Here, we describe the neural mechanisms of antennal positioning in hawk moths from behavioral, neuroanatomical and neurophysiological perspectives. The behavioral experiments indicated that a set of sensory bristles called Böhm's bristles (or hair plates) mediate antennal positioning during flight. When these sensory structures were ablated from the basal segments of their antennae, moths were unable to bring their antennae into flight position, causing frequent collisions with the flapping wing. Fluorescent dye-fills of the underlying sensory and motor neurons revealed that the axonal arbors of the mechanosensory bristle neurons spatially overlapped with the dendritic arbors of the antennal motor neurons. Moreover, the latency between the activation of antennal muscles following stimulation of sensory bristles was also very short (<10 ms), indicating that the sensorimotor connections may be direct. Together, these data show that Böhm's bristles control antennal positioning in moths via a reflex mechanism. Because the sensory structures and motor organization are conserved across most Neoptera, the mechanisms underlying antennal positioning, as described here, are likely to be conserved in these diverse insects.

Exploring the coding space of tactile localization in the antennal system of the stick insect

Exploring the coding space of tactile localization in the antennal system of the stick insect

Antennal Morphology and Sensilla of Asian Multicolored Ladybird Beetles,Harmonia axyridisPallas (Coleoptera: Coccinellidae)

We investigated the antennal morphology, sensillar types, and sensillar distribution in the dark (“melanic”) and the light (“succinea”) forms of Asian multicolored ladybirds, H. axyridis, using scanning electron microscopy (SEM). Antennae of both sexes of H. axyridis consist of the scape, pedicel, and nine flagellomeres. Seven sensillar types are distinguished: four types of sensilla trichodeae (s.tr), four types of sensilla basiconicae (s.ba), four types of sensilla chaetica, and one type each of sensilla coeloconica (s.co), sensilla sporangium (s.sp), sensilla placoidea (s.pl), and Böhm bristle (s.bm). Sensilla trichodea are the most numerous; sensilla chaetica are the next most abundant. The number of other sensillar types is greatly reduced. On the tip of the 9th flagellomere, various types of sensilla are densely packed, except for s.bm and s.pl. No remarkable differences are found in the antennal size, shape, and sensillar types between the melanic and succinea forms of H. axyridis, but there is a difference in the total number of s.tr.2 between the two forms. No differences are found in the antennal size and the total number of sensillae between males and females of each form. According to the distribution of sensillae and sensillar functions reported in the past, s.tr are presumed to be pheromone receptors in H. axyridis, s.ch may function as mechanoreceptors and chemoreceptors, s.ba and s.co are postulated as plant volatiles receptors and chemo-, thermo-, or hygroreceptions, respectively, and s.bm may be related to perceiving the antennal position and movement.

Antennal and locomotor responses to attractive and aversive odors in the searching cockroach

The behavioral responses to attractive and aversive odors were examined in blinded adult male cockroaches under tethered-walking conditions. A sex pheromone-like stimulant derived from adult virgin females and artificially synthesized limonene were used as attractive and aversive odor sources, respectively. When a searching animal was stimulated with the attractive female-derived odor, the horizontal deflections of both the antennae were increased, and in most cases the vertical antennal positions were shifted downward. The stimulation also significantly decreased the walking speed of the animal. These behavioral changes imply a careful search in the immediate surroundings. The aftereffect of the sex pheromone was more pronounced on locomotion than on antennal movement. On the other hand, stimulation with the aversive odor (limonene) tended to suppress active antennal movement, and also increased the walking speed. Immediately after the withdrawal of the aversive odor, the active movement of the antennae was resumed, and the walking speed rapidly decreased to a level approximately the same as that of the control period. These results indicate that the responses to the qualitatively opposite types of odor are reciprocal to each other with regard to both antennal movement and locomotion.

Longevity and detection of persistent foraging trails in Pharaoh's ants, Monomorium pharaonis (L.)

Pheromone trails provide a positive feedback mechanism for many animal species, and facilitate the sharing of information about food, nest or mate location. How long pheromone trails persist determines how long these environmental memories are accessible to conspecifics. We determined the time frame over which Pharaoh's ant colonies can re-establish a long-lived trail and how the behaviour of individual workers contributes to trail re-establishment. We used artificially constrained pheromone trails on paper to investigate trail longevity and individual responses. Trails formed by traffic of 1000?2000 ant passages could be re-established after 24 h, and after 48 h for 4000?8000 ant passages. Only 27.5% of individual foragers were highly successful in a bioassay testing the ability to detect trails established 24 h earlier. Trail-finding ability was significantly correlated with a low antennal position. Long-lived trail detection scores increased significantly in 57% of foragers after 5 h of food deprivation and isolation, but declined again after feeding. In a control study, only 9% of foragers changed their scores, when isolated with food present. A high degree of conservatism was found such that, regardless of treatment, 21% always failed the bioassay and 17% always succeeded. Our demonstration of long-lived components in Pharaoh's ant trails and of a behavioural specialization in `pathfinding? shows that pheromone trails are more complex at the individual level than is generally recognized.

In vivo-application of anti-proctolin-antiserum affects antennal flight posture in crickets.

Tethered crickets flying in a wind tunnel adopt a characteristic posture in which the antennae are pointed in parallel and anteriorly into the headwind. Although the firing rates of antennal motoneurons are largely reduced after the start of a flight sequence, the associated postural changes of the antennae are small. It is hypothesised that proctolin, which is present in antennal motoneurons, stabilises the prolonged antennal forward position. To test this hypothesis, proctolin was blocked by anti-proctolin antiserum injections into one antennal base in otherwise intact behaving crickets. The antiserum quickly led to prolonged backward deflections of the treated antennae in 65% of cases. It then took more than one hour for the deflected posture to revert to a normal flight posture. It appears that proctolin is necessary to produce muscle tension large enough to hold the antennae in a forward position and to compensate for the headwind drag. Proctolin, therefore, acts to generate force with reduced electrical activity of motoneurons and muscles.

Mechanosensory control of antennal movement by the scapal hair plate in the American cockroach.

The voluntary movement of antennae of blinded cockroaches was examined in the tethered-walking condition. An object of metal plate was presented to a tip of a single antenna in order to induce tactile orientation behavior. Horizontal movements of the antenna before and during the object presentation were analyzed both before and after ablation of a mechanosensory organ, the scapal hair plate (S-HP), at the base of antenna. The resting antennal position shifted outwardly by about 20 degrees after the S-HP ablation. Spontaneous antennal movements in ablated animals became stiff and wider ranged. The tactile object was set at two different horizontal positions, 45 degrees and 90 degrees clockwise to the head, for the right side antenna. The number of contacts in a constant test period was significantly decreased in the tests at 45 degrees after ablation. Trajectories of antennal movements before and after contacts were categorized into four patterns. In the case that an antenna made contact with the object during its abduction (outward) movement, it then passed the object outwardly or withdrew inwardly. These were termed "outward-pass (O-P)" and "outward-withdrawal (O-W)" patterns, respectively. Similarly, contacts during the adduction (inward) movement were divided into "inward-pass (I-P)" or "inward-withdrawal (I-W)" pattern. Significant effects of the S-HP ablation appeared in the tests at 90 degrees : the I-P pattern mostly disappeared and was replaced by the I-W pattern. The results strongly suggest that the S-HP has crucial roles for controlling both spontaneous and stimulated movements of the cockroach antenna.

Tactile motor learning in the antennal system of the honeybee ( Apis mellifera L.)

Honeybees fixed in small tubes scan an object within the range of the antennae by touching it briefly and frequently. In our experiments the animals were able to scan an object for several minutes with the antennae. After moving the object out of the range of the antennae, the animals showed antennal movements for several minutes that were correlated with the position of the removed object. These changes of antennal movements are called “behavioural plasticity” and are interpreted as a form of motor learning. Bees showed behavioural plasticity only for objects with relatively large surfaces. Plasticity was more pronounced in bees whose compound eyes were occluded. Behavioural plasticity was related to the duration of object presentation. Repeated presentations of the object increased the degree of plasticity. After presentation durations of 30 min the animals showed a significant increase of antennal positions related to the surface of the object and avoidance of areas corresponding to the edges. Behavioural plasticity was compared with reward-dependent learning by conditioning bees to objects. The results of motor learning and reward-dependent conditioning suggest that bees have tactile spatial memory.

Courtship and intersexual signaling in the parasitic waspCotesia rubecula (Hymenoptera: Braconidae)

The courtship behavior of the parasitic wasp Cotesia rubeculawas studied in a flight tunnel using standard quantitative ethological techniques. Emission of a female sex pheromone induces searching and signaling behavior in males. Males combine wing-fanning, which produces low-frequency airborne sound, with “pulsing” behavior, which transmits a vibrational signal through the substrate to the female and induces her receptivity. Female receptivity is indicated by a stereotyped antennal position, which may provide a visual or tactile signal to courting males. Comparison of successful and unsuccessful courtships indicated that courtship success was dependent primarily on the effective production or reception of the male pulse signal. Overall, the sequence of courtship behavior was similar to that reported for other parasitic wasps.