insect-controlled-robot-mobile-robot-platform-to-evaluate-odor

Insect-controlled Robot: A Mobile Robot Platform to Evaluate the Odor-tracking Capability of an Insect

Robotic odor source localization has been a challenging area and one to which biological knowledge has been expected to contribute, as finding odor ...

The University of Tokyo

the university of tokyo

The 3rd axillary muscles (3AXMs) in the mesothorax in hawkmoths are direct flight muscles and pull forewings back along to the body axis. The 3AXMs are regarded as steering muscles because of their changeable activities during turning flight under tethered conditions. We investigated activities of the upper unit of the 3AXMs during free flight with a micro-telemetry device and captured body and wing movements by high-speed cameras. The 3AXM was activated with 1 to 3 spikes per each wingbeat cycle but sometimes ceased to fire. The phase of the onset of the activities was, even though it was variable, close to the phase of the elevator muscle activities. Therefore the upper unit of the 3AXM activities would affect upstroke properties phasically including wing retractions. We focused on longitudinal flight control and identified a correlation between the phase of the 3AXM and body pitch angle, which is important kinematical parameter for longitudinal control in insect flight. The phasic changes of the 3AXM activities would support quick changes in longitudinal control.

Changing motor patterns of the 3rd axillary muscle activities associated with longitudinal control in freely flying hawkmoths.

By combining optical triangulation with the comb-fringe technique and dual-channel telemetry, wing kinematics and body attitudes accompanying muscle activities of free-flying male hawkmoths were recorded synchronously when they performed flight manoeuvres elicited by a female sex pheromone. The results indicate that the wing leading edge angular position at the ventral stroke reversal, which can be decomposed by two orthogonal angular parameters (a flapping angle and a deviation angle), is well controllable. Two specific flight muscles, the dorsal-ventral muscle (DVM, indirect muscle, a wing elevator) and the third axillary muscle (3AXM, direct muscle, a wing retractor), can modulate the flapping angle and the deviation angle, respectively, by means of regulating the firing timing of muscle activities. The firing timing can be expressed by the firing latency absolutely, which is just before the timing of ventral stroke reversal. The results illustrate that lengthening the firing latency of the DVM and of the 3AXM can increase the flapping angle and the deviation angle, respectively, which both strengthen the downstroke at the ventral stroke reversal. The relationship of bilateral asymmetry shows that the bilateral differences in the firing latency of the DVM and of the 3AXM will cause bilateral differences in the wing position, which accompany the variations of yaw and roll angles in time course. This implies the contribution of the two muscles to active steering controls during turning or banking, though the DVM being an indirect muscle was generally treated as a power generator. Finally, the relationship between the pitch angle and the 3AXM latency, deduced from the relationships between the pitch angle and the deviation angle and between the deviation angle and the 3AXM latency, shows that lengthening the 3AXM latency can increase the pitch angle at the ventral stroke reversal by moving the wing tip far away from the centre of gravity of the body, which indicates a functional role of the 3AXM in active pitching control.

Active control of free flight manoeuvres in a hawkmoth, Agrius convolvuli.

Flight behaviors in various insect species are closely correlated with their mechanical and neuronal properties. Compared to locusts and flies which have been intensively studied, moths have "intermediate" properties in terms of the neurogenic muscle activations, power generation by indirect muscles, and two-winged-insect-like flapping behavior. Despite these unique characteristics, little is known about the neuronal mechanisms of flight control in moths. We investigated projections of the wing mechanosensory afferents in the central nervous system (CNS) of the hawkmoth, Agrius convolvuli, because the mechanosensory proprioceptive feedback has an essential role for flight control and would be presumably optimized for insect species. We conducted anterograde staining of nine afferent nerves from the fore- and hindwings. All of these afferents projected into the prothoracic, mesothoracic and metathoracic ganglia (TG1, 2 and 3) and had ascending fibers to the head ganglia. Prominent projection areas in the TG1-3 and suboesophageal ganglion (SOG) were common between the forewing, hindwing and contralateral forewing afferents, suggesting that information from different wings are converged at multiple levels presumably for coordinating wing flapping. On the other hand, differences of projections between the fore- and hindwing afferents were observed especially in projection areas of the tegulae in the TG1 and contralateral projections of the anterior forewing nerve in the TGs and SOG, which would reflect functional differences between corresponding mechanoreceptors on each wing. Afferents comprising groups of the campaniform sensilla at the wing bases had prominent ascending pathways to the SOG, resembling the head-neck motor system for gaze control in flies. Double staining of the wing afferents and flight or neck motoneurons also indicated potential connectivity between them. Our results suggest multiple roles of the wing proprioceptive feedback for flight and provide the anatomical basis for further understanding of neuronal mechanisms of the flight system in moths.

Central projections of the wing afferents in the hawkmoth, Agrius convolvuli.

To elucidate the dynamic information processing in a brain underlying adaptive behavior, it is necessary to understand the behavior and corresponding neural activities. This requires animals which have clear relationships between behavior and corresponding neural activities. Insects are precisely such animals and one of the adaptive behaviors of insects is high-accuracy odor source orientation. The most direct way to know the relationships between neural activity and behavior is by recording neural activities in a brain from freely behaving insects. There is also a method to give stimuli mimicking the natural environment to tethered insects allowing insects to walk or fly at the same position. In addition to these methods an 'insect-machine hybrid system' is proposed, which is another experimental system meeting the conditions necessary for approaching the dynamic processing in the brain of insects for generating adaptive behavior. This insect-machine hybrid system is an experimental system which has a mobile robot as its body. The robot is controlled by the insect through its behavior or the neural activities recorded from the brain. As we can arbitrarily control the motor output of the robot, we can intervene at the relationship between the insect and the environmental conditions.

Insect-machine hybrid system for understanding and evaluating sensory-motor control by sex pheromone in Bombyx mori.

Several insects require both olfactory and visual cues during odour-source localisation to successfully locate an odour source. In the male silkmoth, Bombyx mori, detection of the female sex pheromone triggers a programmed walking pattern, starting from a surge (straight-line walking) followed by zigzag walking. Although pheromone-triggered behaviour in silkmoths is well understood, the role of visual cues remains obscure. To address this question, we performed behavioural experiments on tethered-walking moths by recording their locomotion during stimulation with a pheromone and a visual motion pattern (optic flow). The experiments were conducted under open- and closed-loop visual stimuli. We found that the use of optic flow input was determined by the behavioural state of surge and zigzagging. Silkmoths exhibited an optomotor response, which is a behavioural visual response, by turning towards the same direction as optic flow stimuli only during surge, but not during zigzagging. In addition, modulation of the zigzag walking pattern was observed when the moths were presented with biased closed-loop visual stimuli (visual feedback with biased constant optic flow); however, the directional preference mechanism was different from that of the optomotor response. Based on these findings, we suggest that the optomotor response is utilised for course control during straight-line walking, whereas the absence of optomotor response during zigzagging is used to effectively perform the programmed walking pattern. Considering the neural basis of programmed behaviour, we speculate that at least two visual pathways are involved in the state-dependent use of optic flow during odour tracking behaviour in silkmoths.

Dynamic use of optic flow during pheromone tracking by the male silkmoth, Bombyx mori.

Odour plume tracking is an essential behaviour for animal survival. A fundamental strategy for this is to move upstream and then across-stream. Male silkmoths, Bombyx mori, display this strategy as a pre-programmed sequential behaviour. They walk forward (surge) in response to the female sex pheromone and perform a zigzagging 'mating dance'. Though pre-programmed, the surge direction is modulated by bilateral olfactory input and optic flow. However, the nature of the interaction between these two sensory modalities and contribution of the resultant motor command to localizing an odour source are still unknown. We evaluated the ability of the silkmoth to localize an odour source under conditions of disturbed sensory-motor coupling, using a silkmoth-driven mobile robot. The significance of the bilateral olfaction of the moth was confirmed by inverting the olfactory input to the antennae, or its motor output. Inversion of the motor output induced consecutive circling, which was inhibited by covering the visual field of the moth. This suggests that the corollary discharge from the motor command and the reafference of self-generated optic flow generate compensatory signals to guide the surge accurately. Additionally, after inverting the olfactory input, the robot successfully tracked the odour plume by using a combination of behaviours. These results indicate that accurate guidance of the reflexive surge by integrating bilateral olfactory and visual information with innate pre-programmed behaviours increases the flexibility to track an odour plume even under disturbed circumstances.

A simple behaviour provides accuracy and flexibility in odour plume tracking--the robotic control of sensory-motor coupling in silkmoths.

The interaction between neuromuscular systems and body mechanics plays an important role in the production of coordinated movements in animals. Lepidopteran insects move their wings by distortion of the thorax structure via the indirect flight muscles (IFMs), which are activated by neural signals at every stroke. However, how the action of these muscles affects thorax deformation and wing kinematics is poorly understood. We measured the deformation of the dorsal thorax (mesonotum) of tethered flying hawkmoths, Agrius convolvuli, using a high-speed laser profilometer combined with simultaneous recordings of electromyograms and wing kinematics. We observed that locally amplified mesonotum deformation near the wing hinges ensures sufficient wing movement. Furthermore, phase asymmetry in IFM activity leads to phase asymmetry in mesonotum oscillations and wingbeats. Our results revealed the flexibility and controllability of the single structure of the mesonotum by neurogenic action of the IFMs.

Article	Year
Changing motor patterns of the 3rd axillary muscle activities associated with longitudinal control in freely flying hawkmoths. Zoological science\| PubMed ID: 14993822	2004
Active control of free flight manoeuvres in a hawkmoth, Agrius convolvuli. The Journal of experimental biology\| PubMed ID: 18203998	2008
Central projections of the wing afferents in the hawkmoth, Agrius convolvuli. Journal of insect physiology\| PubMed ID: 21867710	2011
Insect-machine hybrid system for understanding and evaluating sensory-motor control by sex pheromone in Bombyx mori. Journal of comparative physiology. A, Neuroethology, sensory, neural, and behavioral physiology\| PubMed ID: 23749329	2013
Dynamic use of optic flow during pheromone tracking by the male silkmoth, Bombyx mori. The Journal of experimental biology\| PubMed ID: 24829328	2014
A simple behaviour provides accuracy and flexibility in odour plume tracking--the robotic control of sensory-motor coupling in silkmoths. The Journal of experimental biology\| PubMed ID: 26486361	2015
Flexibility and control of thorax deformation during hawkmoth flight. Biology letters\| PubMed ID: 26740560	2016

Noriyasu Ando

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