scholarly journals The roles of vision and antennal mechanoreception in hawkmoth flight control

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Ajinkya Dahake ◽  
Anna L Stöckl ◽  
James J Foster ◽  
Sanjay P Sane ◽  
Almut Kelber
Keyword(s):  
Visual System ◽  
Visual Feedback ◽  
Flight Control ◽  
Sensory Feedback ◽  
Body Position ◽  
Temporal Frequency ◽  
Macroglossum Stellatarum ◽  
Position And Orientation ◽  
Open Question ◽  
Compensatory Interactions

Flying animals need continual sensory feedback about their body position and orientation for flight control. The visual system provides essential but slow feedback. In contrast, mechanosensory channels can provide feedback at much shorter timescales. How the contributions from these two senses are integrated remains an open question in most insect groups. In Diptera, fast mechanosensory feedback is provided by organs called halteres and is crucial for the control of rapid flight manoeuvres, while vision controls manoeuvres in lower temporal frequency bands. Here, we have investigated the visual-mechanosensory integration in the hawkmoth Macroglossum stellatarum. They represent a large group of insects that use Johnston’s organs in their antennae to provide mechanosensory feedback on perturbations in body position. Our experiments show that antennal mechanosensory feedback specifically mediates fast flight manoeuvres, but not slow ones. Moreover, we did not observe compensatory interactions between antennal and visual feedback.

scholarly journals The roles of vision and antennal mechanoreception in hawkmoth flight control

2018 ◽  
Author(s):  
Ajinkya Dahake ◽  
Anna Stöckl ◽  
James J. Foster ◽  
Sanjay P. Sane ◽  
Almut Kelber
Keyword(s):  
Visual Feedback ◽  
Flight Control ◽  
High Speed ◽  
Sensory Feedback ◽  
Body Position ◽  
Temporal Frequency ◽  
Macroglossum Stellatarum ◽  
Position And Orientation ◽  
Open Question ◽  
Artificial Flowers

Flying animals need constant sensory feedback about their body position and orientation for flight control. The visual system provides essential but slow feedback. In contrast, mechanosensory channels can provide feedback at much shorter timescales. How the contributions from these two senses are integrated remains an open question in most insect groups. In Diptera, fast mechanosensory feedback is provided by organs called halteres, and is crucial for the control of rapid flight manoeuvres, while vision controls manoeuvres in lower temporal frequency bands. Here we have investigated the visual-mechanosensory integration in an insect which lacks halteres: the hawkmoth Macroglossum stellatarum. They represent a large group of insects that use Johnston’s organs in their antennae to provide mechanosensory feedback on perturbations in body position. High-speed videos of freely-flying hawkmoths hovering at stationary or oscillating artificial flowers showed that positional fidelity during flight was reduced in flagella ablated animals, but was recovered after flagella re-attachment. Our experiments show that antennal mechanosensory feedback specifically mediates fast flight manoeuvres, but not slow ones. Differences in the latency of visual feedback (in different light intensities) affected all antennal conditions equally, suggesting there was no compensatory interaction between antennal and visual feedback under the tested conditions. These results establish the importance of antennal mechanosensors in providing rapid mechanosensory feedback for finer control of flight manoeuvres, acting in parallel to visual feedback.

Plasticity in the Visual System Is Correlated With a Change in Lifestyle of Solitarious and Gregarious Locusts

2004 ◽  
Vol 91 (1) ◽  
pp. 1-12 ◽  
Author(s):  
Thomas Matheson ◽  
Stephen M. Rogers ◽  
Holger G. Krapp
Keyword(s):  
Visual System ◽  
Flight Control ◽  
Schistocerca Gregaria ◽  
Movement Detector ◽  
Time To Collision ◽  
Angular Extent ◽  
Behavioral Phase ◽  
Contralateral Movement ◽  
Gregarious Locusts ◽  
And Behavior

We demonstrate pronounced differences in the visual system of a polyphenic locust species that can change reversibly between two forms (phases), which vary in morphology and behavior. At low population densities, individuals of Schistocerca gregaria develop into the solitarious phase, are cryptic, and tend to avoid other locusts. At high densities, individuals develop instead into the swarm-forming gregarious phase. We analyzed in both phases the responses of an identified visual interneuron, the descending contralateral movement detector (DCMD), which responds to approaching objects. We demonstrate that habituation of DCMD is fivefold stronger in solitarious locusts. In both phases, the mean time of peak firing relative to the time to collision nevertheless occurs with a similar characteristic delay after an approaching object reaches a particular angular extent on the retina. Variation in the time of peak firing is greater in solitarious locusts, which have lower firing rates. Threshold angle and delay are therefore conserved despite changes in habituation or behavioral phase state. The different rates of habituation should contribute to different predator escape strategies or flight control for locusts living either in a swarm or as isolated individuals. For example, increased variability in the habituated responses of solitarious locusts should render their escape behaviors less predictable. Relative resistance to habituation in gregarious locusts should permit the continued responsiveness required to avoid colliding with other locusts in a swarm. These results will permit us to analyze neuronal plasticity in a model system with a well-defined and controllable behavioral context.

The Role of Online Visual Feedback for the Control of Target-Directed and Allocentric Hand Movements

2011 ◽  
Vol 105 (2) ◽  
pp. 846-859 ◽  
Author(s):  
Lore Thaler ◽  
Melvyn A. Goodale
Keyword(s):  
Visual Feedback ◽  
Visual Information ◽  
Sensory Feedback ◽  
Sensory Information ◽  
Movement Control ◽  
Sensorimotor Control ◽  
Hand Movements ◽  
Cast Doubt ◽  
Target Locations

Studies that have investigated how sensory feedback about the moving hand is used to control hand movements have relied on paradigms such as pointing or reaching that require subjects to acquire target locations. In the context of these target-directed tasks, it has been found repeatedly that the human sensory-motor system relies heavily on visual feedback to control the ongoing movement. This finding has been formalized within the framework of statistical optimality according to which different sources of sensory feedback are combined such as to minimize variance in sensory information during movement control. Importantly, however, many hand movements that people perform every day are not target-directed, but based on allocentric (object-centered) visual information. Examples of allocentric movements are gesture imitation, drawing, or copying. Here we tested if visual feedback about the moving hand is used in the same way to control target-directed and allocentric hand movements. The results show that visual feedback is used significantly more to reduce movement scatter in the target-directed as compared with the allocentric movement task. Furthermore, we found that differences in the use of visual feedback between target-directed and allocentric hand movements cannot be explained based on differences in uncertainty about the movement goal. We conclude that the role played by visual feedback for movement control is fundamentally different for target-directed and allocentric movements. The results suggest that current computational and neural models of sensorimotor control that are based entirely on data derived from target-directed paradigms have to be modified to accommodate performance in the allocentric tasks used in our experiments. As a consequence, the results cast doubt on the idea that models of sensorimotor control developed exclusively from data obtained in target-directed paradigms are also valid in the context of allocentric tasks, such as drawing, copying, or imitative gesturing, that characterize much of human behavior.

Processing of Natural Time Series of Intensities in the Early Visual System of the Blowfly

Perception ◽  
1997 ◽  
Vol 26 (1_suppl) ◽  
pp. 24-24 ◽  
Author(s):  
J H van Hateren
Keyword(s):  
Time Series ◽  
Visual System ◽  
Visual Processing ◽  
Time Course ◽  
Temporal Frequency ◽  
Power Spectra ◽  
Calliphora Vicina ◽  
Intensity Measurements ◽  
Natural Time ◽  
Early Visual System

The first steps of processing in the visual system of the blowfly are well suited for studying the relationship between the properties of the environment and the function of visual processing (eg Srinivasan et al, 1982 Proceedings of the Royal Society, London B216 427; van Hateren, 1992 Journal of Comparative Physiology A171 157). Although the early visual system appears to be linear to some extent, there are also reports on functionally significant nonlinearities (Laughlin, 1981 Zeitschrift für Naturforschung36c 910). Recent theories using information theory for understanding the early visual system perform reasonably well, but not quite as well as the real visual system when confronted with natural stimuli [eg van Hateren, 1992 Nature (London)360 68]. The main problem seems to be that they lack a component that adapts with the right time course to changes in stimulus statistics (eg the local average light intensity). In order to study this problem of adaptation with a relatively simple, yet realistic, stimulus I recorded time series of natural intensities, and played them back via a high-brightness LED to the visual system of the blowfly ( Calliphora vicina). The power spectra of the intensity measurements and photoreceptor responses behave approximately as 1/ f, with f the temporal frequency, whilst those of second-order neurons (LMCs) are almost flat. The probability distributions of the responses of LMCs are almost gaussian and largely independent of the input contrast, unlike the distributions of photoreceptor responses and intensity measurements. These results suggest that LMCs are in effect executing a form of contrast normalisation in the time domain.

scholarly journals Vision-based flight control in the hawkmoth Hyles lineata

2014 ◽  
Vol 11 (91) ◽  
pp. 20130921 ◽  
Author(s):  
Shane P. Windsor ◽  
Richard J. Bomphrey ◽  
Graham K. Taylor
Keyword(s):  
Flight Control ◽  
Insect Flight ◽  
Linear Time ◽  
Temporal Frequency ◽  
Sensory Modality ◽  
Flight Dynamics ◽  
Energetic Cost ◽  
Linear Time Invariant ◽  
Hyles Lineata ◽  
And Control

Vision is a key sensory modality for flying insects, playing an important role in guidance, navigation and control. Here, we use a virtual-reality flight simulator to measure the optomotor responses of the hawkmoth Hyles lineata , and use a published linear-time invariant model of the flight dynamics to interpret the function of the measured responses in flight stabilization and control. We recorded the forces and moments produced during oscillation of the visual field in roll, pitch and yaw, varying the temporal frequency, amplitude or spatial frequency of the stimulus. The moths’ responses were strongly dependent upon contrast frequency, as expected if the optomotor system uses correlation-type motion detectors to sense self-motion. The flight dynamics model predicts that roll angle feedback is needed to stabilize the lateral dynamics, and that a combination of pitch angle and pitch rate feedback is most effective in stabilizing the longitudinal dynamics. The moths’ responses to roll and pitch stimuli coincided qualitatively with these functional predictions. The moths produced coupled roll and yaw moments in response to yaw stimuli, which could help to reduce the energetic cost of correcting heading. Our results emphasize the close relationship between physics and physiology in the stabilization of insect flight.

Auditorily Paced Keytapping Performance during Synchronous, Decreased, and Delayed Visual Feedback

1968 ◽  
Vol 26 (3) ◽  
pp. 731-743 ◽  
Author(s):  
Raymond S. Karlovich ◽  
James T. Graham
Keyword(s):  
Visual Feedback ◽  
Motor Performance ◽  
Sensory Feedback ◽  
Sensory Modality ◽  
Sensation Level ◽  
Feedback Stimulus ◽  
Dependent Variables ◽  
Kinesthetic Feedback ◽  
Temporal Deviation ◽  
Delayed Visual Feedback

20 young adult female Ss tapped on a tapping key to low, mid, and high sensation-level pure-tone auditory-pacing stimuli while being exposed to synchronous visual-feedback, delayed visual-feedback, and decreased sensory-feedback conditions. The stroboscopic visual-feedback stimulus was judged to be as bright as the mid-sensation-level auditory stimulus was loud in a preliminary cross-modality matching study. The dependent variables evaluated were tapping error, temporal deviation of the taps from the onset of the pacing stimuli, and tap duration. Few tapping errors occurred under any of the conditions which indicated that the auditory sensory modality is effective in regulating motor performance even when temporally distorted visual feedback is associated with the performance. Tapping deviation data strongly suggested that the relative perceptual magnitudes between the auditory pacing stimuli and the delayed visual-feedback stimulus are important factors in determining the speed of motor response. Tap durations were greater during decreased sensory-feedback and delayed visual-feedback conditions than during synchronous visual-feedback conditions, and it was speculated that these changes occurred due to an increase in tactual and kinesthetic feedback employed by Ss to counterbalance the distorted and decreased sensory feedbacks.

The Effects of Visual and Proprioceptive Feedback on Motor Learning

1975 ◽  
Vol 19 (2) ◽  
pp. 162-165 ◽  
Author(s):  
Jack A. Adams ◽  
Daniel Gopher ◽  
Gavan Lintern
Keyword(s):  
Motor Learning ◽  
Visual Feedback ◽  
Sensory Feedback ◽  
Closed Loop ◽  
Motor Program ◽  
Absolute Error ◽  
Proprioceptive Feedback ◽  
Knowledge Of Results ◽  
And Performance ◽  
Effective Source

A self paced linear positioning task was used to study the effects of visual and proprioceptive feedback on learning and performance. Subjects were trained with knowledge of results (KR) and tested without it. The analysis of the absolute error scores of the no-KR trials is discussed in this paper. Visual feedback was the more effective source of sensory feedback, but proprioceptive feedback was also effective. An observation that the response did not become independent of sensory feedback as a result of learning, was interpreted as supporting Adams closed loop theory of motor learning in preference to the motor program hypothesis. Other data showed that the presence of visual feedback during learning could inhibit the later effectiveness of proprioceptive feedback.

scholarly journals Maximally efficient prediction in the early fly visual system may support evasive flight maneuvers

2021 ◽  
Vol 17 (5) ◽  
pp. e1008965
Author(s):  
Siwei Wang ◽  
Idan Segev ◽  
Alexander Borst ◽  
Stephanie Palmer
Keyword(s):  
Visual System ◽  
Flight Control ◽  
Vertical Motion ◽  
Compartmental Modeling ◽  
Optimal Prediction ◽  
Motor Center ◽  
Motor Pathway ◽  
Efficient Prediction ◽  
Sensory Prediction ◽  
Fine Tune

The visual system must make predictions to compensate for inherent delays in its processing. Yet little is known, mechanistically, about how prediction aids natural behaviors. Here, we show that despite a 20-30ms intrinsic processing delay, the vertical motion sensitive (VS) network of the blowfly achieves maximally efficient prediction. This prediction enables the fly to fine-tune its complex, yet brief, evasive flight maneuvers according to its initial ego-rotation at the time of detection of the visual threat. Combining a rich database of behavioral recordings with detailed compartmental modeling of the VS network, we further show that the VS network has axonal gap junctions that are critical for optimal prediction. During evasive maneuvers, a VS subpopulation that directly innervates the neck motor center can convey predictive information about the fly’s future ego-rotation, potentially crucial for ongoing flight control. These results suggest a novel sensory-motor pathway that links sensory prediction to behavior.

scholarly journals Gaze stabilisation behaviour is anisotropic across visual field locations in zebrafish

2019 ◽  
Author(s):  
Florian A. Dehmelt ◽  
Rebecca Meier ◽  
Julian Hinz ◽  
Takeshi Yoshimatsu ◽  
Clara A. Simacek ◽  
...  
Keyword(s):  
Visual Field ◽  
Visual System ◽  
Temporal Frequency ◽  
Visual Fields ◽  
Visual Space ◽  
Relevant Information ◽  
Stimulus Size ◽  
Motion Vision ◽  
Optokinetic Response ◽  
Retinal Photoreceptor

AbstractMany animals have large visual fields, and sensory circuits may sample those regions of visual space most relevant to behaviours such as gaze stabilisation and hunting. Despite this, relatively small displays are often used in vision neuroscience. To sample stimulus locations across most of the visual field, we built a spherical stimulus arena with 14,848 independently controllable LEDs, measured the optokinetic response gain of immobilised zebrafish larvae, and related behaviour to previously published retinal photoreceptor densities. We measured tuning to steradian stimulus size and spatial frequency, and show it to be independent of visual field position. However, zebrafish react most strongly and consistently to lateral, nearly equatorial stimuli, consistent with previously reported higher spatial densities in the central retina of red, green and blue photoreceptors. Upside-down experiments suggest further extra-retinal processing. Our results demonstrate that motion vision circuits in zebrafish are anisotropic, and preferentially monitor areas with putative behavioural relevance.Author summaryThe visual system of larval zebrafish mirrors many features present in the visual system of other vertebrates, including its ability to mediate optomotor and optokinetic behaviour. Although the presence of such behaviours and some of the underlying neural correlates have been firmly established, previous experiments did not consider the large visual field of zebrafish, which covers more than 160° for each eye. Given that different parts of the visual field likely carry unequal amount of behaviourally relevant information for the animal, this raises the question whether optic flow is integrated across the entire visual field or just parts of it, and how this shapes behaviour such as the optokinetic response. We constructed a spherical LED arena to present visual stimuli almost anywhere across their visual field, while tracking horizontal eye movements. By displaying moving gratings on this LED arena, we demonstrate that the optokinetic response, one of the most prominent visually induced behaviours of zebrafish, indeed strongly depends on stimulus location and stimulus size, as well as on other parameters such as the spatial and temporal frequency of the gratings. This location dependence is consistent with areas of high retinal photoreceptor densities, though evidence suggests further extraretinal processing.

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