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

2019 ◽  
Author(s):  
Siwei Wang ◽  
Idan Segev ◽  
Alexander Borst ◽  
Stephanie Palmer

AbstractThe 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.Author summarySurvival-critical behaviors shape neural circuits to translate sensory information into strikingly fast predictions, e.g. in escaping from a predator faster than the system’s processing delay. We show that the fly visual system implements fast and accurate prediction of its visual experience. This provides crucial information for directing fast evasive maneuvers that unfold over just 40ms. Our work shows how this fast prediction is implemented, mechanistically, and suggests the existence of a novel sensory-motor pathway from the fly visual system to a wing steering motor neuron. Echoing and amplifying previous work in the retina, our work hypothesizes that the efficient encoding of predictive information is a universal design principle supporting fast, natural behaviors.

2021 ◽  
Vol 17 (5) ◽  
pp. e1008965
Author(s):  
Siwei Wang ◽  
Idan Segev ◽  
Alexander Borst ◽  
Stephanie Palmer

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.


1976 ◽  
Vol 9 (3) ◽  
pp. 311-375 ◽  
Author(s):  
Werner Reichardt ◽  
Tomaso Poggio

An understanding of sensory information processing in the nervous system will probably require investigations with a variety of ‘model’ systems at different levels of complexity.Our choice of a suitable model system was constrained by two conflicting requirements: on one hand the information processing properties of the system should be rather complex, on the other hand the system should be amenable to a quantitative analysis. In this sense the fly represents a compromise.In these two papers we explore how optical information is processed by the fly's visual system. Our objective is to unravel the logical organization of the fly's visual system and its underlying functional and computational principles. Our approach is at a highly integrative level. There are different levels of analysing and ‘understanding’ complex systems, like a brain or a sophisticated computer.


2021 ◽  
Vol 11 (11) ◽  
pp. 1506
Author(s):  
Annalisa Tosoni ◽  
Emanuele Cosimo Altomare ◽  
Marcella Brunetti ◽  
Pierpaolo Croce ◽  
Filippo Zappasodi ◽  
...  

One fundamental principle of the brain functional organization is the elaboration of sensory information for the specification of action plans that are most appropriate for interaction with the environment. Using an incidental go/no-go priming paradigm, we have previously shown a facilitation effect for the execution of a walking-related action in response to far vs. near objects/locations in the extrapersonal space, and this effect has been called “macro-affordance” to reflect the role of locomotion in the coverage of extrapersonal distance. Here, we investigated the neurophysiological underpinnings of such an effect by recording scalp electroencephalography (EEG) from 30 human participants during the same paradigm. The results of a whole-brain analysis indicated a significant modulation of the event-related potentials (ERPs) both during prime and target stimulus presentation. Specifically, consistent with a mechanism of action anticipation and automatic activation of affordances, a stronger ERP was observed in response to prime images framing the environment from a far vs. near distance, and this modulation was localized in dorso-medial motor regions. In addition, an inversion of polarity for far vs. near conditions was observed during the subsequent target period in dorso-medial parietal regions associated with spatially directed foot-related actions. These findings were interpreted within the framework of embodied models of brain functioning as arising from a mechanism of motor-anticipation and subsequent prediction error which was guided by the preferential affordance relationship between the distant large-scale environment and locomotion. More in general, our findings reveal a sensory-motor mechanism for the processing of walking-related environmental affordances.


Author(s):  
Paolo Solari ◽  
Giorgia Sollai ◽  
Francesco Palmas ◽  
Andrea Sabatini ◽  
Roberto Crnjar

The integration of sensory information with adequate motor outputs is critical for animal survival. Here, we present an innovative technique based on a non-invasive closed-circuit device consisting of a perfusion/stimulation chamber chronically applied on a single leg of the crayfish Procambarus clarkii. Using this technique, we focally stimulated the leg inside the chamber and studied the leg-dependent sensory-motor integration involving other sensory appendages, such as antennules and maxillipeds, which remain unstimulated outside the chamber. Results show that the stimulation of a single leg with chemicals, such as disaccharides, is sufficient to trigger a complex search behaviour involving locomotion coupled with the reflex activation of antennules and maxillipeds. This technique can be easily adapted to other decapods and/or other sensory appendages. Thus, it has opened possibilities for studying sensory-motor integration evoked by leg stimulation in whole aquatic animals under natural conditions to supplement, with a direct approach, current ablation/silencing techniques.


2004 ◽  
Vol 91 (1) ◽  
pp. 1-12 ◽  
Author(s):  
Thomas Matheson ◽  
Stephen M. Rogers ◽  
Holger G. Krapp

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.


2012 ◽  
Vol 5 (1) ◽  
pp. 1-10
Author(s):  
Mateusz Woźniak

Brain system responsible for visual perception has been extensively studied. Visual system analyses a wide variety of stimuli in order to let us create adaptive representation of surrounding world. But among vast amounts of processed information come visual cues describing our own bodies. These cues constitute our so-called body-image. We tend to perceive it as a relatively stable structure but recent research, especially within the domain of virtual reality, introduces doubts to this assumption. New problems appear concerning perceiving others’ and our own bodies in virtual space and how does it influence our experience of ourselves and true reality. Recent studies show that how we see our avatars influence how we behave in artificial worlds. It introduces a brand new way of thinking about human embodiment. Virtual reality allows us to transcend beyond the casual visual-sensory-motor integration and create new ways to experience embodiment, temporarily replacing permanent body image with almost any imaginable digital one. Santrauka Smegenų sistema, atsakinga už vizualųjį suvokimą, yra nuodugniai ištirta. Vizualioji sistema analizuoja plačią akstinų įvairovę, padedančią mums sukurti adaptuotą supančio pasaulio reprezentaciją. Tačiau tarp didelio kiekio apdorotos informacijos kyla vizualiosios užuominos, atvaizduojančios mūsų pačių kūnus. Šios užuominos steigia vadinamąjį kūną-atvaizdą. Mes linkstame jį suvokti kaip sąlygiškai stabilią struktūrą, tačiau dabartiniai tyrimai, o ypač tie, kurie vykdomi virtualiojoje realybėje, tokia prielaida verčia suabejoti. Kyla naujų problemų, suvokiant kitų ir mūsų pačių kūnus virtualiojoje erdvėje bei kokios įtakos tai turi mūsų pačių savęs ir tikrosios realybės patyrimui. Nūdieniai tyrinėjimai atskleidžia, kad tai, kaip mes suvokiame savąjį kūniškumą, turi įtakos tam, kaip elgiamės dirbtiniuose pasauliuose. Tai steigia visiškai naują žmogiškojo kūniškumo suvokimo būdą. Virtualioji realybė leidžia mums peržengti paprastą vizualinęjutiminę-motorinę integraciją ir kurti naujus būdus patirti kūniškumą, palaipsniui pakeičiant ilgalaikį kūno atvaizdą bet kokiu įsivaizduojamu skaitmeniniu.


2010 ◽  
Vol 8 (55) ◽  
pp. 171-185 ◽  
Author(s):  
Nicola Rohrseitz ◽  
Steven N. Fry

Behavioural control in many animals involves complex mechanisms with intricate sensory-motor feedback loops. Modelling allows functional aspects to be captured without relying on a description of the underlying complex, and often unknown, mechanisms. A wide range of engineering techniques are available for modelling, but their ability to describe time-continuous processes is rarely exploited to describe sensory-motor control mechanisms in biological systems. We performed a system identification of visual flight speed control in the fruitfly Drosophila , based on an extensive dataset of open-loop responses previously measured under free flight conditions. We identified a second-order under-damped control model with just six free parameters that well describes both the transient and steady-state characteristics of the open-loop data. We then used the identified control model to predict flight speed responses after a visual perturbation under closed-loop conditions and validated the model with behavioural measurements performed in free-flying flies under the same closed-loop conditions. Our system identification of the fruitfly's flight speed response uncovers the high-level control strategy of a fundamental flight control reflex without depending on assumptions about the underlying physiological mechanisms. The results are relevant for future investigations of the underlying neuromotor processing mechanisms, as well as for the design of biomimetic robots, such as micro-air vehicles.


2015 ◽  
Vol 93 (12) ◽  
pp. 961-975 ◽  
Author(s):  
Douglas L. Altshuler ◽  
Joseph W. Bahlman ◽  
Roslyn Dakin ◽  
Andrea H. Gaede ◽  
Benjamin Goller ◽  
...  

Bird flight is a remarkable adaptation that has allowed the approximately 10 000 extant species to colonize all terrestrial habitats on earth including high elevations, polar regions, distant islands, arid deserts, and many others. Birds exhibit numerous physiological and biomechanical adaptations for flight. Although bird flight is often studied at the level of aerodynamics, morphology, wingbeat kinematics, muscle activity, or sensory guidance independently, in reality these systems are naturally integrated. There has been an abundance of new studies in these mechanistic aspects of avian biology but comparatively less recent work on the physiological ecology of avian flight. Here we review research at the interface of the systems used in flight control and discuss several common themes. Modulation of aerodynamic forces to respond to different challenges is driven by three primary mechanisms: wing velocity about the shoulder, shape within the wing, and angle of attack. For birds that flap, the distinction between velocity and shape modulation synthesizes diverse studies in morphology, wing motion, and motor control. Recently developed tools for studying bird flight are influencing multiple areas of investigation, and in particular the role of sensory systems in flight control. How sensory information is transformed into motor commands in the avian brain remains, however, a largely unexplored frontier.


2018 ◽  
Author(s):  
Daniel Knebel ◽  
Johanna Wörner ◽  
Jan Rillich ◽  
Leonard Nadler ◽  
Amir Ayali ◽  
...  

AbstractThe neural control of insect locomotion is distributed among various body segments. Local pattern-generating circuits at the thoracic ganglia interact with incoming sensory signals and central descending commands from the head ganglia. The evidence from different insect preparations suggests that the subesophageal ganglion (SEG) may play an important role in locomotion-related tasks. In a previous study, we demonstrated that the locust SEG modulates the coupling pattern between segmental leg CPGs in the absence of sensory feedback. Here, we investigated its role in processing and transmitting sensory information to the leg motor centers, and mapped the major related neural pathways. Specifically, the intra- and inter-segmental transfer of leg-feedback were studied by simultaneously monitoring motor responses and descending signals from the SEG. Our findings reveal a crucial role of the SEG in the transfer of intersegmental, but not intrasegmental, signals. Additional lesion experiments, in which the intersegmental connectives were cut at different locations, together with double nerve staining, indicated that sensory signals are mainly transferred to the SEG via the connective contralateral to the stimulated leg. We therefore suggest that, similar to data reported for vertebrates, insect leg sensory-motor loops comprise contralateral ascending pathways to the head and ipsilateral descending ones.


2018 ◽  
Author(s):  
Miaomiao Jin ◽  
Jeffrey M. Beck ◽  
Lindsey L. Glickfeld

AbstractSensory information is encoded by populations of cortical neurons. Yet, it is unknown how this information is used for even simple perceptual choices such as discriminating orientation. To determine the computation underlying this perceptual choice, we took advantage of the robust adaptation in the mouse visual system. We find that adaptation increases animals’ thresholds for orientation discrimination. This was unexpected since optimal computations that take advantage of all available sensory information predict that the shift in tuning and increase in signal-to-noise ratio in the adapted condition should improve discrimination. Instead, we find that the effects of adaptation on behavior can be explained by the appropriate reliance of the perceptual choice circuits on target preferring neurons, but the failure to discount neurons that prefer the distractor. This suggests that to solve this task the circuit has adopted a suboptimal strategy that discards important task-related information to implement a feed-forward visual computation.


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