Biology subjects

Krapp, H. G.

Publications and source records attributed to Krapp, H. G..

11 recordsLinked to original sources

bioRxiv2026

The Effective Visual Acuity of Butterflies in Flight

The spatial visual acuity of an eye is determined by both the spatial sampling density of the retina and the angular sensitivity of individual photoreceptors. In insect compound eyes, these are respectively characterised by the interommatidial angle, {Delta}{varphi}, and photoreceptor acceptance angle, {Delta}{rho}. During movement, however, finite photoreceptor integration times cause retinal image motion to broaden the effective acceptance angle, potentially degrading spatial resolution beyond its anatomical limit. This problem is especially acute in flying insects, which experience large rotational velocities during locomotion and must actively stabilise gaze to limit retinal image motion. Butterflies present a particularly demanding case because their flight is characterised by large, wingbeat-coupled thoracic oscillations. Here, we quantify how gaze stabilisation limits motion blur in freely flying Monarch butterflies Danaus plexippus by combining free-flight kinematic reconstruction of the head and thorax with separate intracellular measurements of photoreceptor acceptance angles and integration times from quiescent butterflies. We found that, without head compensation, thoracic oscillations would broaden the effective photoreceptor acceptance angle from its quiescent value of 2.17{degrees} to 9.38{degrees} during take-off. Compensatory head movements substantially reduced this motion-induced broadening, limiting the effective acceptance angle to 5.28{degrees}. Nevertheless, this 2.4-fold broadening of effective photoreceptor acceptance angle represents a substantial degradation of spatial acuity in flight, highlighting motion blur as an important constraint on the visual ecology of flying butterflies.

neuroscience↗

bioRxiv2026

State dependant modulation of optic flow-processing lobula plate cells in butterflies

Increasing experimental evidence suggests that biological systems cancel predictable components of sensory signals while maintaining sensitivity to externally induced state changes. This strategy provides task-specific sensor responses for posture, locomotion, and gaze control. A prime example is found in interneurons that respond to visual image shifts resulting from the relative motion between an animal's eyes and its visual surroundings. Such optic flow-processing interneurons, found across phyla and are particularly well characterized in Dipteran and other flying insects. We studied optic flow-processing interneurons in the Monarch butterfly whose large and highly contrasted wings sweep through the visual field with every wing-beat cycle, potentially obscuring interneuron output signals. Our results show baseline spiking activity increases when animals flap their wings, and individual spikes are phase-locked to the wing-beat cycle, even in the dark, when no visual motion input is available. A qualitative estimate of the interneurons' response to directional wing motion through its receptive field is not sufficient to explain the recorded activity patterns. Our results suggest that an additional internal signal suppresses responses to wing-induced visual motion to support effective vision-based stabilization reflexes. These findings support the principle that self-generated signals are suppressed while sensitivity to external modulation is preserved.

neuroscience↗

bioRxiv2026

Wing mechanosensory modulation of optic flow-sensitive descending neurons in butterflies

Visual motion processing in flying insects is strongly modulated by behavioural state, yet the mechanisms by which mechanosensory feedback contributes to this modulation remain poorly understood. Here we show that wing mechanosensation alone is sufficient to modulate a subset of optic flow-sensitive descending neurons (WFDNs) in butterflies. Airflow stimulation of the wings, mimicking flight conditions, increased baseline firing rates and reduced response latencies in WFDNs, without altering response gain or temporal frequency tuning. These effects indicate that mechanosensory modulation acts through mechanisms distinct from those governing other state-dependent changes in visual processing. Consistent with this interpretation, previous work has shown that baseline firing and response latency can be rapidly modulated, whereas gain changes arise through slower neuromodulatory pathways. Mechanosensory modulation was cell-type specific: the horizontally tuned WFDNL neuron was consistently affected across individuals, whereas other WFDN types were largely insensitive, likely reflecting the unilateral airflow stimuli used here. Interestingly, WFDNL modulation arose exclusively from mechanosensory input from the proximal area of the wing, not from distal wing deformation. This suggests that descending visual pathways require only coarse gain or excitability modulation rather than detailed information about wing shape or strain, leaving fast reflexive control of distal wing deformation to local ganglionic circuits. Together, our results demonstrate that wing mechanosensation selectively modulates visual descending pathways by altering excitability and timing rather than visual feature encoding, supporting the existence of multiple, parallel mechanisms for state-dependent visual modulation during flight.

neuroscience↗

bioRxiv2025

Spectral Matched Filtering in the Butterfly Visuomotor System

Color provides an important dimension for object detection and classification. In most animals, color- and motion-vision are largely separated throughout early stages of visual processing. However, accumulating evidence indicates crosstalk between chromatic and achromatic pathways. Here we investigate the spectral sensitivity of the butterfly motion-vision pathway at the level of pre-motor descending neurons (DNs), which connect the brain to thoracic motor centres. Butterflies engage in fast agile flight within often-colorful visual ecologies, which may heighten evolutionary pressure to integrate color- and motion-vision. Indeed, we observed a separation of spectral sensitivities that matches the functional properties of butterfly DNs, such that wide-field optic flow-sensitive DNs involved in stabilisation reflexes have effectively broadband spectral responses, whilst target-selective DNs involved in target-tracking are comparatively narrowband and match conspecific wing coloration. Our findings demonstrate an integration of color- and motion-vision within a pre-motor neuronal bottleneck that controls behavior.

neuroscience↗

bioRxiv2025

Adaptive feedforward speed control in Drosophila

Insects demonstrate remarkable agility in flight despite constant changes in flight dynamics throughout their lives. However, it is unclear whether such resilience is conferred via purely feedback control or whether adaptive feedforward control mechanisms are present. This study examines whether adaptive feedforward control mechanisms are present in Drosophila melanogaster flight, by comparing the free-flight trajectories with and without wing damage and antennae ablation. Flies with partial wing excisions exhibited increased flight speeds in the dark compared to intact-wing controls. Upon exposure to visual contrast in light, the clipped-wing flies reduced their speed comparable to that of the control group flies. Notably, the lower speed persisted upon returning to the dark, indicating an enduring change to the flight controller. To discern between feedforward adaptation and a change in mechanosensory feedback gains, we replicated the experiment after ablating the antennal arista, the primary mechanosensors for sensing airspeed. Although flies with ablated antennae flew with greater variance in speed, they displayed a parallel trend in mean speed adaptation: increased speed in the dark, compensation in the light, and sustained lower speed in subsequent dark conditions. This consistent pattern strongly supports the involvement of adaptive feedforward control rather than the adjustment of mechanosensory feedback gains. Our investigation unveils an adaptive strategy in D. Melanogaster flight, illustrating its ability to set flight speed through adaptive feedforward control mechanisms.

bioengineering↗

bioRxiv2024

Motion vision is tuned to maximize sensorimotor energy transfer in blowfly flight

Insects achieve agile flight using a sensor-rich control architecture whose embodiment eliminates the need for complex computation. For example, their visual systems are tuned to detect the optic flow associated with specific self-motions, but what functional principle does this tuning embed and how does it facilitate motor control? Here we test the hypothesis that evolution co-tunes physics and physiology by aligning an insects sensors to its dynamically-significant modes of self-motion. Specifically, we show that the tuning of the blowfly motion vision system maximizes the flow of signal energy from gust disturbances and control inputs to sensor outputs, jointly optimizing observability and controllability. This evolutionary principle differs from the conventional engineering-design paradigm of optimizing state estimation, with implications for novel robotic systems combining high performance with low power-consumption.

neuroscience↗

bioRxiv2023

A control engineering perspective on the advantages of efference copies

Biological systems have evolved to perform high-speed voluntary movements whilst maintaining robustness and stability. This paper examines a control architecture based on the principles of efference copies found in insect sensorimotor control which we call the fully-separable-degrees-of-freedom (FSDoF) controller. Within a control engineering framework, we benchmark the advantages of this control architecture against two common engineering control schemes: a pure feedback (PFB) controller and a Smith predictor (SP). Our study identifies three advantages of the FSDoF for biology. It is advantageous in controlling systems with sensor delays, and it can effectively handle noise. Thirdly, it allows biological sensors to increase their operating range. We evaluate the robustness of the FSDoF controller and show that it achieves improved performance with equal stability margins and robustness. Finally, we discuss variations of the FSDoF which theoretically provide the same performance.

bioengineering↗

bioRxiv2022

Generating spatiotemporal patterns of linearly polarised light at high frame rates for insect vision research

Polarisation vision is commonplace among invertebrates; however, most experiments focus on determining behavioural and/or neurophysiological responses to static polarised light sources rather than moving patterns of polarised light. To this end, we designed a polarisation stimulation device based on superimposing polarised and non-polarised images from two projectors, which can display moving patterns at frame rates exceeding invertebrate flicker fusion frequencies. A linear polariser fitted to one projector enables moving patterns of polarised light to be displayed, whilst the other projector contributes arbitrary intensities of non-polarised light to yield moving patterns with a defined polarisation and intensity contrast. To test the device, we measured receptive fields of polarisation sensitive Argynnis paphia butterfly photoreceptors for both non-polarised and polarised light. We then measured local motion sensitivities of the optic flow-sensitive lobula plate tangential cell H1 in Calliphora vicina blowflies under both polarised and non-polarised light, finding no polarisation sensitivity in this neuron.

neuroscience↗

bioRxiv2021

Passive inertial damping improves high-speed gaze stabilization in hoverflies

Gaze stabilization reflexes reduce motion blur and simplify the processing of visual information by keeping the eyes level. These reflexes typically depend on estimates of the rotational motion of the body, head, and eyes, acquired by visual or mechanosensory systems. During rapid movements, there can be insufficient time for sensory feedback systems to estimate rotational motion, requiring additional mechanisms. Solutions to this common problem are likely to be adapted to an animals behavioral repertoire. Here, we examine gaze stabilization in three families of dipteran flies, each with distinctly different flight behaviors. Through frequency response analysis based on tethered-flight experiments, we demonstrate that fast roll oscillations of the body lead to a stable gaze in hoverflies, whereas the reflex breaks down at the same speeds in blowflies and horseflies. Surprisingly, the high-speed gaze stabilization of hoverflies does not require sensory input from the halteres, their low-latency balance organs. Instead, we show how the behavior is explained by a hybrid control system that combines a sensory-driven, active stabilization component mediated by neck muscles, and a passive component which exploits physical properties of the animals anatomy--the mass and inertia of its head. This adaptation requires hoverflies to have specializations of the head-neck joint that can be employed during flight. Our comparative study highlights how species-specific control strategies have evolved to support different visually-guided flight behaviors. SIGNIFICANCE STATEMENTAcross the animal kingdom, reflexes are found which stabilize the eyes to reduce the impact of motion blur on vision--analogous to the image stabilization functions found in modern cameras. These reflexes can be complex, often combining predictions about planned movements with information from multiple sensory systems which continually measure self-motion and provide feedback. The processing of this information in the nervous system incurs time delays which impose limits on performance when fast stabilization is required. Hoverflies overcome the limitations of sensory-driven stabilization reflexes by exploiting the passive stability provided by the head during roll perturbations with particularly high rotational kine-matics. Integrating passive and active mechanisms thus extends the useful range of vision and likely facilitates distinctive aspects of hoverfly flight.

neuroscience↗

bioRxiv2021

Impact of walking speed and motion adaptation on optokinetic nystagmus-like head movements in the blowfly Calliphora

The optokinetic nystagmus is a gaze-stabilizing mechanism reducing motion blur by rapid eye rotations against the direction of visual motion, followed by slower syndirectional eye movements minimizing retinal slip speed. Flies control their gaze through head turns controlled by neck motor neurons receiving input directly, or via descending neurons, from well-characterized directional-selective interneurons sensitive to visual wide-field motion. Locomotion increases the gain and speed sensitivity of these interneurons, while visual motion adaptation in walking animals has the opposite effects. To find out whether flies perform an optokinetic nystagmus, and how it may be affected by locomotion and visual motion adaptation, we recorded head movements of blowflies on a trackball stimulated by progressive and rotational visual motion. Flies flexibly responded to rotational stimuli with optokinetic nystagmus-like head movements, independent of their locomotor state. The temporal frequency tuning of these movements, though matching that of the upstream directional-selective interneurons, was only mildly modulated by walking speed or visual motion adaptation. Our results suggest flies flexibly control their gaze to compensate for rotational wide-field motion by a mechanism similar to an optokinetic nystagmus. Surprisingly, the mechanism is less state-dependent than the response properties of directional-selective interneurons providing input to the neck motor system.

animal behavior and cognition↗

bioRxiv2016

Spike interval coding of translatory optic flow and depth from motion in the fly visual system

Many animals use the visual motion generated by travelling in a line, the translatory optic flow, to successfully navigate obstacles: near objects appear larger and to move more quickly than distant ones. Flies are experts at navigating cluttered environments, and while their visual processing of rotatory optic flow is understood in exquisite detail, how they process translatory optic flow remains a mystery. Here, we present novel cell types that have motion receptive fields matched to translation self-motion, the vertical translation (VT) cells. One of these, the VT1 cell, encodes forwards sideslip self-motion, and fires action potentials in clusters of spikes, spike bursts. We show that the spike burst coding is size and speed-tuned, and is selectively modulated by parallax motion, the relative motion experienced during translation. These properties are spatially organized, so that the cell is most excited by clutter rather than isolated objects. When the fly is presented with a simulation of flying past an elevated object, the spike burst activity is modulated by the height of the object, and the single spike rate is unaffected. When the moving object alone is experienced, the cell is weakly driven. Meanwhile, the VT2-3 cells have motion receptive fields matched to the lift axis. In conjunction with previously described horizontal cells, the VT cells have the properties required for the fly to successfully navigate clutter and encode its movements along near cardinal axes of thrust, lift and forward sideslip.

neuroscience↗