Differential adaptation to visual motion allows robust encoding of optic flow in the dragonfly

An important task for any aerial creature is the ability to ascertain their own movement (ego-motion) through their environment. Neurons thought to underlie this behaviour have been well-characterised in many insect models including flies, moths and bees. However, dragonfly wide-field motion pathways remain undescribed. Some species of Dragonflies, such as Hemicordulia tau, engage in hawking behaviour, hovering in a single area for extended periods of time whilst also engaging in fast-moving patrols and highly dynamic pursuits of prey and conspecifics. These varied flight behaviours place very different constraints on establishing ego-motion from optic flow cues hinting at a sophisticated wide-field motion analysis system capable of detecting both fast and slow motion. We characterised wide-field motion sensitive neurons via intracellular recordings in Hemicordulia dragonflies finding similar properties to those found in other species. We found that the spatial and temporal tuning properties of these neurons were broadly similar but differed significantly in their adaptation to sustained motion. We categorised a total of three different subclasses, finding differences between subclasses in their motion adaptation and response to the broadband statistics of natural images. The differences found correspond well with the dynamics of the varied behavioural tasks hawking dragonflies perform. These findings may underpin the exquisite flight behaviours found in dragonflies. They also hint at the need for the great complexity seen in dragonfly early visual processing.

Download Full-text

Disentangling of Local and Wide-Field Motion Adaptation

Frontiers in Neural Circuits ◽

10.3389/fncir.2021.713285 ◽

2021 ◽

Vol 15 ◽

Author(s):

Jinglin Li ◽

Miriam Niemeier ◽

Roland Kern ◽

Martin Egelhaaf

Keyword(s):

Optic Flow ◽

Visual Processing ◽

Visual Motion ◽

Spatial Scales ◽

Stimulus Level ◽

The Other ◽

Wide Field ◽

Local Motion ◽

Motion Direction ◽

Motion Adaptation

Motion adaptation has been attributed in flying insects a pivotal functional role in spatial vision based on optic flow. Ongoing motion enhances in the visual pathway the representation of spatial discontinuities, which manifest themselves as velocity discontinuities in the retinal optic flow pattern during translational locomotion. There is evidence for different spatial scales of motion adaptation at the different visual processing stages. Motion adaptation is supposed to take place, on the one hand, on a retinotopic basis at the level of local motion detecting neurons and, on the other hand, at the level of wide-field neurons pooling the output of many of these local motion detectors. So far, local and wide-field adaptation could not be analyzed separately, since conventional motion stimuli jointly affect both adaptive processes. Therefore, we designed a novel stimulus paradigm based on two types of motion stimuli that had the same overall strength but differed in that one led to local motion adaptation while the other did not. We recorded intracellularly the activity of a particular wide-field motion-sensitive neuron, the horizontal system equatorial cell (HSE) in blowflies. The experimental data were interpreted based on a computational model of the visual motion pathway, which included the spatially pooling HSE-cell. By comparing the difference between the recorded and modeled HSE-cell responses induced by the two types of motion adaptation, the major characteristics of local and wide-field adaptation could be pinpointed. Wide-field adaptation could be shown to strongly depend on the activation level of the cell and, thus, on the direction of motion. In contrast, the response gain is reduced by local motion adaptation to a similar extent independent of the direction of motion. This direction-independent adaptation differs fundamentally from the well-known adaptive adjustment of response gain according to the prevailing overall stimulus level that is considered essential for an efficient signal representation by neurons with a limited operating range. Direction-independent adaptation is discussed to result from the joint activity of local motion-sensitive neurons of different preferred directions and to lead to a representation of the local motion direction that is independent of the overall direction of global motion.

Download Full-text

Directional selectivity and its use in early visual processing

Proceedings of the Royal Society of London Series B Biological Sciences ◽

10.1098/rspb.1981.0001 ◽

1981 ◽

Vol 211 (1183) ◽

pp. 151-180 ◽

Cited By ~ 348

Keyword(s):

Visual Processing ◽

Visual Motion ◽

Time Derivative ◽

Receptive Fields ◽

Specific Model ◽

Zero Crossings ◽

Second Stage ◽

Early Visual Processing ◽

Local Direction ◽

Zero Values

The construction of directionally selective units, and their use in the processing of visual motion, are considered. The zero crossings of ∇ 2 G(x, y) ∗ I(x, y) are located, as in Marr & Hildreth (1980). That is, the image is filtered through centre-surround receptive fields, and the zero values in the output are found. In addition, the time derivative ∂[∇ 2 G(x, y) ∗ l(x, y) ]/∂ t is measured at the zero crossings, and serves to constrain the local direction of motion to within 180°. The direction of motion can be determined in a second stage, for example by combining the local constraints. The second part of the paper suggests a specific model of the information processing by the X and Y cells of the retina and lateral geniculate nucleus, and certain classes of cortical simple cells. A number of psychophysical and neurophysiological predictions are derived from the theory.

Download Full-text

Wide-Field Feedback Neurons Dynamically Tune Early Visual Processing

Neuron ◽

10.1016/j.neuron.2014.04.023 ◽

2014 ◽

Vol 82 (4) ◽

pp. 887-895 ◽

Cited By ~ 35

Author(s):

John C. Tuthill ◽

Aljoscha Nern ◽

Gerald M. Rubin ◽

Michael B. Reiser

Keyword(s):

Visual Processing ◽

Wide Field ◽

Early Visual Processing

Download Full-text

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

10.1101/086934 ◽

2016 ◽

Author(s):

Kit D. Longden ◽

Martina Wicklein ◽

Benjamin J. Hardcastle ◽

Stephen J. Huston ◽

Holger G. Krapp

Keyword(s):

Optic Flow ◽

Visual Processing ◽

Visual Motion ◽

Receptive Fields ◽

Cell Types ◽

Spike Burst ◽

Cluttered Environments ◽

Single Spike ◽

Self Motion ◽

Spike Bursts

SummaryMany 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.

Download Full-text

Impact of visual motion adaptation on neural responses to objects and its dependence on the temporal characteristics of optic flow

Journal of Neurophysiology ◽

10.1152/jn.00359.2010 ◽

2011 ◽

Vol 105 (4) ◽

pp. 1825-1834 ◽

Cited By ~ 7

Author(s):

Pei Liang ◽

Roland Kern ◽

Rafael Kurtz ◽

Martin Egelhaaf

Keyword(s):

Optic Flow ◽

Visual Motion ◽

Induced Response ◽

Neural Responses ◽

Neuronal Responses ◽

Motion Adaptation ◽

Preferred Direction ◽

Pure Rotation ◽

Normal Behavior ◽

Natural Dynamics

It is still unclear how sensory systems efficiently encode signals with statistics as experienced by animals in the real world and what role adaptation plays during normal behavior. Therefore, we studied the performance of visual motion-sensitive neurons of blowflies, the horizontal system neurons, with optic flow that was reconstructed from the head trajectories of semi-free-flying flies. To test how motion adaptation is affected by optic flow dynamics, we manipulated the seminatural optic flow by targeted modifications of the flight trajectories and assessed to what extent neuronal responses to an object located close to the flight trajectory depend on adaptation dynamics. For all types of adapting optic flow object-induced response increments were stronger in the adapted compared with the nonadapted state. Adaptation with optic flow characterized by the typical alternation between translational and rotational segments produced this effect but also adaptation with optic flow that lacked these distinguishing features and even pure rotation at a constant angular velocity. The enhancement of object-induced response increments had a direction-selective component because preferred-direction rotation and natural optic flow were more efficient adaptors than null-direction rotation. These results indicate that natural dynamics of optic flow is not a basic requirement to adapt neurons in a specific, presumably functionally beneficial way. Our findings are discussed in the light of adaptation mechanisms proposed on the basis of experiments previously done with conventional experimenter-defined stimuli.

Download Full-text

Motion Adaptation Leads to Parsimonious Encoding of Natural Optic Flow by Blowfly Motion Vision System

Journal of Neurophysiology ◽

10.1152/jn.00308.2005 ◽

2005 ◽

Vol 94 (3) ◽

pp. 1761-1769 ◽

Cited By ~ 6

Author(s):

J. Heitwerth ◽

R. Kern ◽

J. H. van Hateren ◽

M. Egelhaaf

Keyword(s):

Optic Flow ◽

Visual Motion ◽

Vision System ◽

Relevant Information ◽

Spike Timing ◽

Motion Vision ◽

Motion Adaptation ◽

Time Motion ◽

Count Response ◽

Latency Jitter

Neurons sensitive to visual motion change their response properties during prolonged motion stimulation. These changes have been interpreted as adaptive and were concluded, for instance, to adjust the sensitivity of the visual motion pathway to velocity changes or to increase the reliability of encoding of motion information. These conclusions are based on experiments with experimenter-designed motion stimuli that differ substantially with respect to their dynamical properties from the optic flow an animal experiences during normal behavior. We analyze for the first time motion adaptation under natural stimulus conditions. The experiments are done on the H1-cell, an identified neuron in the blowfly visual motion pathway that has served in many previous studies as a model system for visual motion computation. We reconstructed optic flow perceived by a blowfly in free flight and used this behaviorally generated optic flow to study motion adaptation. A variety of measures (variability in spike count, response latency, jitter of spike timing) suggests that the coding quality does not improve with prolonged stimulation. However, although the number of spikes decreases considerably during stimulation with natural optic flow, the amount of information that is conveyed stays nearly constant. Thus the information per spike increases, and motion adaptation leads to parsimonious coding without sacrificing the reliability with which behaviorally relevant information is encoded.

Download Full-text

AN ANALOG VLSI INPLEMENTATION OF A VISUAL INTERNEURON: ENHANCED SENSORY PROCESSING THROUGH BIOPHYSICAL MODELING

International Journal of Neural Systems ◽

10.1142/s012906579900037x ◽

1999 ◽

Vol 09 (05) ◽

pp. 391-395 ◽

Cited By ~ 9

Author(s):

REID R. HARRISON ◽

CHRISTOF KOCH

Keyword(s):

Sensory Processing ◽

Visual Processing ◽

Visual Motion ◽

Gain Control ◽

Analog Vlsi ◽

Neuronal Model ◽

Wide Field ◽

Motion Information ◽

Biophysical Modeling ◽

Pattern Size

Flies are capable of rapid, coordinated flight through unstructured environments. This flight is guided by visual motion information that is extracted from photoreceptors in a robust manner. One feature of the fly's visual processing that adds to this robustness is the saturation of wide-field motion-sensitive neuron responses with increasing pattern size. This makes the cell's responses less dependent on the sparseness of the optical flow field while retaining motion information. By implementing a compartmental neuronal model in silicon, we add this "gain control" to an existing analog VLSI model of fly vision. This results in enhanced performance in a compact, low-power CMOS motion sensor. Our silicon system also demonstrates that modern, biophysically-detailed models of neural sensory processing systems can be instantiated in VLSI hardware.

Download Full-text

Acute Application of Imidacloprid Alters the Sensitivity of Direction Selective Motion Detecting Neurons in an Insect Pollinator

Frontiers in Physiology ◽

10.3389/fphys.2021.682489 ◽

2021 ◽

Vol 12 ◽

Author(s):

Elisa Rigosi ◽

David C. O’Carroll

Keyword(s):

Flight Control ◽

Visual Processing ◽

Visual Cues ◽

Visual Motion ◽

Plant Protection ◽

Control Treatment ◽

Wide Field ◽

General Effect ◽

The Brain

Cholinergic pesticides, such as the neonicotinoid imidacloprid, are the most important insecticides used for plant protection worldwide. In recent decades, concerns have been raised about side effects on non-target insect species, including altered foraging behavior and navigation. Although pollinators rely on visual cues to forage and navigate their environment, the effects of neonicotinoids on visual processing have been largely overlooked. To test the effect of acute treatment with imidacloprid at known concentrations in the brain, we developed a modified electrophysiological setup that allows recordings of visually evoked responses while perfusing the brain in vivo. We obtained long-lasting recordings from direction selective wide-field, motion sensitive neurons of the hoverfly pollinator, Eristalis tenax. Neurons were treated with imidacloprid (3.9 μM, 0.39 μM or a sham control treatment using the solvent (dimethylsulfoxide) only. Exposure to a high, yet sub-lethal concentration of imidacloprid significantly alters their physiological response to motion stimuli. We observed a general effect of imidacloprid (3.9 μM) increasing spontaneous activity, reducing contrast sensitivity and giving weaker directional tuning to wide-field moving stimuli, with likely implications for errors in flight control, hovering and routing. Our electrophysiological approach reveals the robustness of the fly visual pathway against cholinergic perturbance (i.e., at 0.39 μM) but also potential threatening effects of cholinergic pesticides (i.e., evident at 3.9 μM) for the visual motion detecting system of an important pollinator.

Download Full-text

The cholinergic pesticide imidacloprid impairs contrast and direction sensitivity in motion detecting neurons of an insect pollinator

10.1101/295576 ◽

2018 ◽

Cited By ~ 1

Author(s):

Elisa Rigosi ◽

David C. O’Carroll

Keyword(s):

Flight Control ◽

Visual Processing ◽

Visual Cues ◽

Visual Motion ◽

Plant Protection ◽

Wide Field ◽

Insect Pollinator ◽

Direction Sensitivity ◽

Spontaneous Firing Rate

AbstractCholinergic pesticides such as the neonicotinoid imidacloprid are the most important insecticides used for plant protection worldwide. In recent decades concerns have been raised about side effects on non-target insect species, including altered foraging behaviour and navigation. Although pollinators rely on visual cues to forage and navigate their environment, the effect of neonicotinoids on visual processing have been largely overlooked. Here we describe a modified electrophysiological setup that allowed recordings of visually evoked responses while perfusing the brain in vivo. Long-lasting recordings from wide-field motion sensitive neurons of the hoverfly pollinator, Eristalis tenax, revealed that sub-lethal exposure to imidacloprid alters their physiological response to motion stimuli. We observed substantially increased spontaneous firing rate, reduced contrast sensitivity and weaker directional tuning to wide-field moving stimuli. This approach reveals sub-lethal effects of imidacloprid in the visual motion detecting system of an important pollinator with likely implications for flight control, hovering and routing.

Download Full-text

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

10.1101/2021.10.18.464799 ◽

2021 ◽

Author(s):

Kit D. Longden ◽

Anna Schützenberger ◽

Ben J Hardcastle ◽

Holger G Krapp

Keyword(s):

Motor Neurons ◽

Visual Motion ◽

Walking Speed ◽

Optokinetic Nystagmus ◽

Frequency Tuning ◽

Temporal Frequency ◽

Motion Blur ◽

Head Movements ◽

Wide Field ◽

Motion Adaptation

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.

Download Full-text