Rafael Kurtz

Neural encoding of behaviourally relevant visual-motion information in the fly

Information processing in visual systems is constrained by the spatial and temporal characteristics of the sensory input and by the biophysical properties of the neuronal circuits. Hence, to understand how visual systems encode behaviourally relevant information, we need to know about both the computational capabilities of the nervous system and the natural conditions under which animals normally operate. By combining behavioural, neurophysiological and computational approaches, it is now possible in the fly to assess adaptations that process visual-motion information under the constraints of its natural input. It is concluded that neuronal operating ranges and coding strategies appear to be closely matched to the inputs the animal encounters under behaviourally relevant conditions.

Spatial vision in insects is facilitated by shaping the dynamics of visual input through behavioral action

Insects such as flies or bees, with their miniature brains, are able to control highly aerobatic flight maneuvres and to solve spatial vision tasks, such as avoiding collisions with obstacles, landing on objects, or even localizing a previously learnt inconspicuous goal on the basis of environmental cues. With regard to solving such spatial tasks, these insects still outperform man-made autonomous flying systems. To accomplish their extraordinary performance, flies and bees have been shown by their characteristic behavioral actions to actively shape the dynamics of the image flow on their eyes (“optic flow”). The neural processing of information about the spatial layout of the environment is greatly facilitated by segregating the rotational from the translational optic flow component through a saccadic flight and gaze strategy. This active vision strategy thus enables the nervous system to solve apparently complex spatial vision tasks in a particularly efficient and parsimonious way. The key idea of this review is that biological agents, such as flies or bees, acquire at least part of their strength as autonomous systems through active interactions with their environment and not by simply processing passively gained information about the world. These agent-environment interactions lead to adaptive behavior in surroundings of a wide range of complexity. Animals with even tiny brains, such as insects, are capable of performing extraordinarily well in their behavioral contexts by making optimal use of the closed action–perception loop. Model simulations and robotic implementations show that the smart biological mechanisms of motion computation and visually-guided flight control might be helpful to find technical solutions, for example, when designing micro air vehicles carrying a miniaturized, low-weight on-board processor.

Synaptic transfer of dynamic motion information between identified neurons in the visual system of the blowfly

Synaptic transmission is usually studied in vitro with electrical stimulation replacing the natural input of the system. In contrast, we analyzed in vivo transfer of visual motion information from graded-potential presynaptic to spiking postsynaptic neurons in the fly. Motion in the null direction leads to hyperpolarization of the presynaptic neuron but does not much influence the postsynaptic cell, because its firing rate is already low during rest, giving only little scope for further reductions. In contrast, preferred-direction motion leads to presynaptic depolarizations and increases the postsynaptic spike rate. Signal transfer to the postsynaptic cell is linear and reliable for presynaptic graded membrane potential fluctuations of up to approximately 10 Hz. This frequency range covers the dynamic range of velocities that is encoded with a high gain by visual motion-sensitive neurons. Hence, information about preferred-direction motion is transmitted largely undistorted ensuring a consistent dependency of neuronal signals on stimulus parameters, such as motion velocity. Postsynaptic spikes are often elicited by rapid presynaptic spike-like depolarizations which superimpose the graded membrane potential. Although the timing of most of these spike-like depolarizations is set by noise and not by the motion stimulus, it is preserved at the synapse with millisecond precision.

Object representation and distance encoding in three-dimensional environments by a neural circuit in the visual system of the blowfly

Three motion-sensitive key elements of a neural circuit, presumably involved in processing object and distance information, were analyzed with optic flow sequences as experienced by blowflies in a three-dimensional environment. This optic flow is largely shaped by the blowflys saccadic flight and gaze strategy, which separates translational flight segments from fast saccadic rotations. By modifying this naturalistic optic flow, all three analyzed neurons could be shown to respond during the intersaccadic intervals not only to nearby objects but also to changes in the distance to background structures. In the presence of strong background motion, the three types of neuron differ in their sensitivity for object motion. Object-induced response increments are largest in FD1, a neuron long known to respond better to moving objects than to spatially extended motion patterns, but weakest in VCH, a neuron that integrates wide-field motion from both eyes and, by inhibiting the FD1 cell, is responsible for its object preference. Small but significant object-induced response increments are present in HS cells, which serve both as a major input neuron of VCH and as output neurons of the visual system. In both HS and FD1, intersaccadic background responses decrease with increasing distance to the animal, although much more prominently in FD1. This strong dependence of FD1 on background distance is concluded to be the consequence of the activity of VCH that dramatically increases its activity and, thus, its inhibitory strength with increasing distance.

Robust integration of motion information in the fly visual system revealed by single cell photoablation.

In the brain, sensory information needs often to be read out from the ensemble activity of presynaptic neurons. In the most basic case, this may be accomplished by an individual postsynaptic neuron. In the visual system of the blowfly, an identified motion-sensitive spiking neuron is known to be postsynaptic to an ensemble of graded-potential presynaptic input elements. Both the presynaptic and postsynaptic neurons were shown previously to be capable of representing the velocity of preferred-direction motion reliably and linearly over a large frequency range of velocity fluctuations. Accordingly, the synaptic transfer properties of the connecting excitatory synapses between individual input elements and the postsynaptic neuron were shown to be linear over a similar range of presynaptic membrane potential fluctuations. It was not known, however, how the postsynaptic neuron integrates and reads out the presynaptic ensemble activity. We were able to compare the response properties of the integrating cell before and after eliminating individual presynaptic elements by a laser ablation technique. For most of the input elements, we found that their elimination strongly affected the activity of the postsynaptic neuron but did not degrade its performance to encode motion with constant and time-varying velocity. Our results suggest that the integration of individual synaptic inputs within the neural circuit operates with some redundancy. This feature might help the postsynaptic neuron to encode in a highly robust way the direction and the velocity of self-motion of the animal.

Adaptation accentuates responses of fly motion-sensitive visual neurons to sudden stimulus changes

Adaptation in sensory and neuronal systems usually leads to reduced responses to persistent or frequently presented stimuli. In contrast to simple fatigue, adapted neurons often retain their ability to encode changes in stimulus intensity and to respond when novel stimuli appear. We investigated how the level of adaptation of a fly visual motion-sensitive neuron affects its responses to discontinuities in the stimulus, i.e. sudden brief changes in one of the stimulus parameters (velocity, contrast, grating orientation and spatial frequency). Although the neurons overall response decreased gradually during ongoing motion stimulation, the response transients elicited by stimulus discontinuities were preserved or even enhanced with adaptation. Moreover, the enhanced sensitivity to velocity changes by adaptation was not restricted to a certain velocity range, but was present regardless of whether the neuron was adapted to a baseline velocity below or above its steady-state velocity optimum. Our results suggest that motion adaptation helps motion-sensitive neurons to preserve their sensitivity to novel stimuli even in the presence of strong tonic stimulation, for example during self-motion.

Direction-selective adaptation in fly visual motion-sensitive neurons is generated by an intrinsic conductance-based mechanism.

Motion-sensitive neurons in the blowfly brain present an ideal model system to study the cellular mechanisms and functional significance of adaptation to visual motion. Various adaptation processes have been described, but it is still largely unknown which of these processes are generated in the motion-sensitive neurons themselves and which originate at more peripheral processing stages. By input resistance measurements I demonstrate that direction-selective adaptation is generated by an activity-dependent conductance increase in the motion-sensitive neurons. Based on correlations between dendritic Ca(2+) accumulation and slow hyperpolarizing after-potentials following excitatory stimulation, a regulation of direction-selective adaptation by Ca(2+) has previously been suggested. In the present study, however, adaptation phenomena are not evoked when the cytosolic Ca(2+) concentration is elevated by ultraviolet photolysis of caged Ca(2+) in single neurons rather than by motion stimulation. This result renders it unlikely, that adaptation in fly motion-sensitive neurons is regulated by bulk cytosolic Ca(2+).

Octopaminergic modulation of contrast gain adaptation in fly visual motion-sensitive neurons

Locomotor activity like walking or flying has recently been shown to alter visual processing in several species. In insects, the neuromodulator octopamine is thought to play an important role in mediating state changes during locomotion of the animal [K.D. Longden & H.G. Krapp (2009) J. Neurophysiol., 102, 3606–3618; (2010) Front. Syst. Neurosci., 4, 153; S.N. Jung et al. (2011)J. Neurosci., 31, 9231–9237]. Here, we used the octopamine agonist chlordimeform (CDM) to mimic effects of behavioural state changes on visual motion processing. We recorded from identified motion‐sensitive visual interneurons in the lobula plate of the blowfly Calliphora vicina. In these neurons, which are thought to be involved in visual guidance of locomotion, motion adaptation leads to a prominent attenuation of contrast sensitivity. Following CDM application, the neurons maintained high contrast sensitivity in the adapted state. This modulation of contrast gain adaptation was independent of the activity of the recorded neurons, because it was also present after stimulation with visual motion that did not result in deviations from the neurons’ resting activity. We conclude that CDM affects presynaptic inputs of the recorded neurons. Accordingly, the effect of CDM was weak when adapting and test stimuli were presented in different parts of the receptive field, stimulating separate populations of local presynaptic neurons. In the peripheral visual system adaptation depends on the temporal frequency of the stimulus pattern and is therefore related to pattern velocity. Contrast gain adaptation could therefore be the basis for a shift in the velocity tuning that was previously suggested to contribute to state‐dependent processing of visual motion information in the lobula plate interneurons.

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

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.

Neuronal representation of visual motion and orientation in the fly medulla.

In insects, the first extraction of motion and direction clues from local brightness modulations is thought to take place in the medulla. However, whether and how these computations are represented in the medulla stills remain widely unknown, because electrical recording of the neurons in the medulla is difficult. As an effort to overcome this difficulty, we employed local electroporation in vivo in the medulla of the blowfly (Calliphora vicina) to stain small ensembles of neurons with a calcium-sensitive dye. We studied the responses of these neuronal ensembles to spatial and temporal brightness modulations and found selectivity for grating orientation. In contrast, the responses to the two opposite directions of motion of a grating with the same orientation were similar in magnitude, indicating that strong directional selectivity is either not present in the types of neurons covered by our data set, or that direction-selective signals are too closely spaced to be distinguished by our calcium imaging. The calcium responses also showed a bell-shaped dependency on the temporal frequency of drifting gratings, with an optimum higher than that observed in one of the subsequent processing stages, i.e., the lobula plate. Medulla responses were elicited by on- as well as off-stimuli with some spatial heterogeneity in the sensitivity for “on” and “off”, and in the polarity of the responses. Medulla neurons thus show similarities to some established principles of motion and edge detection in the vertebrate visual system.