Convergent escape behaviour from distinct visual processing of impending collision in fish and grasshoppers.

In animal species ranging from invertebrate to mammals, visually guided escape behaviours have been studied using looming stimuli, the two-dimensional expanding projection on a screen of an object approaching on a collision course at constant speed. The peak firing rate or membrane potential of neurons responding to looming stimuli often tracks a fixed threshold angular size of the approaching stimulus that contributes to the triggering of escape behaviours. To study whether this result holds more generally, we designed stimuli that simulate acceleration or deceleration over the course of object approach on a collision course. Under these conditions, we found that the angular threshold conveyed by collision detecting neurons in grasshoppers was sensitive to acceleration whereas the triggering of escape behaviours was less so. In contrast, neurons in goldfish identified through the characteristic features of the escape behaviours they trigger, showed little sensitivity to acceleration. This closely mirrored a broader lack of sensitivity to acceleration of the goldfish escape behaviour. Thus, although the sensory coding of simulated colliding stimuli with non-zero acceleration probably differs in grasshoppers and goldfish, the triggering of escape behaviours converges towards similar characteristics. Approaching stimuli with non-zero acceleration may help refine our understanding of neural computations underlying escape behaviours in a broad range of animal species. KEY POINTS: A companion manuscript showed that two mathematical models of collision-detecting neurons in grasshoppers and goldfish make distinct predictions for the timing of their responses to simulated objects approaching on a collision course with non-zero acceleration. Testing these experimental predictions showed that grasshopper neurons are sensitive to acceleration while goldfish neurons are not, in agreement with the distinct models proposed previously in these species using constant velocity approaches. Grasshopper and goldfish escape behaviours occurred after the stimulus reached a fixed angular size insensitive to acceleration, suggesting further downstream processing in grasshopper motor circuits to match what was observed in goldfish. Thus, in spite of different sensory processing in the two species, escape behaviours converge towards similar solutions. The use of object acceleration during approach on a collision course may help better understand the neural computations implemented for collision avoidance in a broad range of species.

Approaching object acceleration differentially affects the predictions of neuronal collision avoidance models.

The processing of visual information for collision avoidance has been investigated at the biophysical level in several model systems. In grasshoppers, the (so-called) [Formula: see text] model captures reasonably well the visual processing performed by an identified neuron called the lobular giant movement detector as it tracks approaching objects. Similar phenomenological models have been used to describe either the firing rate or the membrane potential of neurons responsible for visually guided collision avoidance in other animals. Specifically, in goldfish, the [Formula: see text] model has been proposed to describe the Mauthner cell, an identified neuron involved in startle escape responses. In the vinegar fly, a third model was developed for the giant fiber neuron, which triggers last resort escapes immediately before an impending collision. One key property of these models is their prediction that peak neuronal responses occur at a fixed delay after the simulated approaching object reaches a threshold angular size on the retina. This prediction is valid for simulated objects approaching at a constant speed. We tested whether it remains valid when approaching objects accelerate. After characterizing and comparing the models' responses to accelerating and constant speed stimuli, we find that the prediction holds true for the [Formula: see text] and the giant fiber model, but not for the [Formula: see text] model. These results suggest that acceleration in the approach trajectory of an object may help distinguish and further constrain the neuronal computations required for collision avoidance in grasshoppers, fish and vinegar flies.

Molecular characterization and distribution of the voltage-gated sodium channel, Para, in the brain of the grasshopper and vinegar fly.

Voltage-gated sodium (NaV) channels, encoded by the gene para, play a critical role in the rapid processing and propagation of visual information related to collision avoidance behaviors. We investigated their localization by immunostaining the optic lobes and central brain of the grasshopper Schistocerca americana and the vinegar fly Drosophila melanogaster with an antibody that recognizes the channel peptide domain responsible for fast inactivation gating. NaV channels were detected at high density at all stages of development. In the optic lobe, they revealed stereotypically repeating fascicles consistent with the regular structure of the eye. In the central brain, major axonal tracts were strongly labeled, particularly in the grasshopper olfactory system. We used the NaV channel sequence of Drosophila to identify an ortholog in the transcriptome of Schistocerca. The grasshopper, vinegar fly, and human NaV channels exhibit a high degree of conservation at gating and ion selectivity domains. Comparison with three species evolutionarily close to Schistocerca identified splice variants of Para and their relation to those of Drosophila. The anatomical distribution of NaV channels molecularly analogous to those of humans in grasshoppers and vinegar flies provides a substrate for rapid signal propagation and visual processing in the context of visually-guided collision avoidance.

Active membrane conductances and morphology of a collision detection neuron broaden its impedance profile and improve discrimination of input synchrony.

How neurons filter and integrate their complex patterns of synaptic inputs is central to their role in neural information processing. Synaptic filtering and integration are shaped by the frequency-dependent neuronal membrane impedance. Using single and dual dendritic recordings in vivo, pharmacology, and computational modeling, we characterized the membrane impedance of a collision detection neuron in the grasshopper Schistocerca americana. This neuron, the lobula giant movement detector (LGMD), exhibits consistent impedance properties across frequencies and membrane potentials. Two common active conductances gH and gM, mediated respectively by hyperpolarization-activated cyclic nucleotide-gated (HCN) channels and by muscarine-sensitive M-type K+ channels, promote broadband integration with high temporal precision over the LGMD's natural range of membrane potentials and synaptic input frequencies. Additionally, we found that a model based on the LGMD's branching morphology increased the gain and decreased the delay associated with the mapping of synaptic input currents to membrane potential. More generally, this was true for a wide range of model neuron morphologies, including those of neocortical pyramidal neurons and cerebellar Purkinje cells. These findings show the unexpected role played by two widespread active conductances and by dendritic morphology in shaping synaptic integration.NEW & NOTEWORTHY Neuronal filtering and integration of synaptic input patterns depend on the electrochemical properties of dendrites. We used an identified collision detection neuron in grasshoppers to examine how its morphology and two conductances affect its membrane impedance in relation to the computations it performs. The neuronal properties examined are ubiquitous and therefore promote a general understanding of neuronal computations, including those in the human brain.

Optogenetic manipulation of medullary neurons in the locust optic lobe.

The locust is a widely used animal model for studying sensory processing and its relation to behavior. Due to the lack of genomic information, genetic tools to manipulate neural circuits in locusts are not yet available. We examined whether Semliki Forest virus is suitable to mediate exogenous gene expression in neurons of the locust optic lobe. We subcloned a channelrhodopsin variant and the yellow fluorescent protein Venus into a Semliki Forest virus vector and injected the virus into the optic lobe of locusts ( Schistocerca americana). Fluorescence was observed in all injected optic lobes. Most neurons that expressed the recombinant proteins were located in the first two neuropils of the optic lobe, the lamina and medulla. Extracellular recordings demonstrated that laser illumination increased the firing rate of medullary neurons expressing channelrhodopsin. The optogenetic activation of the medullary neurons also triggered excitatory postsynaptic potentials and firing of a postsynaptic, looming-sensitive neuron, the lobula giant movement detector. These results indicate that Semliki Forest virus is efficient at mediating transient exogenous gene expression and provides a tool to manipulate neural circuits in the locust nervous system and likely other insects. NEW & NOTEWORTHY Using Semliki Forest virus, we efficiently delivered channelrhodopsin into neurons of the locust optic lobe. We demonstrate that laser illumination increases the firing of the medullary neurons expressing channelrhodopsin and elicits excitatory postsynaptic potentials and spiking in an identified postsynaptic target neuron, the lobula giant movement detector neuron. This technique allows the manipulation of neuronal activity in locust neural circuits using optogenetics.

M current regulates firing mode and spike reliability in a collision-detecting neuron.

All animals must detect impending collisions to escape and reliably discriminate them from nonthreatening stimuli, thus preventing false alarms. Therefore, it is no surprise that animals have evolved highly selective and sensitive neurons dedicated to such tasks. We examined a well-studied collision-detection neuron in the grasshopper ( Schistocerca americana) using in vivo electrophysiology, pharmacology, and computational modeling. This lobula giant movement detector (LGMD) neuron is excitable by inputs originating from each ommatidia of the compound eye. It possesses many intrinsic properties that increase its selectivity to objects approaching on a collision course, including switching between burst and nonburst firing. In this study, we demonstrate that the LGMD neuron exhibits a large M current, generated by noninactivating K+ channels, that shortens the temporal window of dendritic integration, regulates a firing mode switch between burst and isolated spiking, increases the precision of spike timing, and increases the reliability of spike propagation to downstream motor centers. By revealing how the M current increases the LGMD's ability to detect impending collisions, our results suggest that similar channels may play an analogous role in other collision detection circuits. NEW & NOTEWORTHY The ability to reliably detect impending collisions is a critical survival skill. The nervous systems of many animals have developed dedicated neurons for accomplishing this task. We used a mix of in vivo electrophysiology and computational modeling to investigate the role of M potassium channels within one such collision-detecting neuron and show that through regulation of burst firing and enhancement of spiking reliability, the M current increases the ability to detect impending collisions.

Pre-synaptic Muscarinic Excitation Enhances the Discrimination of Looming Stimuli in a Collision-Detection Neuron.

Visual neurons that track objects on a collision course are often finely tuned to their target stimuli because this is critical for survival. The presynaptic neural networks converging on these neurons and their role in tuning them remain poorly understood. We took advantage of well-known characteristics of one such neuron in the grasshopper visual system to investigate the properties of its presynaptic input network. We find the structure more complex than hitherto realized. In addition to dynamic lateral inhibition used to filter out background motion, presynaptic circuits include normalizing inhibition and excitatory interactions mediated by muscarinic acetylcholine receptors. These interactions preferentially boost responses to coherently expanding visual stimuli generated by colliding objects, as opposed to spatially incoherent controls, helping to discriminate between them. Hence, in addition to active dendritic conductances within collision-detecting neurons, multiple layers of inhibitory and excitatory presynaptic connections are needed to finely tune neural circuits for collision detection.

Feedforward Inhibition Conveys Time-Varying Stimulus Information in a Collision Detection Circuit.

Feedforward inhibition is ubiquitous as a motif in the organization of neuronal circuits. During sensory information processing, it is traditionally thought to sharpen the responses and temporal tuning of feedforward excitation onto principal neurons. As it often exhibits complex time-varying activation properties, feedforward inhibition could also convey information used by single neurons to implement dendritic computations on sensory stimulus variables. We investigated this possibility in a collision-detecting neuron of the locust optic lobe that receives both feedforward excitation and inhibition. We identified a small population of neurons mediating feedforward inhibition, with wide visual receptive fields and whose responses depend both on the size and speed of moving stimuli. By studying responses to simulated objects approaching on a collision course, we determined that they jointly encode the angular size of expansion of the stimulus. Feedforward excitation, on the other hand, encodes a function of the angular velocity of expansion and the targeted collision-detecting neuron combines these two variables non-linearly in its firing output. Thus, feedforward inhibition actively contributes to the detailed firing-rate time course of this collision-detecting neuron, a feature critical to the appropriate execution of escape behaviors. These results suggest that feedforward inhibition could similarly convey time-varying stimulus information in other neuronal circuits.

Collision Avoidance: Broadening the Toolkit for Directionally Selective Motion Computations.

Visually-guided escape behaviors are critical for survival. New research reveals how neurons selectively coding for local motion directions can be assembled into collision detecting ones using a simple recipe.

Escape behavior: linking neural computation to action.

A new study uses a combination of physiological and optogenetic techniques to identify visual neurons in fruit flies that detect approaching objects, and whose activation is integral in escaping an oncoming threat.

Degree of neuromuscular facilitation is correlated with contribution to walking in leg muscles of two species of crab.

Despite decades of work on the neuromuscular physiology of crustacean leg muscles, little is known about how physiological differences between these muscles relate to their behavioral usage. We studied a sideways walking shore crab, Carcinus maenas, and a forward walking spider crab, Libinia emarginata, as part of our work to understand the neural control of locomotion. The two species differed significantly in facilitation at neuromuscular junctions for every muscle studied. Further, these differences are correlated exactly with the walking use of the muscles. The forward walking spider crab showed more facilitation in muscles which operate joints having larger ranges of motion in forward walking. Likewise, greater facilitation was seen in muscles more active during sideways walking in the predominantly sideways walking shore crab. These differences even occur between muscles innervated by the same motor neuron, and become more evident with higher stimulus frequency. The increased presynaptic facilitation might allow selective recruitment of fibers innervated by the same motor neuron and aid in temporal filtering.