Predator versus Prey: Locust Looming-Detector Neuron and Behavioural Responses to Stimuli Representing Attacking Bird Predators

Many arthropods possess escape-triggering neural mechanisms that help them evade predators. These mechanisms are important neuroethological models, but they are rarely investigated using predator-like stimuli because there is often insufficient information on real predator attacks. Locusts possess uniquely identifiable visual neurons (the descending contralateral movement detectors, DCMDs) that are well-studied looming motion detectors. The DCMDs trigger ‘glides’ in flying locusts, which are hypothesised to be appropriate last-ditch responses to the looms of avian predators. To date it has not been possible to study glides in response to stimuli simulating bird attacks because such attacks have not been characterised. We analyse video of wild black kites attacking flying locusts, and estimate kite attack speeds of 10.8±1.4 m/s. We estimate that the loom of a kite’s thorax towards a locust at these speeds should be characterised by a relatively low ratio of half size to speed (l/|v|) in the range 4–17 ms. Peak DCMD spike rate and gliding response occurrence are known to increase as l/|v| decreases for simple looming shapes. Using simulated looming discs, we investigate these trends and show that both DCMD and behavioural responses are strong to stimuli with kite-like l/|v| ratios. Adding wings to looming discs to produce a more realistic stimulus shape did not disrupt the overall relationships of DCMD and gliding occurrence to stimulus l/|v|. However, adding wings to looming discs did slightly reduce high frequency DCMD spike rates in the final stages of object approach, and slightly delay glide initiation. Looming discs with or without wings triggered glides closer to the time of collision as l/|v| declined, and relatively infrequently before collision at very low l/|v|. However, the performance of this system is in line with expectations for a last-ditch escape response.     

Synchronized neural input shapes stimulus selectivity in a collision-detecting neuron

How higher-order sensory neurons generate complex selectivity from their simpler inputs is a fundamental question in neuroscience. The lobula giant movement detector (LGMD) is such a visual neuron in the locust Schistocerca americana that responds selectively to objects approaching on a collision course or their two-dimensional projections, looming stimuli [1-4]. To study how this selectivity arises, we designed an apparatus allowing us to stimulate, individually and independently, a sizable fraction of the ～15,000 elementary visual inputs impinging retinotopically onto the LGMD's dendritic fan [5-7] (Figure?1Ai). We then recorded intracellularly in?vivo throughout the visual pathway, assessing the LGMD's activity and that of all three successive presynaptic stages conveying local excitatory inputs. Our results suggest that as collision becomes increasingly imminent, the strength of these inputs increases, whereas their latency decreases. This latency decrease favors summation of inputs activated sequentially throughout the looming sequence, making the neuron maximally sensitive to collision-bound trajectories. Thus, the LGMD's selectivity arises partially from presynaptic mechanisms that synchronize a large population of inputs during a looming stimulus and subsequent detection by postsynaptic mechanisms within the neuron itself. Analogous mechanisms are likely to underlie the tuning properties of visual neurons in other species as well.     

Collision avoidance and a looming sensitive neuron: size matters but biggest is not necessarily best

Locusts possess visual neurons that can be uniquely identified in each locust and that respond selectively to looming stimuli, giving the animal a warning of impending collision. It has been suggested that one such neuron, the lobula giant movement detector (LGMD), issues this warning by generating a peak in its response that occurs ca. 25 ms after a looming object reaches a subtense of 17 degrees on the eye. This peak is proposed to be a trigger for escape behaviour. We use both modelling and electrophysiological techniques to show that this early peak in LGMD response is not the 'essential functional variable' used naturally by the locust to trigger escape, but rather results from the unnaturally large stimulus used in the previous experimental work. The natural predators of Locusta in Africa, where the locust evolved, are small birds such as the fiscal shrike Lanius collaris humeralis and the carmine bee-eater Merops nubicus, with pectoral diameters of 40-45 mm (measurements from museum specimens). Locusta in flight are less than 100 mm wing tip to wing tip. When a locust views small approaching objects, the response of the LGMD continues to increase throughout the object's approach and the locust is able to trigger escape behaviours without the LGMD response peaking prior to collision.     

A look into the cockpit of the developing locust: Looming detectors and predator avoidance

For many animals, the visual detection of looming stimuli is crucial at any stage of their lives. For example, human babies of only 6 days old display evasive responses to looming stimuli (Bower et al. [1971]: Percept Psychophys 9: 193–196). This means the neuronal pathways involved in looming detection should mature early in life. Locusts have been used extensively to examine the neural circuits and mechanisms involved in sensing looming stimuli and triggering visually evoked evasive actions, making them ideal subjects in which to investigate the development of looming sensitivity. Two lobula giant movement detectors (LGMD) neurons have been identified in the lobula region of the locust visual system: the LGMD1 neuron responds selectively to looming stimuli and provides information that contributes to evasive responses such as jumping and emergency glides. The LGMD2 responds to looming stimuli and shares many response properties with the LGMD1. Both neurons have only been described in the adult. In this study, we describe a practical method combining classical staining techniques and 3D neuronal reconstructions that can be used, even in small insects, to reveal detailed anatomy of individual neurons. We have used it to analyze the anatomy of the fan‐shaped dendritic tree of the LGMD1 and the LGMD2 neurons in all stages of the post‐embryonic development of Locusta migratoria. We also analyze changes seen during the ontogeny of escape behaviors triggered by looming stimuli, specially the hiding response. © 2014 Wiley Periodicals, Inc. Develop Neurobiol 74: 1078–1095, 2014     

Behavioural relevance of polarization sensitivity as a target detection mechanism in cephalopods and fishes

Aquatic habitats are rich in polarized patterns that could provide valuable information about the environment to an animal with a visual system sensitive to polarization of light. Both cephalopods and fishes have been shown to behaviourally respond to polarized light cues, suggesting that polarization sensitivity (PS) may play a role in improving target detection and/or navigation/orientation. However, while there is general agreement concerning the presence of PS in cephalopods and some fish species, its functional significance remains uncertain. Testing the role of PS in predator or prey detection seems an excellent paradigm with which to study the contribution of PS to the sensory assets of both groups, because such behaviours are critical to survival. We developed a novel experimental set-up to deliver computer-generated, controllable, polarized stimuli to free-swimming cephalopods and fishes with which we tested the behavioural relevance of PS using stimuli that evoke innate responses (such as an escape response from a looming stimulus and a pursuing behaviour of a small prey-like stimulus). We report consistent responses of cephalopods to looming stimuli presented in polarization and luminance contrast; however, none of the fishes tested responded to either the looming or the prey-like stimuli when presented in polarization contrast.     

Multisensory integration of looming signals by rhesus monkeys

Looming objects produce ecologically important signals that can be perceived in both the visual and auditory domains. Using a preferential looking technique with looming and receding visual and auditory stimuli, we examined the multisensory integration of looming stimuli by rhesus monkeys. We found a strong attentional preference for coincident visual and auditory looming but no analogous preference for coincident stimulus recession. Consistent with previous findings, the effect occurred only with tonal stimuli and not with broadband noise. The results suggest an evolved capacity to integrate multisensory looming objects.     

Naturalistic Stimulus Structure Determines the Integration of Audiovisual Looming Signals in Binocular Rivalry

Rapid integration of biologically relevant information is crucial for the survival of an organism. Most prominently, humans should be biased to attend and respond to looming stimuli that signal approaching danger (e.g. predator) and hence require rapid action. This psychophysics study used binocular rivalry to investigate the perceptual advantage of looming (relative to receding) visual signals (i.e. looming bias) and how this bias can be influenced by concurrent auditory looming/receding stimuli and the statistical structure of the auditory and visual signals.Subjects were dichoptically presented with looming/receding visual stimuli that were paired with looming or receding sounds. The visual signals conformed to two different statistical structures: (1) a ‘simple’ random-dot kinematogram showing a starfield and (2) a “naturalistic” visual Shepard stimulus. Likewise, the looming/receding sound was (1) a simple amplitude- and frequency-modulated (AM-FM) tone or (2) a complex Shepard tone. Our results show that the perceptual looming bias (i.e. the increase in dominance times for looming versus receding percepts) is amplified by looming sounds, yet reduced and even converted into a receding bias by receding sounds. Moreover, the influence of looming/receding sounds on the visual looming bias depends on the statistical structure of both the visual and auditory signals. It is enhanced when audiovisual signals are Shepard stimuli.In conclusion, visual perception prioritizes processing of biologically significant looming stimuli especially when paired with looming auditory signals. Critically, these audiovisual interactions are amplified for statistically complex signals that are more naturalistic and known to engage neural processing at multiple levels of the cortical hierarchy.     

Accumulation of continuously time-varying sensory evidence constrains neural and behavioral responses in human collision threat detection

Evidence accumulation models provide a dominant account of human decision-making, and have been particularly successful at explaining behavioral and neural data in laboratory paradigms using abstract, stationary stimuli. It has been proposed, but with limited in-depth investigation so far, that similar decision-making mechanisms are involved in tasks of a more embodied nature, such as movement and locomotion, by directly accumulating externally measurable sensory quantities of which the precise, typically continuously time-varying, magnitudes are important for successful behavior. Here, we leverage collision threat detection as a task which is ecologically relevant in this sense, but which can also be rigorously observed and modelled in a laboratory setting. Conventionally, it is assumed that humans are limited in this task by a perceptual threshold on the optical expansion rate–the visual looming–of the obstacle. Using concurrent recordings of EEG and behavioral responses, we disprove this conventional assumption, and instead provide strong evidence that humans detect collision threats by accumulating the continuously time-varying visual looming signal. Generalizing existing accumulator model assumptions from stationary to time-varying sensory evidence, we show that our model accounts for previously unexplained empirical observations and full distributions of detection response. We replicate a pre-response centroparietal positivity (CPP) in scalp potentials, which has previously been found to correlate with accumulated decision evidence. In contrast with these existing findings, we show that our model is capable of predicting the onset of the CPP signature rather than its buildup, suggesting that neural evidence accumulation is implemented differently, possibly in distinct brain regions, in collision detection compared to previously studied paradigms.     

Gliding behaviour elicited by lateral looming stimuli in flying locusts

We challenged tethered, flying locusts with visual stimuli looming from the side towards one eye in a way that mimics the approach of a predatory bird. Locusts respond to the lateral approach of a looming object with steering movements and a stereotyped, rapid behaviour in which the wingbeat pattern ceases and the wings are swept into a gliding posture. This gliding behaviour may cause the locust to dive. The gliding posture is maintained for 200 ms or more after which flight is resumed with an increased wingbeat frequency or else the wings are folded. A glide begins with a strong burst of activity in the mesothoracic second tergosternal motor neuron (no. 84) on both sides of the locust. Recordings of descending contralateral movement detector (DCMD) activity in a flying locust show that it responds to small (80-mm diameter) looming stimuli during tethered flight, with a prolonged burst of spikes that tracks stimulus approach and reaches peak instantaneous frequencies as, or after, stimulus motion ceases. There is a close match between the visual stimuli that elicit a gliding behaviour and those that are effective at exciting the DCMD neuron. Wing elevation into the gliding posture occurs during a maintained burst of high frequency DCMD spikes.     

Responses of descending neurons to looming stimuli in the praying mantis <Emphasis Type="Italic">Tenodera aridifolia</Emphasis>

Responses to visual stimuli of some neurons that descend the nerve cord from the brain were recorded extracellularly in the mantis Tenodera aridifolia. Most of the recorded neurons showed their largest responses to looming stimuli that simulated a black circle approaching towards the mantis. The neurons showed a transient excitatory response to a gradually darkening or receding circle. The neurons showed sustained excitation to the linearly expanding stimuli, but the spike frequency decreased rapidly. The responses of the neurons were affected by both the diameter and the speed of looming stimuli. Faster or smaller looming stimuli elicited a higher peak frequency. These responses were observed in both recordings from the connective between suboesophageal and prothoracic ganglia and the connective between prothoracic and mesothoracic ganglia. There was a one-to-one correspondence of spike firing between these two recordings with a fixed delay. The neurons had the receptive field on ipsilateral side to its axon at the cervical connective. These results suggest that there is a looming-sensitive descending neuron, with an axon projecting over prothoracic ganglion, in the mantis nervous system.     

Tracking improves performance of biological collision avoidance models

Collision avoidance models derived from the study of insect brains do not perform universally well in practical collision scenarios, although the insects themselves may perform well in similar situations. In this article, we present a detailed simulation analysis of two well-known collision avoidance models and illustrate their limitations. In doing so, we present a novel continuous-time implementation of a neuronally based collision avoidance model. We then show that visual tracking can improve performance of these models by allowing an relative computation of the distance between the obstacle and the observer. We compare the results of simulations of the two models with and without tracking to show how tracking improves the ability of the model to detect an imminent collision. We present an implementation of one of these models processing imagery from a camera to show how it performs in real-world scenarios. These results suggest that insects may track looming objects with their gaze.     

Role of wing pronation in evasive steering of locusts

Evasive steering is crucial for flying in a crowded environment such as a locust swarm. We investigated how flying locusts alter wing-flapping symmetry in response to a looming object approaching from the side. Desert locusts (Schistocerca gregaria) were tethered to a rotatable shaft that allowed them to initiate a banked turn. A visual stimulus of an expending disk on one side of the locust was used to evoke steering while recording the change in wingbeat kinematics and electromyography (EMG) of metathoracic wing depressors. Locusts responded to the looming object by rolling to the contralateral direction. During turning, EMG of hindwing depressors showed an omission of one action potential in the subalar depressor (M129) of the hindwing inside the turn. This omission was associated with increased pronation of the same wing, reducing its angle-of-attack during the downstroke. The link between spike-omission in M129 and wing pronation was verified by stimulating the hindwing depressor muscles with an artificial motor pattern that included the misfire of M129. These results suggest that hindwing pronation is instrumental in rotating the body to the side opposite of the approaching threat. Turning away from the threat would be highly adaptive for collision avoidance when flying in dense swarms.     

A simple vision-based algorithm for decision making in flying Drosophila

Animals must quickly recognize objects in their environment and act accordingly. Previous studies indicate that looming visual objects trigger avoidance reflexes in many species [1-5]; however, such reflexes operate over a close range and might not detect a threatening stimulus at a safe distance. We analyzed how fruit flies (Drosophila melanogaster) respond to simple visual stimuli both in free flight and in a tethered-flight simulator. Whereas Drosophila, like many other insects, are attracted toward long vertical objects [6-10], we found that smaller visual stimuli elicit not weak attraction but rather strong repulsion. Because aversion to small spots depends on the vertical size of a moving object, and not on looming, it can function at a much greater distance than expansion-dependent reflexes. The opposing responses to long stripes and small spots reflect a simple but effective object classification system. Attraction toward long stripes would lead flies toward vegetative perches or feeding sites, whereas repulsion from small spots would help them avoid aerial predators or collisions with other insects. The motion of flying Drosophila depends on a balance of these two systems, providing a foundation for studying the neural basis of behavioral choice in a genetic model organism.     

A Comparison of Different Informative Vibrotactile Forward Collision Warnings: Does the Warning Need to Be Linked to the Collision Event?

Recent research demonstrates that auditory and vibrotactile forward collision warnings presenting a motion signal (e.g., looming or apparent motion across the body surface) can facilitate speeded braking reaction times (BRTs). The purpose of the present study was to expand on this work by directly comparing warning signals in which the motion conveyed was constant across all collision events with signals in which the speed of motion was dependent on the closing velocity (CV). Two experiments were conducted using a simulated car-following task and BRTs were measured. In Experiment 1, increasing intensity (looming) vibrotactile signals were presented from a single tactor attached to the driver''s waist. When the increase in intensity was CV-linked, BRTs were significantly faster as compared to a no-warning condition, however, they were not significantly different from constant intensity and CV-independent looming warnings. In Experiment 2, a vertical array of three tactors was used to create motion either towards (upwards) or away (downwards) from the driver''s head. When the warning signal presented upwards motion that was CV-linked, BRTs were significantly faster than all other warning types. Downwards warnings led to a significantly higher number of brake activations in false alarm situations as compared to upwards moving warnings. The effectiveness of dynamic tactile collision warnings would therefore appear to depend on both the link between the warning and collision event and on the directionality of the warning signal.     

Solitary and gregarious locusts differ in circadian rhythmicity of a visual output neuron

Locusts demonstrate remarkable phenotypic plasticity driven by changes in population density. This density dependent phase polyphenism is associated with many physiological, behavioral, and morphological changes, including observations that cryptic solitarious (solitary-reared) individuals start to fly at dusk, whereas gregarious (crowd-reared) individuals are day-active. We have recorded for 24-36 h, from an identified visual output neuron, the descending contralateral movement detector (DCMD) of Schistocerca gregaria in solitarious and gregarious animals. DCMD signals impending collision and participates in flight avoidance maneuvers. The strength of DCMD's response to looming stimuli, characterized by the number of evoked spikes and peak firing rate, varies approximately sinusoidally with a period close to 24 h under constant light in solitarious locusts. In gregarious individuals the 24-h pattern is more complex, being modified by secondary ultradian rhythms. DCMD's strongest responses occur around expected dusk in solitarious locusts but up to 6 h earlier in gregarious locusts, matching the times of day at which locusts of each type are most active. We thus demonstrate a neuronal correlate of a temporal shift in behavior that is observed in gregarious locusts. Our ability to alter the nature of a circadian rhythm by manipulating the rearing density of locusts under identical light-dark cycles may provide important tools to investigate further the mechanisms underlying diurnal rhythmicity.     

Escapes with and without preparation: The neuroethology of visual startle in locusts

Locusts respond to the images of approaching (looming) objects with responses that include gliding while in flight and jumping while standing. For both of these responses there is good evidence that the DCMD neuron (descending contralateral movement detector), which carries spike trains from the brain to the thoracic ganglia, is involved. Sudden glides during flight, which cause a rapid loss of height, are last-chance manoeuvres without prior preparation. Jumps from standing require preparation over several tens of milliseconds because of the need to store muscle-derived energy in a catapult-like mechanism. Locusts’ DCMD neurons respond selectively to looming stimuli, and make connections with some motor neurons and interneurons known to be involved in flying and jumping. For glides, a burst of high-frequency DCMD spikes is a key trigger. For jumping, a similar burst can influence timing, but neither the DCMD nor any other single interneuron has been shown to be essential for triggering any stage in preparation or take-off. Responses by the DCMD to looming stimuli can alter in different behavioural contexts: in a flying locust, arousal ensures a high level of both DCMD responsiveness and glide occurrence; and there are significant differences in DCMD activity between locusts in the gregarious and the solitarious phase.     

Responses of tectal neurons to contrasting stimuli: an electrophysiological study in the barn owl

The saliency of visual objects is based on the center to background contrast. Particularly objects differing in one feature from the background may be perceived as more salient. It is not clear to what extent this so called "pop-out" effect observed in humans and primates governs saliency perception in non-primates as well. In this study we searched for neural-correlates of pop-out perception in neurons located in the optic tectum of the barn owl. We measured the responses of tectal neurons to stimuli appearing within the visual receptive field, embedded in a large array of additional stimuli (the background). Responses were compared between contrasting and uniform conditions. In a contrasting condition the center was different from the background while in the uniform condition it was identical to the background. Most tectal neurons responded better to stimuli in the contrsating condition compared to the uniform condition when the contrast between center and background was the direction of motion but not when it was the orientation of a bar. Tectal neurons also preferred contrasting over uniform stimuli when the center was looming and the background receding but not when the center was receding and the background looming. Therefore, our results do not support the hypothesis that tectal neurons are sensitive to pop-out per-se. The specific sensitivity to the motion contrasting stimulus is consistent with the idea that object motion and not large field motion (e.g., self-induced motion) is coded in the neural responses of tectal neurons.     

A pair of motion-sensitive neurons in the locust encode approaches of a looming object

Neurons in the locust visual system encode approaches of looming stimuli and are implicated in production of escape behaviours. The lobula giant movement detector (LGMD) and its postsynaptic partner, the descending contralateral movement detector (DCMD) compute characteristics of expanding edges across the locust eye during a loom and DCMD synapses onto motor elements associated with behaviour. We identified another descending interneuron within the locust ventral nerve cord. We named this neuron the late DCMD (LDCMD) as it responds later during an approach, with the firing rate peaking at about the time of collision. LDCMD produced lower amplitude, broader action potentials that were associated with an afterhyperpolarization, whereas DCMD action potentials showed a brief afterhyperpolarization often followed by an afterdepolarization. Within the mesothoracic ganglion, the primary LDCMD axon located adjacent to the DCMD axon, was thinner and lacked collateral projections to the lateral region of the neuropil. When compared with DCMD, LDCMD fired with fewer spikes during a loom and showed weaker habituation to repeated approaches. Coincidence of LDCMD and DCMD firing increased during object approach. Our findings indicate the presence of an additional motion-sensitive descending neuron in the locust that encodes temporally distinct properties of an approaching object.     

Effects of stimuli shape and polarization in evoking deimatic patterns in the European cuttlefish, Sepia officinalis, under varying turbidity conditions

Cuttlefish possess the complex ability to identify approaching threats and then to selectively express the appropriate defense. We examined the visual cues used by Sepia officinalis cuttlefish during predator detection and the responses they selected. Using computer-generated stimuli, we set out to quantitate the deimatic responses to artificial looming stimuli of different shapes and contrasts. Defensive behavior gradually intensified as geometrical shapes resembled an image of a fish. Therefore, in addition to an object’s size or its sudden increase in size, cuttlefish use form recognition to identify a threat. Cuttlefish demonstrated equal performance in predator detection trough clear water when presented with intensity versus polarization contrasts. However, when the water turbidity increased, the cuttlefish still detected looming fish shapes based on polarization contrast even when intensity information alone did not suffice. These results demonstrate the interplay between intensity and polarization information transmission and processing in the spatial domain. As nectobenthic organisms, cuttlefish probably experience low visibility conditions on a regular basis. The ability to see further into turbid water and to better detect an approaching object would be beneficial for their survival.     

The effects of flow on schooling Devario aequipinnatus: school structure,startle response and information transmission

To assess how flow affects school structure and threat detection, startle response rates of solitary and small groups of giant danio Devario aequipinnatus to visual looming stimuli were compared in flow and no‐flow conditions. The instantaneous position and heading of each D. aequipinnatus was extracted from high‐speed videos. Behavioural results indicate that (1) school structure is altered in flow such that D. aequipinnatus orient upstream while spanning out in a crosswise direction, (2) the probability of at least one D. aequipinnatus detecting the visual looming stimulus is higher in flow than no flow for both solitary D. aequipinnatus and groups of eight D. aequipinnatus; however, (3) the probability of three or more individuals responding is higher in no flow than in flow. These results indicate a higher probability of stimulus detection in flow but a higher probability of internal transmission of information in no flow. Finally, results were well predicted by a computational model of collective fright response that included the probability of direct detection (based on signal detection theory) and indirect detection (i.e. via interactions between group members) of threatening stimuli. This model provides a new theoretical framework for analysing the collective transfer of information among groups of fishes and other organisms.