Roger Douglas Santer

Motor activity and trajectory control during escape jumping in the locust Locusta migratoria

We investigated the escape jumps that locusts produce in response to approaching objects. Hindleg muscular activity during an escape jump is similar to that during a defensive kick. Locusts can direct their escape jumps up to 50° either side of the direction of their long axis at the time of hindleg flexion, allowing them to consistently jump away from the side towards which an object is approaching. Variation in jump trajectory is achieved by rolling and yawing movements of the body that are controlled by the fore- and mesothoracic legs. During hindleg flexion, a locust flexes the foreleg ipsilateral to its eventual jump trajectory and then extends the contralateral foreleg. These foreleg movements continue throughout co-contraction of the hindleg tibial muscles, pivoting the locust’s long axis towards its eventual jump trajectory. However, there are no bilateral differences in the motor programs of the left and right hindlegs that correlate with jump trajectory. Foreleg movements enable a locust to control its jump trajectory independent of the hindleg motor program, allowing a decision on jump trajectory to be made after the hindlegs have been cocked in preparation for a jump.

Arousal facilitates collision avoidance mediated by a looming-sensitive visual neuron in a flying locust

Locusts have two large collision-detecting neurons, the descending contralateral movement detectors (DCMDs) that signal object approach and trigger evasive glides during flight. We sought to investigate whether vision for action, when the locust is in an aroused state rather than a passive viewer, significantly alters visual processing in this collision-detecting pathway. To do this we used two different approaches to determine how the arousal state of a locust affects the prolonged periods of high-frequency spikes typical of the DCMD response to approaching objects that trigger evasive glides. First, we manipulated arousal state in the locust by applying a brief mechanical stimulation to the hind leg; this type of change of state occurs when gregarious locusts accumulate in high-density swarms. Second, we examined DCMD responses during flight because flight produces a heightened physiological state of arousal in locusts. When arousal was induced by either method we found that the DCMD response recovered from a previously habituated state; that it followed object motion throughout approach; and--most important--that it was significantly more likely to generate the maintained spike frequencies capable of evoking gliding dives even with extremely short intervals (1.8 s) between approaches. Overall, tethered flying locusts responded to 41% of simulated approaching objects (sets of 6 with 1.8 s ISI). When we injected epinastine, the neuronal octopamine receptor antagonist, into the hemolymph responsiveness declined to 12%, suggesting that octopamine plays a significant role in maintaining responsiveness of the DCMD and the locust to visual stimuli during flight.

Preparing for escape: an examination of the role of the DCMD neuron in locust escape jumps

Many animals begin to escape by moving away from a threat the instant it is detected. However, the escape jumps of locusts take several hundred milliseconds to produce and the locust must therefore be prepared for escape before the jumping movement can be triggered. In this study we investigate a locust’s preparations to escape a looming stimulus and concurrent spiking activity in its pair of uniquely identifiable looming-detector neurons (the descending contralateral movement detectors; DCMDs). We find that hindleg flexion in preparation for a jump occurs at the same time as high frequency DCMD spikes. However, spikes in a DCMD are not necessary for triggering hindleg flexion, since this hindleg flexion still occurs when the connective containing a DCMD axon is severed or in response to stimuli that cause no high frequency DCMD spikes. Such severing of the connective containing a DCMD axon does, however, increase the variability in flexion timing. We therefore propose that the DCMD contributes to hindleg flexion in preparation for an escape jump, but that its activity affects only flexion timing and is not necessary for the occurrence of hindleg flexion.

A bio-inspired visual collision detection mechanism for cars : Combining insect inspired neurons to create a robust system

The lobula giant movement detector (LGMD) of locusts is a visual interneuron that responds with an increasing spike frequency to an object approaching on a direct collision course. Recent studies involving the use of LGMD models to detect car collisions showed that it could detect collisions, but the neuron produced collision alerts to non-colliding, translating, stimuli in many cases. This study presents a modified model to address these problems. It shows how the neurons pre-synaptic to the LGMD show a remarkable ability to filter images, and only colliding and translating stimuli produce excitation in the neuron. It then integrates the LGMD network with models based on the elementary movement detector (EMD) neurons from the fly visual system, which are used to analyse directional excitation patterns in the biologically filtered images. Combining the information from the LGMD neuron and four directionally sensitive neurons produces a robust collision detection system for a wide range of automotive test situations.

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° 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 objects approach and the locust is able to trigger escape behaviours without the LGMD response peaking prior to collision.

Retinally-generated saccadic suppression of a locust looming-detector neuron: investigations using a robot locust

A fundamental task performed by many visual systems is to distinguish apparent motion caused by eye movements from real motion occurring within the environment. During saccadic eye movements, this task is achieved by inhibitory signals of central and retinal origin that suppress the output of motion-detecting neurons. To investigate the retinally-generated component of this suppression, we used a computational model of a locust looming-detecting pathway that experiences saccadic suppression. This model received input from the camera of a mobile robot that performed simple saccade-like movements, allowing the models response to simplified real stimuli to be tested. Retinally-generated saccadic suppression resulted from two inhibitory mechanisms within the looming-detectors input architecture. One mechanism fed inhibition forward through the network, inhibiting the looming-detectors initial response to movement. The second spread inhibition laterally within the network, suppressing the looming-detectors maintained response to movement. These mechanisms prevent a loomingdetector model response to whole-field visual stimuli. In the locust, this mechanism of saccadic suppression may operate in addition to centrally-generated suppression. Because lateral inhibition is a common feature of early visual processing in many organisms, we discuss whether the mechanism of retinally-generated saccadic suppression found in the locust looming-detector model may also operate in these species.

Agonistic signals received by an arthropod filiform hair allude to the prevalence of near-field sound communication

Arthropod filiform hairs respond to air particle movements and are among the most sensitive animal sensory organs. In many species, they are tuned to detect predators or prey and trigger escape or prey capture behaviours. Here we show for the first time that these hairs also receive intraspecific near-field sound signals in an arachnid. During agonistic encounters, whip spiders (Arachnida, Amblypygi) perform antenniform leg vibration (ALV) displays that have significantly longer duration in contest winners than losers. During an ALV display: (i) the vibrating antenniform leg of the displaying whip spider is positioned close to the trichobothria (filiform hairs) on its opponents walking legs, (ii) the vibrating antenniform leg can excite these trichobothria via air movements and without direct contact, (iii) the antenniform leg of the displaying whip spider vibrates at a frequency that causes particularly strong, sustained excitation and little adaptation in the trichobothria, and (iv) the duration of an ALV display can be extracted from the response of a trichobothrium. Since filiform hairs are widespread among arthropods, communication via such hairs could be extremely prevalent.

Locust’s Looming Detectors for Robot Sensors

Visual systems in the animal kingdom are incredibly good at extracting useful information from what can often be a very complicated world. Many of these systems can provide inspiration for the design of our own ’seeing machines’ which we can then use in a variety of applications. Our own research is concerned with the detection of ’looming’ or motion in depth. Our biological inspiration is the locust, Locusta migratoria, which possesses two uniquely identifiable neurons (the LGMD and DCMD) that respond preferentially to movements directly towards the animal. The way in which these cells are able to identify such stimuli is now becoming well understood. As such, we have been able to create a plausible computational model of the afferent inputs to these neurons that has been shown to respond in a locust-like way to looming stimuli. This model is now being used to control the movements of a mobile robot within a simplified visual environment. We aim to continue the development of this model so that it may one day function within the same visual world as the locust itself.

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.

Tactile learning by a whip spider, Phrynus marginemaculatus C.L. Koch (Arachnida, Amblypygi).

The ability of animals to learn and remember underpins many behavioural actions and can be crucial for survival in certain contexts, for example in finding and recognising a habitual refuge. The sensory cues that an animal learns in such situations are to an extent determined by its own sensory specialisations. Whip spiders (Arachnida, Amblypygi) are nocturnal and possess uniquely specialised sensory systems that include elongated ‘antenniform’ forelegs specialised for use as chemo- and mechanosensory feelers. We tested the tactile learning abilities of the whip spider Phrynus marginemaculatus in a maze learning task with two tactile cues of different texture—one associated with an accessible refuge, and the other with an inaccessible refuge. Over ten training trials, whip spiders got faster and more accurate at finding the accessible refuge. During a subsequent test trial where both refuges were inaccessible, whip spiders searched for significantly longer at the tactile cue previously associated with the accessible refuge. Using high-speed cinematography, we describe three distinct antenniform leg movements used by whip spiders during tactile examination. We discuss the potential importance of tactile learning in whip spider behaviour and a possible role for their unique giant sensory neurons in accessing tactile information.