Responses of a pair of flying locusts to lateral looming visual stimuli

We presented a pair of locusts flying loosely tethered with laterally looming discs. Two experiments tested whether looming-evoked flight behaviour was affected by the presence (1) or relative position (2) of a conspecific. We recorded: the type of behavioural response, motion within 6 degrees of freedom, behavioural onset time and duration, distance between individuals and relative direction of motion. Response distributions of the locust furthest from the stimulus (L1) were not affected by the presence or relative position of a conspecific, whereas distributions of the closer locust (L2) were affected by its position relative to the stimulus. Motion tracks of L1 were affected by the presence of L2, which generated relatively robust responses directed forward and away from the stimulus. Translational and rotational motion of L1 differed across treatments in both experiments, whereas L2 motion was less sensitive to the presence or position of a conspecific. The start and duration of the behaviour were invariant to the presence or position of a conspecific and locust pairs maintained a fixed distance during responses to looming. Results suggest that looming-evoked behaviour is influenced by visual cues from a conspecific in the vicinity.     

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.     

Role of spike-frequency adaptation in shaping neuronal response to dynamic stimuli

Spike-frequency adaptation is the reduction of a neuron’s firing rate to a stimulus of constant intensity. In the locust, the Lobula Giant Movement Detector (LGMD) is a visual interneuron that exhibits rapid adaptation to both current injection and visual stimuli. Here, a reduced compartmental model of the LGMD is employed to explore adaptation’s role in selectivity for stimuli whose intensity changes with time. We show that supralinearly increasing current injection stimuli are best at driving a high spike count in the response, while linearly increasing current injection stimuli (i.e., ramps) are best at attaining large firing rate changes in an adapting neuron. This result is extended with in vivo experiments showing that the LGMD’s response to translating stimuli having a supralinear velocity profile is larger than the response to constant or linearly increasing velocity translation. Furthermore, we show that the LGMD’s preference for approaching versus receding stimuli can partly be accounted for by adaptation. Finally, we show that the LGMD’s adaptation mechanism appears well tuned to minimize sensitivity for the level of basal input. This article is part of a special issue on Neuronal Dynamics of Sensory Coding.     

Control of flight by means of lateral visual stimuli in gregarious desert locusts, Schistocerca gregaria

Abstract. Tethered flying locusts were stimulated either by a periodic grating or by a spotted 'swarm-simulating' pattern moving horizontally, parallel to their longitudinal body axis within their lateral visual fields. The direction of movement of the pattern was changed periodically from progressive to regressive and vice versa.
Both kinds of patterns induced a correlated modulation of yaw-torque and thrust. The two measured flight parameters were modulated independently of each other. Each parameter either increased with progressive and decreased with regressive pattern motion or vice versa. The characteristic curves of thrust and yaw-torque responses - i.e. response amplitude versus contrast frequency resp. angular velocity – measured upon stimulation with the periodic grating between 2 and 70 Hz were at a maximum at 10 Hz and decreased at higher and lower contrast frequencies. The shape of the curves was nearly identical. The characteristic curves measured upon stimulation with the 'swarm-simulating' pattern between 60 and 1500^o s^-1 could be simulated using the spatial wavelength content of the pattern and the characteristic curves for periodic gratings.
Therefore, we suggest that the speed and direction of locusts' flight result from the optomotor effectiveness of the pattern image formed by the neighbouring individuals under free flight. The measured responses would thus contribute to the common orientation of groups of locusts within a migrating swarm and thus to swarm cohesion.     

Visual control of steering in locust flight: the effects of head movement on responses to roll stimuli

The contribution of head movement to the control of roll responses in flying locusts (Locusta migratoria) has been examined (i) on a flight balance, recording the angles through which the locust turns when following an artificial horizon; (ii) by recording activity in a pair of flight muscles in restrained conditions; and (iii) by observations on free flying locusts. Responses were compared when the head was free to turn about the thorax, as normal, and when the head was waxed to the thorax, blocking any relative motion between the two (head-fixed). These experiments suggest that the major signal generating corrective roll manoeuvres is the visual error between the angle of the head and the horizon, rather than a signal that includes a measure of the head-thorax angle.

Auditory-evoked evasive manoeuvres in free-flying locusts and moths

We presented free-flying locusts (Locusta migratoria L.) with sounds that varied in temporal structure and carrier frequency as they flew toward a light source in a flight room under controlled temperature and light conditions. Previous studies have shown tethered locusts react more often to trains of 30-kHz pulses than to pulse trains below 10 kHz. Further, this acoustic startle response has been suggested to function in bat-avoidance. We expected free-flying locusts to respond similarly; however, we found locusts responded to all sounds we presented, not just high-frequency, bat-like sounds. Response rates of turns, loops, and dives varied from 6% to 26% but were statistically independent of carrier frequency and/or pulse structure. Free-flying moths and tethered locusts were tested using a subset of our acoustic stimuli under the same temperature and light conditions as the free-flying locusts. Moth responses were carrier frequency dependent as were responses of tethered locusts positioned along the flight path observed in our free-flight trials. All responses were unaffected by a 90% reduction in room light. We conclude that locusts possess an acoustic startle response evocable in free flight, however, free-flying locusts do not show the same discrimination observed in tethered locusts under similar conditions.Abbreviations ASR acoustic startle response - dB SPL decibel sound pressure level (RMS re: 20 Pa)     

Auditory interneurons in locusts produce directional head and abdomen movements

Locusts (Locusta migratoria) were stimulated with pulses of pure tones of frequencies between 5 kHz and 25 kHz. Interneurons responding to these stimuli (auditory interneurons) were recorded intracellularly and identified by dye injection. Their output functions were investigated by injection of depolarizing current during simultaneous registration of components of flight steering behavior of the animals, i.e. movements of the head and the abdomen and flight activity. Three different types of effects were found, corresponding to 3 functional classes of interneurons:

Behavioral analysis of polarization vision in tethered flying locusts

For spatial navigation many insects rely on compass information derived from the polarization pattern of the sky. We demonstrate that tethered flying desert locusts (Schistocerca gregaria) show e-vector-dependent yaw-torque responses to polarized light presented from above. A slowly rotating polarizer (5.3° s^–1) induced periodic changes in yaw torque corresponding to the 180° periodicity of the stimulus. Control experiments with a rotating diffuser, a weak intensity pattern, and a stationary polarizer showed that the response is not induced by intensity gradients in the stimulus. Polarotaxis was abolished after painting the dorsal rim areas of the compound eyes black, but remained unchanged after painting the eyes except the dorsal rim areas. During rotation of the polarizer, two e-vectors (preferred and avoided e-vector) induced no turning responses: they were broadly distributed from 0 to 180° but, for a given animal, were perpendicular to each other. The data demonstrate polarization vision in the desert locust, as shown previously for bees, flies, crickets, and ants. Polarized light is perceived through the dorsal rim area of the compound eye, suggesting that polarization vision plays a role in compass navigation of the locust.     

Neuromagnetic responses elicited by auditory stimuli in dichotic listening

We measured N1m and P2m components of the magnetic field responses that were elicited by random series of a tone burst given to the left ear and a monosyllabic speech sound given to the right ear. The magnetic responses had smaller amplitudes and/or longer peak latencies of the N1m and the P2m when the stimulus was preceded by a stimulus at the same ear than when preceded by a stimulus at the different ear. This reduction of the response by preceding stimulation of the same ear was significant over the hemisphere contralateral, but not ipsilateral, to the ear stimulated. The peak latencies of N1m and P2m were significantly longer in the response over the hemisphere contralateral than ipsilateral to the stimulated ear.     

Activity of descending contralateral movement detector neurons and collision avoidance behaviour in response to head-on visual stimuli in locusts

We recorded the activity of the right and left descending contralateral movement detectors responding to 10-cm (small) or 20-cm (large) computer-generated spheres approaching along different trajectories in the locust's frontal field of view. In separate experiments we examined the steering responses of tethered flying locusts to identical stimuli. The descending contralateral movement detectors were more sensitive to variations in target trajectory in the horizontal plane than in the vertical plane. Descending contralateral movement detector activity was related to target trajectory and to target size and was most sensitive to small objects converging on a direct collision course from above and to one side. Small objects failed to induce collision avoidance manoeuvres whereas large objects produced reliable collision avoidance responses. Large targets approaching along a converging trajectory produced steering responses that were either away from or toward the side of approach of the object, whereas targets approaching along trajectories that were offset from the locust's mid-longitudinal body axis primarily evoked responses away from the target. We detected no differences in the discharge properties of the descending contralateral movement detector pair that could account for the different collision avoidance behaviours evoked by varying the target size and trajectories. We suggest that descending contralateral movement detector properties are better suited to predator evasion than collision avoidance.     

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.     

The role of contact chemoreception in egg-laying behaviour of locusts

Following selection of an appropriate egg-laying site desert locusts lay their eggs at depths in soil by digging their abdomen into the substrate using rhythmic movements of their abdomen and hard, sclerotised ovipositor valves. We have analysed the role of contact chemoreception on egg-laying behaviour and on the rhythmic digging movements of the valves. All chemicals tested acted aversively and reduced both the duration spent egg-laying and the number of eggs laid, with the concentration at which they became aversive being dependent on whether the chemical was normally present in the diet. Chemicals such as sucrose and a lysine glutamate salt prevented egg-laying only at much higher concentrations than known anti-feedants such as nicotine hydrogen tartrate and hydroquinine. Similarly for animals in which fictive digging movements were induced all chemicals stopped the digging rhythm, with sucrose and sodium chloride inhibiting the rhythm at relatively high concentrations compared to NHT and hydroquinone. We conclude that for both egg-laying behaviour and rhythmic digging that the aversiveness of a chemical rather than its identity per se plays a major role in regulating behaviour.     

Adjustment of flight speed of gregarious desert locusts (Orthoptera: Acrididae) flying side by side

In tethered flying locusts, optomotor thrust responses induced by translatory pattern motion within the lateral visual fields were studied under closed-loop conditions. By modulating thrust in a compensatory manner, locusts counteracted a bias motion superposed on the thrust-related motion. This way, pattern speed was kept at 0° s^–1, indicating the set point of the respective optomotor control circuit. Though the quality of bias compensation varied greatly, it was largely independent from pattern characteristics. It might indicate that the gain of behavior not only is controlled by an automatic mechanism but also is affected by spontaneous modulations. Compensation of bias motion was critically dependent on the relation between self- and bias-generated motion: Locusts did not take control over pattern motion if self- and bias-generated motion differed greatly. Instead, locusts adopted a constant, supposingly preferred, thrust value. Therefore, flight speed is assumed to be controlled by two systems: the optomotor and a preferred thrust system. In free flight, an equalization of the flight speed of locusts within a swarm might result from similar behavior. In combination with a presumed coordination of the locusts' course direction, this may explain the continued cohesion of swarms in the field.     

DNA methylation changes elicited by social stimuli in the brains of worker honey bees

Social environments are notoriously multifactorial, yet studies in rodents have suggested that single variables such as maternal care can in fact be disentangled and correlated with specific DNA methylation changes. This study assesses whether non-detrimental social environmental variation in a highly plastic social insect is correlated with epigenomic modifications at the DNA methylation level. Honey bee workers perform tasks such as nursing and foraging in response to the social environment in the hive, in an age-linked but not age-dependent manner. In this study, the methylation levels of 83 cytosine-phosphate-guanosine dinucleotides over eight genomic regions were compared between the brains of age-matched bees performing nursing or foraging tasks. The results reveal more changes correlated with task than with chronological age, and also hive-associated methylation at some sites. One methylation site from a gene encoding Protein Kinase C binding protein 1 was consistently more methylated in foragers than nurses, which is suggested to lead to production of task-specific protein isoforms via alternative splicing. This study illustrates the ability of the neural epigenome to dynamically respond to complex social stimuli.     

Food selection by locusts: The rôle of learning in rejection behaviour

The food selection behaviour of male fifth instar nymphs of Locusta migratoria was monitored on the host plant wheat and on the non-host plants Senecio vulgaris, S. jacobaea and Brassica oleracea. The non-hosts were rejected, but the mode of rejection altered with time in a way which suggested associative learning. This hypothesis was tested and the results discussed in relation to classical theories of learning.

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La sélection des aliments chez les criquets: Le rôle de l'apprentissage dans le comportement de rejet

Résumé Des larves mâles de cinquième stade de Locusta migratoria ont été placées dans des cages avec des végétaux qui pouvaient être changées sans troubler les insectes. Le contact avec des pieds de blé entraînait généralement une palpation suivie de morsures et alors d'alimentation continue. Les plantes non-hôtes Senecio vulgaris, S. jacobaea et Brassica oleracea étaient rejetées, d'abord après morsures suivant la palpation, mais ultérieurement par palpation seule. Nous avons vérifié l'hypothèse que la sensation obtenue par palpation était initialement inadéquate pour provoquer le rejet, ce qui était assuré par les morsures ultérieures mais qu'avec l'expérience l'insecte apprenait à lier la sensation de palpation avec celle de morsures et progressivement rejetait après palpation seule. Ainsi les 8 premiers contacts avec des aliments désagréables ont été observés, soit quant S. vulgaris était présenté continuellement, soit quand S. vulgaris était remplacé par une autre plante désagréable après 4 contacts. Une analyse mathématique des résultats révèle une tendance au rejet par palpation seule à travers les contacts successifs, et que cette tendance est interrompue et se restaure quand l'espace végétal est changé. Ces résultats sond discutés dans le contexte des théories de l'apprentissage et on en a conclu que le phénomène observé est le résultat d'un apprentissage associatif.

     

Sharks modulate their escape behavior in response to predator size,speed and approach orientation

Escape responses are often critical for surviving predator–prey interactions. Nevertheless, little is known about how predator size, speed and approach orientation impact escape performance, especially in larger prey that are primarily viewed as predators. We used realistic shark models to examine how altering predatory behavior and morphology (size, speed and approach orientation) influences escape behavior and performance in Squalus acanthias, a shark that is preyed upon by apex marine predators. Predator models induced C-start escape responses, and increasing the size and speed of the models triggered a more intense response (increased escape turning rate and acceleration). In addition, increased predator size resulted in greater responsiveness from the sharks. Among the responses, predator approach orientation had the most significant impact on escapes, such that the head-on approach, as compared to the tail-on approach, induced greater reaction distances and increased escape turning rate, speed and acceleration. Thus, the anterior binocular vision in sharks renders them less effective at detecting predators approaching from behind. However, it appears that sharks compensate by performing high-intensity escapes, likely induced by the lateral line system, or by a sudden visual flash of the predator entering their field of view. Our study reveals key aspects of escape behavior in sharks, highlighting the modulation of performance in response to predator approach.     

Cerebral-evoked responses elicited by direct stimulation of the lateral spinothalamic tract in the human

The authors recorded cerebral-evoked responses elicited by direct stimulation of the human lateral spinothalamic tract (LST) during percutaneous cordotomy to investigate central conduction of noxious stimuli. These responses consisted of four negative potentials, peak latency being 3.8 (N1), 8.4 (N2), 12.2 (N3) and 21.9 (N4) ms respectively. N1 showed wide distribution over the scalp and was considered to be of subcortical origin. N2-N4 were distributed in both the temporal and central area. The different distribution pattern of N2-N4 from conventional somatosensory-evoked potential suggested a different projection of LST from the medial lemniscus system.     

Acoustic startle/escape reactions in tethered flying locusts: motor patterns and wing kinematics underlying intentional steering

We simultaneously recorded flight muscle activity and wing kinematics in tethered, flying locusts to determine the relationship between asymmetric depressor muscle activation and the kinematics of the stroke reversal at the onset of wing depression during attempted intentional steering manoeuvres. High-frequency, pulsed sounds produced bilateral asymmetries in forewing direct depressor muscles (M97, 98, 99) that were positively correlated with asymmetric forewing depression and asymmetries in stroke reversal timing. Bilateral asymmetries in hindwing depressor muscles (M127 and M128 but not M129) were positively correlated with asymmetric hindwing depression and asymmetries in the timing of the hindwing stroke reversal; M129 was negatively correlated with these shifts. Hindwing depressor asymmetries and wing kinematic changes were smaller and shifted in opposite direction than corresponding measurements of the forewings. These findings suggest that intentional steering manoeuvres employ bulk shifts in depressor muscle timing that affect the timing of the stroke reversals thereby establishing asymmetric wing depression. Finally, we found indications that locusts may actively control the timing of forewing rotation and speculate this may be a mechanism for generating steering torques. These effects would act in concert with forces generated by asymmetric wing depression and angle of attack to establish rapid changes in direction.Abbreviations ASR acoustic startle response - dB SPL decibel sound pressure level (re: 20 Pa RMS) - EMG electromyogram - FWA forewing asymmetry - HWA hindwing asymmetry     

Predator and heterospecific stimuli alter behaviour in cattle

Wild and domestic ungulates modify their behaviour in the presence of olfactory and visual cues of predators but investigations have not exposed a domestic species to a series of cues representing various predators and other ungulate herbivores. We used wolf (Canis lupus), mountain lion (Puma concolor), and mule deer (Odocoileus hemionus) stimuli (olfactory and visual), and a control (no stimuli) to experimentally test for differences in behaviour of cattle (Bos taurus) raised in Arizona. We measured (1) vigilance, (2) foraging rates, (3) giving up density (GUD) of high quality foods and (4) time spent in high quality forage locations in response to location of stimuli treatments. In general, we found a consistent pattern in that wolf and deer treatments caused disparate results in all 4 response variables. Wolf stimuli significantly increased cattle vigilance and decreased cattle foraging rates; conversely, deer stimuli significantly increased cattle foraging rate and increased cattle use of high quality forage areas containing stimuli. Mountain lion stimuli did not significantly impact any of the 4 response variables. Our findings suggest that domestic herbivores react to predatory stimuli, can differentiate between stimuli representing two predatory species, and suggest that cattle may reduce antipredatory behaviour when near heterospecifics.