Aimed limb movements in a hemimetabolous insect are intrinsically compensated for allometric wing growth by developmental mechanisms.

For aimed limb movements to remain functional, they must be adapted to developmental changes in body morphology and sensory-motor systems. Insects use their limbs to groom the body surface or to dislodge external stimuli, but they face the particular problem of adapting these movements to step-like changes in body morphology during metamorphosis or moulting. Locusts are hemimetabolous insects in which the imaginal moult to adulthood results in a sudden and dramatic allometric growth of the wings relative to the body and the legs. We show that, despite this, hind limb scratches aimed at mechanosensory stimuli on the wings remain targeted to appropriate locations after moulting. In juveniles, the tips of the wings extend less than halfway along the abdomen, but in adults they extend well beyond the posterior end. Kinematic analyses were used to examine the scratching responses of juveniles (fifth instars) and adults to touch of anterior (wing base) and posterior (distal abdomen) targets that develop isometrically, and to wing tip targets that are anterior in juveniles but posterior in adults. Juveniles reach the (anterior) wing tip with the distal tibia of the hind leg using anterior rotation of the thoraco-coxal and coxo-trochanteral ('hip') joints and flexion of the femoro-tibial ('knee') joint. Adults, however, reach the corresponding (but now posterior) wing tip using posterior rotation of the hip and extension of the knee, reflecting a different underlying motor pattern. This change in kinematics occurs immediately after the adult moult without learning, indicating that the switch is developmentally programmed.

Motor inhibition affects the speed but not accuracy of aimed limb movements in an insect.

When reaching toward a target, human subjects use slower movements to achieve higher accuracy, and this can be accompanied by increased limb impedance (stiffness, viscosity) that stabilizes movements against motor noise and external perturbation. In arthropods, the activity of common inhibitory motor neurons influences limb impedance, so we hypothesized that this might provide a mechanism for speed and accuracy control of aimed movements in insects. We recorded simultaneously from excitatory leg motor neurons and from an identified common inhibitory motor neuron (CI1) in locusts that performed natural aimed scratching movements. We related limb movement kinematics to recorded motor activity and demonstrate that imposed alterations in the activity of CI1 influenced these kinematics. We manipulated the activity of CI1 by injecting depolarizing or hyperpolarizing current or killing the cell using laser photoablation. Naturally higher levels of inhibitory activity accompanied faster movements. Experimentally biasing the firing rate downward, or stopping firing completely, led to slower movements mediated by changes at several joints of the limb. Despite this, we found no effect on overall movement accuracy. We conclude that inhibitory modulation of joint stiffness has effects across most of the working range of the insect limb, with a pronounced effect on the overall velocity of natural movements independent of their accuracy. Passive joint forces that are greatest at extreme joint angles may enhance accuracy and are not affected by motor inhibition.

Passive resting state and history of antagonist muscle activity shape active extensions in an insect limb.

Limb movements can be driven by muscle contractions, external forces, or intrinsic passive forces. For lightweight limbs like those of insects or small vertebrates, passive forces can be large enough to overcome the effects of gravity and may even generate limb movements in the absence of active muscle contractions. Understanding the sources and actions of such forces is therefore important in understanding motor control. We describe passive properties of the femur-tibia joint of the locust hind leg. The resting angle is determined primarily by passive properties of the relatively large extensor tibiae muscle and is influenced by the history of activation of the fast extensor tibiae motor neuron. The resting angle is therefore better described as a history-dependent resting state. We selectively stimulated different flexor tibiae motor neurons to generate a range of isometric contractions of the flexor tibiae muscle and then stimulated the fast extensor tibiae motor neuron to elicit active tibial extensions. Residual forces in the flexor muscle have only a small effect on subsequent active extensions, but the effect is larger for distal than for proximal flexor motor neurons and varies with the strength of flexor activation. We conclude that passive properties of a lightweight limb make substantial and complex contributions to the resting state of the limb that must be taken into account in the patterning of neuronal control signals driving its active movements. Low variability in the effects of the passive forces may permit the nervous system to accurately predict their contributions to behavior.

Functional recovery of aimed scratching movements after a graded proprioceptive manipulation.

To demonstrate the role of proprioceptive feedback in aimed limb movements, we induced graded changes in the signals provided by the principal receptor in a leg of a locust. The femoro-tibial chordotonal organ (FCO) of the hindleg monitors extension and flexion movements of the tibia and provides the main source of proprioceptive feedback about tibial kinematics. The FCO apodeme (tendon) was surgically shortened by different amounts to provide a systematic bias to this feedback, and aimed scratching movements were analyzed over the week after surgery. Shortening the apodeme led to increased firing of sensory neurons of the FCO at flexed joint angles and is thus functionally similar to flexing the tibia. Immediately after surgery, limb movements shifted dorsally and posteriorly, driven by overextension of the femoro-tibial joint and changes at other joints of the limb. The extent of tibial overextension reflected the extent of apodeme shortening. Overextension would tend to renormalize the FCO feedback signal and can be explained by known interjoint reflex pathways. Our data demonstrate that proprioceptive feedback provides a graded signal that is used to control these aimed limb movements. Over the course of 7 d after surgery, there was a functional recovery in aiming as the overall patterns of movement returned toward control values driven by reciprocal compensatory changes at two joints. The sensory to motor pathways are monosynaptic and oligosynaptic in this system, thus providing us with a powerful opportunity to investigate further the sensorimotor transformations and plasticity of aimed limb movements.

Spatiotemporal receptive field properties of a looming-sensitive neuron in solitarious and gregarious phases of the desert locust.

Desert locusts (Schistocerca gregaria) can transform reversibly between the swarming gregarious phase and a solitarious phase, which avoids other locusts. This transformation entails dramatic changes in morphology, physiology, and behavior. We have used the lobula giant movement detector (LGMD) and its postsynaptic target, the descending contralateral movement detector (DCMD), which are visual interneurons that detect looming objects, to analyze how differences in the visual ecology of the two phases are served by altered neuronal function. Solitarious locusts had larger eyes and a greater degree of binocular overlap than those of gregarious locusts. The receptive field to looming stimuli had a large central region of nearly equal response spanning 120 degrees x 60 degrees in both phases. The DCMDs of gregarious locusts responded more strongly than solitarious locusts and had a small caudolateral focus of even further sensitivity. More peripherally, the response was reduced in both phases, particularly ventrally, with gregarious locusts showing greater proportional decrease. Gregarious locusts showed less habituation to repeated looming stimuli along the eye equator than did solitarious locusts. By contrast, in other parts of the receptive field the degree of habituation was similar in both phases. The receptive field organization to looming stimuli contrasts strongly with the receptive field organization of the same neurons to nonlooming local-motion stimuli, which show much more pronounced regional variation. The DCMDs of both gregarious and solitarious locusts are able to detect approaching objects from across a wide expanse of visual space, but phase-specific changes in the spatiotemporal receptive field are linked to lifestyle changes.

Compensatory plasticity at an identified synapse tunes a visuomotor pathway.

We characterized homeostatic plasticity at an identified sensory-motor synapse in an insect, which maintains constant levels of motor drive as locusts transform from their solitarious phase to their gregarious swarming phase. The same mechanism produces behaviorally relevant changes in response timing that can be understood in the context of an animal's altered behavioral state. For individual animals of either phase, different looming objects elicited different spiking responses in a visual looming detector interneuron, descending contralateral movement detector (DCMD), yet its synaptic drive to a leg motoneuron, fast extensor tibiae (FETi), always had the same maximum amplitude. Gregarious locust DCMDs produced more action potentials and had higher firing frequencies, but individual postsynaptic potentials (PSPs) elicited in FETi were half the amplitude of those in solitarious locusts. A model suggested that this alone could not explain the similarity in overall amplitude, and we show that facilitation increased the maximum compound PSP amplitude in gregarious animals. There was the same linear relationship between times of peak DCMD firing before collision and the size/velocity of looming objects in both phases. The DCMD-FETi synapse transformed this relationship nonlinearly, such that peak amplitudes of compound PSPs occurred disproportionately earlier for smaller/faster objects. Furthermore, the peak PSP amplitude occurred earlier in gregarious than in solitarious locusts, indicating a differential tuning. Homeostatic modulation of the amplitude, together with a nonlinear synaptic transformation of timing, acted together to tune the DCMD-FETi system so that swarming gregarious locusts respond earlier to small moving objects, such as conspecifics, than solitarious locusts.

Passive joint forces are tuned to limb use in insects and drive movements without motor activity.

BACKGROUND: Limb movements are generally driven by active muscular contractions working with and against passive forces arising in muscles and other structures. In relatively heavy limbs, the effects of gravity and inertia predominate, whereas in lighter limbs, passive forces intrinsic to the limb are of greater consequence. The roles of passive forces generated by muscles and tendons are well understood, but there has been little recognition that forces originating within joints themselves may also be important, and less still that these joint forces may be adapted through evolution to complement active muscle forces acting at the same joint. RESULTS: We examined the roles of passive joint forces in insect legs with different arrangements of antagonist muscles. We first show that passive forces modify actively generated movements of a joint across its working range, and that they can be sufficiently strong to generate completely passive movements that are faster than active movements observed in natural behaviors. We further demonstrate that some of these forces originate within the joint itself. In legs of different species adapted to different uses (walking, jumping), these passive joint forces complement the balance of strength of the antagonist muscles acting on the joint. We show that passive joint forces are stronger where they assist the weaker of two antagonist muscles. CONCLUSIONS: In limbs where the dictates of a key behavior produce asymmetry in muscle forces, passive joint forces can be coadapted to provide the balance needed for the effective generation of other behaviors.

Microarray-based transcriptomic analysis of differences between long-term gregarious and solitarious desert locusts.

Desert locusts (Schistocerca gregaria) show an extreme form of phenotypic plasticity and can transform between a cryptic solitarious phase and a swarming gregarious phase. The two phases differ extensively in behavior, morphology and physiology but very little is known about the molecular basis of these differences. We used our recently generated Expressed Sequence Tag (EST) database derived from S. gregaria central nervous system (CNS) to design oligonucleotide microarrays and compare the expression of thousands of genes in the CNS of long-term gregarious and solitarious adult desert locusts. This identified 214 differentially expressed genes, of which 40% have been annotated to date. These include genes encoding proteins that are associated with CNS development and modeling, sensory perception, stress response and resistance, and fundamental cellular processes. Our microarray analysis has identified genes whose altered expression may enable locusts of either phase to deal with the different challenges they face. Genes for heat shock proteins and proteins which confer protection from infection were upregulated in gregarious locusts, which may allow them to respond to acute physiological challenges. By contrast the longer-lived solitarious locusts appear to be more strongly protected from the slowly accumulating effects of ageing by an upregulation of genes related to anti-oxidant systems, detoxification and anabolic renewal. Gregarious locusts also had a greater abundance of transcripts for proteins involved in sensory processing and in nervous system development and plasticity. Gregarious locusts live in a more complex sensory environment than solitarious locusts and may require a greater turnover of proteins involved in sensory transduction, and possibly greater neuronal plasticity.

Motor control of aimed limb movements in an insect.

Limb movements that are aimed toward tactile stimuli of the body provide a powerful paradigm with which to study the transformation of motor activity into context-dependent action. We relate the activity of excitatory motor neurons of the locust femoro-tibial joint to the consequent kinematics of hind leg movements made during aimed scratching. There is posture-dependence of motor neuron activity, which is stronger in large amplitude (putative fast) than in small (putative slow and intermediate) motor neurons. We relate this posture dependency to biomechanical aspects of the musculo-skeletal system and explain the occurrence of passive tibial movements that occur in the absence of agonistic motor activity. There is little recorded co-activation of antagonistic tibial extensor and flexor motor neurons, and there is differential recruitment of proximal and distal flexor motor neurons. Large-amplitude motor neurons are often recruited soon after a switch in joint movement direction. Motor bursts containing large-amplitude spikes exhibit high spike rates of small-amplitude motor neurons. The fast extensor tibiae neuron, when recruited, exhibits a pattern of activity quite different to that seen during kicking, jumping, or righting: there is no co-activation of flexor motor neurons and no full tibial flexion. Changes in femoro-tibial joint angle and angular velocity are most strongly dependent on variations in the number of motor neuron spikes and the duration of motor bursts rather than on firing frequency. Our data demonstrate how aimed scratching movements result from interactions between biomechanical features of the musculo-skeletal system and patterns of motor neuron recruitment.

Asphericity in supernova explosions from late-time spectroscopy.

Core-collapse supernovae (CC-SNe) are the explosions that announce the death of massive stars. Some CC-SNe are linked to long-duration gamma-ray bursts (GRBs) and are highly aspherical. One important question is to what extent asphericity is common to all CC-SNe. Here we present late-time spectra for a number of CC-SNe from stripped-envelope stars and use them to explore any asphericity generated in the inner part of the exploding star, near the site of collapse. A range of oxygen emission-line profiles is observed, including a high incidence of double-peaked profiles, a distinct signature of an aspherical explosion. Our results suggest that all CC-SNe from stripped-envelope stars are aspherical explosions and that SNe accompanied by GRBs exhibit the highest degree of asphericity.

The effects of temperature on peripheral neuronal function in eurythermal and stenothermal crustaceans.

To determine whether neuronal function in Antarctic crustaceans is adapted to the low and narrow range of temperatures at which these animals live, we have compared conduction velocities in the peripheral nervous systems of two temperate species, the decapod Carcinus maenas and the isopod Ligia oceanica, and two Antarctic species, the isopod Glyptonotus antarcticus and the amphipod Paraceradocus gibber. Neuronal conduction velocity differs among the species in the order C. maenas > G. antarcticus > P. gibber > L. oceanica. When measured at the normal environmental temperatures characteristic of each species, conduction velocity of the Antarctic peracarid P. gibber is greater than that of its similar sized temperate relative L. oceanica, demonstrating complete thermal compensation. The temperate decapod C. maenas has a higher thermal dependence of neuronal conduction velocity than either of the Antarctic species, G. antarcticus and P. gibber, but the temperate L. oceanica does not. These data, when collated with published values, indicate that peracarid crustaceans (L. oceanica, G. antarcticus and P. gibber) have lower neuronal conduction velocities and a lower thermal dependence of neuronal conduction velocity than do other arthropods, irrespective of habitat. There is a linear dependence of conduction velocity on temperature down to -1.8 degrees C in all three species. Our data extend by more than 10 degrees the lower range of temperatures at which conduction velocities have been tested systematically in previous studies. The upper thermal block of neuronal conduction is similar in C. maenas, G. antarcticus, P. gibber and L. oceanica at 24.5, 19.5, 21.5 and 19.5 degrees C, respectively. This suggests that failure to conduct action potentials is not what determines the mortality of Antarctic invertebrates at approximately 10 degrees C. The excitability of axons in the leg nerve of G. antarcticus is not affected by temperatures ranging from -1.8 to +18 degrees C. The responses of sensory neurones activated by movements of spines on the leg, however, are strongly modulated by temperature, with maximal responses at 5-10 degrees C; well above the normal environmental temperature range for the species. The responses fail at 20-22 degrees C. The number of large diameter axons (which produce the fast action potentials recorded in this study) is the same in L. oceanica and G. antarcticus, but the median axon diameter is greater in L. oceanica than G. antarcticus. In G. antarcticus, however, there are glial wrappings around some large (>5 microm diameter) axons that may increase their conduction velocity. Such wrappings are not found in L. oceanica.

An asymmetric energetic type Ic supernova viewed off-axis, and a link to gamma ray bursts.

Type Ic supernovae, the explosions after the core collapse of massive stars that have previously lost their hydrogen and helium envelopes, are particularly interesting because of their link with long-duration gamma ray bursts. Although indications exist that these explosions are aspherical, direct evidence has been missing. Late-time observations of supernova SN 2003jd, a luminous type Ic supernova, provide such evidence. Recent Subaru and Keck spectra reveal double-peaked profiles in the nebular lines of neutral oxygen and magnesium. These profiles are different from those of known type Ic supernovae, with or without a gamma ray burst, and they can be understood if SN 2003jd was an aspherical axisymmetric explosion viewed from near the equatorial plane. If SN 2003jd was associated with a gamma ray burst, we missed the burst because it was pointing away from us.

Graded limb targeting in an insect is caused by the shift of a single movement pattern.

Grooming responses are movements of a multi-jointed limb that are targeted toward a stimulus site on the body. To be successful, they require a continuous transformation of stimulus location into a corresponding motor pattern or selection and blending of a subset of cardinal motor patterns. Tactile stimulation of one forewing of a locust elicits characteristic grooming movements of the ipsilateral hind leg. An initial targeted trajectory that moves the tarsus toward the site of stimulation is followed by a cyclic trajectory in the region of the stimulus. We have analyzed both components of this behavior to quantify the relative effects of somatotopic stimulus position and leg start posture on three parameters: initial movement direction, accuracy, and grooming distribution. Accuracy and grooming distribution were significantly affected by the stimulus location but were not influenced by the initial leg posture. Both cues systematically shifted the initial movement direction from the onset of the response. The subsequent cyclic component of grooming movements forms a behavioral continuum with no clustering in joint angle space. We therefore conclude that forewing grooming in locusts is generated by a single movement pattern that is continuously shifted by a sensory cue signaling position on the forewing surface. Both vertebrates and invertebrates can switch between distinct movement forms to groom different parts of their bodies. Our data provide the first evidence that invertebrates, like vertebrates, also have graded control of limb targeting within the somatosensory receptive field of a single form of motor response.

Wing hair sensilla underlying aimed hindleg scratching of the locust.

The anatomy and physiology of exteroceptors on the surfaces of the wings have been described in many insects, but their roles in behaviour have been less well studied. They have often been assumed to have a role primarily in flight. We show that the wings of the locust Schistocerca gregaria possess at least three different hair types with characteristic patterns of distribution that determine the probability of eliciting targeted hindleg scratching behaviour. The different hair types are defined by their morphology and innervation. The shortest hairs (14-46 microm) are basiconic receptors containing both chemosensory and mechanosensory afferents. They are distributed widely across the dorsal surfaces of the forewings; some are located on the ventral surfaces of the hindwings, but none are found on the ventral surfaces of the forewings or the dorsal surfaces of the hindwings. Medium length hairs (73-159 microm) are found on all wing surfaces, but are restricted to the veins, principally the subcosta on the dorsal surface of the forewings. The longest hairs (316-511 microm) are found only on the postcubitus vein on the dorsal surfaces of the forewings, so that they form a pair of dorsal rows when the wings are folded at rest. Touching the dorsal surface of a forewing can elicit aimed scratching movements of a hindleg, and we show that the probability of eliciting a scratch differs for different stimulus sites and for different start positions of the hind leg. The effectiveness of different stimulus sites can be correlated with the distribution of tactile hairs on the dorsal forewing surface. Touching the long hairs provides the strongest drive to elicit a scratch, and ablating them reduces the probability to almost zero. We conclude that input from forewing tactile hairs plays an important role in eliciting hindleg scratching and encodes the spatial location required for targeting.

Plasticity in the visual system is correlated with a change in lifestyle of solitarious and gregarious locusts.

We demonstrate pronounced differences in the visual system of a polyphenic locust species that can change reversibly between two forms (phases), which vary in morphology and behavior. At low population densities, individuals of Schistocerca gregaria develop into the solitarious phase, are cryptic, and tend to avoid other locusts. At high densities, individuals develop instead into the swarm-forming gregarious phase. We analyzed in both phases the responses of an identified visual interneuron, the descending contralateral movement detector (DCMD), which responds to approaching objects. We demonstrate that habituation of DCMD is fivefold stronger in solitarious locusts. In both phases, the mean time of peak firing relative to the time to collision nevertheless occurs with a similar characteristic delay after an approaching object reaches a particular angular extent on the retina. Variation in the time of peak firing is greater in solitarious locusts, which have lower firing rates. Threshold angle and delay are therefore conserved despite changes in habituation or behavioral phase state. The different rates of habituation should contribute to different predator escape strategies or flight control for locusts living either in a swarm or as isolated individuals. For example, increased variability in the habituated responses of solitarious locusts should render their escape behaviors less predictable. Relative resistance to habituation in gregarious locusts should permit the continued responsiveness required to avoid colliding with other locusts in a swarm. These results will permit us to analyze neuronal plasticity in a model system with a well-defined and controllable behavioral context.

Mechanosensory-induced behavioural gregarization in the desert locust Schistocerca gregaria.

Desert locusts show an extreme form of phenotypic plasticity, changing between a cryptic solitarious phase and a swarming gregarious phase that differ in many aspects of behaviour, physiology and appearance. Solitarious locusts show rapid behavioural phase change in response to tactile stimulation directed to the hind femora. Repeatedly touching as little as one quarter of the anterior (outer) surface area of a hind femur produced full behavioural gregarization within 4 h. Solitarious locusts have approximately 30% more mechanosensory trichoid sensilla on the hind femora than do gregarious locusts but have similar or fewer numbers of sensilla elsewhere on the legs. Tactile stimulation of a hind femur in solitarious locusts that had been restrained so that they could not move their legs failed to induce any behavioural gregarization. Patterned electrical stimulation of metathoracic nerve 5, which innervates the hind leg, however, produced full gregarization in restrained locusts. Our data show for the first time that the gregarizing signal combines both exteroceptive and proprioceptive components, which travel in both nerves 5B1 and 5B2, and provides us with a powerful experimental method with which to elicit and study neuronal plasticity in this system. Acetic acid odour, a strong chemosensory stimulus that activates the same local processing pathways as exteroceptive stimuli, failed to elicit behavioural gregarization, suggesting an early segregation in the central nervous system of the mechanosensory signals that leads to gregarization.

Substantial changes in central nervous system neurotransmitters and neuromodulators accompany phase change in the locust.

Desert locusts (Schistocerca gregaria) can undergo a profound transformation between solitarious and gregarious forms, which involves widespread changes in behaviour, physiology and morphology. This phase change is triggered by the presence or absence of other locusts and occurs over a timescale ranging from hours, for some behaviours to change, to generations, for full morphological transformation. The neuro-hormonal mechanisms that drive and accompany phase change in either direction remain unknown. We have used high-performance liquid chromatography (HPLC) to compare amounts of 13 different potential neurotransmitters and/or neuromodulators in the central nervous systems of final instar locust nymphs undergoing phase transition and between long-term solitarious and gregarious adults. Long-term gregarious and solitarious locust nymphs differed in 11 of the 13 substances analysed: eight increased in both the brain and thoracic nerve cord (including glutamate, GABA, dopamine and serotonin), whereas three decreased (acetylcholine, tyramine and citrulline). Adult locusts of both extreme phases were similarly different. Isolating larval gregarious locusts led to rapid changes in seven chemicals equal to or even exceeding the differences seen between long-term solitarious and gregarious animals. Crowding larval solitarious locusts led to rapid changes in six chemicals towards gregarious values within the first 4 h (by which time gregarious behaviours are already being expressed), before returning to nearer long-term solitarious values 24 h later. Serotonin in the thoracic ganglia, however, did not follow this trend, but showed a ninefold increase after a 4 h period of crowding. After crowding solitarious nymphs for a whole larval stadium, the amounts of all chemicals, except octopamine, were similar to those of long-term gregarious locusts. Our data show that changes in levels of neuroactive substances are widespread in the central nervous system and reflect the time course of behavioural and physiological phase change.