Tonic effects of stationary luminous slits on the discharge rates of some locust visual interneurones

The presence of an illuminated slit in the visual field of a locust compound eye produced changes in the tonic discharge rate of the DCMD and three other visual interneurones, recorded in a connective. The DCMD discharge peaked initially in the range of low slit subtenses, but over a period of minutes of exposure its character changed so that there was a rise at high subtenses also. When the luminance of a slit of fixed subtense was increased in steps, there was an initial rise then a sharp fall in discharge, indicating an abrupt onset of inhibition. Lateral spread of inhibition could account for the peak in response to slits, at a subtense falling well within the acceptance angle of a single ommatidium. The results show the ability of some visual interneurones to maintain a changed level of discharge in the presence of a stationary object in the visual field of the eye.     

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.     

Multiplexing of motor information in the discharge of a collision detecting neuron during escape behaviors

Locusts possess an identified neuron, the descending contralateral movement detector (DCMD), conveying visual information about impending collision from the brain to thoracic motor centers. We built a telemetry system to simultaneously record, in freely behaving animals, the activity of the DCMD and of motoneurons involved in jump execution. Cocontraction of antagonistic leg muscles, a required preparatory phase, was triggered after the DCMD firing rate crossed a threshold. Thereafter, the number of DCMD spikes predicted precisely motoneuron activity and jump occurrence. Additionally, the time of DCMD peak firing rate predicted that of jump. Ablation experiments suggest that the DCMD, together with a nearly identical ipsilateral descending neuron, is responsible for the timely execution of the escape. Thus, three distinct features that are multiplexed in a single neuron's sensory response to impending collision-firing rate threshold, peak firing time, and spike count-probably control three distinct motor aspects of escape behaviors.     

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.     

Heat shock-induced thermoprotection of action potentials in the locust flight system.

There is increasing evidence that heat shock (HS) has long-term effects on electrophysiological properties of neurons and synapses. Prior HS protects neural circuitry from a subsequent heat stress but little is known about the mechanisms that mediate this plasticity and induce thermotolerance. Exposure of Locusta migratoria to HS conditions of 45 degrees C for 3 h results in thermotolerance to hitherto lethal temperatures. Locust flight motor patterns were recorded during tethered flight at room temperature, before and after HS. In addition, intracellular action potentials (APs) were recorded from control and HS motoneurons in a semi-intact preparation during a heat stress. HS did not alter the timing of representative depressor or elevator muscle activity, nor did it affect the ability of the locust to generate a steering motor pattern in response to a stimulus. However, HS did increase the duration of APs recorded from neuropil segments of depressor motoneurons. Increases in AP duration were associated with protection of AP generation against failure at subsequent elevated temperatures. Failure of AP generation at high temperatures was preceded by a concomitant burst of APs and depolarization of the membrane. The protective effects of HS were mimicked by pharmacological blockade of I(K+) with tetraethylammonium (TEA). Taken together, these findings are consistent with a hypothesis that HS protects neuronal survival and function via K+ channel modulation.     

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.     

The effects of stimulus area and intensity on the on/off ratio of some locust visual interneurones

The on- and off-discharges of three types of locust visual interneurones were recorded in response to luminous discs ranging in subtense from 0.4 to 25°. For the DCMD neurone there was a clear reciprocal relationship between ON and OFF, with large on- and small off-responses at 0.4°, and the reverse at 25° disc subtense. Most of the changeover from almost pure ON to almost pure OFF discharges occurred in the subtense range up to 2°, i.e. within the acceptance angle of one ommatidium or the angle between adjacent ommatidia. This behaviour was not found at low luminance levels, where ON and OFF followed parallel courses. These findings suggest the existence of strong inhibition, augmenting rapidly with increase in target subtense, as also with luminance as shown in separate experiments. For the DCMD the off-response had the characteristics of a simple rebound excitation, following a short period of light exposure.The other visual interneurones (M and S) behaved differently. They did not show reciprocity of ON and OFF, but instead their responses followed parallel courses with increase in subtense, resembling those of the DCMD at low luminance. Nonetheless, like the DCMD, they did show peaking of the on-response at certain subtenses and luminance, although at much higher levels. The inhibitory activity defining the responses of M and S neurones appeared much less effective than that associated with the DCMD. This could be due to greater complexity in their central connexions, of which nothing is known.     

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.     

Peaking of response in locust visual interneurones to objects of small angular subtense

One compound eye of an immobilised locust viewed a large screen on to which were projected discs of light for periods of 2 sec every 40 sec. The spike response was counted concurrently in the DCMD and the next largest axon in the contralateral nerve cord connective. The average score for 10 trials, after correction for background was plotted for a series of discs subtending a range of angles from 0.05 to 84°.It was found that the response of the DCMD peaked sharply and consistently at a subtense of 0.3°, and fell away to a low plateau or to zero over the range 2° to 84°. The response could exceed background down to subtenses as low as 0.05° (3′ of arc). The response of the next largest axon also showed an early peak, but it was inhibitory and resembled a mirror image of that of the DCMD, although it did not always coincide, ranging from 0.2 to 0.3°. The response, by contrast with the DCMD, rose to a high level at large subtenses, forming a flat peak.No explanation in optical terms could be found for this peaking at small subtenses, and a scheme is proposed by which a peak response could develop by the interaction of excitatory and inhibitory processes in the optic lobe.The peak value of 0.3° corresponds with the resolution limit for moving periodic patterns repeatedly demonstrated by Burtt and Catton (e.g. 1962, 1969). Such peaking behaviour would serve to lift the response curve of the whole visual system at high spatial frequencies, and thus extend the resolution limit.With stepwise reduction in intensity of a small luminous target there was a steep fall in the DCMD response, but a similar reduction for a large target had only a small effect. This could be explained by assuming that excitatory processes were prevalent for small targets, subtending about 0.3°, whereas for larger targets the excitatory and inhibitory processes came into balance over a wide range of intensities, thereby stabilising the response, at a low level.     

Heat shock‐induced thermoprotection of action potentials in the locust flight system

There is increasing evidence that heat shock (HS) has long‐term effects on electrophysiological properties of neurons and synapses. Prior HS protects neural circuitry from a subsequent heat stress but little is known about the mechanisms that mediate this plasticity and induce thermotolerance. Exposure of Locusta migratoria to HS conditions of 45°C for 3 h results in thermotolerance to hitherto lethal temperatures. Locust flight motor patterns were recorded during tethered flight at room temperature, before and after HS. In addition, intracellular action potentials (APs) were recorded from control and HS motoneurons in a semi‐intact preparation during a heat stress. HS did not alter the timing of representative depressor or elevator muscle activity, nor did it affect the ability of the locust to generate a steering motor pattern in response to a stimulus. However, HS did increase the duration of APs recorded from neuropil segments of depressor motoneurons. Increases in AP duration were associated with protection of AP generation against failure at subsequent elevated temperatures. Failure of AP generation at high temperatures was preceded by a concomitant burst of APs and depolarization of the membrane. The protective effects of HS were mimicked by pharmacological blockade of I with tetraethylammonium (TEA). Taken together, these findings are consistent with a hypothesis that HS protects neuronal survival and function via K⁺ channel modulation. © 2001 John Wiley & Sons, Inc. J Neurobiol 49: 188–199, 2001     

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.     

Behavioural phase change in the Australian plague locust, Chortoicetes terminifera, is triggered by tactile stimulation of the antennae

Density-dependent phase polyphenism is a defining characteristic of the paraphyletic group of acridid grasshoppers known as locusts. The cues and mechanisms associated with crowding that induce behavioural gregarization are best understood in the desert locust, Schistocerca gregaria, and involve a combination of sensory inputs from the head (visual and olfactory) and mechanostimulation of the hind legs, acting via a transient increase in serotonin in the thoracic ganglia. Since behavioural gregarization has apparently arisen independently multiple times within the Acrididae, the important question arises as to whether the same mechanisms have been recruited each time. Here we explored the roles of visual, olfactory and tactile stimulation in the induction of behavioural gregarization in the Australian plague locust, Chortoicetes terminifera. We show that the primary gregarizing input is tactile stimulation of the antennae, with no evidence for an effect of visual and olfactory stimulation or tactile stimulation of the hind legs. Our results show that convergent behavioural responses to crowding have evolved employing different sites of sensory input in the Australian plague locust and the desert locust.     

Using a mobile robot to study locust collision avoidance responses

The visual systems of insects perform complex processing using remarkably compact neural circuits, yet these circuits are often studied using simplified stimuli which fail to reveal their behaviour in more complex visual environments. We address this issue by testing models of these circuits in real-world visual environments using a mobile robot. In this paper we focus on the lobula giant movement detector (LGMD) system of the locust which responds selectively to objects which approach the animal on a collision course and is thought to trigger escape behaviours. We show that a neural network model of the LGMD system shares the preference for approaching objects and detects obstacles over a range of speeds. Our results highlight aspects of the basic response properties of the biological system which have important implications for the behavioural role of the LGMD.     

Presence of Heat Shock mRNAs in Field Crown Soybeans

Our laboratory has extensively defined many parameters of the heat shock (HS) response in etiolated soybean (Glycine max [L.] Merr.) hypocotyls, including the identification of cDNA clones for mRNAs encoding several low molecular weight HS proteins. We have now investigated the response of mature plants to a HS in a growth chamber and to high temperature stress under field conditions. Soybean plants show induction of HS mRNAs when the temperature of the chamber is rapidly shifted from 28°C to 45°C. This temperature of induction is significantly higher than the optimal induction temperature for etiolated hypocotyls, probably reflecting the ability of mature plants to lower their leaf temperatures below the ambient air temperature through transpirational cooling. Samples of soybean leaves were taken from an irrigated and a nonirrigated field during a 24-h period when midday temperatures reached 40°C. Several HS mRNAs were present in samples from both fields, although the levels of these mRNAs were much higher in nonirrigated leaves. This differential response of HS mRNA steady state levels was not a response to water stress, since water-stressed plants at 28°C did not induce HS mRNAS. Rather, these quantitative differences are probably due to differences in actual leaf temperatures between irrigated and nonirrigated leaves. The presence of these HS mRNAS in field-grown plants suggests that HS proteins are produced as part of the normal plant response to high temperature.     

Discharge patterns of locust visual interneurones

The spike discharges of the descending contralateral movement detector (DCMD) neurone, and of some smaller visual interneurones (S-units), were recorded in the ventral nerve cord of adult Schistocerca gregaria Forsk., in response to a stationary disc (25^o) or a small spot (0.2^o) stimulus. The discharge rate of each neurone was plotted over a period of 5 s exposure; the total number of spikes in this period was also noted. The DCMD response to the 25^o disc was a high-frequency burst falling off quickly to a low rate; the 0.2^o spot evoked a prolonged discharge with an early peak in rate. In S-units the discharge was prolonged with both targets; the rate rose to an early peak in each case, with a much higher rate for the larger disc. For the DCMD the total number of spikes per stimulus (5 s) was greater for the 0.2^o spot; for S-units it was greater for the 25^o disc. Thus an increase of about 30-fold in the number of ommatidia stimulated resulted in a fall in the total DCMD response to about one-quarter; a similar increase evoked a rise of about 6-fold in the S-unit response. When the 25^o disc was presented at progressively reduced intensities the total spike response of the DCMD rose steadily to a maximum at about 2.9 μ W m^-2; using the same procedure the spike output of S-units, initially high, declined monotonically. The role of inhibition in these results is discussed.     

Exposure to heat shock affects thermosensitivity of the locust flight system

The natural habitat of the migratory locust, Locusta migratoria, is likely to result in locusts being heat stressed during their normal adult life. It is known that locusts exhibit a heat-shock response: exposure to 45°C for 3 h induces thermotolerance and the expression of heat-shock proteins. We investigated the effects of exposure to heat-shock conditions on the thermosensitivity of flight rhythm generation in tethered, intact animals and in deafferented preparations. Heat shock had no effect on wingbeat frequency measured at the start of flight sequences, nor did it affect the postimaginal maturation of this parameter. During sustained flight, heat shock slowed the characteristic asymptotic reduction of wingbeat frequency. Wingbeat frequency of heat-shocked animals was less sensitive to temperature in the range 24° to 47°C than that of control animals, and the upper temperature limit, above which flight rhythms could not be produced, was 6° to 7°C higher in heat-shocked animals. These results were mirrored in the response of deafferented preparations, indicating that modifications in the properties of the flight neuromuscular system were involved in mediating the response of the intact animal. We propose that exposure to heat shock had the adaptive consequences of reducing thermosensitivity of the neural circuits in the flight system and allowing them to operate at higher temperatures. © 1996 John Wiley & Sons, Inc.     

The electrophysiological bases for linear and for nonlinear product term lateral inhibition and the consequences for wide field textured stimuli

The electrophysiological bases of linear, and of nonlinear product term recurrent lateral inhibition are defined and the general equations derived. Defining texture as sinusoidal spatial luminance functions, the response characteristics of nonlinear product term lateral inhibitory arrays to wide field textured stimuli are derived, and applications to locust DCMD and Y retinal ganglion cells discussed.     

Responses of locust visual interneurones to transiently-illuminated slits,paired spots,annuli and disc arrays

One compound eye of an immobilised locust viewed a large screen on to which could be projected a slit of variable width, parallel thin slits of variable separation, large discs or annuli, pairs of small discs or large arrays of small discs. The on-response in the contralateral cervical connective, for both the DCMD and a smaller axon group (M-spikes), was recorded over a period of 2 sec coinciding with the period of illumination. The normal spontaneous discharge of the connective is described. For a single slit the DCMD response peaked in the range 0.02–0.7° of width subtense, the most common result being 0.05°. The M-axon group showed a negative peak at a corresponding subtense. Comparing the responses to single bars and paired slits of the same overall subtense, it was found that below about 1° these were not discriminated by either type of neurone. At higher subtenses the DCMD showed preference for paired slits, the M-axons for solid bars. Comparing responses to arrays of spots with those to uniformly illuminated areas, neither the DCMD nor the M-axon group showed discrimination at angles less than 1°, but at higher angles the DCMD showed preference for arrays and the M-axons for solid areas. Annuli were more effective stimuli than were discs of the same size. Near the edge of large-area targets it was possible to detect spatial transients in excitability. Two small spots produced interaction over a wide range of separations, affording evidence for wide-range mutual inhibition affecting both types of interneurone, and for short-range facilitation for the M-axon group only.     

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.     

A role for oxygen delivery and extracellular magnesium in limiting cold tolerance of the sub-antarctic stone crab Paralomis granulosa?

A low capacity for regulation of extracellular Mg(2+) has been proposed to exclude reptant marine decapod crustaceans from temperatures below 0°C and thus to exclude them from the high Antarctic. To test this hypothesis and to elaborate the underlying mechanisms in the most cold-tolerant reptant decapod family of the sub-Antarctic, the Lithodidae, thermal tolerance was determined in the crab Paralomis granulosa (Decapoda, Anomura, Lithodidae) using an acute stepwise temperature protocol (-1°, 1°, 4°, 7°, 10°, and 13°C). Arterial and venous oxygen partial pressures (Po(2)) in hemolymph, heartbeat and ventilation beat frequencies, and hemolymph cation composition were measured at rest and after a forced activity (righting) trial. Scopes for heartbeat and ventilation beat frequencies and intermittent heartbeat and scaphognathite beat rates at rest were evaluated. Hemolymph [Mg(2+)] was experimentally reduced from 30 mmol L(-1) to a level naturally observed in Antarctic caridean shrimps (12 mmol L(-1)) to investigate whether the animals remain more active and tolerant to cold (-1°, 1°, and 4°C). In natural seawater, righting speed was significantly slower at -1° and 13°C, compared with acclimation temperature (4°C). Arterial and venous hemolymph Po(2) increased in response to cooling even though heartbeat and ventilation beat frequencies as well as scopes decreased. At rest, ionic composition of the hemolymph was not affected by temperature. Activity induced a significant increase in hemolymph [K(+)] at -1° and 1°C. Reduction of hemolymph [Mg(2+)] did not result in an increase in activity, an increase in heartbeat and ventilation beat frequencies, or a shift in thermal tolerance to lower temperatures. In conclusion, oxygen delivery in this cold-water crustacean was not acutely limiting cold tolerance, and animals may have been constrained more by their functional capacity and motility. In contrast to earlier findings in temperate and subpolar brachyuran crabs, these constraints remained insensitive to changing Mg(2+) levels.