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Escape behavior in the cockroach: distributed neural processing.

Escape reactions are often considered to be among the simplest behaviors. The nerve circuits guiding these reactions are also generally thought to be simple. For instance, in several species a single interneuron is sufficient to trigger normal escape. The evasive response of the cockroach, however, appears to be more complex both behaviorally and physiologically. In this review, several complications of the behavior are pointed out, based on a recent computer-graphic analysis of the leg movements. Next described is the cooperative role of several interneurons--not just one--in evoking an escape turn away from the stimulus. A model of this multicellular code for stimulus direction is then presented that correctly predicts the turning behavior under many different experimental conditions. Finally, an overall scheme of the information processing for escape behavior is presented.

Animals↗

Insect tissues, not microorganisms, produce linoleic acid in the house cricket and the American cockroach.

Biosynthesis of linoleic acid, 18:2 (n-6), was unambiguously demonstrated to occur in the cockroach, Periplaneta americana, and the cricket, Acheta domesticus. Axenic tissue from both of these insect species was demonstrated by radio-gas-liquid chromatography (radio-GLC) and radio-high-performance liquid chromatography (radio-HPLC) to incorporate [1-14C]acetate and [1-14C]oleate into this essential fatty acid.

Animals↗

Phosphoramidon enhances allatostatin-mediated inhibition of juvenile hormone biosynthesis in the corpora allata of the cockroach, Diploptera punctata.

Use of enkephalinase inhibitor phosphoramidon in the in vitro radiochemical assay for juvenile hormone biosynthesis enhanced allatostatin-mediated inhibition of hormone production by corpora allata of the cockroach, Diploptera punctata. Significant increases in inhibition in day 2 virgin female CA by AST 1 (at 10(-7) M) and AST 4 (10(-8)-10(-7) M) were observed in the presence of phosphoramidon (10(-5) M or greater). No significant increase in inhibition were seen in CA from day 6 mated females with AST 4 (10(-9)-10(-7) M) and phosphoramidon combined. Phosphoramidon alone had no effect on JH biosynthesis. Analysis of allatostatin content of the CA, as determined by ELISA, revealed that addition of phosphoramidon to the medium increased the endogenous allatostatin content in CA of virgin and mated females. The similarity in primary structure between allatostatins and enkephalin-like peptides and their similar distribution makes it probable that phosphoramidon acts by preventing breakdown of allatostatins within the CA.

Amino Acid Sequence↗

End product specificity of triacylglycerol lipases from intestine, fat body, muscle and haemolymph of the American cockroach, Periplaneta americana L.

The triacylglycerol-hydrolyzing capacity of tissue homogenates has been investigate for midgut, fat body, thoracic musculature and haemolymph of the American cockroach, Periplaneta americana. The greatest lipolytic activity was demonstrated in midgut homogenates with decreasing levels of activity present in fat body, muscle and haemolymph. Comparison of the lipolytic products resulting from triacylglycerol hydrolysis indicates that midgut homogenates effect the production of sn-2-monoacylglycerols and free fatty acids, whereas the other tissues that were examined favor the accumulation of diacylglycerols. Stereospecific analysis of the diacylglycerol products of triacylglycerol hydrolysis demonstrated that the lipolytic activities of midgut and muscle homogenates result in the production of a racemic mixture of the sn-1,2- and sn-2,3-enantiomers, but the fat body and haemolymph show a preference for the accumulation of the sn-1,2-isomer.

Animals↗

3-Hydroxy-2-butanone and the first encounter fight in the male lobster cockroach, Nauphoeta cinerea.

Although agonistic behavior in the male lobster cockroach, Nauphoeta cinerea, has been known for more than 40 years, this is the first study to directly collect and quantify the emitted pheromones. In the present study, emitted volatile pheromones were collected from each male pair for 60 min during the first encounter fight and identified and quantified by gas chromatography-mass spectrometry. The major compound collected was 3-hydroxy-2-butanone (3H-2B). The strength of the attack by the dominant male was classified into three categories from weakest (C) to strongest (A). Of the 92 pairs, eight (8.7%) showed no agonistic interactions, and the amount of 3H-2B collected was 121.8+/-37.7 ng/male pair. In the five pairs (5.4%) displaying attack strength C, the amount of 3H-2B collected was 689.6+/-273.7 ng/male pair, and the attack duration was 9.6+/-2.4 min. In the 53 pairs (57.6%) showing attack strength B, the corresponding values were 5396.2+/-449.0 ng/male pair and 22.7+/-1.6 min, while those for the 26 pairs (28.3%) showing attack strength A were 7910.4+/-1120.6 ng/male pair and 24.9+/-2.9 min. For both attack strengths A and B, a linear relationship was found between the amount of 3H-2B collected and attack duration, suggesting that the longer the duration of the attack, the more 3H-2B was emitted. In addition, the rate of 3H-2B emission for attack strength A was significantly higher than that for attack strength B. Using Vaseline-coating, we demonstrated that, in the first encounter fight, the 3H-2B was emitted by the dominant male.

Acetoin↗

Phylogeny and biogeography of wood-feeding cockroaches, genus Salganea Stål (Blaberidae: Panesthiinae), in Southeast Asia based on mitochondrial DNA sequences.

Molecular phylogenetic relationships among 25 species of the wood-feeding cockroach belonging to the genus Salganea Stål (Panesthiinae; Blaberidae) in Southeast Asia were analyzed based on the DNA sequence of the complete mitochondrial cytochrome oxidase II (COII) gene. Most basal relationships among species of Salganea are poorly resolved by both neighbor-joining and nonweighted parsimony analyses, suggesting the possibility of a hard polytomy due to a rapid and potentially simultaneous radiation early in the history of the genus. For more apical relationships, however, some interesting phylogenetic relationships were recognized. The monophyly of the two species groups, morio and foveolata, the former of which is distributed mainly in the Sunda lands (containing the Malay Peninsula, Sumatra, Java, and Borneo), whereas the latter is Sulawesi endemic, was strongly supported. Based on the inferred phylogenetic patterns and recent palaeogeographic scenario for Southeast Asia, it is suggested that a radiation of Salganea species occurred in Southeast Asia presumably in the early Tertiary, and several barriers against dispersal and gene flow, such as the formation of straits or high mountains, have arisen from the middle Tertiary.

Animals↗

Force detection in cockroach walking reconsidered: discharges of proximal tibial campaniform sensilla when body load is altered.

We examined the mechanisms underlying force feedback in cockroach walking by recording sensory and motor activities in freely moving animals under varied load conditions. Tibial campaniform sensilla monitor forces in the leg via strains in the exoskeleton. A subgroup (proximal receptors) discharge in the stance phase of walking. This activity has been thought to result from leg loading derived from body mass. We compared sensory activities when animals walked freely in an arena or on an oiled glass plate with their body weight supported. The plate was oriented either horizontally (70-75% of body weight supported) or vertically (with the gravitational vector parallel to the substrate). Proximal sensilla discharged following the onset of stance in all load conditions. In addition, activity was decreased in the middle third of the stance phase when the effect of body weight was reduced. Our results suggest that sensory discharges early in stance result from forces generated by contractions of muscles that press the leg as a lever against the substrate. These forces can unload legs already in stance and assure the smooth transition of support among the limbs. Force feedback later in stance may adjust motor output to changes in leg loading.

Animals↗

Control of obstacle climbing in the cockroach, Blaberus discoidalis. I. Kinematics.

An advantage of legged locomotion is the ability to climb over obstacles. We studied deathhead cockroaches as they climbed over plastic blocks in order to characterize the leg movements associated with climbing. Movements were recorded as animals surmounted 5.5-mm or 11-mm obstacles. The smaller obstacles were scaled with little change in running movements. The higher obstacles required altered gaits, leg positions and body posture. The most frequent sequence used was to first tilt the front of the body upward in a rearing stage, and then elevate the center of mass to the level of the top of the block. A horizontal running posture was re-assumed in a leveling-off stage. The action of the middle legs was redirected by rotations of the leg at the thoracal-coxal and the trochanteral-femoral joints. The subsequent extension movements of the coxal-trochanteral and femoral-tibial joints were within the range seen during horizontal running. The structure of proximal leg joints allows for flexibility in leg use by generating subtle, but effective changes in the direction of leg movement. This architecture, along with the resulting re-direction of movements, provides a range of strategies for both animals and walking machines.

Animals↗

Wasp uses venom cocktail to manipulate the behavior of its cockroach prey.

The sting of the parasitoid wasp Ampulex compressa is unusual, as it induces a transient paralysis of the front legs followed by grooming behavior and then by a long-term hypokinesia of its cockroach prey. Because the wasp's goal is to provide a living meal for its newborn larva, the behavioral changes in the prey are brought about by manipulating the host behavior in a way beneficial to the wasp and its offspring. To this end, the wasp injects its venom cocktail with two consecutive stings directly into the host's central nervous system. The first sting in the thorax causes a transient front leg paralysis lasting a few minutes. This paralysis is due to the presence of a venom component that induces a postsynaptic block of central cholinergic synaptic transmission. Following the head sting, dopamine identified in the venom appears to induce 30 min of intense grooming. During the long-term hypokinesia that follows the grooming, specific behaviors of the prey are inhibited while others are unaffected. We propose that the venom represses the activity of head ganglia neurons thereby removing the descending excitatory drive to the thoracic neurons.

Animals↗

Sensing the effect of body load in legs: responses of tibial campaniform sensilla to forces applied to the thorax in freely standing cockroaches.

Sense organs in the legs that detect body weight are an important component in the regulation of posture and locomotion. We tested the abilities of tibial campaniform sensilla, receptors that can monitor forces in the cockroach leg, to encode variations in body load in freely standing animals. Small magnets were attached to the thorax and currents were applied to a coil below the substrate. Sensory and motor activities were monitored neurographically. The tibial sensilla could show vigorous discharges to changing forces when animals stood upon their legs and actively supported the body weight. Firing of individual afferents depended upon the orientation of the receptor's cuticular cap: proximal sensilla (oriented perpendicular to the leg axis) discharged to force increases while distal receptors (parallel to the leg) fired to decreasing forces. Proximal sensillum discharges were prolonged and could encode the level of load when increases were sustained. Firing of the trochanteral extensor motoneuron was also strongly modulated by changing load. In some postures, sensillum discharges paralleled changes in motor frequency consistent with a known interjoint reflex. These findings demonstrate that tibial campaniform sensilla can monitor the effects of body weight upon the legs and may aid in generating support of body load.

Animals↗

Walking on a 'peg leg': extensor muscle activities and sensory feedback after distal leg denervation in cockroaches.

Previous studies in insects demonstrated that leg coordination changes following complete ablation of distal limb segments. However, normal coordination was restored when small 'peg leg' prostheses were attached to leg stumps to permit substrate contact. We have adapted this paradigm to preserve appropriate leg mass and inertia by severing all nerves and muscle tendons in the femur of the cockroach hind leg and converting the animal's own limb into a peg leg. Recordings of muscle activities and leg movements before and after denervation showed that: (1) the 'peg leg' is actively used in walking and regular bursts occur in motoneurons to leg extensor muscles; (2) driving of motoneuron activity is sufficient to produce 'fictive' bursting in a muscle whose tendon (apodeme) is cut in the ablation; and (3) similar motoneuron activities are found in walking on an oiled glass surface, when the effects of body weight and mechanical coupling are minimized. When distal segments were completely severed in these preparations, leg use and muscle bursting were disrupted but could be restored if the stumps were pressed against the substrate. These results support the hypothesis that feedback from receptors in proximal leg segments indicating forces allows for active leg use in walking.

Animals↗

Common motor mechanisms support body load in serially homologous legs of cockroaches in posture and walking.

We studied the mechanisms underlying support of body load in posture and walking in serially homologous legs of cockroaches. Activities of the trochanteral extensor muscle in the front or middle legs were recorded neurographically while animals were videotaped. Body load was increased via magnets attached to the thorax and varied through a coil below the substrate. In posture, tonic firing of the slow trochanteral extensor motoneuron (Ds) in each leg was strongly modulated by changing body load. Rapid load increases produced decreases in body height and sharp increments in extensor firing. The peak of extensor activity more closely approximated the maximum velocity of body displacement than the body position. In walking, extensor bursts in front and middle legs were initiated during swing and continued into the stance phase. Moderate tonic increases in body load elicited similar, specific, phase dependent changes in both legs: extensor firing was not altered in swing but was higher after foot placement in stance. These motor adjustments to load are not anticipatory but apparently depend upon sensory feedback. These data are consistent with previous findings in the hind legs and support the idea that body load is countered by common motor mechanisms in serially homologous legs.

Animals↗

Extracellular long-term recordings of the isolated accessory medulla, the circadian pacemaker center of the cockroach Leucophaea maderae, reveal ultradian and hint circadian rhythms.

In the cockroach Leucophaea maderae transplantation studies located the circadian pacemaker center, which controls locomotor activity rhythms, to the accessory medulla (AMe), ventromedially to the medulla of the brain's optic lobes. The AMe is densely innervated via GABA- and manyfold peptide-immunoreactive neurons. They express ultradian action potential oscillations in the gamma frequency range and form phase-locked assemblies of synchronously spiking cells. Peptide application resulted in transient rises of extracellularly recorded activity. It remained unknown whether transient rises in spontaneous electrical activity as a possible indication of peptide release occur in the isolated circadian clock in a rhythmic manner. In extracellular glass electrode recordings of the isolated AMe in constant darkness, which lasted at least 12 h, the distribution of daytime-dependent changes in activity independently of the absolute action potential frequency was examined. Rapid, transient changes in activity preferentially occurred at the mid-subjective night, with a minimum at the middle of the subjective day, hinting the presence of circadian rhythms in the isolated circadian clock. Additionally, ultradian rhythms in activity change that are multiples of a fundamental 2 h period were observed. We hypothesize that circadian rhythms might originate from coupled ultradian oscillations, possibly already at the single cell level.

Action Potentials↗

Descending control of turning behavior in the cockroach, Blaberus discoidalis.

Legged locomotion has evolved as the most effective form of movement through unpredictable and tortuous environments. Upon encountering an obstacle, an animal must evaluate the object with its sense organs then use the information it acquires to direct appropriate transitional behaviors, such as turning. Previous studies using genetic and surgical lesions implicate the central body complex (CBC) in control of such transitional behaviors of various insects. In this study, lesions of the CBC and surrounding brain regions were used to examine the effects of damage on turning in free-moving and tethered cockroaches. Lesions were performed either as sagittal incisions or by inserting small pieces of foil into regions of the brain. Locomotor behaviors of intact and lesioned animals were compared using high speed video and kinematic analysis. The lesions locations were determined through histological methods. Sagittal lesions to the CBC often result in continuous or incorrect turns. Foil lesions in the CBC also increase the probability that individuals will show turning deficits. The location and degree of the lesion had a strong effect on the animal's ability to turn. These data strongly suggest that the CBC mediates the effects of head sense organs that produce changes in the direction of walking.

Animals↗

Leg kinematics and muscle activity during treadmill running in the cockroach, Blaberus discoidalis: I. Slow running.

We have combined high-speed video motion analysis of leg movements with electromyogram (EMG) recordings from leg muscles in cockroaches running on a treadmill. The mesothoracic (T2) and metathoracic (T3) legs have different kinematics. While in each leg the coxa-femur (CF) joint moves in unison with the femurtibia (FT) joint, the relative joint excursions differ between T2 and T3 legs. In T3 legs, the two joints move through approximately the same excursion. In T2 legs, the FT joint moves through a narrower range of angles than the CF joint. In spite of these differences in motion, no differences between the T2 and T3 legs were seen in timing or qualitative patterns of depressor coxa and extensor tibia activity. The average firing frequencies of slow depressor coxa (Ds) and slow extensor tibia (SETi) motor neurons are directly proportional to the average angular velocity of their joints during stance. The average Ds and SETi firing frequency appears to be modulated on a cycle-by-cycle basis to control running speed and orientation. In contrast, while the frequency variations within Ds and SETi bursts were consistent across cycles, the variations within each burst did not parallel variations in the velocity of the relevant joints.

Animals↗

Indirect synaptic inputs from filiform hair sensory neurons contribute to the receptive fields of giant interneurons in the first-instar cockroach.

The first-instar cockroach, Periplaneta americana, detects air movements using four filiform hair sensilla, which make synaptic connections to seven pairs of giant interneurons (GIs) in the terminal abdominal ganglion. The directional sensitivities of some of the GIs, predicted from their patterns of monosynaptic inputs, may not be the same as in the second instar or adult. Intracellular recordings were made to determine the contribution of polysynaptic inputs to the receptive fields of first-instar GIs. The ventral GI1, and the dorsal GI5, GI6, and GI7 were all found to have indirect synaptic inputs from filiform afferents. The indirect inputs were excitatory to GI1, GI5, and GI7, and inhibitory to GI6 and GI7. The indirect excitatory input to GI1 was predicted to alter qualitatively its receptive field, allowing it to respond to wind from the side of the animal, as in the adult. Inhibition was predicted to sharpen the receptive fields of GI6 and GI7. The inhibitory postsynaptic potentials reversed 6-8 mV below resting potential and were blocked by picrotoxin, indicating that they are GABAergic. Indirect excitation also altered the predicted receptive field of GI7, one of the inputs being an unusual "off-response" to movement of a filiform hair in its inhibitory direction.

Animals↗