Localization of the site of effect of a wasp's venom in the cockroach escape circuitry

Libersat, Frédéric; Haspel, Gal; Casagrand, Janet L.; Fouad, Karim

doi:10.1007/s003590050331

Cited by 22 publications

(12 citation statements)

References 42 publications

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“…Stung cockroaches show very little spontaneous or provoked activity such as escape (Fouad et al, 1994;Libersat et al, 1999). In contrast, our results did not show any differences between stung and control cockroaches in spontaneous or provoked grooming, righting behavior, or ability to fly in a wind tunnel (Weisel-Eichler and Libersat, 2002).…”

Section: Wasp Venom Injection Induces Long-term Hypokinesia and Changcontrasting

confidence: 83%

Parasitoid wasp uses a venom cocktail injected into the brain to manipulate the behavior and metabolism of its cockroach prey

Gal¹,

Rosenberg²,

Libersat³

2005

Arch Insect Biochem Physiol

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Unlike other venomous predators, the parasitoid wasp Ampulex compressa incapacitates its prey, the cockroach Periplaneta americana, to provide a fresh food supply for its offspring. We first established that the wasp larval development, from egg laying to pupation, lasts about 8 days during which the cockroach must remain alive but immobile. To this end, the wasp injects a cocktail of neurotoxins to manipulate the behavior of the cockroach. The cocktail is injected directly into the head ganglia using biosensors located on the stinger. The head sting induces first 30 min of intense grooming followed by hypokinesia during which the cockroach is unable to generate an escape response. In addition, stung cockroaches survive longer, lose less water, and consume less oxygen. Dopamine contained in the venom appears to be responsible for inducing grooming behavior. For the hypokinesia, our hypothesis is that the injected venom affects neurons located in the head ganglia, which send descending tonic input to bioaminergic neurons. These, in turn, control the thoracic premotor circuitry for locomotion. We show that the activity of identified octopaminergic neurons from the thoracic ganglia is altered in stung animals. The alteration in the octopaminergic neurons' activity could be one of the mechanisms by which the venom modulates the escape circuit in the cockroach's central nervous system and metabolism in the peripheral system.

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Section: Wasp Venom Injection Induces Long-term Hypokinesia and Changcontrasting

confidence: 83%

Parasitoid wasp uses a venom cocktail injected into the brain to manipulate the behavior and metabolism of its cockroach prey

Gal¹,

Rosenberg²,

Libersat³

2005

Arch Insect Biochem Physiol

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“…We have shown that these behavioral modifications are evoked by the sting in the head rather than by the sting in the thorax (Fouad et al, 1994). In addition, we have shown that the venom has no effect on the cockroach's neuromuscular junction (Fouad et al, 1996) and that specific motor behaviors are modulated while others, such as flight, are little affected (Fouad et al, 1994;Libersat et al, 1999;Weisel-Eichler and Libersat, 2002). Thus, the venom appears to target the central nervous system (CNS) in the head to modulate specific behaviors.…”

Section: Introductionmentioning

confidence: 90%

“…Instead, it applies the unique strategy of behavioral modulation of the cockroach (Fouad et al, 1994(Fouad et al, , 1996Piek et al, 1984;Weisel-Eichler et al, 1999;Williams, 1942). The stung prey first grooms extensively (WeiselEichler et al, 1999), after which it becomes sluggish and is not responsive to various stimuli (Fouad et al, 1994(Fouad et al, , 1996Libersat et al, 1999). The wasp grabs one of the antennae of the cockroach, which follows docilely to a suitable oviposition location, where it will serve a few days later as an immobilized fresh food source for the wasp's offspring (Williams, 1942;Piek et al, 1984;Fouad et al, 1994).…”

Section: Introductionmentioning

confidence: 96%

Direct injection of venom by a predatory wasp into cockroach brain

2003

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In this article, we provide direct evidence for injection of venom by a wasp into the central nervous system of its cockroach prey. Venomous predators use neurotoxins that generally act at the neuromuscular junction, resulting in different types of prey paralysis. The sting of the parasitoid wasp Ampulex compressa is unusual, as it induces grooming behavior, followed by a long-term lethargic state of its insect prey, thus ultimately providing a living meal for the newborn wasp larvae. These behavioral modifications are induced only when a sting is inflicted into the head. These unique effects of the wasp venom on prey behavior suggest that the venom targets the insect's central nervous system. The mechanism by which behavior modifying compounds in the venom transverse the blood-brain barrier to induce these central and long-lasting effects has been the subject of debate. In this article, we demonstrate that the wasp stings directly into the target ganglia in the head of its prey. To prove this assertion, we produced "hot" wasps by injecting them with (14)C radiolabeled amino acids and used a combination of liquid scintillation and light microscopy autoradiography to trace radiolabeled venom in the prey. To our knowledge, this is the first direct evidence documenting targeted delivery of venom by a predator into the brain of its prey.

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“…The cockroach is not paralyzed, but rendered helplessly submissive after the wasp stings into its head to cause 30 min of excessive grooming (Weisel-Eichler et al, 1999) followed by a 2-to 5-week long lethargic state (Fouad et al, 1994(Fouad et al, , 1996Libersat et al, 1999). In this lethargic state, the cockroach is unresponsive, and does not initiate movement (Fouad et al, 1994(Fouad et al, , 1996Libersat et al, 1999). It is docilely led by the wasp to a burrow to be later consumed alive by its larvae.…”

Section: Introductionmentioning

confidence: 98%

Wasp venom blocks central cholinergic synapses to induce transient paralysis in cockroach prey

Haspel

Libersat

2003

J. Neurobiol.

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The parasitoid wasp Ampulex compressa induces a set of unique behavioral effects upon stinging its prey, the cockroach. It stings into the first thoracic segment inducing 2 to 3 min of transient flaccid paralysis of the front legs. This facilitates a second sting in the cockroach's head that induces 30 min of excessive grooming followed by a 2 to 5-week long lethargic state. In the present study, we examine the immediate effect of the first sting, which is a transient paralysis of the front legs. Using radiolabeled wasps, we demonstrate that the wasp injects its venom directly into the cockroach's first thoracic ganglion. The artificial injection of milked venom into a thoracic ganglion abolishes spontaneous and evoked responses of the motoneurons associated with leg movements. To investigate the physiological mechanism of action of the venom, we injected venom into the last abdominal ganglion of the cockroach, which houses a well-characterized cholinergic synapse. Injected venom abolishes both sensory-evoked and agonist-evoked postsynaptic potentials recorded in the postsynaptic neuron for 2 to 3 min without affecting action potential propagation. Thus, the venom blocking effect has a postsynaptic component that follows the same time course as the transient paralysis induced by the thoracic sting. Finally, injection of a nicotinic antagonist in the front thoracic ganglion induces paralysis of the front legs. We conclude that the transient paralytic effect of the thoracic sting can be mainly accounted for by the presence of a venom active component that induces a postsynaptic block of central cholinergic synaptic transmission.

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Localization of the site of effect of a wasp's venom in the cockroach escape circuitry

Cited by 22 publications

References 42 publications

Parasitoid wasp uses a venom cocktail injected into the brain to manipulate the behavior and metabolism of its cockroach prey

Parasitoid wasp uses a venom cocktail injected into the brain to manipulate the behavior and metabolism of its cockroach prey

Direct injection of venom by a predatory wasp into cockroach brain

Wasp venom blocks central cholinergic synapses to induce transient paralysis in cockroach prey

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