Abstract
BackgroundThe parasitoid Jewel Wasp hunts cockroaches to serve as a live food supply for its offspring. The wasp stings the cockroach in the head and delivers a cocktail of neurotoxins directly inside the prey's cerebral ganglia. Although not paralyzed, the stung cockroach becomes a living yet docile ‘zombie’, incapable of self-initiating spontaneous or evoked walking. We show here that such neuro-chemical manipulation can be attributed to decreased neuronal activity in a small region of the cockroach cerebral nervous system, the sub-esophageal ganglion (SEG). A decrease in descending permissive inputs from this ganglion to thoracic central pattern generators decreases the propensity for walking-related behaviors.Methodology and Principal FindingsWe have used behavioral, neuro-pharmacological and electrophysiological methods to show that: (1) Surgically removing the cockroach SEG prior to wasp stinging prolongs the duration of the sting 5-fold, suggesting that the wasp actively targets the SEG during the stinging sequence; (2) injecting a sodium channel blocker, procaine, into the SEG of non-stung cockroaches reversibly decreases spontaneous and evoked walking, suggesting that the SEG plays an important role in the up-regulation of locomotion; (3) artificial focal injection of crude milked venom into the SEG of non-stung cockroaches decreases spontaneous and evoked walking, as seen with naturally-stung cockroaches; and (4) spontaneous and evoked neuronal spiking activity in the SEG, recorded with an extracellular bipolar microelectrode, is markedly decreased in stung cockroaches versus non-stung controls.Conclusions and SignificanceWe have identified the neuronal substrate responsible for the venom-induced manipulation of the cockroach's drive for walking. Our data strongly support previous findings suggesting a critical and permissive role for the SEG in the regulation of locomotion in insects. By injecting a venom cocktail directly into the SEG, the parasitoid Jewel Wasp selectively manipulates the cockroach's motivation to initiate walking without interfering with other non-related behaviors.
Highlights
Animals are not automatons that react identically every time they encounter the same stimulus [1]
Gal et al [18] demonstrated that the wasp actively searches for, at least, the supra-esophageal ganglion (SupEG) inside the cockroach’s head capsule during the head sting. These findings suggest that the behavioral changes observed in stung cockroaches result from the neurotoxic effects of the venom on the SupEG, the sub-esophageal ganglion (SEG), or both
We quantified the stinging behavior of wasps to which three groups of cockroaches were presented (n = 8 cockroaches in each group; Fig. 1A): (1) SEG-ablated cockroaches, namely cockroaches from which the SEG had been surgically removed prior to the sting; (2) Neck-connectives (NC)cut cockroaches, in which the neck connectives between the thorax and the SEG were cut prior to the sting
Summary
Animals are not automatons that react identically every time they encounter the same stimulus [1]. Changes in the internal physiological state of an animal alter its responsiveness to stimuli and affect its motivation to engage in a given behavior Such processes and their underlying neuronal substrates have been the subject of extensive study for decades [2,3,4]. Through millions of years of co-evolution, a few animal species have evolved unique strategies to control the motivation of their prey to engage in specific behaviors, thereby manipulating the prey in most exceptional ways [9]. One such example is the parasitoid Jewel Wasp (Ampulex compressa) which depresses the drive of its prey to engage in locomotion [10]. A decrease in descending permissive inputs from this ganglion to thoracic central pattern generators decreases the propensity for walking-related behaviors
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