A wasp manipulates neuronal activity in the sub-esophageal ganglion to decrease the drive for walking in its cockroach prey.
BACKGROUND
The 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.


RESULTS
We 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
We 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.
Gal
Ram
R
Department of Life Sciences, Ben-Gurion University of the Negev, Be'er-Sheva, Israel. galra@bgu.ac.il
Libersat
Frederic
F
D000818:Animals; D001522:Behavior, Animal; D003058:Cockroaches / Q000502:physiology*; D004924:Escape Reaction / Q000187:drug effects*; D005724:Ganglia; D006790:Host-Parasite Interactions; D009498:Neurotoxins / Q000494:pharmacology; D011235:Predatory Behavior; D016138:Walking; D014862:Wasp Venoms / Q000494:pharmacology*; D014863:Wasps / Q000502:physiology*
D009498:Neurotoxins; D014862:Wasp Venoms
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