Role of the Sub-Esophageal Ganglion in the Regulation of Insect Locomotion: Lessons from Predatory Wasps and Zombie Cockroaches

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 neurotoxic venom cocktail directly inside the prey's cerebral ganglia. Although not paralyzed, the stung cockroach becomes a living yet docile 'zombie' incapable of self-initiating walking or escape running. Our goal was to identify the neuronal substrate responsible for this venom-induced neuro-chemical manipulation of the cockroach locomotion. We show that the decrease in the drive for walking can be attributed to a decrease in neuronal activity in a small region of the cockroach cerebral nervous system, the sub-esophageal ganglion (SEG). Specifically, 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 searches and targets the SEG during the stinging sequence; (2) injecting a sodium channel blocker 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 as compared with non-stung controls. Our data strongly provides evidence for a critical and permissive role of 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.