Parasites often alter the behavior of their hosts in ways that are ultimately beneficial to the parasite or its offspring. Although the alteration of host behavior by parasites is a widespread phenomenon, the underlying neuronal mechanisms are only beginning to be understood. Here, we focus on recent advances in the study of behavioral manipulation via modulation of the host central nervous system. We elaborate on a few case studies, in which recently published data provide explanations for the neuronal basis of parasite-induced alteration of host behavior. Among these, we describe how a worm may influence the nervous system of its cricket host and manipulate the cricket into committing suicide by jumping into water. We then focus on Ampulex compressa, which uses an Alien-like strategy for the sake of its offspring. Unlike most venomous hunters, this wasp injects venom directly into specific cerebral regions of its cockroach prey. As a result of the sting, the cockroach remains alive but immobile, but not paralyzed, and serves to nourish the developing wasp larva.

In insects, thoracic pattern generators are modulated by the two head ganglia, the supraesophageal ganglion (brain) and the subesophageal ganglion, which act as higher-order neuronal centers. To explore the contribution of each head ganglion to the initiation and maintenance of specific motor behaviors in cockroaches (Periplaneta americana), we performed specific lesions to remove descending inputs from either the brain or the subesophageal ganglion or both, and quantified the behavioral outcome with a battery of motor tasks. We show that 'emergency' behaviors, such as escape, flight, swimming or righting, are initiated at the thoracic level independently of descending inputs from the head ganglia. Yet, the head ganglia play a major role in maintaining these reflexively initiated behaviors. By separately removing each of the two head ganglia, we show that the brain excites flight behavior and inhibits walking-related behaviors, whereas the subesophageal ganglion exerts the opposite effects. Thus, control over specific motor behaviors in cockroaches is anatomically and functionally compartmentalized. We propose a comprehensive model in which the relative permissive versus inhibitory inputs descending from the two head ganglia, combined with thoracic afferent sensory inputs, select a specific thoracic motor pattern while preventing the others.

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.

The parasitoid wasp A. compressa hunts cockroaches as a live food supply for its offspring. The wasp selectively injects venom into the cerebral ganglia of the prey to induce long-term hypokinesia [1-5], during which the stung cockroach, although not paralyzed, does not initiate spontaneous walking and fails to escape aversive stimuli. This allows the wasp to grab the cockroach by the antenna and walk it to a nest much like a dog on a leash. There, the wasp lays an egg on the prey, seals the nest, and leaves. The stung cockroach, however, does not fight to escape its tomb but rather awaits its fate, being consumed alive by the hatching larva over several days. We investigated whether the venom-induced hypokinesia is a result of an overall decrease in arousal or, alternatively, a specific decrease in the drive to initiate or maintain walking. We found that the venom specifically affects both the threshold for the initiation and the maintenance of walking-related behaviors. Nevertheless, the walking pattern generator itself appears to be intact. We thus report that the venom, rather than decreasing overall arousal, manipulates neuronal centers within the cerebral ganglia that are specifically involved in the initiation and maintenance of walking.

SummaryMillions of years of co-evolution have driven parasites to display very complex and exquisite strategies to manipulate the behaviour of their hosts. However, although parasite-induced behavioural manipulation is a widespread phenomenon, the underlying neuronal mechanisms are only now beginning to be deciphered. Here, we review recent advancements in the study of the mechanisms by which parasitoid wasps use chemical warfare to manipulate the behaviour of their insect hosts. We focus on a particular case study in which a parasitoid wasp (the jewel wasp Ampulex compressa) performs a delicate brain surgery on its prey (the American cockroach Periplaneta americana) to take away its motivation to initiate locomotion. Following a brief background account of parasitoid wasps that manipulate host behaviour, we survey specific aspects of the unique effects of the A. compressa venom on the regulation of spontaneous and evoked behaviour in the cockroach host.