Suppression of host nocifensive behavior by parasitoid wasp venom.

The parasitoid wasp Ampulex compressa envenomates the brain of its host the American cockroach (Periplaneta americana), thereby making it a behaviorally compliant food supply for its offspring. The target of venom injection is a locomotory command center in the brain called the central complex. In this study, we investigate why stung cockroaches do not respond to injuries incurred during the manipulation process by the wasp. In particular, we examine how envenomation compromises nociceptive signaling pathways in the host. Noxious stimuli applied to the cuticle of stung cockroaches fail to evoke escape responses, even though nociceptive interneurons projecting to the brain respond normally. Hence, while nociceptive signals are carried forward to the brain, they fail to trigger robust nocifensive behavior. Electrophysiological recordings from the central complex of stung animals demonstrate decreases in peak firing rate, total firing, and duration of noxious-evoked activity. The single parameter best correlated with altered noxious-evoked behavioral responses of stung cockroaches is reduced duration of the evoked response in the central complex. Our findings demonstrate how the reproductive strategy of a parasitoid wasp is served by venom-mediated elimination of aversive, nocifensive behavior in its host.

On the Role of the Head Ganglia in Posture and Walking in Insects.

In insects, locomotion is the result of rhythm generating thoracic circuits and their modulation by sensory reflexes and by inputs from the two head ganglia, the cerebral and the gnathal ganglia (GNG), which act as higher order neuronal centers playing different functions in the initiation, goal-direction, and maintenance of movement. Current knowledge on the various roles of major neuropiles of the cerebral ganglia (CRG), such as mushroom bodies (MB) and the central complex (CX), in particular, are discussed as well as the role of the GNG. Thoracic and head ganglia circuitries are connected by ascending and descending neurons. While less is known about the ascending neurons, recent studies in large insects and Drosophila have begun to unravel the identity of descending neurons and their appropriate roles in posture and locomotion. Descending inputs from the head ganglia are most important in initiating and modulating thoracic central pattern generating circuitries to achieve goal directed locomotion. In addition, the review will also deal with some known monoaminergic descending neurons which affect the motor circuits involved in posture and locomotion. In conclusion, we will present a few issues that have, until today, been little explored. For example, how and which descending neurons are selected to engage a specific motor behavior and how feedback from thoracic circuitry modulate the head ganglia circuitries. The review will discuss results from large insects, mainly locusts, crickets, and stick insects but will mostly focus on cockroaches and the fruit fly, Drosophila.

Nociceptive Pathway in the Cockroach Periplaneta americana.

Detecting and avoiding environmental threats such as those with a potential for injury is of crucial importance for an animal's survival. In this work, we examine the nociceptive pathway in an insect, the cockroach Periplaneta americana, from detection of noxious stimuli to nocifensive behavior. We show that noxious stimuli applied to the cuticle of cockroaches evoke responses in sensory axons that are distinct from tactile sensory axons in the sensory afferent nerve. We also reveal differences in the evoked response of post-synaptic projection interneurons in the nerve cord to tactile versus noxious stimuli. Noxious stimuli are encoded in the cockroach nerve cord by fibers of diameter different from that of tactile and wind sensitive fibers with a slower conduction velocity of 2-3 m/s. Furthermore, recording from the neck-connectives show that the nociceptive information reaches the head ganglia. Removing the head ganglia results in a drastic decrease in the nocifensive response indicating that the head ganglia and the nerve cord are both involved in processing noxious stimuli.

Mind Control: How Parasites Manipulate Cognitive Functions in Their Insect Hosts.

Neuro-parasitology is an emerging branch of science that deals with parasites that can control the nervous system of the host. It offers the possibility of discovering how one species (the parasite) modifies a particular neural network, and thus particular behaviors, of another species (the host). Such parasite-host interactions, developed over millions of years of evolution, provide unique tools by which one can determine how neuromodulation up-or-down regulates specific behaviors. In some of the most fascinating manipulations, the parasite taps into the host brain neuronal circuities to manipulate hosts cognitive functions. To name just a few examples, some worms induce crickets and other terrestrial insects to commit suicide in water, enabling the exit of the parasite into an aquatic environment favorable to its reproduction. In another example of behavioral manipulation, ants that consumed the secretions of a caterpillar containing dopamine are less likely to move away from the caterpillar and more likely to be aggressive. This benefits the caterpillar for without its ant bodyguards, it is more likely to be predated upon or attacked by parasitic insects that would lay eggs inside its body. Another example is the parasitic wasp, which induces a guarding behavior in its ladybug host in collaboration with a viral mutualist. To exert long-term behavioral manipulation of the host, parasite must secrete compounds that act through secondary messengers and/or directly on genes often modifying gene expression to produce long-lasting effects.

Do Quiescence and Wasp Venom-Induced Lethargy Share Common Neuronal Mechanisms in Cockroaches?

The escape behavior of a cockroach may not occur when it is either in a quiescent state or after being stung by the jewel wasp (Ampulex compressa). In the present paper, we show that quiescence is an innate lethargic state during which the cockroach is less responsive to external stimuli. The neuronal mechanism of such a state is poorly understood. In contrast to quiescence, the venom-induced lethargic state is not an innate state in cockroaches. The Jewel Wasp disables the escape behavior of cockroaches by injecting its venom directly in the head ganglia, inside a neuropile called the central complex a 'higher center' known to regulate motor behaviors. In this paper we show that the coxal slow motoneuron ongoing activity, known to be involved in posture, is reduced in quiescent animals, as compared to awake animals, and it is further reduced in stung animals. Moreover, the regular tonic firing of the slow motoneuron present in both awake and quiescent cockroaches is lost in stung cockroaches. Injection of procaine to prevent neuronal activity into the central complex to mimic the wasp venom injection produces a similar effect on the activity of the slow motoneuron. In conclusion, we speculate that the neuronal modulation during the quiescence and venom-induced lethargic states may occur in the central complex and that both states could share a common neuronal mechanism.