Frederic Libersat

Manipulation of Host Behavior by Parasitic Insects and Insect Parasites

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.

Monoamines and the Orchestration of Behavior

Abstract Animals possess a rich repertoire of behaviors, each generated by the orchestrated activity of assemblies of neurons. Neuromodulators, and particularly monoamines, have been found to play a role in the recruitment of such assemblies. The role of specific monoamines in the modulation of behavior has been particularly well studied using invertebrate animals as models. In these animals, the neuronal assemblies underlying a behavior often consist of fewer neurons than those in vertebrates, and in many cases the activity of specific neurons can be causally linked to the expression of a specific behavior. In this overview, we illustrate the concept of chemical orchestration of behavior, using well-studied models of how monoamines modulate complex and long-lasting behaviors in invertebrate animals.

Frequency as a releaser in the courtship song of two crickets, Gryllus bimaculatus (de Geer) and Teleogryllus oceanicus: a neuroethological analysis

Abstract1.The courtship behavior of male field crickets, Gryllus bimaculatus (De Geer) and Teleogryllus oceanicus, is a complex, multimodal behavioral act that involves acoustic signals (a courtship song; Fig. 1A,B). The dominant frequency is 4.5 kHz for T. oceanicus song (Fig. 1A) and 13.5 kHz for G. bimaculatus (Fig. IB).2.When courting males are deprived of their courtship song by wing amputation, their courtship success declines markedly but is restored when courting is accompanied by tape-recordings of their courtship songs or a synthetic courtship song with only the dominant frequency of the natural song; other naturally occurring frequency components are ineffective for restoring mating success (Figs. 4, 5).3.It has been suggested that an identified auditory interneuron, AN2, plays a critical role in courtship success. Chronic recordings of AN2 in an intact, tethered female show that AN2s response to the natural courtship song and synthesized songs at 4.5 and 13.5 kHz is similar in T. oceanicus. By contrast, in G. bimaculatus, AN2s response to the natural courtship song and synthesized song at 13.5 kHz, but not at 4.5 kHz, is similar (Figs. 2,3).4.In behavioral experiments, playback of a 30 kHz synthetic courtship song in G. bimaculatus does not restore courtship success, yet this same stimulus elicits as strong a response from AN2 as does the normal courtship song (Fig. 6). Thus, contrary to earlier work by others, we conclude AN2 is not, by itself, a critical neural link in the courtship behavior of these two species of crickets.

Mechanisms of dendritic maturation.

The highly complex geometry of dendritic trees is crucial for neural signal integration and the proper wiring of neuronal circuits. The morphogenesis of dendritic trees is regulated by innate genetic factors, neuronal activity, and external molecular cues. How each of these factors contributes to dendritic maturation has been addressed in the developing nervous systems of animals ranging from insects to mammals. The results of such investigations have shown that the contribution of intrinsic and extrinsic factors and activity, however, appear to be weighted differentially in different types of neurons, in different brain areas, and especially in different species. Moreover, it appears that dozens of molecules have been found to regulate dendritic maturation, but it is almost certain that each molecule plays only a specific role in this formidable cooperative venture. This article reviews our current knowledge and understanding of the role of various factors in the establishment of the architecture of mature dendritic trees.

Neuromodulation of the escape behavior of the cockroach Periplaneta americana by the venom of the parasitic wasp Ampulex compressa

Abstract1.The wasp Ampulex compressa hunts cockroaches as food for her offspring. Stung cockroaches show little spontaneous movement although they are able to move. Wind stimuli to the cerci, which normally produce escape responses, are no longer effective in stung cockroaches. In the present paper, we have searched for neural correlates responsible for the impairment of the escape behavior by the venom.2.In control cockroaches, a typical motor response in the coxal depressor muscle to wind or tactile stimuli consists of an initial burst of the fast and slow depressor motoneurons followed by rhythmic discharges. In stung cockroaches, both stimuli evoke only a burst in the slow but no discharge activity in the fast depressor neuron. Intracellular recordings from the fast depressor motoneuron in stung cockroaches demonstrate that it still receives synaptic input, though subthreshold, from thoracic interneurons associated with the wind mediated escape circuitry. Discharge activity of the slow motoneuron lacks the rhythmic bursting pattern characteristic for slow walking in control animals.3.Yet, the venom affects neither the response of descending mechanosensitive giant interneurons to tactile stimuli nor the response of the abdominal giant interneurons to wind stimuli, both of which are known to excite the thoracic interneurons. The venom has also no effect on neuromuscular signal transmission.

Dynamics of learning‐induced spine redistribution along dendrites of pyramidal neurons in rats

We have previously shown that olfactory‐discrimination (OD) learning is accompanied by enhanced spine density along proximal apical dendrites of layer II pyramidal neurons in the piriform (olfactory) cortex. Here we studied the temporal dynamics of learning‐induced modifications in dendritic spine density throughout the dendritic trees of these neurons. We observed a transient increase in proximal apical spine density after OD learning, suggesting a strengthening of intrinsic excitatory inputs interconnecting neurons within the olfactory cortex. By contrast, the afferent pathway receiving direct input from the olfactory bulb shows spine pruning, suggesting that the connectivity is weakened. The changes in spine density can be attributed to a net change in number of spines, as the morphometric parameters of the dendrites are unaffected by learning. We suggest that spine density changes may represent a mechanism of selective synaptic reorganization required for olfactory learning consolidation.

New vistas on the initiation and maintenance of insect motor behaviors revealed by specific lesions of the head ganglia

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.

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 preys 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 Findings 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 and Significance We have identified the neuronal substrate responsible for the venom-induced manipulation of the cockroachs 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 cockroachs motivation to initiate walking without interfering with other non-related behaviors.

Octopamine partially restores walking in hypokinetic cockroaches stung by the parasitoid wasp Ampulex compressa.

SUMMARY When stung by the parasitoid wasp Ampulex compressa, cockroaches Periplaneta americana enter a hypokinetic state that is characterized by little, if any, spontaneous locomotor activity. In the present study we investigate the effect of an octopamine receptor agonist and an antagonist on the locomotor behavior of stung and control cockroaches. We show that in cockroaches stung by a wasp the octopamine receptor agonist chlordimeform induces a significant increase in spontaneous walking. In good agreement, in control individuals an octopamine receptor antagonist significantly reduces walking activity. Adipokinetic hormone I (AKH-I) promotes spontaneous walking in controls but does not do so in stung individuals, which suggests that the venom effect is most probably not mediated by AKH-I. Dopamine receptor agonists or antagonists had no significant effect on the spontaneous walking of stung or control cockroaches, respectively. The effect of the octopamine receptor agonist was maximal when injected into the brain, suggesting that the wasp venom interferes with octopaminergic modulation of walking initiation in central structures of the cockroach brain.

Venom effects on monoaminergic systems

The monoamines, dopamine, epinephrine, histamine, norepinephrine, octopamine, serotonin and tyramine serve many functions in animals. Many different venoms have evolved to manipulate monoaminergic systems via a variety of cellular mechanisms, for both offensive and defensive purposes. One common function of monoamines present in venoms is to produce pain. Some monoamines in venoms cause immobilizing hyperexcitation which precedes venom-induced paralysis or hypokinesia. A common function of venom components that affect monoaminergic systems is to facilitate distribution of other venom components by causing vasodilation at the site of injection or by increasing heart rate. Venoms of some scorpions, spiders, fish and jellyfish contain adrenergic agonists or cause massive release of catecholamines with serious effects on the cardiovascular system, including increased heart rate. Other venom components act as agonists, antagonists or modulators at monoaminergic receptors, or affect release, reuptake or synthesis of monoamines. Most arthropod venoms have insect targets, yet, little attention has been paid to possible effects of these venoms on monoaminergic systems in insects. Further research into this area may reveal novel effects of venom components on monoaminergic systems at the cellular, systems and behavioral levels.