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

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. 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 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

A Parasitoid Wasp Manipulates the Drive for Walking of Its Cockroach Prey

SummaryThe 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

What can parasitoid wasps teach us about decision-making in insects?

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.</jats:p

Neuroparasitology of Parasite–Insect Associations

Insect behavior can be manipulated by parasites, and in many cases, such manipulation involves the central and peripheral nervous system. Neuroparasitology is an emerging branch of biology that deals with parasites that can control the nervous system of their host. The diversity of parasites that can manipulate insect behavior ranges from viruses to macroscopic worms and also includes other insects that have evolved to become parasites (notably, parasitic wasps). It is remarkable that the precise manipulation observed does not require direct entry into the insect brain and can even occur when the parasite is outside the body. We suggest that a spatial view of manipulation provides a holistic approach to examining such interactions. Integration across approaches from natural history to advanced imaging techniques, omics, and experiments will provide new vistas in neuroparasitology. We also suggest that for researchers interested in the proximate mechanisms of insect behaviors, studies of parasites that have evolved to control such behavior is of significant value. </jats:p

Control of Cercal Position During Flight in the Cockroach: A Mechanism for Regulating Sensory Feedback

ABSTRACT In a flying cockroach, the response of cereal wind receptors to standard wind stimuli was reduced by 40 % compared with when the animal was at rest. While flying, rhythmic bursts of action potentials, phase-locked to the wingbeat rhythm, descended the nerve cord. These bursts appeared responsible for a phase-locked rhythmic discharge of cereal motor neurones. This, in turn, evoked a cereal displacement, maintained throughout flight. It is suggested that this displacement causes a pressure block of the sensory nerve, since it has recently been shown that experimental displacement of the cercus in a non-flying cockroach causes a similar degree of sensory reduction (40%) by means of such a mechanism (Libersat, Goldstein &amp; Camhi, 1987). The functional significance of this means of sensory reduction is discussed.</jats:p