Wasp venom injected into the prey's brain modulates thoracic identified monoaminergic neurons

Abstract

The wasp Ampulex compressa injects a cocktail of neurotoxins into the brain of its cockroach prey to induce an enduring change in the execution of locomotory behaviors. Our hypothesis is that the venom injected into the brain indirectly alters the activity of monoaminergic neurons, thus changing the levels of monoamines that tune the central synapses of locomotory circuits. The purpose of the present investigation was to establish whether the venom alters the descending control, from the brain, of octopaminergic neurons in the thorax. This question was approached by recording the activity of specific identified octopaminergic neurons after removing the input from the brain or after a wasp sting into the brain. We show that the activity of these neurons is altered in stung and "brainless" animals. The spontaneous firing rate of these neurons in stung and brainless animals is approximately 20% that in control animals. Furthermore, we show that an identified octopamine neuron responds more weakly both to sensory stimuli and to direct injection of current in all treated groups. The alteration in the activity of octopamine neurons is likely to be part of the mechanism by which the wasp induces a change in the behavioral state of its prey and also affects its metabolism by reducing the potent glycolytic activator fructose 2,6-bisphosphate in leg muscle. To our knowledge, this is the first direct evidence of a change in electrical activity of specific monoaminergic neurons that can be so closely associated with a venom-induced change in behavioral state of a prey animal.

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

“…Supporting this hypothesis are the findings of previous studies showing that the activity of thoracic dorsal unpaired median (DUM) neurons, a population of thoracic OA-releasing neurons, is decreased in stung cockroaches (e.g. Rosenberg et al, 2006). Because OA is an important excitatory neuromodulator in insects, it appears that the cerebral circuits targeted by the wasp's venom affect at least, directly or indirectly, the excitability of thoracic DUM neurons to decrease the drive for walking.…”

Lessons in Mind Control: Trends in Research on the Molecular Mechanisms behind Parasite-Host Behavioral Manipulation

“…Adult wasps are also known to inject venom into the CNS of insects, resulting in the loss of self-driven movement, ultimately enabling the wasp to continue its reproductive cycle (Libersat et al, 2009). Currently, empirical evidence from the jewel wasp-cockroach host-parasite system suggests a component of this venom alters the activity of neuron populations involved in regulating OA, and thus locomotive ability (Rosenberg et al, 2006). If we contrast this to the larval wasp disrupting OA breakdown in the caterpillar, it may suggest altering OA does not have merely digestive, but also locomotor effects similar to that of adult wasp venom on the cockroach.…”

“…Increasingly this seems to be the case in host parasite systems (Thomas et al, 2005;Adamo, 2012;Houte et al, 2013;Libersat and Gal, 2014). For example, looking back to the jewel wasp-cockroach parasite-host system, evidence suggests OA is regulated through indirect mechanisms (Rosenberg et al, 2006). This is surprising considering, as a host-parasite system, it would be one of the most likely to directly manipulate neuromodulator levels in the host, given the relatively similar body sizes between the host and parasite, and the precise control over where the wasp can target its manipulation (Libersat and Gal, 2014).…”

Octopamine partially restores walking in hypokinetic cockroaches stung by the parasitoid waspAmpulex compressa

“…The increase in walking duration observed in OA-injected stung cockroaches suggests that OA might be either depleted or not secreted after a sting. In support of this hypothesis, we showed previously that the activity level of octopaminergic neurons in the thoracic ganglia is strongly depressed in stung cockroaches (Rosenberg et al, 2006). The question as to whether or not this also occurs in octopaminergic neurons in the head ganglia remains to be investigated by direct intracellular recording.…”

“…One of the neuronal signatures of this hypokinetic state is a change in the activity of neurons secreting octopamine (OA), a monoamine specific to invertebrates. In stung animals the spontaneous firing rate of thoracic octopaminergic neurons is dramatically decreased and the neurons respond more weakly to both sensory stimuli and direct injection of current (Rosenberg et al, 2006). It seems likely that the observed alteration in the activity of octopaminergic neurons is part of the mechanism by which the wasp induces a change in the behavioral state of its prey.…”