Using sophisticated techniques to silence or activate specific neurons, researchers from Stanford University have established that a simple behaviour used by fruit fly larvae to evade attack from parasitic wasps is triggered by a type of sensory neuron that is similar to the neurons which respond to painful stimuli in mammals.
Although little is known about the somatosensory system of fruit flies, several lines of evidence have implicated sensory cells called multidendritic neurons as nociceptors (cells that are responsive to noxious chemical, mechanical or thermal stimuli).
First, with their multiply branched and naked endings which innervate the epidermis, they resemble the nociceptors of vertebrates. Second, multidendritic neurons express an ion channel called painless, which is necessary for the response to noxious stimuli, and which was identified in a mutant fly strain that is unresponsive to such stimuli.
The researchers used genetic targeting to deliver tetanus toxin specifically to the four different types of multidendritic neurons. This effectively silences the cells by binding to and destroying one of the proteins involved in neurotransmitter release.
In larvae with type IV neurons silenced in this way, the rolling behaviour in response to noxious thermal stimuli applied by the researchers was abolished. By contrast, in larvae with types I and II neurons silenced, the rolling behaviour was present but slightly uncoordinated, suggesting that these cells are involved in proprioception.
The researchers then used a newly-developed technique called channelrhodopsin photoactivation to activate and inhibit the neurons rapidly. They found that pulses of blue light which activated the type IV neurons would also elicit the rolling behaviour, and that rolling ceased in response to pulses of a differently-coloured light that inactivated the cells. Light activation of type II and III neurons elicited in the larvae a distinct accordion-like wave of muscle contractions.
Surprisingly, the rolling tended to occur in the direction of, rather than away from, the heat probe used by the experimenters to elicit the behaviour. This was found to help the larvae evade attacks from parasitic wasps: rolling may deflect the wasp’s oviposter, which normally penetrates the cuticle during an attack so that the wasp can lay an egg inside the larva.
Type IV neurons share another similarity with their mammalian counterparts: they are the only type of multidendritic neurons whose processes cross the midline of the embryo to form synapses with cells on the other side. This organization is similar to that of the ascending fibres which carry pain information from the spinal cord in mammals (the fibres cross the midline within the brain before reaching the higher order somatosensory areas).
It is, however, unclear whether or not the fruit fly’s brain is involved in the rolling behaviour. The fruit fly larva’s response to noxious stimuli may be more like a reflex: the sensory neurons that detect the stimulus transmit signals to the motor neurons which control the muscles, in the absence of any involvement by the brain.
However, rolling and similar behaviours involve complex and co-ordinated patterns of muscle activity throughout the body, and so may be under the control of central pattern generators in the brain. But even if the brain is involved, it is unlikely that fruit flies feel pain as we do, because human pain has emotional aspects which are processed in the association areas of the cerebral cortex.
Hwang, R. Y., et al. (2007). Nociceptive Neurons Protect Drosophila Larvae from Parasitoid Wasps. Curr. Biol. doi: 10.1016/j.cub.2007.11.029 [Abstract]