You've just arrived in a new city, and you are rather hungry, so you start exploring the streets to find a suitable place to eat. All moving creatures need to inspect their surroundings and they have developed distinct motor exploratory strategies to do so efficiently. But where in the central nervous system are the neural networks that generate and regulate these exploratory routines located? In a recent paper published in Current Biology, Jimena Berni, Michael Bate and their colleagues at the University of Cambridge, UK, have explored this question by using the simple and genetically tractable nervous system of the Drosophila larva.
This larva displays an exploratory behaviour that consists of straight crawling – generated by forward wave-like contractions of its body wall – interspersed by turns. Turns are decision-making points during which the larva stops, swings its head to sample the environment, and then commences crawling along a new trajectory. Like other animals, the larvae can modify their exploratory strategy in response to different environmental conditions and internal states by varying the duration of forward crawling and the frequency and direction of turns. To understand the differential role of brain and ventral nerve cord circuits underpinning this behaviour, the authors genetically engineered larvae in which the anterior part of their central nervous system – the brain and suboesophageal ganglion – could be remotely switched off in a reversible way in freely behaving animals.
The team first showed that when they inhibited the activity of all brain neurons the larvae could still perform normal peristaltic waves. Thus, the circuits producing crawling do not reside in the brain, but in the ventral nerve cord.
But what about the networks controlling the key decision of when and how to turn? The authors counted the number and angle of turns performed by these effectively ‘brainless’ larvae and found that turning frequency and angle were indistinguishable from those of larvae with functioning brains. This demonstrates that the networks producing the default exploratory locomotor programme in the larvae reside in the ventral nerve cord, and can operate normally without a functioning brain. But how is this exploratory behaviour modified by the larva under changing environmental conditions?
The researchers first assayed the exploratory abilities of the temporarily ‘brainless’ larvae in response to the odour of a drop of yeast, which is a powerful natural modifier of exploratory behaviour in larvae. It is well established that the networks responsible for the key processing steps of olfactory information reside in the brain. Therefore, unsurprisingly, the ‘brainless’ larvae were unable to modify their exploratory routine in response to the odour. The authors then decided to try using a stimulus that might be less dependent on brain processing, so they turned to light. An array of light receptors covers the larval body wall, and although the way in which this visual information is processed remains unknown, it is possible that some processing might occur locally within the ventral nerve cord. Berni and colleagues found that ‘brainless’ larvae display a completely normal and coordinated avoidance response to light.
These results reveal that the ventral nerve cord of the larva contains all the necessary circuit elements to produce an effective exploratory strategy and to modify it in response to environmental cues, such as light, without involving the brain. However, the brain is responsible for adjusting the larva's exploration strategy in response to other environmental sensory inputs, such as olfactory information, during goal-directed behaviour.
The elegant use of Drosophila genetic tools by Berni and co-workers has for the first time made it possible to remove brain function reversibly in a freely behaving animal. This led to the unexpected finding that the brain is dispensable for the explorative behavioural programme displayed by larvae. In the future, similar approaches might become feasible in vertebrate model organisms to find out just how brainless some of our own behaviour might be.
