One of the reasons why we choose to study the brains of flies, rather than those of our closer vertebrate relatives, is the relatively small number of neurons in these tiny brains, and the fact that single neurons can be reproducibly identified and targeted across different animals. This allows us to dissect specific sets of neurons – known in the business as circuits – that are involved in specific tasks, to unveil how each neuron contributes to the processing in the brain, and to work out why this is relevant to the animal’s needs and evolutionary pressures.
One example of such a circuit is that in the fly brain that processes visual motion. In the fly brain, the areas responsible processing information from the eyes are the optic lobes. Here, the third layer of visual processing is the lobula plate, and neurons here, known as tangential cells, respond to motion across the visual field (that is, their electrical activity is changed when motion is presented in their visual field). Many studies have shown that these cells in fact respond to optic flow: the motion of a visual scene caused by moving through the environment. Try walking forwards: the objects around you appear to move past your eyes in a very stereotyped pattern, which is
different from the pattern when you spin in circles. For flies, this kind of visual information is very important, as it tells the fly about its own motion, which is essential for online in-flight corrections. Distinct sets of lobula plate tangential cells respond to different components of optic flow – some, for example, to optic flow caused by forward translation, and others to rotations about specific body axes. The VS cells are a group of tangential cells that respond during such rotations. Detecting these rotations allows the fly to correct for them, using its wings and neck to stabilise its body, in much the same way as we can unconsciously correct for the effect of a sudden gust of wind whilst walking.
When not in flight, this kind of rotation does not affect the fly, and so detecting these components of optic flow is not so essential. As such, when the fly is buzzing around, signalling by the VS cells is strongly enhanced compared to when it is on solid ground. First, the resting membrane potential of the cells is increased – which means that it is much easier to produce spikes, the electrical signals that neurons use to transmit information. Also, the response of the neurons to visual motion becomes much stronger. This demonstrates how the processing of sensory information is strongly dependent on the state of the animal, so that valuable processing power is dedicated only to that information that is relevant to the current behaviour.
The mechanisms that generate this modulation of VS cell responses during flight were the subject of a recent paper from the lab of Michael Dickinson. They developed a sophisticated setup, where the fly is fixed in place from above, but is free to move its wings, as if flying. A screen in front of the fly presents visual stimuli, a camera below tracks the fly’s motion, and a puffer jolts the animal into flight using a short air puff. Electrical recordings were used to measure the responses of VS cells to motion presented on the screen under different conditions. Flight enhances their responses to visual motion at certain speeds (or temporal frequencies, a measure of the speed at which bars are moving across the screen).
Octopamine is a molecule used for communication between some neurons in insects and other invertebrates, much like dopamine or serotonin, which are found in the human brain. In locusts, octopamine levels rise during flight, and this is thought to produce the dramatic changes in their physiology seen when they fly. So, thought the authors of this study, octopamine is a likely candidate to cause the in-flight modulation of VS cell responses in flies. First, they showed that applying octopamine to the brain has a similar effect on VS cells responses as flight itself. Next, they look at the activity of neurons that release octopamine, and, sure enough, they become more active during flight. Expressing a heat-sensitive channel specifically in these octopamine-expressing neurons allow them to be activated by heat, and doing so also increases VS cell responses to visual motion. Conversely, inactivating these same neurons prevents the modulation of VS cell responses by flight. Therefore, overall the release of octopamine is sufficient to boost VS cell responses, and is also necessary for this boost.
Interestingly, the effect of octopamine seems to be restricted to the boost of responsiveness to visual motion during flight. The shift in baseline membrane potential of VS cells during flight appears to be independent of octopamine, suggesting that different mechanisms converge to increase VS cell responsiveness during flight. One possibility is that this separate effect is due to input from mechanoreceptors, which detect air flow on the body surface during flight, a reliable indicator of active motion.
This neat study adds to the wealth of literature showing that, from the nematode worm to the primate brain, neuromodulators (chemicals that modulate neural signals rather than directly transmitting them) play an essential role in altering how the brain processes information depending on the state of the animal. This ensures that precious resources are dedicated primarily to those tasks that are important for the current behaviour, and to those behaviours that will keep the animal fit and healthy, ensuring its survival and reproduction. After all, the ability to survive and reproduce is what drives evolution – and so all the intricate and complex mechanisms in our brains have evolved to do just this.