What the fly’s nose tells the fly’s brain

Significance This work is significant for three reasons. First, a new way the brain represents information is identified, one in which the information present in a large population of neurons can be gotten from a small subset of any neurons rather that from a subset of certain specific neurons. Second, the nature of the combinatorial code used to specify odor identity is identified, and this same type of code may be used in other contexts. Third, the way fly olfaction works can potentially provide a model for understanding the function of important vertebrate brain regions that appear to share the same neural circuit architecture. The fly olfactory system has a three-layer architecture: The fly’s olfactory receptor neurons send odor information to the first layer (the encoder) where this information is formatted as combinatorial odor code, one which is maximally informative, with the most informative neurons firing fastest. This first layer then sends the encoded odor information to the second layer (decoder), which consists of about 2,000 neurons that receive the odor information and “break” the code. For each odor, the amplitude of the synaptic odor input to the 2,000 second-layer neurons is approximately normally distributed across the population, which means that only a very small fraction of neurons receive a large input. Each odor, however, activates its own population of large-input neurons and so a small subset of the 2,000 neurons serves as a unique tag for the odor. Strong inhibition prevents most of the second-stage neurons from firing spikes, and therefore spikes from only the small population of large-input neurons is relayed to the third stage. This selected population provides the third stage (the user) with an odor label that can be used to direct behavior based on what odor is present.