Stimulus selection and novelty detection via divergent synaptic plasticity in an olfactory circuit

In nature, diverse sensory signals fluctuate in time and in space. Odors, for example, are distorted by wind into narrow filaments. When multiple spatially distinct odor sources exist, these filaments interleave but do not intermix. Such odor landscapes pose complementary challenges to animals – such as the fruit fly – that depend on olfaction to find food or mating partners. First, to select the best odor to track back to its source, the olfactory system must compare information from different filaments over relatively long timescales. Second, to remain on high alert to unexpected changes, such as a sudden increase in filament frequency, the olfactory system must respond to novelty on relatively short timescales.

In Drosophila, projection neurons (PNs) innervating different glomeruli encode different but overlapping sets of odors. Similarly tuned PNs tend to target the same lateral horn neurons (LHNs). We investigated the odor coding transformation between PNs and LHNs, focusing on two LHN types that receive projections from the same two PNs. To mimic natural odor filaments, we delivered repeated pulses of odors that privately activate each of these two PNs while recording LHN activity with voltage imaging or electrophysiology.

Despite receiving input from the same PNs, the two LHN types perform different operations. One LHN type responded to either odor presented in isolation but suppressed responses to the weaker odor when interleaved in time. This implements stimulus selection. The other LHN type suppressed responses to each odor independently over repeated pulses. This implements novelty detection. Paired recordings from connected PN-LHN pairs showed that synapses from the same PN operate with different short-term plasticity dynamics for different LHN targets. Synaptic dynamics were well-matched to odor coding dynamics of each LHN. This illustrates how variations in a basic building block of neural circuits (short-term plasticity) can implement diverse and complementary functions.