Circuit and cellular mechanisms facilitate the transformation from dense to sparse coding in the insect olfactory system

Abstract

Transformations between sensory representations are shaped by neural mechanisms at the cellular and the circuit level. In the insect olfactory system encoding of odor information undergoes a transition from a dense spatio-temporal population code in the antennal lobe to a sparse code in the mushroom body. However, the exact mechanisms shaping odor representations and their role in sensory processing are incompletely identified. Here, we investigate the transformation from dense to sparse odor representations in a spiking model of the insect olfactory system, focusing on two ubiquitous neural mechanisms: spike-frequency adaptation at the cellular level and lateral inhibition at the circuit level. We find that cellular adaptation is essential for sparse representations in time (temporal sparseness), while lateral inhibition regulates sparseness in the neuronal space (population sparseness). The interplay of both mechanisms shapes spatio-temporal odor representations, which are optimized for discrimination of odors during stimulus onset and offset. Response pattern correlation across different stimuli showed a non-monotonic dependence on the strength of lateral inhibition with an optimum at intermediate levels, which is explained by two counter-acting mechanisms. In addition, we find that odor identity is stored on a prolonged time scale in the adaptation levels but not in the spiking activity of the principal cells of the mushroom body, providing a testable hypothesis for the location of the so-called odor trace.

Significance Statement In trace conditioning experiments, insects, like vertebrates, are able to form an associative memory between an olfactory stimulus and a temporally separated reward. Forming this association requires a prolonged odor trace. However, spiking responses in the mushroom body, the principal site of olfactory learning, are brief and bound to the odor onset (temporal sparseness). We implemented a spiking network model that relies on spike-frequency adaptation to reproduce temporally sparse responses. We found that odor identity is reliably encoded in the neurons’ adaptation levels, which are mediated by spike-triggered calcium influx. Our results suggest that a prolonged odor trace is established in the calcium levels of the relevant neuronal population. This prediction has found recent experimental support in the fruit fly.