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.
- efficient coding
- lateral inhibition
- odor trace
- sensory processing
- spike frequency adaptation
- spiking neural network
Footnotes
Authors report no conflict of interest.
This research is supported by the German Research Foundation (grant no. 403329959) within the Research Unit 'Structure, Plasticity and Behavioral Function of the Drosophila mushroom body' (DFG-FOR 2705, https://www.uni-goettingen.de/en/601524.html). RB received a scholarship from the Research Training Group "Sensory Computation in Neural Systems" (DFG-RTG 1589) funded by the German Research Foundation.
This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
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