Summary
Adaptation often implements an efficient coding strategy to align neuron sensitivity to relevant stimuli. However, when sensory information is encoded in populations of neurons, adaptation of individual units could deteriorate stimulus information relevant for behavior. One prominent example is the encoding of olfactory information, which occurs at the population level. We show that if individual ORNs were to adapt following an efficient coding principle, contrast information would be lost at the population level, impairing the detection of ON and OFF stimuli. Surprisingly, adaptation of ORN firing responses is compensated at the axon terminal, where calcium transients are kept background-invariant by inhibitory feedback. We demonstrate that achieving this invariance across different background conditions requires an adaptation strategy that shifts response amplitude, rather than sensitivity as predicted by the efficient coding principle. This background invariance is passed on to second-order olfactory neurons, through facilitation of vesicle release that involves modulation of Unc13 proteins. We conclude that synaptic and circuit computations compensate peripheral firing rate adaptation, enhancing the separation of ON and OFF contrasts, while preserving the identity of ON stimuli in population codes. Our findings identify a strategy that allows neural circuits to minimize the cost of information transmission while preserving information content.
Competing Interest Statement
The authors have declared no competing interest.
