Behavior varies even among genetically identical animals raised in the same environment. However, little is known about the circuit or anatomical origins of this individuality. Here, we demonstrate a neural correlate of odor preference behavior in the olfactory sensory periphery. Namely, idiosyncratic calcium responses in projection neuron (PN) dendrites and densities of the presynaptic protein Bruchpilot in olfactory receptor neuron (ORN) axon terminals correlate with individual preferences in a choice between two aversive odorants. The ORN-PN synapse appears to be a locus of individuality where microscale variation gives rise to idiosyncratic behavior. Simulating microscale stochasticity in ORN-PN synapses of a 3062 neuron model of the antennal lobe recapitulates patterns of variation in PN calcium responses matching experiments. Conversely, stochasticity in other compartments of this circuit does not recapitulate those patterns. Our results demonstrate how physiological and microscale structural circuit variations can give rise to individual behavior, even when genetics and environment are held constant.
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