Multiple Memory Traces After Associative Learning in the Honey Bee Antennal Lobe

We investigated the effect of associative learning on early sensory processing, by combining classical conditioning with in vivo calcium-imaging of secondary olfactory neurons, the projection neurons (PNs) in the honey bee antennal lobe (AL). We trained bees in a differential conditioning paradigm in which one odour (A+) was paired with a reward, while another odour (B-) was presented without a reward. Two to five hours after differential conditioning, the two odour-response patterns became more different in bees that learned to discriminate between A and B, but not in bees that did not discriminate. This learning-related change in neural odour representations can be traced back to glomerulus-specific neural plasticity, which depended on the response profile of the glomerulus before training. (i) Glomeruli responding to A but not to B generally increased in response strength. (ii) Glomeruli responding to B but not to A did not change in response strength. (iii) Glomeruli responding to A and B decreased in response strength. (iv) Glomeruli not responding to A or B increased in response strength. The data are consistent with a neural network model of the AL, which we based on two plastic synapse types and two well-known learning rules: associative, reinforcer-dependent Hebbian plasticity at synapses between olfactory receptor neurons (ORNs) and PNs; and reinforcer-independent Hebbian plasticity at synapses between local interneurons and ORNs. The observed changes strengthen the idea that odour learning optimizes odour representations, and facilitates the detection and discrimination of learned odours.