Multiple memory traces after associative learning in the honey bee antennal lobe

Abstract

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.

Neural substrate for higher-order learning in an insect: Mushroom bodies are necessary for configural discriminations

“…In the bee, a convergence between odor and sucrose pathways also exists at the level of the AL and the LH because VUMmx1, the instructive neuron that signals the presence of sucrose reward in the bee brain, contacts the olfactory circuit at these stages besides that of the MBs (50). Functional and structural changes have been found in the ALs of adult bees after elemental olfactory learning in the laboratory (66)(67)(68) or shortly after emergence in the hive (69,70). We thus suggest that, in the absence of functional MBs, elemental learning is still possible via the ALs.…”

Asymmetric neural coding revealed by in vivo calcium imaging in the honey bee brain

“…Calcium imaging data came from the same published and unpublished dataset from our previous study [23]. The recordings were performed on either the left or the right AL.…”

“…In total, 66 bees were imaged, 33 left ALs and 33 right ALs. Details of the imaging method can be found elsewhere [23]. Briefly, PNs of both ALs were stained with the calcium-sensitive dye Fura-2 dextran (Invitrogen).…”

Investment in higher order central processing regions is not constrained by brain size in social insects

“…Lastly, interpreting brain component ratios (such as C/AO) as reflecting relative investment in cognitive function versus sensory input [49] discounts the importance of peripheral regions to information processing and behavioural output. In social bees, for example, neither the OLs or the ALs simply relay sensory information to the Cs for processing: visual input is highly processed in the OLs prior to reaching the Cs [77][78][79][80], and plastic changes causally linked to the formation and retrieval of olfactory memories occur in the ALs, upstream of olfactory information processing by the Cs [81,82]. Insects that rely on fast, high-acuity vision (such as fast fliers or, among the ants, visual predators), for example, may be likely to have large OLs, whereas insects that rely heavily on visual or olfactory memory (such as honeybees or navigating desert ants) may invest disproportionately in mushroom body neuropil, including the Cs.…”