Abstract
One of the most important tasks of the brain is to learn and remember information associated with food. Studies in mice and Drosophila have shown that sugar rewards must be metabolisable to form lasting memories, but few other animals have been studied. Here, we trained adult, worker honeybees (Apis mellifera) in two olfactory tasks (massed and spaced conditioning) known to affect memory formation to test how the schedule of reinforcement and the nature of a sugar reward affected learning and memory. The antennae and mouthparts of honeybees were most sensitive to sucrose but glucose and fructose were equally phagostimulatory. Whether or not bees could learn the tasks depended on sugar identity and concentration. However, only bees rewarded with glucose or sucrose formed robust long-term memory. This was true for bees trained in both the massed and spaced conditioning tasks. Honeybees fed with glucose or fructose exhibited a surge in haemolymph sugar of greater than 120mM within 30s that remained elevated for as long as 20min after a single feeding event. For bees fed with sucrose, this change in haemolymph glucose and fructose occurred with a 30s delay. Our data showed that olfactory learning in honeybees was affected by sugar identity and concentration, but that olfactory memory was most strongly affected by sugar identity. Taken together, these data suggest that the neural mechanisms involved in memory formation sense rapid changes in haemolymph glucose that occur during and after conditioning.
Highlights
The brain has been shaped by natural selection to learn to associate cues that predict the occurrence of nutritiously valuable food
The mouthparts of bees were much more sensitive to sucrose than to fructose or glucose (Fig. 1B), with as many as 80% being willing to consume a droplet of 0.3 M sucrose whereas < 20% of the bees would consume a 0.3 M droplet of glucose or fructose (Fig. 1B, Table S2, sugar: χ52 = 38.2, P < 0.001)
Our previous research established that bees formed a lasting olfactory memory when they were fed a reward during conditioning of the proboscis extension response (PER) (Wright et al, 2007)
Summary
The brain has been shaped by natural selection to learn to associate cues that predict the occurrence of nutritiously valuable food. An important mechanism for assessing food value and forming lasting memories of sensory cues is through post-ingestive signalling. Studies in Drosophila indicate that flies form lasting memories for several metabolisable sugars including fructose and glucose (Burke and Waddell, 2011; Dus et al, 2013, 2011; Miyamoto et al, 2012; Musso et al, 2015; Perisse et al, 2013) This could indicate that the mechanisms of post-ingestive nutrient detection or memory formation in insects and mammals are different
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